| A | B | C | D | E | F | G | H | I | J | K | L | M | N | O | P | Q | R | S | T | U | V | W | X | Y | Z | |
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1 | Review of existing scientific literature (with linked references) | |||||||||||||||||||||||||
2 | Cognitive Proxies | Pig | Chicken | Carp | Salmon | Octopus | Shrimp | Crab | Crayfish | Bee | Black soldier fly | Silkworm | ||||||||||||||
3 | A not B detour test | Explorative behaviour and spatial memory were tested in a novel detour paradigm in pigs differing in housing environment during rearing and in Backtest classification. They subsequently blocked the direct route to the exit, forcing animals to find a detour (MT1 test). This test was repeated once to investigate the relative improvement, i.e. detour learning (MT2 test). Performance was substantially improved in MT2, indicating that once a goal is apparent, pigs are able to solve a complex spatial memory task easily (Jansen et al., 2009). | Two-day-old chicks, Gallus gallus domesticus, were tested in a detour situation requiring them to abandon a clear view of a desired goal (a small red object on which they had been imprinted) in order to achieve that goal. The chicks were placed in a closed corridor, at one end of which was a barrier with a small window through which the goal was visible. Two symmetrical apertures placed midline to the corridor allowed the chicks to adopt routes passing around the barrier. After entering the apertures, chicks showed searching behaviour for the goal and appeared able to localize it, turning either right or left depending on their previous direction of turn. Thus, in the absence of any local orienting cues emanating from the goal, chicks were aware of the existence of an object that was no longer visible and could represent its spatial localization in egocentric coordinates (Regolin et al. 1995). Chicks, Gallus gallus domesticus, of 2 and 6 days of age were presented with a goal-object that was made to disappear behind one of two screens opposite each other. Chicks proved able to choose the correct screen when the goal-object was a social partner (i.e., a red ball on which they had been imprinted), whereas they searched at random behind either screen when the goal-object was a palatable prey (i.e. a mealworm). Chicks, however, appeared able to make use of the directional cue provided by the movement of the mealworm when tested in the presence of a cagemate. These results suggest that previous failure to obtain detour behaviour in the double screen test in the chick was not due to a cognitive limitation, but rather to the evocation of fear responses to the novel environment that interfered with the correct execution of the spatial task (Regolin et al. 1995b). | No studies of carp or other closely related species could be found. However, closely related cyprinids, zebrafish (Danio rerio) and goldfish (Carassius aurata), can successfully solve a simple detour task that requires them to “temporarily abandon the view of the goal-object (a group of conspecifics) to circumvent an obstacle” (Sovrano et al. 2018). | They trained bumblebees (Bombus impatiens) with two types of task that they believe represented challenges unlike any they have evolved to respond to. These involved dragging various-sized caps aside and rotating discs through varying arcs away from the entrances of artificial flowers (via detours of up to three body lengths), to access a reward hidden beneath. Further, they successfully trained bees to use disc colour as a discriminative stimulus predicting whether rotating discs clockwise or counterclockwise would reveal the reward. In this detour task, bumblebees successfully moved various-sized combi-nations of caps aside, even though this required their deviating from, and then returning to, the very spot that they first had to visit to start to move the caps aside. This true, complex operant conditioning demonstrated that bumblebees can learn novel, arbitrary behavioural sequences, manipulating and moving items in ways that seem far from any natural task that they would encounter, and doing so flexibly in response to specific discriminative stimuli. This adds to growing evidence of impressive behavioural plasticity and learning abilities in bees, and suggests new approaches for probing their cognitive abilities in the future (Mirwan et al., 2015). | |||||||||||||||||||||
4 | Attention bias | During anticipation of the aversive event, naive pigs tended to show more tail low. During the aversive event, naive pigs tended to defecate more, while they played more during the rewarding event. These results suggest that pigs might use physical signals in an affect-driven attention bias (ADAB) or it could be a normal communication signal - discussed in (Crump et al., 2018) (Reimert et al., 2013). | Using the tonic immobility paradigm (i.e., catatonic response to restraint), chickens show learned helplessness (i.e., unresponsiveness when cannot escape uncontrollable stressors) attentional shifts. Specifically, when observing eyespots, chickens in a learned helplessness condition took longer to recover motion than control birds but did so faster if an unaffected conspecific was present. Learned helplessness research suggests attentional shifts are associated with anxiety and depression-like states (Rodd et al. 1997). | Unknown. No studies of carp could be found. Preliminary studies on zebrafish (Danio rerio), a closely related cyprinid, have demonstrated zebrafish are capable of learning tasks which require sustained attention (Parker et al., 2012b) and are able to form and maintain an attentional set (Parker et al., 2012a). However, the attentional capacity of zebrafish has not yet been fully assessed (e.g. Echevarria et al., 2011) and attention has not yet been investigated. | Lean yes: some cephalopod species exhibit behavioural biases that might be driven by attention biases. For example, cephalopods show lateralized brain function, when specific functions are processed by either the left or the right side of the brain (Vallortigara 2000; Rogers et al. 2013; Versace & Vallortigara 2015). When viewing prey, octopuses display lateral biases for either the left or the right eye, but eye preference is present only at the individual level; there is no systematic left- or rightward bias at the population level (Byrne et al. 2002; 2004). Behavioural biases in arm use have also been observed in octopuses (Byrne et al. 2006), but again at the individual level not the population level. Research on cuttlefish have shown that one side of the brain is specialized to process information used for predation, and the other side is used for monitoring and scrutinizing potetnial predators (Schnell et al. 2016). In the context of camouflage, cuttlefish predominately use their right eye and associated neural structure to adjust the overall brightness of their camouflage pattern (Schnell et al. 2018). | Spatial cueing tasks (Posner, 1980) also quantify attention biases through reaction-times to a valence-neutral target. No studies, to the authors knowledge, have adapted the emotional spatial cueing task for animals (Crump et al., 2018). However, non-valenced predictive cue paradigms have been successful with honeybees (Eckstein et al., 2013), as well as macaques, rats, chickens and archerfish (Crump et al., 2018). | ||||||||||||||||||||
5 | Body awareness | (Broom, 2010) proposes the following definition for the term awareness: self-awareness is the cognitive process in an individual when it identifies and has a concept of its body or pos- sessions as being its own so that it can discriminate these from non-self stimuli. Hence he includes body awareness in his study about mirror image representation. | Unknown: no published literature found. However, wild observations suggest that octopuses would make excellent candidates for this type of investigation as they can camouflage to nearly any visual background in their natural ranges. This behaviour suggests that octopuses might have an understanding about the distinction between oneself and their physical environment (i.e., body awareness). Moreover, some species of octopus mimic other animals and masquerade as objects (rocks, moving algae), and thus an octopus might need to understand that their body is distinctly different to their surroundings and can discriminate body from non-self stimuli. | |||||||||||||||||||||||
6 | Communication | Communication during suckling in piglets (Algers and Jensen, 1985). Acoustic allometry aims to identify the specific acoustic correlates of body size within the vocalizations of a given species, and formants are often a useful acoustic cue in this context (Garcia et al., 2016). | Chicken communication consists of a large repertoire of at least 24 distinct vocalizations, as well as different visual displays. But the sophistication of chicken communication comes to the fore front when one examines how these vocalizations are used and the cognitive capacities, they apparently rely upon (Collias 1987; Joos and Collias 2008). | The predominant method of communication between conspecifics reported in the literature appears to be via chemical cues used both for communicating injuries and/or threats (e.g. Wilson et al. 2021a) and conspecific identity (e.g. Sisler & Sorensen 2008). Further, carp exhibit social learning, where information from conspecifics is transferred to naive fish and produces a change in behaviour (e.g. fishing hooks: Wallerius et al. 2020, predator cues: Wilson et al. 2021b). Further, at koi carp appear to engage in some courtship behaviours (e.g. males touching females with their nose and encircling them) which presumably signal a readiness to spawn to potential mating partners (e.g. Haniffa et al. 2007). | In salmonids, social subordination is communicated to conspecifics by the darkening of skin and eyes and dominant fish can be readily identified by their lighter color (e.g. Keenleyside & Yamamoto, 1962; Abbott et al., 1985; O’Connor et al., 1999; Hoglund et al., 2000). Aggression, in the form of lateral displays, nipping/biting, and chasing of conspecifics, is also displayed by juvenile salmonids while they are defending their feeding territories in streams and adult salmonids during nest defence (e.g. Keenleyside & Yamamoto, 1962). As well, salmonids use chemical cues for conspecific and kin identity (e.g. see review by Olsén, 1992; Brown & Brown, 1996; Newcombe & Hartman, 2011) and for spawning (e.g. Moore & Waring, 1996). Although there is currently debate in the literature regarding how homing to natal streams is achieved by anadromous salmonids, both hypotheses include the use of olfactory cues . The olfactory hypothesis suggests that salmonids migrating to the ocean are imprinted to recognise the complete chemical information of their natal stream water, whereas the pheromone hypothesis suggests that adult salmonids are able to locate their natal stream by pheromone trails emitted by juvenile salmon living in the stream and this capacity is inherited (e.g. Hasler, 1966; Nordeng, 1977). Salmonids have also been shown to communicate by means of sound production in the form of growls and snaps during spawning and air movement sounds, although the purpose of air movement sounds have not yet been determined (e.g. Rountree et al., 2018; Johnson et al., 2018). | Cephalopods are not deaf but there is little evidence that they communicate via sounds (Hanlon & Messenger 2018). Social tactile communication appears to be relatively uncommon in cephalopods, but has been observed in mimic octopus (e.g., perform brief touching of suckers) (Hanlon et al. 2008), some cuttlefish (Corner & Moore 1980) and squid species (DiMarco & Hanlon, 1997; van Staaden et al. 2011). Octopuses have a unique taste-by-touch ability, mediated by suckers along the arms, which contain chemotactile receptors (van Giesen et al. 2020). These specialised chemosensory cells are used to explore their environment and manipulate prey (Wells et al. 1965, Young 1971, Sumbre et al. 2001, Hochner 2012, Fouke and Rhodes 2020, van Giesen et al. 2020), facilitating discrimination between stationary and mobile objects and between attractive and aversive substances (van Giesen et al. 2020). The suckers send sensory information via ganglia at the base of the sucker to an arm nerve cord (analogous to the vertebrate spinal cord; Shigeno et al. 2018). Octopuses, as well as cuttlefish and squid, mainly communicate through visual signals and produce complex body patterns for both camouflage and communication. Visual displays in cephalopods are often conspicuous, stereotyped, exaggerated, or specialised to facilitate the transmission of information (Hanlon & Messenger 2018). Although octopuses are considered solitary, with some exceptions, they do produce a range of visual displays particularly during agonistic interactions (Scheel et al. 2016; Hanlon & Messenger 2018). Agonistic displays in octopuses can comprise of dozens of visual signals including stripes, bands, overall darkening or whitening of the head and body (Scheel et al. 2016). These visual signals are typically combined with postural signals such as spreading arms and web, standing tall and elevating the mantle. | There is evidence of communication in various forms across the Decapod order. Although there are no specific studies detailing communication methods in Penaeidae, there is evidence from taxa which share anatomical features. Machrobrachium rosenbergii (Giant freshwater prawn – family: Palaemonidae), Rhynchocinetes typus (Rock shrimp – family: Rhynchocinetidae), Lysmata shrimp (family: Hippolytidae) use sex pheromones and chemical signals for mate attraction and recognition (Bose et al. 2017; Al-Mohsen et al. 2009; Zhang 2009; Diaz & Thiel 2004; Liu et al. 2020; Zhang & Lin 2006) and it is possible that Penaeidae would use a similar strategy. Shrimp and prawns in the Penaeidae family have long antennae which are likely to be used for chemical detection in addition to detecting other sensory information (Vickery et al. 2012). Visual communication cues are also important for rock shrimp, which males rely upon to identify a mate (Diaz & Thiel 2004), whilst acoustic ‘snapping’ is by snapping shrimp to communicate with conspecifics (Hughes 1996; Hughes 2000; Tóth & Duffy 2005) (although snapping shrimp have a characteristic asymmetrically large claw which is used to produce the snap and this is not present in the Penaeidae family making this form of communication unlikely). | Communication is widely documented in many crab species, particularly in fiddler crabs and hermit crabs. The research on communication in the Portunidae family largely focusses on chemical communication, specifically sex-pheromones which have been documented in shore crabs, green crabs and blue crabs (Gleeson 1991; Ekerholm & Hallberg 2005; Bublitz et al. 2008; Bamber & Naylor 2009; Hardege et al. 2011; Fletcher et al. 2021). One study on sex-pheromone (and visual) cues in shore crabs has investigated their influence on agonistic interactions between males of the species. Solitary males initiated fights with males that were already guarding a female (Sneddon et al. 2003). Additionally, this study found that “females approached and performed courtship behaviour to the largest males”. Research on agonistic encounters (which often involve display acts) is also well-reported in the Portunidae family, focusing on the cost of such interactions and the influence of resource value (Smith & Taylor 1993; Sneddon et al. 1997; Fletcher & Hardege 2009). There is some work on the specific courtship display of the blue crab (which is not seen in other Portunid species), in which the male elevates their body by standing high on their legs, opening their chelae and paddling their swimming legs (Kamio et al. 2008; Wood & Derby 1996). Finally, one study on the selection of female blue crabs by males is based on the hue of female red claws (Baldwin & Johnsen 2009). Proprioception (and the organ responsible) has been fairly well-studied in Carcinus Maenas (e.g. Burke 1953;Whitear 1962; Bush 1965), although it’s use in communication is not reported. Since “most, if not all decapods have sensory structures capable of responding to substrate borne vibrational stimuli” (Popper et al. 2001), it is possible that these structures are also used for communication as in other crab families (e.g. fiddler crab: Aicher & Tautz 1990). | Crayfish communication systems have been widely studied (see review by Kubec et al. 2019). Depending on the turbidity of the environment, chemical, visual or mechanical communication systems may be used (Bruski & Dunham 1987; Correia et al. 2007; Bergman et al. 2005). Often, a combination of communication forms are used, for example when selecting a mate, female crayfish require both visual and chemical information to select the larger male (Aquiloni & Gherardi 2007; Aquiloni & Gherardi 2010). Crayfish are social species’, some of which establish stable dominance hierarchies (Gherardi & Daniels 2003), therefore relying on communication to assess the social status of conspecifics during encounters. One study examined the transfer of social information through chemical and mechanical signals (urine release and current generation). They found that although both dominant and subordinate crayfish generated currents, dominant crayfish did so more frequently (Bergman et al. 2005). Additionally, dominant crayfish were more likely to release urine during an encounter with a subordinate and they displayed more agonistic behaviours when urine was released. Similarly, a study found that both hydrodynamic and chemical signals were used more frequently when male-female crayfish pairings were both reproductively active (Simon & Moore 2007). Chemical communication is used by crayfish in many aspects of social behaviour (see review by Moore & Bergman 2005), for example species recognition (Girard, 1852; Dunham 1978), recognition of reproductive status (Ameyaw-Akumfi & Hazlett 1975; Little 1975, 1976), detection of stress or injury in conspecifics (Thorp & Ammerman 1978; Daniels et al. 2004), predator signaling (Jurcak & Moore 2014; Bouwma & Hazlett 2001), agonistic encounters (Huber et al. 2001; Exum et al. 2020; Graham & Angilletta 2021) and to assess the age and status of conspecifics (Graves & Quinn 1998; Wofford et al. 2017; Kubec et al. 2019). Acoustic signaling has been studied in Procambarus clarkii, which occurs largely from sunset to dawn and is associated with intraspecific interactions such as approaching, fighting and tail flipping (Buscaino et al. 2012). Crayfish can produce a signal by beating “the scaphognathite inside the chamber constituted by the efferent branchial channels”, which the authors propose could have an anti-predatory function or to signal an individual’s presence to conspecifics (Favaro et al. 2011). | Studied colonies of M. scutellaris (MS), M. bicolor (MB), M. quadrifasciata (MQ), and M. rufiventris (MR) bees to obtain comparative data on communication about food source by trail-marking. In terms of frequency of marks and efficiency of attracting newcomers, the species are listed in order of success: MR, MS, MB, and MQ, respectively (Kerr, 1994). The stingless bees (Hymenoptera, Apidae, Meliponini) have evolved sophisticated communication systems that allow foragers to recruit nestmates to good resources. Over the past 50 years, a growing body of research has shown that foragers can communicate three-dimensional resource location, uncovered several potential communication mechanisms, and demonstrated new information transfer mechanisms. Some of these mechanisms are unique to stingless bees and some may provide insight into how the ability to encode location information, a form of functionally referential communication, has evolved in the highly social bees. The goal of this review is to examine meliponine recruitment communication, focusing on evidence for contact-based, visual, olfactory, and acoustic communication and what these mechanisms can tell us about the evolution of recruitment communication in stingless bees (Nieh, 2004). | BSF sometimes engage in prolonged courtship rituals (described in Julita et al. 2020). Females may convey to males that they prefer (or do not prefer) a mate following these courtship interactions, indicating some degree of female choice in the species - as well as intraspecific communication (Giunti et al. 2018). | The research on communication in Bombycidae largely reveals the reliance on the sex pheromone bombykol for chemical communication, which is released by female silkmoths to elicit full sexual behaviour in the male moth (e.g. Sandler et al. 2000; Sakurai et al. 2011). Although not in larval silkworms, there is evidence of audible sound production in silkmoth caterpillars (Antheraea polyphemus) from the Saturniidae family (Bombycoidea superfamily). One study found that larvae “produce airbourne sounds, resembling ‘clicks’ with their mandibles”, signaling multiple times in rapid succession (50-55 clicks in approximately 1 min) (Brown et al. 2007). These signals are likely to function as acoustic aposematic signals (Brown et al. 2007) and it is possible that other larval species in the Bombycoidea superfamily are also capable of such signaling. Auditory signaling also plays a role in communication for other lepidopteran moth species, e.g. for courtship “whispering” and long- and short-distance loud intraspecific sexual communication (Nakano et al. 2015). It is thought that “Sexual sound communication in moths may apply to many eared moths, perhaps even a majority” (Nakano et al. 2015). | ||||||||||||||
7 | Cooperative behavior | Wild pigs often cooperatively raise litters of piglets (Fraser et al. 1995). Following an initial period of isolation, a sow will rejoin a group (often family) and this may result in cross-suckling between sows. Additionally, the common warthog often displays cooperative breeding (White & Cameron 2011). Although these are examples of cooperative behaviour in pigs, it has not been proven in an experimental task (however, the task may not have been the most relevant for studying this trait). In this study on Kune Kune pigs: there was no evidence that pigs cooperated by coordinating their actions and by understanding the role of the partner. Rather, it seems that they worked independently, but persistently enough to achieve the common goal (moving a block of wood to obtain a food reward). Whether the failure of taking the partner into account was the result of training and/or testing procedures, a lack of the required cognitive skills or of motivational problems like the lack of impulse control needs to be determined in further studies. Gaining knowledge about the socio-cognitive abilities of pigs and how they can adjust or coordinate their actions to conspecifics have potential implications for their welfare and husbandry practices in relation to their social environment (Koglmüller et al., 2021). | One study on cooperative breeding in the Kalij pheasant (caring for chicks, predator defense, vigilance) (Zeng et al. 2016) . It is however, acknowledged that is it a rare trait in Phasianidae. | No specifically relevant reports for carp could be found, but Tan et al (2019) report that bighead carp (Hypophthalmichthys nobilis) use cooperative and other varied swimming strategies in an experimental vertical slot fishway. Also, kin recognition is possible in zebrafish (Danio rerio), a closely related cyprinid (e.g. Gerlach and Lysiak 2008), but reports of cooperation between unrelated individuals could not be found. There is evidence of cohesive swimming behaviour in carp, which is thought to dilute predation risk (Kim et al. 2019). | Cooperation between related individuals has been observed in Atlantic salmon (Salmo salar) and other salmonids (e.g. Brown & Brown 1992, Quinn & Hara 1986). However, cooperation between unrelated individuals does not appear to occur: e.g., “cooperative behaviour in groups of related juvenile Atlantic salmon was manifest as fewer aggressive interactions, the use of a greater proportion of ‘threat’ behaviour as opposed to fighting, smaller territory size, and improved growth (particularly in subordinates) as compared to non-kin groups” (Fontaine & Dodson 2003). | Currently, there is no evidence of intraspecific cooperation in any octopus species. This is not surprising given that most species of octopus live solitary lives (with some exceptions). There is, however, some evidence of transient interspecific cooperation between octopuses (Octopus cyanea) and various fish species (groupers and other coral reef fish) (Diamant & Shpigel 1985, Forsythe & Hanlon 1997, Sazima et al. 2007, Pereira et al. 2011, Vail et al. 2013, Bayley & Rose, 2020). During many of these interactions, octopuses play the 'lead' role in hunting while other fishes follow the octopus. Many of the followers are opportunistic predators (described as commensalistic or parasitic) (Diamant & Shpigel 1985). In other instances, octopuses follow fish partners (groupers; Vail et al. 2013; and goatfishes; Bayley & Rose 2020) in a manner that is more collaborative. These latter examples show that both octopuses and fish partners can be mutually beneficial (Bshary & Bergmüller 2008) because the hunting associations facilitate prey capture for both hunting parties and both partners play important roles in the hunting process. One study on Octopus cyanea suggest that octopuses prevent exploitation by fish partners by displaying the fish using a punching action with one arm (Sampaio et al. 2021). Such actions have been suggested to reduce opportunistic behaviour by fish and promote cooperation in future interactions (Sampaio et al. 2021). However, future research is needed to rule out alternaitve explanations for these observaitons (e.g. punching might be a form of aggression with delayed benefits). | There is evidence of coordinated ‘snapping’ in snapping shrimp to deter intruders (Tóth & Duffy 2005), but it is unlikely penaeid shrimp and prawns would be able to perform this behaviour due to the lack of specialized claw required. However, there is evidence of dominance hierarchies in pacific white shrimp, suggesting they live in social groups and may also be capable of some form of cooperative behaviour (Bardera et al. 2021). Cleaner shrimp in the Palaemonidae family display a type of cooperative behaviour by cleaning ectoparasites from fish (Chapuis & Bshary 2010), however there is no evidence of cleaning behaviour in the Penaeidae family. | There is evidence of cooperative behaviour in several families of the Brachyura infra-order, for example fiddler crabs (family Ocypodidae) display cooperative neighbourhood defense, with males leaving their own territory to defend a neighbour’s (Booksmythe et al. 2011). Crabs in the Trapeziidae family can form heterosexual pairs with snapping shrimp and allow other mutualistic species’ to occupy the same coral head (McKeon et al. 2012). This strategy enables synergistic defense of the coral. The sentinel crab (Macrophthalmus banzai) performs conspecific allocleaning behaviour (Fujishima & Wada 2013). Although these examples are specific and unique behaviours which have not been reported in the Portunidae family, one study found that clam foraging by blue crabs was more efficient when two crabs were present (Taylor & Eggleston 2000). | There is evidence of cooperative burrowing behvaiour in male and female North American crayfish (Procambarus clarkii) after mating (Haubrock et al. 2019). Additionally, crayfish use chemical communication to signal predator threat which would be used to alert conspecifics to potential danger (Jurcak & Moore 2014; Bouwma & Hazlett 2001). | One key advantage of eusociality is shared defense of the nest, brood, and stored food; nest defense plays an important role in the biology of eusocial bees. Recent studies on honeybees, Apis mellifera, have focused on the placement of de- fensive activity in the overall scheme of division of labor, showing that guard bees play a unique and important role in colony defense. Alarm pheromones function in integrating defensive responses; honey bee alarm pheromone is an excellent example of a multicomponent pheromonal blend. The genetic regulation of defensive behavior is now better understood from the mapping of quantitative trait loci (QTLs) associated with variation in defensiveness. Colony defense in other eusocial bees is less well understood, but enough information is available to provide interesting comparisons between A. mellifera and other species of Apis, as well as with allodapine, halictine, bombine, and meliponine bees. These comparative studies illustrate the wide variety of evolutionary solutions to problems in colony defense in the Apoidea (Breed et al., 2004). Decision making in superorganisms such as honey bee colonies often uses self-organizing behaviors, feedback loops that allow the colony to gather information from multiple individuals and achieve reliable and agile solutions. Honeybees use positive feedback from the waggle dance to allocate colony foraging effort. However, the use of negative feedback signals by superorganisms is poorly understood. They show that conspecific attacks at a food source lead to the production of stop signals, communication that was known to reduce waggle dancing and recruitment but lacked a clear natural trigger. Signalers preferentially targeted nestmates visiting the same food source, on the basis of its odor. During aggressive food competition, attack victims increased signal production by 43 fold. Foragers that attacked competitors or experienced no aggression did not alter signal production. Biting ambush predators also attack foragers at flowers. Simulated biting of foragers or exposure to bee alarm pheromone also elicited signaling (88-fold and 14-fold increases, respectively). This provides the first clear evidence of a negative feedback signal elicited by foraging peril to counteract the positive feedback of the waggle dance. As in intra- and intercellular communication, negative feedback may play an important, though currently underappreciated, role in self-organizing behaviors within superorganisms (Nieh, 2004). | BSF larvae aggregate during feeding, and this may beneficial or harmful to their survival depending on conditions. BSF larvae aggregate, which can cause the accumulation of waste (reducing growth rate), increase energy expenditure (due to intraspecific interactions), present thermoregulatory challenges, and promote competition for resources (although larvae may also be positively benefited by nearby conspecifics sharing their gut microbiota, as in house flies; Zhao et al. 2017). Larval crowding can increase risks of illness by facilitating disease spread (Steinhaus 1958), and potentially increase risk of injury. Reduced densities of 1-2 larvae per cm2 of substrate were found to improve larval survival (Dzepe et al. 2020). There is no specific evidence at this time that larval aggregation is a cooperative initiative; however, the possibility of cooperation should not be discounted, given that aggregation of larvae in other insects can be cooperative. Drosophila melanogaster larvae are capable of engaging in cooperative digging behaviors in liquid foods. This allows them to be more efficient feeders, and perhaps to better avoid predation (Dombrovsky et al, 2017). Additionally, fruit fly adults may share information about food # to cooperatively aggregate on high-quality foods for oviposition without needing to independently assess each food source (Tinette et al, 2004). | A fairly rudimentary example of cooperation in lepidopteran larvae is the aggregation of individuals during feeding for defense. Although there is no specific evidence of this in silkworm larvae, the phenomenon is widespread across lepidoptera (Zalucki et al. 2002) and silkworms do prefer to feed from mulberry leaves with conspecific feeding damage, which may indicate that they are seeking conspecifics to increase foraging efficiency and to aid defense (Mooney et al. 2009). | ||||||||||||||
8 | Cross-modal learning | Chicks associate low/high luminance with left/right spatial position, in absence of prior related experiences or formal training, suggesting crossmodal correspondences are available early on and independent of experience (Loconsole et al. 2021). Ravens appear able to integrate past knowledge across sensory modalities, specifically, in relation to previous knowledge on predator presence (Bugnyar et al, 2013). | No studies of carp could be found, but zebrafish (Danio rerio) appear to learn faster in response to signals involving vision and vibration detection, and are able to “transfer the memory to unimodal conditioning when only given vision or vibration signals” (Wang & Chittka 2011). Fathead minnows (Pimephales promelas), a related cyprinid, also exhibit cross-modal effects, where noise pollution from motorboats interferes with the cyprinid-typical fright reaction to conspecific alarm pheromones (Hasan et al. 2018). | Knowledge is limited but based on available data it appears that common octopuses, Octopus vulgaris, lack cross-modality integration across two sensory systems (i.e., visual and chemotactile). Neuroanatomical and experimental evidence demonstrates that visual and tactile inputs are classified, processed, and stored separately over a series of intersecting neural matrices (Young 1991; 1995). While some components share common pathways and sites in the brain (e.g., frontal and vertical lobes), there is no evidence of interactive associations between two modalities (Allen et al. 1986). The only interactions between visual and tactile learning and memory were a result of the sharing of final common paths to the arms. However, notice that test procedures in this early study involved strong negative reinforcement (i.e., electric shock). Such procedures can cause detrimental effects to the animal's ability to learn and integrate information and thus makes it challenging to interpret the results. Also see multimodal integration (Zullo et al. 2009; Gutnick et al. 2011). | There is evidence of multimodal integration in Decapods, but learning has not been demonstrated specifically. See section on multimodal integration. | There is evidence of multimodal integration in Decapods, but learning has not been demonstrated specifically. See section on multimodal integration. | The power of the small honeybee brain carrying out behavioral and cognitive tasks has been shown repeatedly to be highly impressive. The present study investigates, for the first time, the cross-modal interaction between visual and olfactory learning in Apis cerana. To explore the role and molecular mechanisms of cross-modal learning in A. cerana, the honeybees were trained and tested in a modified Y-maze with seven visual and five olfactory stimulus, where a robust visual threshold for black/white grating (period of 2.8°–3.8°) and relatively olfactory threshold (concentration of 50–25 %) was obtained. Meanwhile, the expression levels of five genes (AcCREB, Acdop1, Acdop2, Acdop3, Actyr1) related to learning and memory were analyzed under different training conditions by real-time RT-PCR. The experimental results indicate that A. cerana could exhibit cross-modal interactions between visual and olfactory learning by reducing the threshold level of the conditioning stimuli, and that these genes may play important roles in the learning process of honeybees (Zhang et al., 2014). | Numerous examples of cross-modal learning and memory retrieval in fruit flies, involving the axons of the mushroom body kenyon cells (Zhang et al, 2013), (Duistermars & Frye 2008), (Okray et al, 2022). | No studies on cross-modal learning in silkworms or lepidopteran larvae found, but there is evidence to suggest that a number of moth species are capable of cross-modal learning and decision-making (e.g. Wessnitze & Webb 2006; Balkenius et al. 2006) including those in the Bombycoidea superfamily (Riffel& Alarcón 2013; Balkenius & Dacke 2013). These studies highlight the importance of combining olfactory and visual cues for lepidopteran species e.g. for feeding, mating and camouflage (Kinoshita et al. 2017; Kang et al. 2014), however it should be noted that the adult silkmoth does not feed during its lifespan and no studies currently exist on this proxy in larvae. Because cross-modal learning is fairly widespread among lepidopterans, it is ecologically plausible that Bombycidae should have this capability and because there is evidence of multisensory-motor integration in the silkmoth (Yamada et al. 2021) I have attributed a “lean yes”. | |||||||||||||||||
9 | Experience projection | Maybe: for example, pigs exhibit complex abilities to utilize and manipulate conspecifics to their advantage in social foraging situations. In a protocol requiring pigs to forage in pairs for hidden food, when one pig was informed as to the location of the food and the other was naïve (a scrounger), the latter was able to exploit the knowledge of the informed pig by following him to the food source and displacing him, thus reducing the time it took for the naïve pig to find food on his own (Held et al., 2000). | (Bugnyar et al. 2016) ran an experience- projection test with ravens. In the self-experience phase, ravens entered a competitor’s empty enclosure, where they could peer through a peephole into their own enclosure. They were then returned to their own enclo- sure and allowed to cache food while hearing sounds made by their competitor in its adjacent enclosure. The ravens used the same strategy they had employed when a competitor watched them through an open window: They cached food quickly and did not return to the cache site. The researchers concluded that the ravens generalized from their own experience with the peep- hole to infer that the competitor could observe them caching food through the hole. | Unknown: experience projection is one method for investigating Theory of Mind helps to distinguish ToM from the 'simpler' process - behaviour reading. No studies on Theory of Mind on octopuses have been found. | ||||||||||||||||||||||
10 | Gratification delay | Clean apple halves were never washed, which indicates that pigs can discriminate between soiled and unsoiled foods and that they are able to delay gratification for long enough to transport and wash the items (Sommern et al., 2016). Results show that older pigs could wait longer for a larger reward than younger pigs (10.6 ± 1.3 s vs. 5.2 ± 1.5 s), thereby confirming the hypothesis of ontogenetic development of self-control in pigs. This self-control is likely to be regulated by the behavioural inhibition system and associated systems (Krause et al., 2021). | Adult chickens may show aspects of self-control, such as tolerating a delay for a greater reward. For instance, when reward size increased from being the same as the instant reward to a much larger “jackpot” reward, more hens (93% compared to 22%) waited for the delayed reward (Abeyesinghe et al. 2005). The lack of testing of self-control in chickens seems surprising, given the evidence of self-control in other birds (e.g. Miller et al., 2019), therefore seems like an area for future research. | Delayed gratification has not been tested in octopus. However, recent research on the common cuttlefish, Sepia officinalis, has demonstrated that cuttelfish are able to delay gratification and wait for a better but delayed reward (Schnell et al. 2021). Using an inter-temporal delay maintenance task, cuttlefish were able to resist the temptation of a mediocre reward, for up to 50–130 s, to obtain the better reward. The same study also tested learning performance using a reversal learning task, whereby the cuttlefish were required to learn to associate a reward with one of two stimuli and then subsequently learn the reverse pattern (i.e., learn to associate the reward with the alternative stimulus). Interestingly, cuttlefish that delayed gratification for longer also performed better in the reversal learning task. This is the first evidence of a link between self-control and learning performance in a non-primate species. | Examining delay discounting in bumblebees may provide valuable knowledge about interspecies variation in self-control, and inform assumption made by both hypotheses. To do that, delay-discounting procedures accounting for bumblebee’s particularities as a specie should be developed. The present study aimed to test and refine a procedure made to study preference reversal as a measure of self-control in bumblebees (Bombus terrestris). Preference reversal was investigated by systematically increasing the delay to access a sweeter reinforcer (5, 10, 15, 20, 25, 30, 35, 40, 45. 50, 60, 70… seconds) in an adjusting delay procedure. Five bumblebees were tested to find the point where they showed preference reversal by choosing less sweet immediate reinforcer. On average, the bumblebees showed preference reversal at 50 s delay in phase 1 and at 55 s in phase 2. Intertrial interval were stable across conditions, showing no systematic variation when delays were increased. Procedural solutions regarding the definitions of choice and method of adjusting delays are discussed (Berby, 2021). | |||||||||||||||||||||
11 | Individual differences / "personality" | If acoustic signals are consistent and related to an individual's personality, these consistent individual differences in signalling may be an important driver in social interactions (Friel et al., 2016). In this study they draw a comparison between individual coping characteristics, rearing conditions and behavioural flexibility in pigs via a reversal learning task (Bolhuis et al., 2004). In this review, over 27 years of personality study in pigs, only 24.1% of the studies reported reliability and even fewer explicitly assessed validity. The backtest was the most common test (used in 67.5% of the studies), though it is unclear what specific trait is being measured. They suggest: in order to move forward with this field, researchers need to agree on consistent terminology and methodologies, and investigate the reliability, validity, and practicality of common personality measures in pigs (O’Malley et al., 2019). | Recent work on animal personality (i.e., consistent variation in behavioural responses of individuals) demonstrates that personality can co-vary with social status, suggesting that also behavioural variation can play an important role in establishment of status. They investigated whether personality could predict the outcome of duels between pairs of morphologically matched male domestic fowl (Gallus gallus domesticus), a species where individuals readily form social hierarchies. They found that males that more quickly explored a novel arena, or remained vigilant for a longer period following the playback of a warning call were more likely to obtain a dominant position. These traits were uncorrelated to each other and were also uncorrelated to aggression during the initial part of the dominance-determining duel. The results indicate that several behavioural traits independently play a role in the establishment of social status, which in turn can have implications for the reproductive success of different personality types (Favati et al. 2014). The results of this study illustrate that social states contribute to both variation and stability in behavioural responses and should therefore be taken into account when investigating and interpreting variation in personality (Favati et al. 2014). | There is evidence that both common carp (Cyprinius carpio: Huntingford et al. 2010) and crucian carp (Carassius carassius: Hulthen et al. 2014) display individual coping strategies/behavioural syndromes comparable to those of other animals that fall along the proactive-reactive or bold-shy continuum. Other cyprinids also exhibit individual differences in personality, such as koi carp (Cyprinus rubrofuscus: e.g. Fife-Cook & Franks 2021) and zebrafish (Danio rerio: e.g. Oswald et al. 2012, Wong et al. 2019). There is also evidence that differences in personality are associated with differences in a variety of other characteristics in carp, for example: respiratory function (e.g. Jenjan et al. 2013), behavioural plasticity (e.g. Hulthen et al. 2014), and metabolic rate (e.g. Huntingford et al. 2010). | There is considerable evidence that Atlantic salmon and other related salmonids display individual coping strategies/behavioural syndromes comparable to those of other animals that fall along the proactive-reactive or bold-shy continuum, at multiple different lifestages. For example, Serrano et al. (2011) and Thornqvist et al. (2015) have found evidence for personality in fry (recently hatched), Church & Grant (2018) in young-of-the-year fingerlings (< 1 year old), Kittelsen et al. (2009) in juveniles (1-2 years old), Damsgard et al. (2019) in smolts, and Korsoen et al. (2012) in adults. Personality also appears to be consistent across time (at least across intervals of 3 months: Serrano et al. 2011). There is also evidence that differences in personality are associated with differences in a variety of other characteristics, for example: susceptibility to pathogens (e.g. Kittelsen et al. 2009), behavioural plasticity (e.g. Thomson et al. 2012), competitive strategy (Frost et al. 2006), growth rate (e.g. Korsoen et al. 2012, Damsgard et al. 2019), and brain gene expression in response to stress (e.g. Thornqvist et al. 2015). | Major individual differences have been observed amongst octopuses (Mather 1991a, 1991b) (incl. O. vulgaris, O. rubescens. O. dofleini). One study by Mather & Anderson (1993) suggests that East Pacific red octopuses (O. rubescens) varied on three personality or temperament dimensions including activity, reactivity, and avoidance. The amount of variance explained by these dimensions of octopus behaviour was 45%. By comparison, this proprotion is larger than the variance (32.5%) explained for nine factors of personality in human infants (Sanson et al. 1987). Another study on O. bimaculoides suggests that, in the first 9 weeks of life, behavioural development in octopuses is an individualistic and idiosyncratic process (Sinn et al. 2001). Specifically, individual octopses differed in their active engagement, arousal/readiness, aggression, and avoidance/disinterest. Interestingly, appearance of early temperamental traits (monitored in week 3) was not clearly predictive of later traits at week 6 and 9 (Sinn et al. 2001). One explanation for octopuses having such large individual variation is that variability is useful in the context of heterogenous habitats. Behavioural and temperamental variablity among individuals might help a population survive in varibale, unpredictable, and changing environments (see Katano 1987; Slater 1981). Another explanation is that different temperaments might be beneficial in habitats where competition is high; octopuses with individualistic behavioural styles could seek specific niches where competition is less intense. For instance, highly active and engaged individuals might be expected to have lower survival rates in habitats that have low prey and high predator densities. This has been observed in both O. vulgaris (Mather & O'Dor 1991) and O. cyanea (Hanlon et al. 1999), whereby behavioural differences amongst octopuses were linked to different predator densities. Finally, the life history of octopuses might select for behavioural variation because they do not receive parental care but must navigate complex environments from hatching without any guidance (Wells 1962; Boletzky 1987). Are personality traits consistent over time? One study on gloomy octopus, Octopus tetricus, showed that personality traits were not repeatable across multiple test days. For instance, an individual that was aggressive, bold, and exploratory on one day could be submissive, shy, and stationary the next day when tested in the same context (Pronk et al. 2010). The researchers termed this inconsistency 'episodic personality'. Similiar patterns have been observed in dumpling squid, Euprymna tasmanica. Adult dumpling squid showed context-specific personality traits during feeding and threat tests, but these traits were only repeatable in the threat tests (i.e., more mature squid showed increased levels of feeding shyness throughout testing; Sinn & Moltschaniwskyj 2005). | There is a fair amount of evidence of individual differences and personality across the Decapod order. In a study on Penaeid shrimp (pacific white shrimp) individual differences were found: “dominance influenced feeding behaviour; subordinates spent longer on the feeding area whereas dominants explored the test arena more, however, these differences were minimised at high density” (Bardara et al. 2021). The most inferable studies to the Penaeidae family are those on species in the Palaemonidae family, which. There is evidence of individual differences in behavioural innovation in rock pool shrimp, with smaller and hungrier individuals being the more likely innovators (Duffield et al. 2015). There is also evidence of risk-prone and risk-averse foraging behaviour in this species with consistent, bold ‘risky’ behaviour being negatively correlated with resource acquisition (Maskrey et al. 2018). A different study found that rockpool prawns were temporally consistent in a range of behaviours, including activity, exploration and boldness and found correlations in individuals between these traits (Chapman et al. 2013). They also found sex differences in these personality proxies. | The majority of the literature on personality in crabs is on hermit crabs, although there are some studies on Portunidae. The boldness of the swimming crab Portunus trituberculatus was positively correlated with activity and bold individuals were more likely to initiate and win a fight, whereas shyer individuals displayed more hesitant behaviour (Su et al. 2019; Su et al. 2022). In the same species boldness and aggressiveness characteristics were assessed in both adults and juveniles. Personality classification across each age group was consistent and personality was different between males of the different ages; juveniles were more aggressive, but less bold than adults (Liang et al. 2020). One study looked at social conformity in shore crabs and found that individual differences influenced their likelihood to conform (Fürtbauer & Fry 2018). | The studies on personality in crayfish largely monitor the impact of extrinsic factors on aspects of personality. One study looking at the potential effects of climate change has found that a slight temperature increase influenced activity, boldness and aggressiveness in Procambarus clarkii (Zhao & Feng 2015). In another study on Faxonius virilis crayfish, individuals with bold personalities displayed increased behavioural sensitivity to the herbicide atrazine (Steele & Moore 2019). Following exposure bold crayfish displayed a shy-like escape response, whereas individuals which were originally classified as “shy” displayed no behavioural shift following exposure to the herbicide. Increased parasite load in rusty crayfish caused individuals to become bolder in threatening contexts and less exploratory in novel environments (MacKay & Moore 2021). A number of experiments focus on measures of boldness, aggression, exploration and activity in both laboratory and field experiments (Edwards et al. 2018; Reisinger et al. 2020), for example studies of the invasive species Faxonius limosus suggests that it displays more boldness characteristics than the native species Pontastacus leptodactylus (Pârvulescu et al. 2021). There is also a large body of work on dominance hierarchies in crayfish, with individuals displaying different social ranks (e.g. Gherardi & Daniels 2003; Aquiloni et al. 2012). Additionally, there is evidence that agonistic interactions are state and sex dependent (Stocker & Huber 2001; Warren et al. 2009). | It is now recognized that many vertebrates and a few invertebrates show individual-specific consistency in their behaviour across time and context, sometimes in ways that can be paralleled with human personality. Their work aimed at assessing behavioural consistency in a social insect: the bumblebee Bombus terrestris. They focused on a behavioural dimension commonly used in personality studies: the response of an individual to novelty (neophilia/neophobia spectrum). They used a foraging paradigm to quantify individual bees’ response to novel flower colours and to assess the repeatability of this response over time. As for vertebrates, most individual bumblebees responded to a novel stimulus by increasing the time they spent investigating it compared to known stimuli. Using a new statistical approach, the consistency model, they found that individual bees tended to be consistent in their response to novelty over a few hours but were not consistent in their behaviour over 3 days. They conclude that for the neophilia/neophobia paradigm used here, bumblebee foragers do not fulfil the criteria for animal personality in the common sense of the term. Instead their behavioural response to novelty appears to be plastic, varying on a day to day basis (Muller et al., 2010). However, there is evidence of consistent inter-individual variation in worker honey bee behaviour, which the authors suggest provides evidence of personality in honeybess (Walton & Toth 2016). Furthermore, another study suggetss that two distinct cognitive phenotypes exist in worker honeybees and trhis influences their personality and behaviour (Tait & Naug 2020). There are several studies which mention personality of swarms at a colony level, with swarms collectively behaving differently under certain conditions (Wray et al. 2011; Wray & Seeley 2011). | Different black soldier fly males may be more or less aggressive in their mating behaviors, but this appears to be related to body size and thus may stem from the same basic 'aggressive' behaviors being exhibited more or less successfully by different individuals (Mollá-Albaladejo & Sánchez-Alcañiz 2021), (Jones & Tomberlin, 2021). | There is evidence of individual differences in the sexual behaviour of silkmoths (although this may be driven by physical or genetic differences rather than a difference in personality). Silkmoths can exhibit gynandromorphy and one study found individual differences in the sexual behaviour of 232 gynandromorph moths (Obara & Tamazawa 1982). They found that 32 moths displayed atypical bisexual behaviors – “The bisexual behaviors were classified into four behavioral types: ‘dual personality’, ‘schizophrenic’, ‘intersexual’ and ‘sequence-crossed’. The dual personality gynandromorphs behaved like a male at one time and like a female at another. The schizophrenics displayed male and female behaviors simultaneously in different parts of their body. The intersexuals showed a mixed type of male and female behaviours. The sequence-crossed animals performed the wrong sexual behaviour (e.g. female) in the context of one sex (e.g. male) when the behaviour of the other sex (i.e. male) would normally have been appropriate”. Other studies on personality in Bombycidae have not been performed, however there is evidence of different personality traits in some lepidopteran species. A few studies have investigated boldness in the speckled wood butterfly (Kaiser et al. 2019; Kaiser et al. 2020) and one has demonstrated consistency in personality across life stages, suggesting personality is present during larval stages (Kaiser et al. 2018). | ||||||||||||||
12 | Inhibitory control | The “quality group” displayed faster learning in the discrimination test (number of sessions until 90% of the animals completed the discrimination test: “quality group”−3 days vs. “quantity group”−5 days) and reached a higher level of impulse control in the delay-of-gratification test compared to the “quantity group” (maximum delay that was mastered: “quality group”−24 s vs. “quantity group”−8 s). These results demonstrate that impulse control is present in piglets but that the opportunity to get a highly preferred reward is more valued than the opportunity to get more of a given reward. This outcome also underlines the crucial role of motivation in cognitive test paradigms. Further investigations will examine whether impulse control is related to traits that are relevant to animal husbandry and welfare (Zebunke et al., 2018). | Cognitive abilities allow animals to navigate through complex, fluctuating environments. In this study, they tested the performance of a captive group of eight crows, Corvus corone and 10 domestic chickens, Gallus gallus domesticus, in the cylinder task, as a test of motor inhibitory control and reversal learning as a measure of learning ability and behavioural flexibility. Four crows and nine chickens completed the cylinder task, eight crows and six chickens completed the reversal learning experiment. Crows performed better in the cylinder task compared with chickens. In the reversal learning experiment, species did not significantly differ in the number of trials until the learning criterion was reached. The performance in the reversal learning experiment did not correlate with performance in the cylinder task in chickens. Our results suggest crows to possess better motor inhibitory control compared with chickens. By contrast, learning performance in a reversal learning task did not differ between the species, indicating similar levels of behavioural flexibility (Wascher et al. 2021). | No studies of carp could be found. However, Lucon-Xiccato & Bertolucci (2020) showed that zebrafish are capable of inhibitory control during a test where the fish were exposed to a prey stimulus placed inside a transparent tube, which initially elicited attack behavior (Lucon-Xiccato & Bertolucci, 2020). However, the zebrafish showed a rapid reduction in the number of attacks towards the prey, which indicated the ability to inhibit their foraging behaviour and this ability varied across three genetically separated wild-type strains and across different individuals within strains (suggesting that zebrafish show heritable within-species differences in inhibitory control; Lucon-Xiccato & Bertolucci (2020). As well, Lucon-Xiccato et al. (2020) demonstrated that inhibitory control in zebrafish correlates with cerebral lateralization, the tendency to process information with one brain hemisphere or the other. Individual zebrafish that preferentially observed a social stimulus with their right eye and thus processed social information with their left brain hemisphere, inhibited foraging behaviour more efficiently. Thus, Lucon-Xiccato et al. (2020) suggest selective pressures that maintain lateralization variability in populations might provide indirect selection for variability in inhibitory control. | There is some evidence that suggests octopuses are capable of inhibitory control. There is no published literature on octopuses that test inhibitory control using an A-not-B task or the cylinder task. However, reversal learning as well as serial reversal learning has been identified in octopuses. Reversal learning tasks measure behavioural functions that are related to response inhibition or inhibitory control. Specifically, subjects must suppress one response while engaging actively in another to receive a reward. This means that the octopus is experiencing a strong motivational impulse to respond post reversal. It's important to note that reversal learning may reflect selective response inhibition, as opposed to more general behavioural inhibition. | Impulsivity, the widespread preference for a smaller and more immediate reward over a larger and more delayed reward, is known to vary across species, and the metabolic and social hypotheses present contrasting explanations for this variation. However, this presents a paradox for an animal such as the honeybee, which is highly social, yet has a high metabolic rate. We test between these two competing hypotheses by investigating the effect of hunger on impulsivity in bees isolated from their social environment. Using an olfactory conditioning assay, we trained individuals to associate a small and a large reward with or without a delay, and we tested their choice between the two rewards at different levels of starvation. We found an increase in impulsive behaviour and an associated increase in dopamine levels in the brain with increasing starvation. These results suggest that the energetic state of an individual, even in a eusocial group, is a critical driver of impulsivity, and that the social harmony of a group can be threatened when the energetic states of the group members are in conflict (Mayack and Naug, 2015). | ||||||||||||||||||||
13 | Judgment bias | Subjects learned the required discrimination task (positive vs. negative stimulus) and showed consistent differences in approach latencies toward and exploration of stimuli of different valence. Hence, the subjects' expectations could be inferred from their behavior. However, repeated social isolation had no effect on judgment of ambiguous stimuli and on both basal and test-related cortisol levels. In conclusion, the spatial judgment approach seems to provide a useful tool to detect and discriminate diverse affective states in domestic pigs based on their responses to graded ambiguous stimuli (Düpjan et al., 2013). | Judgment bias paradigms typically require training animals to respond differently to two separate stimuli, which result in positive and negative-valence outcomes. An ambiguous “probe” stimulus is introduced during the test condition, and the animal’s response to the probe is interpreted as “optimistic” or “pessimistic” depending on whether it is like the positive or negative stimulus (Crump et al. 2018). For example, (Hernandez et al. 2015) found that stress and reward order influenced latency to respond to cues and “acute stress enhances sensitivity to a previously rewarding outcome without affecting judgement bias in laying hens”. Using a cognitive bias paradigm, where chickens experience a reward (mealworm) vs a punishment (puff of air) following exposure to low-temperature housing (aversive experience), they are less likely to peck ambiguous stimuli than those housed at a preferred temperature (Deakin et al. 2016). It is important to try to distinguish “true bias effects” (e.g., proportion of times an ambiguous stimulus is selected) from other measures (e.g., speed of response) (Freire 2020). (Nicol et al. 2011) explored link with decision-making (i.e., balancing decision to move and explore an environment to find food with risk of predator), with use of 3 environments differing in foraging and predator threat, and found chickens tended to select high foraging and low predator environment. This choice was also associated with lower stress levels and fewer “negative-state” related behaviours (e.g., head shaking, standing alert) (Freire 2020). Chicks exposed to cold stress did not appear to differ in jugement bias compared to controls, though they did show higher motivation for social reinstatement, indicating a sensitivity to additional unpredictable stressors. Judgement bias was related to dopamine turnover rate in mesencephalon, being higher in chicks wth a more optimistic response. Additionally, environmental enrichment can reduce stress-induced negative judgement bias (Zidar et al. 2018). Increased levels of corticosterone (stress hormone) result in more ‘pessimistic’ judgement bias in boiler chickens (Iyasere et al. 2017). | No studies of carp could be found, but two examples exist in a closely related species, zebrafish. Tan (2017) was “unable to condition fish to an appropriate level for subsequent judgment bias testing”. But Espigares et al. (2021) were able to teach zebrafish a go/no-go task such that fish were able to discriminate between cues, however the authors did not subsequently manipulate the affective state of the subjects in a known way (e.g. via fluoxetine treatment, etc.) to fully validate their test. However, in this same study, tert−/− mutant zebrafish with telomere deficiencies did respond pessimistically in the task (though it is unknown whether being a tert−/− mutant actually alters affective state). It is unlikely that carp would have fundamentally different abilities from zebrafish, with respect to judgment bias. | Unknown. No studies of salmonids could be found. | Some cephalopod species exhibit behavioural biases that might be driven by attention biases. For example, cephalopods show lateralized brain function, when specific functions are processed by either the left or the right side of the brain (Vallortigara 2000; Rogers et al. 2013; Versace & Vallortigara 2015). When viewing prey, octopuses display lateral biases for either the left or the right eye, but eye preference is present only at the individual level; there is no systematic left- or rightward bias at the population level (Byrne et al. 2002; 2004). Behavioural biases in arm use have also been observed in octopuses (Byrne et al. 2006), but again at the individual level not the population level. Research on cuttlefish have shown that one side of the brain is specialized to process information used for predation, and the other side is used for monitoring and scrutinizing potetnial predators (Schnell et al. 2016). In the context of camouflage, cuttlefish predominately use their right eye and associated neural structure to adjust the overall brightness of their camouflage pattern (Schnell et al. 2018). From Schnell and Vallortigara 2019 | Not in Portunidae, but the hermit crab Pagurus bernhardus spends more time investigating a new shell if it has previously received a small electric shock (Elwood and Appel 2009). | After a fight, the winner crayfish keeps on display “repetitive hostile behaviour resembling psychological harassment in humans” (Bacqué-Cazenave et al., 2017). The winning condition may trigger positively biased behaviour in crayfish. Also, while normally nigger crayfish are more likely to win against smaller crayfish, if they fight against a smaller crayfish with previous winning experience they are instead likely to lose. The ‘winner effect' remains for several days (Kamada and Nagayama 2021). | Whether animals experience human-like emotions is controversial and of immense societal concern. Because animals cannot provide subjective reports of how they feel, emotional state can only be inferred using physiological, cognitive, and behavioral measures. In humans, negative feelings are reliably correlated with pessimistic cognitive biases, defined as the increased expectation of bad outcomes. Recently, mammals and birds with poor welfare have also been found to display pessimistic-like decision making, but cognitive biases have not thus far been explored in invertebrates. Here, they ask whether honeybees (Apis mellifera) display a pessimistic cognitive bias when they are subjected to an anxiety-like state induced by vigorous shaking designed to simulate a predatory attack. They show for the first time that agitated bees are more likely to classify ambiguous stimuli as predicting punishment. Shaken bees also have lower levels of hemolymph dopamine, octopamine, and serotonin. In demonstrating state-dependent modulation of categorization in bees, and thereby a cognitive component of emotion, they show that the bees' response to a negatively valenced event has more in common with that of vertebrates than previously thought. This finding reinforces the use of cognitive bias as a measure of negative emotional states across species and suggests that honeybees could be regarded as exhibiting emotions (Bateson et al., 2011). | A study on Drosophila found that flies which were shaken (supposedly induced a negative affective state) were less likely to apporach the ambiguous odour than control flies. The authors state "we cannot say whether such states are consciously experienced, but use of this model organism's versatile experimental tool kit may facilitate elucidation of their neural and genetic basis" (Deakin et al. 2018). | ||||||||||||||||
14 | Memory bias | Overnight social isolation in pigs decreases salivary cortisol but does not impair spatial learning and memory or performance in a decision-making task (van der Staay et al., 2016). Responses of conventional pigs and Göttingen miniature pigs in an active choice judgement bias task (Murphy et al. 2013). | Memory bias has been tested in rats (Burman and Mendl, 2018), where changes in performance were linked with social status and associated affective states. It does not appear to have been tested in chickens or related bird species yet - “to our knowledge, there is only one paper describing an animal test of a memory bias, which was published… in rats” (Kostal et al. 2020). | |||||||||||||||||||||||
15 | Mental Time Travel | For example, pigs appear to be able to use ‘what’ and ‘where’ information about more and less-preferred food to organise their foraging behaviour. It may thus be possible to take the next step and ask whether this important domestic species can also use ‘when’ information (Held et al., 2005). The pigs showed an overall preference for confinement in crates associated with short durations instead of those associated with longer durations, demonstrating that they were sensitive to differences in elapsed time in the two crates. Furthermore, the pigs used a variety of sensory cues (visual patterns and direction) to make that decision. However, the pigs in this study did not show all the behaviors expected from the time perception hypothesis (Špinka et al., 1998). There have also been several studies evidencing episodic-like memory in pigs (Kouwenberg et al 2009; Kouwenberg et al. 2012) | Matching-to-sample paradigms in chickens indicate episodic-like memory, as hens can complete these tasks, though with short delays i.e., seconds (Marino 2017). Chickens were comparable to primates in remembering the trajectory of a hidden ball up to 180 seconds if the ball is observed moving, and up to 1 minute if the movement is invisible (Vallortigara et al. 1998; Marino 2017). Chicks and adult chickens can remember the “where” and “what” information about food (Forkman 2000). Future planning: hens were trained to peck a touchscreen 6 minutes after a stimulus presentation and showed increased pecking responses around 6 minutes in unrewarded probe trials, suggesting they could estimate the time interval (Taylor et al. 2002). | No studies of carp could be found, but a study of the closely related cyprinid, zebrafish (Danio rerio), suggests that they may have episodic memory-like abilities (Hamilton et al. 2016). However, though the study successfully incorporated “what” and “where” aspects of a traditional episodic memory task, it used “context” (whether the test chamber had yellow or blue walls) as the “when” aspect instead of time itself. Thus, though the study indicates that zebrafish show potential for demonstrating mental time travel, it is less convincing as a concrete example of episodic memory. | Unknown. No studies of salmonids could be found. | Unknown: no published literature on octopuses. Wild observations show that octopuses, Octopus cyanea, use a variety of different foraging paths over a relatively large area and they do not usually forage the same route on successive days (Forsythe & Hanlon 1997). Perhaps the same foraging paths are avoided across consecutive days because some prey items, such as slow-moving molluscs, would take some time to re-occupy depleted foraging paths. This is an interesting observation and raises the question as to how octopuses are driving such behaviour - are they using episodic-like memory (the retrospective part of mental time travel) to remember what they ate, where they last ate, and how long ago? Such observations have inspired experiments on common cuttlefish, Sepia officinalis. Cuttlefish remember what, where, and when components of a previous forgaing experience (Jozet-Alves et al. 2013) and can quickly adjust their foraging behaviour in response to changing prey conditions by learning and remembering patterns of food availability (Billard et al. 2020a; 2020b). Episodic-like memory is considered a precursor for future planning because it functions as a database to predict future scenarios (Clayton et al. 2003; Schacter et al. 2012). | Elwood (2022) suggests that hermit crabs display a form of future planning when they discard their old shell and move to a new one. He suggests this requires information assessment regarding the properties of the new shell and “how they will fit in the future”. Crabs in the Portunidae family do not habituate shells and so it is not clear whether they would also exhibit this ability. The shore crab Carcinus maenas could not recognise the shelter of choice when its position was changed relative to the shelter, even if it had a strong motivation to do so in order to avoid a noxious stimulus (Magee and Elwood, 2013). This could potentially indicate lack of spatial memory or low level of navigational skills, it is not clear which. The crab Neohelice granulata learns where food will be provided and remembers that spot even 24 hours after trials (Klappenbach et al, 2020). | |||||||||||||||||||
16 | Mirror mark recognition | Seven out of eight pigs who already had experience with mirrors were able to quickly locate food visible only by viewing the mirror. This study demonstrates that the pigs do understand something about their own body as it is reflected in the mirror in relation to the hidden food. Pigs have also been observed making repetitive movements while appearing to watch themselves in a mirror for the first time (Broom, 2010; Broom et al., 2009). | The behavior of domestic chickens (...) the mirror image is perceived as not only another animal, but an unfamiliar one. (...) Presenting a dominant or a alpha chicken from a well-established flock with a mirror elicits considerable hostility accompanied by attempts to attack the reflection, whereas agression in the original group is minimal. Thus, when confronted with a mirror, the chicken appears to make an attempt to establish status lines with this "new" bird (Gallup Jr, 1975) | Unknown. No studies of carp or the closely related cyprinid, zebrafish, could be found. However, the “mirror-biting” test is a common behavioural assay to assess zebrafish aggression (e.g. Pham et al. 2012), wherein the subject responds to its mirror image as though it were a conspecific, but with none of the necessary controls to assess self-recognition vs. conspecific recognition. Responses to these assays are therefore not considered valid examples of self-recognition. Self-recognition (visual and olfactory) has been assessed in cleaner wrasse (Kohda et al. 2019, Kohda et al. 2022) and cichlids (Thunken et al. 2009) with varying success, however it is unlikely that there is physical, ecological, or behavioural homology between these species and cyprinids. | Unknown. No studies of salmonids could be found. Self-recognition (visual and olfactory) has been assessed in cleaner wrasse (Kohda et al. 2019) and cichlids (Thunken et al. 2009) with varying success, however it is unlikely that there is physical, ecological, or behavioural homology between these species and salmonids. | Lean no: octopuses mirror test (i.e., presented with mirror but no mark on skin) by Amodio & Fiorito 2022). While octopus subjects did orient towards the presented mirror they responded to their mirror image as if it were a conspecific and no self-directed behaviour was observed (reviewed in Mather & Kuba 2013 but original 'submitted' manuscript not found). Other reports on Octopus laqueus, O. luteus, Callistoctopus aspilosomatis, Hapalochlaena lunulata, Abdopus aculeatus) do not clearly react to a mirror, rather they retreat (Ikeda 2009). Recent research by Amodio & Fiorito (2022) demonstrated that marked octopuses explored the mark via their arms. However, mark-directed behaviours were also observed in the absence of the mirror and in sham-marked individuals. This suggests that the responses were driven by the proprioceptive stimuli and thus mirror self recognition is unlikely driving the self exploratory behaviour. It might be worthwhile testing whether octopuses can use a mirror to locate hidden food - a way of investigating whether they can use a mirror instrumentally for discovering objects that cannot be perceived directly. | How, why, and when consciousness evolved remain hotly debated topics. Addressing these issues requires considering the distribution of consciousness across the animal phylogenetic tree. Here they propose that at least one invertebrate clade, the insects, has a capacity for the most basic aspect of consciousness: subjective experience. In vertebrates the capacity for subjective experience is supported by integrated structures in the midbrain that create a neural simulation of the state of the mobile animal in space. This integrated and egocentric representation of the world from the animal’s perspective is sufficient for subjective experience. Structures in the insect brain perform analogous functions. Therefore, they argue the insect brain also supports a capacity for subjective experience. In both vertebrates and insects this form of behavioral control system evolved as an efficient solution to basic problems of sensory reafference and true navigation. The brain structures that support subjective experience in vertebrates and insects are very different from each other, but in both cases they are basal to each clade. Hence they propose the origins of subjective experience can be traced to the Cambrian (Barron & Klein, 2016). | |||||||||||||||||||
17 | Motivational trade-off | Pigs from two breeds were tested on an avoidance learning task at ages 21, 40, 80 and 150 days. Duroc pigs were better avoidance learners than Hampshire pigs at all ages tested. The achieved level of learned responses decreased 16% per day during the test. Hence, younger pigs reached higher levels of avoidance learning performance than their older full sibs. The heavier pigs within the litters were the better learners. Weight accounted for 7.2% and 4.6% of the variance within litters for 80- and 150-day learning scores, respectively (Kratzer, 1969). | One study examined the trade-off made by chickens between foraging and predation risk and overall, chickens chose the environments in the pattern predicted - additional foraging opportunity was preferred over additional foraging plus predator risk, which was preferred over the predator risk cue alone (Nicol et al. 2011). Chickens can work to gain a reward: "If the work required for hens to reach food (the ‘price’ of food [cost]) is increased, hens work more to achieve the same intake: their demand for food is ‘inelastic’ (Petherick and Rutter, 1990) and food is therefore a ‘necessity’ (Dawkins, 1990)." In Appleby et al., 2004. Appleby, M.C., Mench, J.A., & Hughes, B.O. (2004). Poultry Behavior and Welfare. Cambridge, MA: CABI Publishing. http://dlib.scu.ac.ir/bitstream/Ebook/87282/2/0851996671.pdf Underlying studies: Petherick, J.C., & Rutter, S.M. (1990). Quantifying motivation using a computer-controlled push-door. Applied Animal Behaviour Science, 27, 159–167. https://www.sciencedirect.com/science/article/abs/pii/0168159190900156 Dawkins, M.S. (1990) From an animal’s point of view: motivation, fitness and animal welfare. Behavioral and Brain Sciences, 13, 1–9. https://www.academia.edu/1276108/From_an_animals_point_of_view_motivation_fitness_and_animal_welfare | No studies of carp could be found, but evidence from closely related cyprinid, goldfish (Carassius auratus), appears in two relevant studies. Dunlop et al. (2006) found that, when conspecifics were visually accessible next to a tank area that fish learned predicted an electric shock, goldfish did not spend time in the shock-area, but did change their position in the remainder of the tank to remain closer to the conspecifics, rather than spending time much farther away from the shock-area (as they do when conspecifics are not present). Millsopp & Laming (2008) found that goldfish were willing to enter the shock-area when food was present therein, and their willingness to enter and attempt feeding increased with increasing food deprivation and with decreasing shock intensity, suggesting“that goldfish balance their need for food against avoidance of an acute noxious stimulus.” There also appears to be at least one piece of evidence from another closely related cyprinid, zebrafish (Danio rerio) that is as yet unpublished (but is briefly described in Sneddon et al. 2014): zebrafish subcutaneously injected with a noxious substance choose a previously unpreferred barren chamber over a preferred enriched one, when analgesia (lidocaine) is dissolved in the barren chamber. It may be pertinent to keep in mind that the two published studies used small sample sizes (between 5-8 subjects exposed to shock, and 20 exposed to feed deprivation). Methodological details are not available for the unpublished work on zebrafish. | No studies of salmon could be found, but there is some evidence from a related salmonid, rainbow trout (Oncorhynchus mykiss). Dunlop et al. (2006) found that, when conspecifics were visually accessible next to a tank area that fish learned predicted an electric shock, trout were “willing to remain in the vicinity of the conspecific while being subjected to low intensity shock stimuli previously shown to elicit avoidance”. It may be pertinent to keep in mind that this study used only 8 trout subjects, and has not yet been replicated. | Currently, there is no direct evidence of motivational trade-offs that balance potential pain against other motivations in octopus or their cephalopd relatives (cuttlefish or squid). Neverthless. their is some indirect evidence demonstrating that injury induces sustained behavioural changes. For e.g. a study on common octopuses, Octopus vulgaris, found that octopuses learn to avoid attacking hermit crabs arms with anemones (noxious stimuli) on their shells and only attack hermit crabs with clean shells. These results suggest that octopuses will abandon hunting opportunities that result in pain. Several other studies on octopus (Boycott & Young 1957; Sutherland et al. 1963; Mackintosh 1964; Fiorito & Scotto 1992; Wells 1978) and cuttlefish (Boal et al. 2000) can rapidly learn to avoid noxious stimuli at the expense of forgoing a desirable item. However, ceasing to interact with a desirable item might be a result of a physiological effect of the aversive stimuli rather than involve a centralised decision-making process. A study on common cuttlefish, Sepia officinalis, demontrates that they can abandon an opportunity to hunt to, instead, exhibit defensive behaviour when exposed to threat (Wilson et al. 2018). Another study showed that cuttlefish produce a freeze reponse (involving mantle compression, ventilation rate reduction & covering of siphon) when exposed to a threat (Bedore et al. 2015). While this study does not show a trade-off between opportunity and reward the results suggest that cuttlefish prioritse minimising detection by a predator over normal respiration behaviour. Several studies on squid (D. pealeii) show that when subjects are injured they change both their responsiveness to threats (Crook et al. 2011; 2014) and schooling behaviour for predator inspection (Oshima et al. 2016), demonstrating that they make different decisions from uninjured squid. However, it is difficult to distinguish whether such behavioural changes are governed by trade-off decision-making or based on increased sensitivity to threat. | No studies on motivational trade-offs in Penaeidae at present, but studies on other shrimp species suggest it may be possible in Penaeidae. A study on rockpool prawns (family: Palaemonidae) suggests that individuals trade-off “risky exploration (which may increase the likelihood of encountering novel resource patches)” and foraging from known limited high-value patches (Maskrey et al. 2018). Another study found that a species of freshwater shrimp (Atya lanipes, family: Atyidae) migrate upstream to locations above waterfalls (presumable energetically expensive), to avoid predation risk (Hein & Crowl 2009). | Shore crabs enter a less preferred well-lit arena to avoid an electric shock in a dark shelter (Magee & Elwood 2013; Magee & Elwood 2016). Weissburg et al. (2012) found that blue crabs weigh up the risk of predation from an odour cue to reach a food reward. Similarly, as the predation risk grows and the habitat patchiness increases juvenile blue crabs are less likely to feed from the edge of the habitat (Macreadie et al. 2012). The shore crab has been shown to make foraging trade-off decisions in the presence of a competitive conspecific (Chakravarti & Cotton 2014), by increasing prey consumption speed (which requires shell-breaking) and risking claw damage, to avoid potential food loss to the competitor. | One study used the interaction between food deprivation (hunger) and competition from conspecifics to measure crayfish decision-making (Mergler et al. 2020). They found that following food deprivation, crayfish responded to food more quickly and with reduced risk-sensitive behaviour when a model competitor was present. Another study looked at the trade-off between risky agonistic interactions, food cues and hunger (Stocker & Huber 2001). | Bumblebees were given the choice between either unheated or noxiously-heated (55°C) feeders with different sucrose concentrations to test whether they were able to trade-off access to sucrose and nocifensive behaviour (Gibbons et al. 2022). They found that bees adjusted their behaviour away from the noxious feeders as the experiment progressed, suggesting they were able to trade-off competing motivational stimuli. There is also evidence that honeybees weigh up perceived danger and atttractiveness of flowers when foraging (Dukas 2001). Bumblebees have displayed self-control by opting for a less-immediate large reward, over an immediate small reward (Cheng et al. 2002). | Adult fruit flies were trained to associate odors with ethanol/sucrose (appetitive). To reach the odor, they needed to cross an electrified barrier (which untrained flies would not cross; 100V). Flies crossed the 100V barrier to reach the odors. Only ethanol-conditioned flies would cross a 120 V barrier to reach the odors (Kaun et al, 2011). | The only study to explore a trade-off in Bombycidae investigated the effects of starvation and mild heat and cold shocks on the thermal tolerance of silkworm larvae (Mir & Qamar 2018). “In the case of heat tolerance, starvation negated the positive effects of both mild cold as well as mild heat shocks and thus indicated the existence of trade-off between these stressors” (Mir & Qamar 2018). Another study on gumleaf skeletonizer caterpillars (Uraba lugens) found that they were less likely to resume feeding following a high-frequency predator attack (or consumed less food), suggesting a trade-off between foraging and predation risk (Low et al. 2014). There is quite a lot of literature on reproductive trade-offs in lepidoptera, however these may be based on innate biases (life history trade-offs) rather than conflicting motivational systems (e.g. Lewis et al. 2010; Gonzalez-Karlsson & Grether 2021; Snell-Rood et al. 2011; trade-off between fecundity and choosiness during oviposition: Jaumann & Snell-Rood 2017). There is also one study which demonstrates a speed-accuracy trade-off in Southern monarch butterflies when foraging from rewarding and unrewarding sources (although some individuals chose a consistently rapid foraging stategy) (Rodrigues 2015). | ||||||||||||||
18 | Multimodal integration | Although not explicitly proven, one study on the startle response as part of the defense cascade in pigs found that "The type of stimulus used also affected DC responses with bin bag and umbrella stimuli, both involving rapid movement, being particularly effective at generating greater startle magnitudes than the balloon. Use of stimuli with a pronounced visual component may thus be more potent inducers of DC responses in pigs compared to purely auditory stimuli." (Statham et al. 2020) | In everyday life we constantly perceive and discriminate between a large variety of sensory inputs, the vast majority of which consist of more than one modality. They performed two experiments to investigate whether chickens use the information present in multimodal signals. To test whether audiovisual stimuli are better detected than visual or acoustic stimuli alone, they first measured the detection threshold with a staircase paradigm. They found that chickens were able to detect weaker stimuli using audiovisual stimuli. Next, they tested whether the multimodal nature of a stimulus also increases the discrimination between two stimuli by measuring the smallest difference that the animals could still distinguish from each other. They found that chickens can discriminate smaller differences using audiovisual stimuli in comparison to visual stimuli alone, but not in comparison to acoustic stimuli alone. Thus, even in a relatively unspecialized species such as the chicken, the benefits of multimodal integration are exploited for sensory processing (Verhaal and Luksch 2016). | No studies of carp could be found, but zebrafish (Danio rerio) appear to learn faster in response to signals involving vision and vibration detection, and are able to “transfer the memory to unimodal conditioning when only given vision or vibration signals” (Wang & Chittka 2011). Fathead minnows (Pimephales promelas), a related cyprinid, also exhibit cross-modal effects, where noise pollution from motorboats interferes with the cyprinid-typical fright reaction to conspecific alarm pheromones (Hasan et al. 2018). Further, depending on their environment, zebrafish shift reliance between sensory modalities: “zebrafish housed in dim light for 6 weeks responded weakly to an optomotor assay, but strongly to an olfactory cue, whereas fish experiencing bright light for 6 weeks responded strongly to the visual optomotor stimulus and weakly in an olfactory assay” (Suriyampola et al. 2020). Multimodal integration in cyprinids is supported by startle response experiments in goldfish (Carassius auratus), where “results showed that adding a low intensity sound early during a visual loom (low visual effectiveness) produced a supralinear increase in startle responsiveness as compared to an increase expected from a linear summation of the two unimodal stimuli. In contrast, adding a sound pip late during the loom (high visual effectiveness) increased responsiveness consistent with a linear multimodal integration of the two stimuli”. McIntyre & Preuss (2019) suggest that “together, the results confirm the Inverse Effectiveness Principle (IEP) of multimodal integration proposed in other species”. | There is evidence from a study showing that octopuses can combine peripheral arm location information with visual input to control goal-directed complex movements (Gutnick et al. 2011). Specifically, octopuses were able to learn how to best position their arm and visually guide it to a location in a set of movements to retrieve a food reward from a three-choice maze. These results support the idea that octopuses are capable of multimodal integration in their central nervous system (see also Zullo et al. 2009). Another recent study demonstrates that Octopus vulgaris integrates different sensory information from chemical and visual cues during food selection (Maselli et al. 2020). However, results indicate that chemical perception provides accurate and faster information in the context of food choice. | Multimodal integration has been reported in a number of decapod species (see review by Hebets & Rundus 2011). There is evidence of visual and chemical information integration for communication in big claw snapping shrimp (family: Alpheidae) (Hughes 1996) and in several crayfish species (family: Parastacidae – Crook et al. 2004; family: Astacidae – Acquistapace et al. 2002; family: Cambaridae – Aquiloni et al. 2009), whilst Aegla longirostri (family: Aeglidae) integrate chemical and physical information resulting from contests during aggressive encounters (Palaoro et al. 2014). Although there are anatomical differences between the species highlighted and Penaeid shrimp and prawns, they do share many features involved in sensory processing including long antennae which are important for receiving tactile and chemical information (Vickery et al. 2012). Additionally, two studies on freshwater shrimp species Xiphocaris elongata (family: Xiphocarididae) Atya lanipes (family: Atyidae) found that multiple predator cues (visual, mechanosensory and chemical signals) presented simultaneously had a greater effect on foraging and hiding behaviour in shrimp than single cues (Crowl & Covich 1994; Ocasio-Torres 2021). | The only evidence of multimodal integration found in Portunidae is by Sneddon et al.2003, which found that the “visual and chemical presence of a receptive female had an impact on contest rules and costs” in make shore crab encounters. There is evidence of multimodal communication in fiddler crabs (family Ocypodidae) during courtship (Takeshita et al. 2018; Mowles et al. 2017). | Multimodal integration has been displayed in Procambarus clarkii females, which rely on both olfaction and vision for sex recognition and mate selection, whilst males require olfaction alone (Aquiloni & Gherardi 2008; Aquiloni et al. 2008; Aquiloni & Gherardi 2010). A study on the local interneurons in the olfactory lobes of the midbrain in Procambarus clarkii indicated that “multimodal integration of chemical and mechanical information occurs at the level of first-order sensory interneurons in the crayfish brain (Mellon 2005; 2012). | The advantages of group living are partially offset by the cognitive challenges associated with maintaining social boundaries. These challenges can give rise to recognition mechanisms that adaptively integrate information across multiple sensory modalities. The valley carpenter bee, Xylocopa varipuncta, nests in dead wood in large aggregations of up to several dozen nests. This study investigates the proximate mechanisms by which returning foragers quickly and reliably identify their own nest entrance within a high-density nesting site. They manipulated long- and short-range visual cues associated with nest entrances, removed chemical cues on the inside of nest entrances and added chemical cues from foreign conspecific bees. By measuring the effect of these manipulations on nest search time and search accuracy, they assessed the importance of visual and olfactory sensory modalities in allowing carpenter bees to locate their nests within aggregations. Their results support the hypothesis that both visual and olfactory cues can facilitate nest localization. Removal of nest olfactory cues did not significantly disrupt homing, suggesting that olfactory information may not be necessary for nest localization when visual information is available. However, the addition of olfactory cues from unfamiliar conspecific bees actually aided nest localization rather than disrupting it, suggesting that bees may use generalized species odour cues for homing. Due to intense nest site competition within aggregations, nest localization may have important social implications for maintenance of high-density nesting (Ostwald et al., 2019). | Many male insects use a combination of chemosensory, acoustic, or visual cues to locate females (Benelli et al. 2014, Bonduriansky 2001). In H. illucens, acoustic signals are likely necessary for male courtship initiation (Giunti et al. 2018). However high-intensity light conditions with specific spectral characteristics have proven to be absolutely critical for encouraging mating in both captive and outdoor populations (Oonincx et al. 2016, Tomberlin & Sheppard 2002, Tingle 1975, Liu et al. 2020, Zhang et al. 2010, Macavei et al. 2020, Klüber et al. 2020, Heussler et al. 2018, Holmes 2010, Nakamura et al. 2016, Gries et al. 2017, Birrell 2018, Schneider 2020). This behavioral data, supported by the increased number of brain cells we found in the optic lobes of males, suggests that visual cues may also be very important for mediating some aspects of male mating behaviors. - from Barrett et al. 2022 preprint listed in J2 | One study investigated multi-sensory integration of visual and wind direction information during female mate searching (olfactory behaviour) in the adult silkmoth (Yamada et al 2021). They found that the silkmoth had the highest navigational success rate when the odor, vision and wind information were accurate - “when the wind is received from the same direction as the odor, the silkmoth takes positive behavior; if the odor is detected but the wind direction is not in the same direction as the odor, the silkmoth behaves more carefully” (Yamada et al 2021). The silkmoth mating dance is thought to be instrumental in the determination of the location of females by integrating pheromone and environmental information (Obara 1979; Ishida et al. 1996). | |||||||||||||||
19 | Navigation strategies | There is evidence that wild boar navigate using their olfactory sense, but also using their cognitive abilities e.g. social learning and spatial memory (Morelle et al. 2014). There is also evidence of spatial memory in domestic pigs, used to navigate spatial tasks (Mendl et al. 1997; Jansen et al. 2009; Elmore et al. 2012). There is also some evidence that wild boar and warthogs demonstrate a magnetic sense, showing preferred body axis alignment from North to South, suggesting this may also be important for navigation (Cerveny et al. 2016). | Domestic chickens (Gallus gallus) can be trained to search for a social stimulus in a specific magnetic direction, and cryptochrome 1a, found in the retina, has been proposed as a receptor molecule mediating magnetic directions. The present study combines immuno-histochemical and behavioural data to analyse the ontogenetic development of this ability. Newly hatched chicks already have a small amount of cryptochrome 1a in their violet cones; on day 5, the amount of cryptochrome 1a reached the same level as in adult chickens, suggesting that the physical basis for magnetoreception is present. In behavioural tests, however, young chicks 5 to 7 days old failed to show a preference of the training direction; on days 8, 9 and 12, they could be successfully trained to search along a specific magnetic axis. Trained and tested again 1 week later, the chicks that had not shown a directional preference on days 5 to 7 continued to search randomly, while the chicks tested from day 8 onward preferred the correct magnetic axis when tested 1 week later. The observation that the magnetic compass is not functional before day 8 suggests that certain maturation processes in the magnetosensitive system in the brain are not yet complete before that day. The reasons why chicks that have been trained before that day fail to learn the task later remain unclear (Denzau et al. 2013). | Common carp common carp (Cyprinus carpio) are one of the most invasive species in the world (Jones & Stuart, 2009). Thus, most of the navigation strategy studies in carp have been focused towards improving understanding of their movement patterns to advance removal programs and reduce abundance (e.g. Jones & Stuart, 2009; Hennen & Brown, 2014). Although there is evidence of site fidelity, homing, and movements over small and large scales in carp (e.g. Stuart & Jones, 2006; Hennen & Brown, 2014), detailed information on the mechanisms of navigation are generally lacking and more research is needed. Zebrafish (Danio rerio), a closely related cyprinid, depend mainly on their sense of vision and the use of their lateral line to navigate theough the environment (e.g. Moorman, 2001). As well, phototaxis has been shown to be a hardwired navigational behavior in zebrafish performed when larvae swim by using a small repertoire of stereotyped movements (i.e. turns versus scoot or bust movements; Budick & O’Malley, 2000; Burgess & Granato, 2007) which are controlled by distinct retinal pathways (Burgess et al., 2010). Lesion studies in goldfish, another closely related cyprinid, have established the connection between the telencephalon of the goldfish and its ability to navigate (López, et al., 2000). | Pacific salmon (Oncorhynchus spp.) are famous for their homing migrations from ocean feeding grounds to their natal river to spawn (for a review see Dittman & Quinn, 1996). During these migrations, salmon travel through diverse habitats (e.g. oceans, lakes, rivers), each requiring distinct sensory capabilities (i.e. sight, odour, hearing, and the lateral line sense) for navigation and these navigation mechanisms include geomagnetic, celestial, olfactory cues, and social interactions between individuals (Dittman & Quinn, 1996; Berdahl et al., 2016). Homing is generally precise and results in reproductively isolated spawning populations with specialized adaptations for their natal habitat (Dittman & Quinn, 1996). The olfactory hypothesis suggests that prior to their seaward migration, juvenile salmon learn (imprint on) odors associated with their natal site and later, as adults, use these odor memories for homing (Hasler, 1966). The pheromone hypothesis suggests that adult salmonids are able to locate their natal stream by pheromone trails emitted by juvenile salmon living in the stream and this capacity is inherited (Nordeng, 1977). | Evidence from both the laboratory and field demonstrates that octopuses use visual cues and spatial memory to navigate. In the field, octopuses (Octopus vulgaris and O. cyanea) travel by jetting through the water, rarely coming into contact with the substrate (Mather 1991a; 1991b; Forsythe & Hanlon 1997). Moreover, octopuses do not retrace their outgoing paths (from their dens) upon return. Consequently, it is unlikely that octopuses use chemical information (i.e. trail following strategy) for navigation. Field data also show that octopuses hunt in several locations/directions from their dens on successive hunts and successive days. Researchers suggest that octopuses use working spatial memory to recall where they have already hunted (i.e. used to remember the distribution of food and already depleted areas) and use reference spatial memory to refer to the spatial information of their environment (i.e. to remember how to find their way back to their den after each hunting trip) (Mather 1991a). In the lab, octopuses, Octopus vulgaris, have been trained to solve detour tasks by moving around opaque partitions to access a crab that is visible behind a transparent barrier but not directly accessible (Schiller 1949; Wells 1964). However, most octopuses needed multiple trials before solving the task. Authors suggest that repeated trials were required because the clear transparent barrier was an unnatural stimulus that the octopuses initially failed to perceive as an obstacle. Results also showed that detour behaviour was visually guided particualrly when tactile contact with the wall was lost (octopuses visually fixatation along the wall). Maze learning experiments in the lab have demonstrated that O. bimacuoides can relocate open escape burrows among six possible locations (Boal et al. 2000) and that O. maya can solve a dry T maze and learn to enter the correct compartmernt to regain access to seawater (Walker et al. 1970). Taken together, these studies show that octopuses have strong spatial learning abilities to help them navigate through novel environments. | Although there are no studies in Penaeidae, navigation has been studied in other Decapods and some in Stomatopods, so it is possible that similar strategies would be observed in Penaeidae which require to navigate in a similar way. There are a number of studies on navigation and orientation in mantis shrimp (order: Stomatopoda), for example one study found that “individuals learn characteristics of their burrows and the environment” (Reaka 1980) and other studies highlight their reliance on object recognition for navigation (Patel et al. 2021; Patel & Cronin 2020a). Additionally, they are able to use an efficient navigational strategy which integrates information about the position of “the sun, overhead polarization patterns, and idiothetic (internal) orientation cues to return home when foraging” (Patel & Cronin 2020b). Studies on Palaemonetes antennarius of the Palaemonidae family shows that “1) orienting factors consist of the sun and polarized light in the sky; (2) the compass mechanism is time-compensated; (3) escape direction is not genetically fixed but (4) is learnt during the shrimp's lifetime and allows ample modification” (Ugolini et al, 1989) and that neither the sun or polarised light alone were sufficient for navigation (Goddard & Forward 1991). | Several studies have reported on the importance of chemoreception for blue crab navigation (Keller et al. 2003; Derby et al. 2016; Weissberg et al. 2003; Page et al. 2011). Specifically, the response Unof foraging blue crabs to the fluid forces (e.g. from turbulent plumes) imposed on their bodies while assessing and acquiring chemical signals from their environment has been documented in a few studies (Weissberg et al. 2003; Keller & Weissburg 2004; Jackson et al. 2007; Page et al. 2011; Weissberg et al. 2012). Another body of work has focused on the importance of sound for navigation and orientation in crabs, although the species used in these studies are largely in the same infraorder (Brachyura), but different families to Portunidae (Radford et al. 2007; Stanley et al. 2012). Recently, there has been a study on the effect of anthropogenic noise on foraging behaviour in crabs. It was found that fewer shore crabs aggregated at a food source when sound levels were artificially elevated (Hubert et al. 2018). The authors suggest that there are a few possible reasons for this, but one is that “crabs eating or interacting at a food item produce sound that attracts others (e.g. Coquereau et al., 2016). Such sounds could have been masked in our experiment during the playback of white noise”. A review on navigation and orientation, largely in fiddler crabs (Brachyura, family: Ocypodidae) is perhaps inferable to other crab species (Fraser 2006). | Homing behaviour has been examined in several species of Cambaridean crayfish, highlighting some differences in the strategies used to home to artificial burrows (Kamran & Moore 2015; Kamran et al. 2018). The importance of chemoreceptors and odour cues for orientation in crayfish has been well documented (Kozlowski et al. 2003; Denissenko et al. 2007; Kimberly et al. 2015), and one study found that “crayfish altered orientation strategies when presented with different spatial arrangements of food cues” (Wolf et al. 2004). Juvenile devil crayfish “are released in surface water and must navigate overland to burrow” (Clay et al. 2017). One study found that in the absence of cues from conspecifics and the soil type, juvenile crayfish integrated multiple terrestrial cues to select a burrow (Clay et al. 2017). Spatial behaviour in maze tasks has been examined in crayfish and has found that Orconectes rusticus are successful in navigating using egocentric cues alone when external visual and tactile cues provided inconsistent information (Tierney et al. 2018). In a similar task, the same species displayed spatial memory for more than a week, suggesting the importance of spatial learning for navigation (Tierney & Andrews 2012). | It is now well known that ants, bees and wasps are guided by olfactory and visual landmarks when following paths and travelling from and returning to their nests (Chittka et al., 1995; Collett, 1992; Janzen, 1971; Mirwan & Kevan, 2015). Bumblebees (Bombus terrestris) move about their environments by flying and by walking. Most experimental studies have addressed navigation during foraging flights, but they presented our experimental bees with the challenge of learning to navigate while walking as they must do in nature within topographically complex spaces containing their nests. They trained bumblebee workers to navigate complex, nine-channel, mazes in the absence of specific visual, chemical or textural cues. They successfully navigated through complex multi-turn mazes (stereotypical “rat mazes”) with several dead-ends by memorizing the entire sequence of appropriate turns, and their choice of correct first turn on entering the maze. Thus, their observed proficiencies indicated that the individual bumblebees had each memorized the maze by learning motor sequences which were not linked to visual, chemical or textural stimuli, and that their memories were triggered by contextual cues associated with the bees’ positions in a sequence. Our findings have implications on natural ambulatory activities inside and outside the colony, and even in practical use as vectors of biological control agents (Mirwan & Kevan, 2015). | There's no research on BSF navigation. However adult BSF do form leks for their mating behaviors, and studies on odorant binding proteins and sensilla morphology suggest that olfactory cues may be important for males navigating to those leks or females looking for suitable oviposition substrates. BSF larvae also have a large number of OBPs that are responsive to different VOCs. However, no data supports the use of these for navigation at this time. BSF larvae do tend to aggregate/crowd in containers*, which may suggest some navigational strategy in seeking out conspecifics. *Rivers DB & Dahlem GA (2013) The Science of Forensic Entomology. Wiley-Blackwell, Chichester, UK. Drosophila melanogaster fruit flies use nearly every sensory stream to navigate their environment (Currier & Nagl, 2020). Navigation strategies can be shaped by environmental predictability (Demir et al, 2020). | The male silkmoth mating dance, which is triggered by female pheromones is used as a model for the investigation of pheromone-induced behaviour (Namiki et al. 2018; Namiki & Kanzaki 2016). “Once male moths sense sex pheromones and then lose the input, they demonstrate zigzag movements, alternating between left and right turns, to increase the probability to contact with the pheromone plume…After the loss of the plume contact, moths repeat clockwise and counterclockwise turning” (Namiki & Kanzaki 2016). There is also evidence to suggest that wing-beating (in the flightless silkmoth) serves to generate thrust and torque (Kanzaki 1998) (whilst also driving air across the antennae to aid pheromone detection - Obara 1979) and there is coordination between wing-movements and walking behavior for orientation (Kanzaki 1998). In another study “high-speed video analysis revealed that changes in the direction of zigzag walking was synchronized with head turning” whilst performing the searching behavior and this involved coordinated activity of the cervical ventral 1 neck motor neuron and ‘flipflop’ descending interneurons (Mishima & Kanzaki 1998). Although there is much less evidence of navigational systems in the silkworm, larvae do display highly specific odor discrimination and are more likely to move towards mature mulberry leaves with conspecific feeding damage than to mature mulberry leaves with no damage (Mooney et al. 2009), indicating the importance of olfaction in navigation. | ||||||||||||||
20 | Numerical cognition | Chicks can discriminate between sets of one and two, or two and three, stimuli, appearing to use number-space mapping in a comparable way to humans (Rugani et al. 2008). They can perform arithmetic operations to a total of five objects (Rugani et al. 2009) and associate the smaller of two quantities with the left, over right, spatial location similarly to humans (Rugani et al. 2015). Many of these paradigms rely on imprinting and do not exclude learning (Marino 2017). | One study showed that Chinese crucian carp (Carassius auratus), qingbo (Spinibarbus sinensis), zebrafish, and guppies use the larger cumulative surface area of a shoal rather than discrete numerical quantities to select for shoal size (Xiong et al., 2018). Additional studies of carp are not available. Further studies of the closely related cyprinid, zebrafish (Danio rerio) show that they preferentially are able to choose the larger shoal over the smaller one (2 vs. 4) when both groups are maintained at the same water temperature, however any preference disappeared when the temperature of the larger group is decreased, thus diminishing the activity of this shoal (Pritchard et al., 2001). Controlling for continuous quantities utilizing an item-by-item procedure, zebrafish are able to choose the larger shoal in numerical comparisons involving both small (1 vs. 2 and 2 vs. 3, but not 3 vs. 4) and large numerosities (4 vs. 6, 4 vs. 8 but not 6 vs. 8) (Potrich et al., 2015). Similar results were obtained in 27 days post fertilization zebrafish larvae in 1 vs. 8 and 1 vs. 3 comparison (Sheardown et al., 2021). Zebrafish were also able to identify the second exit in a series of five equally spaced exits and this performance seemed to rely on numbers (Potrich et al., 2019). However, when the number of exits was increased (from 5 to 9), zebrafish relied on both numerical and spatial cues (Potrich et al., 2019). Messina et al. (2021) combined behavioral tasks with molecular biology assays in zebrafish and showed that the thalamus and the caudal region of dorso-central part of the telencephalon seemed to be activated upon change in numerousness in visual stimuli. In contrast, the retina and the optic tectum mainly responded to changes in continuous magnitude such as stimulus size. | Unknown. No studies of salmonids could be found. A number of useful reviews of numerical cognition in fish exist: Messina et al. (2021), Agrillo & Bisazza (2018), Agrillo et al. (2017). Many fish use quantity assessment to inform ecologically important behavioural decisions (e.g., choosing a larger shoal, deciding where to forage, or what mating or parental care tactic to use; reviewed by Agrillo et al. (2017)). Many of the numerical cognition studies in fish to date have not controlled for the relative magnitude of non-numerical cues (i.e. continuous quantities). Thus, it is possible that fish may be relying on continuous quantities (e.g. surface area, increased activity) rather than discrete numerosities in many of the studies conducted to date. | Unknown: no published literature in octopuses. But research on cuttlefish demonstrates that they have number sense. Specifically, common cuttlefish, Sepia officinalis, are able to distinguish numerical differences among various integers such as 1 vs. 2, 2 vs. 3, 3 vs. 4 and 4 vs. 5 (Yang & Chiao 2016). Moreover, cuttlefish can also discriminate between fraction numbers such as 1 vs. 1.5, 1.5 vs. 2, 2 vs. 2.5 (Huang et al. 2019). These findings suggest that cuttlefish have a primitive fraction number sense that they can use to estimate prey quantity when foraging. | Here, they tested the stingless bee (Trigona fuscipennis), a species representative of a vastly understudied group of tropical pollinators, in a quantity discrimination task. In four experiments, we trained wild, free-flying bees on stimuli that depicted either one or four elements. Subsequently, bees were confronted with a choice between stimuli that matched the training stimulus either in terms of quantity or another stimulus dimension. They found that bees were able to discriminate between the two quantities, but performance differed depending on which quantity was rewarded. Furthermore, quantity was more salient than was shape. However, quantity did not measurably influence the bees' decisions when contrasted with color or surface area. Our results demonstrate that just as honeybees, small-brained stingless bees also possess basic quantitative abilities. Moreover, invertebrate pollinators seem to utilize quantity not only as "last resort" but as a salient stimulus dimension. Our study contributes to the growing body of knowledge on quantitative cognition in invertebrate species and adds to our understanding of the evolution of numerical cognition (Eckert et al., 2021). Honeybees, Apis mellifera, were trained along a row of four identical landmarks (tetrahedral tents 3·46 m high) which were equally spaced in a set-up 300 m long, the feeder being placed between the third and fourth landmarks. In the tests, the number of tents between hive and feeder was altered. Even though many bees continued to search for food at the correct distance, the distance estimation of the bees as a group depended notably on the number of landmarks. If they encountered more landmarks on their way from the hive to the feeder than they had during training, significantly more bees landed at a shorter distance than during control tests with the training landmark set-up. If they encountered fewer landmarks, they flew significantly further. This behaviour meets the basic criteria in most definitions of true counting (Chittka & Geiger, 1995). Although the numerical abilities of many vertebrate species have been investigated in the scientific literature, there are few convincing accounts of invertebrate numerical competence. Honeybees, Apis mellifera, by virtue of their other impressive cognitive feats, are a prime candidate for investigations of this nature. They therefore used the well-established delayed match-to-sample paradigm, to test the limits of honeybees' ability to match two visual patterns solely on the basis of the shared number of elements in the two patterns. Using a y-maze, they found that bees can not only differentiate between patterns containing two and three elements, but can also use this prior knowledge to differentiate three from four, without any additional training. However, bees trained on the two versus three task could not distinguish between higher numbers, such as four versus five, four versus six, or five versus six. Control experiments confirmed that the bees were not using cues such as the colour of the exact configuration of the visual elements, the combined area or edge length of the elements, or illusory contours formed by the elements. To our knowledge, this is the first report of number-based visual generalisation by an invertebrate (Gross et al., 2009). | ||||||||||||||||||||
21 | Object permanence | A rewarded object was hidden in one of three hiding locations with an increasing complexity of the object’s movement through successive test sessions. Subjects were confronted with visible and invisible displacement tasks as well as with transpositions of hidden objects in different contextual settings. Pigs solved visible, but not invisible displacements or transpositions, indicating that they have difficulties to keep track of once hidden and then moved objects (Nawroth et al., 2013). Another study by (Nawroth et al., 2014) states the same and brings up that studies that failed to prove object permanence was due to constraints in the presented paradigm. | Studies with young chicks indicate they can remember that an object exists when it is out of sight (Regolin et al. 1995; Vallortigara et al. 1998). They move towards an imprinting stimulus displaced behind a screen and detour around barriers to locate an imprinting stimulus or conspecific (Freire et al. 2004). Chickens have been tested for the maximum object permanence level they can reach, and several studies support findings that they can reach stage 3 (i.e., subject actively retrieves partially hidden object) of (6 possible stages in) the Piaget (1953) scale (Marino 2017). Little evidence that chickens can reach stage 4 (retrieve a fully hidden object) and limited to social tasks, for instance, chicks had difficulty navigating vertical barriers that fully obstructed a conspecific (Regolin et al. 1995). Rachael notes: this may be compared, for example, with parrots that show stage 6 competence (Pepperberg and Funk, 1990). | No studies of carp could be found. However, the closely related cyprinids, zebrafish (Danio rerio) and goldfish (Carassius aurata), can successfully solve a detour task that requires them to “temporarily abandon the view of the goal-object (a group of conspecifics) to circumvent an obstacle” (Sovrano et al. 2018). It is unlikely that carp would have fundamentally different abilities from zebrafish and goldfish, with respect to object permanence - especially since the phenomenon was observed in two unrelated species as well: Xenotoca eiseni and Pterophyllum scalare. | No studies of salmonids could be found. However, the closely related cyprinids, zebrafish (Danio rerio) and goldfish (Carassius aurata), can successfully solve a detour task that requires them to “temporarily abandon the view of the goal-object (a group of conspecifics) to circumvent an obstacle” (Sovrano et al. 2018). It is unlikely that carp (or indeed) would have fundamentally different abilities from zebrafish and goldfish, with respect to object permanence - especially since the phenomenon was observed in two unrelated species as well: Xenotoca eiseni and Pterophyllum scalare. Aellen et al. (2022) tested cleaner wrasse in an object permanence test, but report that they did not perform better than chance, failing the task. However, the authors note that the task was not designed to be ecologically relevant, which may have hindered the fishes’ ability to demonstrate object permanence. | Unknown: no published literature on octopuses that directly tests for object permanence. However, research on cuttlefish has demonstrated that cuttlefish understand object permanence, the ability to keep track of objects that can no longer be perceived (i.e., object has disappeared from sight) (Sanders & Young 1940). It is likely that octopuses also possess object permanence particularly because their hunting behaviour suggests that they can make predatory decisions about directon of attack even when prey are obstructed from sight (i.e., prey has hidden within rubble or behind a rock). | ||||||||||||||||||||
22 | Perspective taking | An experiment at the University of Bristol found that one out of ten pigs was possibly able to understand what other pigs can see. That pig observed another pig which had view of a maze in which food was being hidden and trailed that pig through the maze to the food. The other pigs involved in the experiment did not. In another study by Held et al. subordinates increased their foraging speed to stay ahead of exploiters (Held et al., 2005; 2001). | The view that imitation, especially imitation that would be considered opaque, requires mechanisms that are as cognitive as perspective taking means that if one studies imitationin animals, one must develop designs that control for the possibility that other, perhaps simpler, mechanisms are involved. For example, animals may be predisposed to engage in certain behaviors (e.g., eating) when others are seen engaging in those behaviors (species-typical behaviors). Piaget (1962) suggested that opaque imitation requires that the observer be able to take the perspective of the demonstrator. Although perspective taking may be within the capacity of animals as genetically close to humans as the great apes, it seems unlikely that pigeonsand Japanese quail are capable of such a level of cognitive inference (Zentall 2006). | Unknown: no published literature on experiments to test for perspective taking in octopuses. Some octopus species (e.g., mimic octopus Thaumoctopus mimicus, algae octopus Abdopus aculeatus) perform elborate deceptive behaviours that suggest some degree of cognitive sophistication such as perspective-taking. For example, mimic octopuses disguise themselves as banded seasnakes as an agonistic response to damselfish and algae octopuses masquarade as moving algae to avoid potential predators. However, to underpin the specific cognitive abilities involved in this deception, such observations need to be corrborated with laboratory controlled experiments to rule out alternative explanations for the observed behaviours. Notice that mimicry can be underpinned by different levels of deception that differ in complexity in regard to the sender's freedom to act (Mitchell 1986) (e.g., pre-given resemblance, predetermined behaviour, customisation of pre-existing behavioural patterns, intended deception). | ||||||||||||||||||||||
23 | Physical reasoning | Pigs received either a physical cue (i.e., the slope of the board hiding the food, the presence or absence of noise from a shaken container, the sight of a baited container changing position) or a human social cue (i.e., touching, pointing, gazing). Subjects performed better when provided with cues on which they had received adequate experience from their environment, thus providing support to the developmental hypothesis. They conclude by suggesting that specific experience on particular stimuli rather than general experience on a wider range of stimuli may explain swine ability to solve both social and physical tasks (Albiach-Serrano et al. 2012). | Newborn domestic chicks (Gallus gallus) were reared singly with a small object that became their social partner. They were then accustomed to rejoining such an imprinting object when it was made to move and disappear behind either one of two identical opaque screens. After disappearance of the imprinting object, chicks were faced with two screens of different slants, or of different height or different width, which may or may not have been compatible with the presence of the imprinting object hidden beneath/behind them. Chicks consistently chose the screen of slant/height/width compatible with the presence of the object beneath/behind it. Preventing chicks from touching and pecking at the imprinting object before testing did not affect the results, suggesting that intuitive reasoning about physical objects is largely independent of specific experience of interaction with objects and of objects' occluding events (Chiandetti and Vallortigara 2011). | Lean yes: octopuses show behavioural characteristics to suggest that they may be capable of physical reasoning. For example, some species of octopus are capable of tool use - they alter the physical properties of another object to mediate the flow of information between themselves and the environment or other organisms by carrying around coconut shells as mobile dens (Finn et al. 2009). Research has also shown that octopuses are sophisticated problem-solvers (e.g., detour task solving in a maze, Schiller 1949; Wells 1964; jar opening, Fiorito et al. 1990; 1998; Anderson & Mather 2010). While tasks presented have not been designed to directly test for physical reasoning (i.e., trap-tube test), octopuses show flexible behaviours that exceed simpler learning mechanisms that do not simply rely on single fixed stratgies like trial-and-error or stimulus-response-associations (Boal 2011; Richter et al. 2016). However, further testing is required to determine whether physical reasoning is an integral part of their problem-solving behaviour. | ||||||||||||||||||||||
24 | Problem-solving | This is the first study to directly compare family dogs and pigs’ problem-solving abilities and shows just how able pigs really are. They are as smart, and a bit more independent than dogs, but found that, in normal circumstances, both animals interacted with humans in a similar way, but when faced with an unsolvable problem, pigs were ‘more persistent than dogs in trying to solve the task, which may reflect their predisposition to solve problems independently (Pérez Fraga et al., 2021). | The ability of animals to perform transitive inference is associated with social group formation and dominance hierarchies. Brain lateralization is also linked to the selective pressures associated with social life. They investigated whether transitive inference is better performed by lateralized than non-lateralized brains. In the domestic chick (Gallus gallus) exposure of eggs to light before hatching leads to the development of lateralization of some visual functions. Thus, it is possible to obtain chicks with strong (light-incubated, Li-chicks) or weak (dark-incubated, Di-chicks) lateralization. Di- and Li-chicks were trained to discriminate stimulus pairs, in order to build a hierarchy (A < B < C < D < E). Chicks were subsequently tested on stimulus pairs never seen together before (AE and BD). Li-chicks performed the discrimination BD better than did Di-chicks, suggesting that exposure to light in the egg leads to an increased ability to carry out representational learning. Moreover, lateralized chicks using their left eye only (right hemisphere) during test showed a better performance than did right eye only (left hemisphere) chicks on the BD task. Females also tended to perform better than males. Results demonstrate that chicks with lateralized brain hemispheres show greater inference, and this is under right hemisphere control: the brain hemisphere that is dominant in social interactions (Daisley et al. 2010). | No study to date has specifically investigated problem solving in carp or closely related species. However, Sovrano et al. (2018) found that zebrafish and goldfish, closely related cyprinids, can successfully solve a detour task that requires them to “temporarily abandon the view of the goal-object (a group of conspecifics) to circumvent an obstacle”, suggesting that they possess some sort of problem solving abilities to enable their success in the task. | No study to date has specifically investigated problem solving in salmonids. One study of brook trout (Salvelinus fontinalis) found that young of the year (<1 year old, 7 replicate subjects) were capable of transitive inference in the context of assessing conspecific social rank within a 5-fish hierarchy (White & Gowan, 2013). Studies on transitive inference in different salmonid species or lifestages are not available. | Octopuses are attracted to novel objects and often show exploratory behaviour towards new objects (Kuba et al. 2006). They have been shown to solve a variety or problems including detour mazes (Schiller 1949; Wells 1964), jar opening tasks (Fiorito et al. 1990; 1998; Anderson & Mather 2010) and container opening tasks that require multiple motor actions including pushing and pulling (Richter et al. 2016). Performance in the latter task demonstrated that octopuses show different problem-solving approaches that exceed simpler learning mechanisms such as trial-and-error and stimulus-response-associations. Octopuses are also capable of generalization learning. Specifically, two-spot octopuses can distinguish between a combination of objects and learn to choose an odd-shaped object in a sequence. Importantly, octopuses can transfer this learning and choose another odd stimulus in a new sequence (Boal 1991). This type of learning allows octopuses to respond to a variety of challenges especially when faced with new information and is thought to a precursor for inferential reasoning. | Although there are no studies in Penaeidae, one study on innovative behaviour in rock pool prawns (family: Palaemonidae) found that “the factors that drive rock pool prawns to innovate differ depending on the conditions in which they find themselves” (Duffield et al. 2015). In two foraging tasks, small and hungry prawns were more likely to be behavioural innovators however, the work “cautions against there being clear causal links between individual cognitive abilities and innovation as we found no evidence for individual consistency between tasks”. These results are likely to be inferable to other species as the authors suggest “contextual variation in the drivers of innovation is likely to be common in animals living in variable environments” (Duffield et al. 2015), such as Peneaid prawn and shrimp living in a similar environment to rockpool prawns. | Bees have numerical cognition, i.e., can solve basic maths problems and bees can use tools and train other bees to use them. In the wild, honeybees have also been shown to use tools to repel wasps which are all signs of problem solving abilities. References: Loukola et al. 2017. Bumblebees show cognitive flexibility by improving on an observed complex behavior. Science Howard et al. 2019. Numerical cognition in honeybees enables addition and subtraction. Scientific Advances Mattila 2020. Honey bees (Apis cerana) use animal feces as a tool to defend colonies against group attack by giant hornets (Vespa soror)Howard et al. 2019. Numerical cognition in honeybees enables addition and subtraction. Scientific Advances Mattila 2020. Honey bees (Apis cerana) use animal feces as a tool to defend colonies against group attack by giant hornets (Vespa soror) | ||||||||||||||||||
25 | Response-slowing | Response-slowing has been tested in primates (e.g., Western lowland gorillas, McGuire and Vonk, 2020), though does not appear to have been tested in chickens or related species (or birds more widely, to my knowledge). | ||||||||||||||||||||||||
26 | Responses to novelty | Heart rates of trained pigs were reduced significantly (P = 0.003) compared to naïve pigs travelling the same course. Both handling ease and handling time were significantly improved for the trained pigs (P = 0.03 and P = 0.01 respectively) compared to naïve pigs. Blood immune measures indicated reduced stress among trained pigs who had lower neutrophil numbers (P = 0.04) and lower total and average phagocytosis (P = 0.001 and P = 0.02) compared with naïve pigs. This study demonstrated that the exposure of pigs to a novel environment clearly causes a mild physiological response (Lewis et al., 2008). Maternal presence reduced food neophobia profoundly as reflected in a reduced latency to touching the food, a higher proportion of piglets sampling the two different food items and a higher intake. Latency to touch the food, however, was affected by maternal presence more strongly for barren-reared piglets than for enriched-reared piglets, and in the absence of the sow, consumption of one novel food type and time spent in the feeding area were higher for enriched-reared piglets (Oostindjer et al., 2011). | Neophobia is present in chickens and varies across individuals (Garnham and Løvlie 2018) for example, individuals vary in their responses to novel arenas ((Favati et al. 2014); domestic chicks) and novel objects ((Zidar et al. 2017); red junglefowl). For example, red junglefowl show consistent individual responses to novel arenas, novel objects (‘personality’ tests) and tonic immobility, change of rewarded stimulus and intramaze change (‘coping style’ tests). Early stimulation decreased frequency of individual escape attempts in novel arena and novel object tests in red junglefowl (Zidar et al. 2017). | No studies of carp could be found. However, zebrafish (Danio rerio), a closely related cyprinid, have been found to have strong neophilic tendencies in novel situations (Lucon-Xiccato and Dadda, 2014). As well, novel object tests involving stationary, submerged objects (e.g. Fior et al., 2018), or floating objects (e.g. Magyary, 2019), have been shown to discriminate between high (neophobic) and low (neophilic) novelty individuals in zebrafish. | Wilson & Stevens (2005) documented between- and within-individual consistency in the behavior of rainbow trout (Oncorhynchus mykiss) during novel feeding and object tests indicating evidence for shy (e.g. neophobic) bold (e.g. neophilic) individuals. Similarly, Church & Grant (2018) showed Atlantic salmon (Slamo salar) juveniles had personality (individual behavioral differences across contexts) for habitat avoidance and attachment, traits which reflect a generalized neophobic response. Ghio et al. (2016) performed a “neophobia test” (i.e. novel object test) with brook trout (Salvelinus fontinalis) to determine whether juveniles with increased cortisol levels had increased neophobia in comparison to juveniles with low levels of cortisol and found no difference between the groups. Mayrand et al. (2019) inivestigated neophilic behaviors in Chinook salmon (Oncorhynchus tshawytscha) using a novel object test and found that at two differences in neophilic behaviors existed between the domestic-wild and domestic-domestic crosses and life history stages. | Octopuses have varied responses to new objects and responses will often depend on their individual personalities (Mather & Anderson 1993; 1999). Responses to a range of stimuli have been investigated in a variety of octopus species (incl. O. dofleini, Mather & Anderson 19993; O. bimaculoides, Sin et al. 2001; O. rubescens, Mather & Anderson 1993; O. vulgaris, Kuba et al. 2006). Individual responses to novel objects in octopuses were formally characterised as an approach and avoidance dichotomy (Maldonado 1963; Mather 1995). Responses are now characterised as (i) activity (explorative interaction between animal and stimulus), (ii) reactivity (defensive reaction where octopus assumes a defensive posture), and (iii) avoidance (octopus retreats and hides from stimulus) (Mather & Anderson 1993). Octopuses are also sensitive to novelty in the context of 'place'. When introduced into a new compartment or tank an octopus can show the different traits outlined above (personal observation) - again this is dependent on personality. | A study on the habituation of the crayfish Procambarus cubensis to a novel environment found that crayfish usually displayed an initial retreat (forwards or backwards) into any maze arm (Shuranova et al. 2005). Crayfish then typically displayed freezing behaviour (for up to 30 min). As individuals became habituated to the environment (over a course of sessions), the initial immobility decreased. The authors of the study report that “anecdotal evidence suggests that crayfish do not accept food when placed in a novel environment. Another study used a novelty stress protocol on crayfish, which exposed them to a number of environmental stressors they had not previously encountered, for example a radio playing hard rock music for 24h (Pagé & Cooper 2004). Individuals which underwent the protocol exhibited more tail flipping behaviour than control animals, suggesting they found the protocol stressful. | It is now recognized that many vertebrates and a few invertebrates show individual-specific consistency in their behaviour across time and context, sometimes in ways that can be paralleled with human personality. Their work aimed at assessing behavioural consistency in a social insect: the bumblebee Bombus terrestris. They focused on a behavioural dimension commonly used in personality studies: the response of an individual to novelty (neophilia/neophobia spectrum). They used a foraging paradigm to quantify individual bees’ response to novel flower colours and to assess the repeatability of this response over time. As for vertebrates, most individual bumblebees responded to a novel stimulus by increasing the time they spent investigating it compared to known stimuli. Using a new statistical approach, the consistency model, they found that individual bees tended to be consistent in their response to novelty over a few hours but were not consistent in their behaviour over 3 days. They conclude that for the neophilia/neophobia paradigm used here, bumblebee foragers do not fulfil the criteria for animal personality in the common sense of the term. Instead their behavioural response to novelty appears to be plastic, varying on a day to day basis (Muller et al., 2010). | ||||||||||||||||||
27 | Reversal learning | In this study they draw a comparison between individual coping characteristics, rearing conditions and behavioural flexibility in pigs via a reversal learning task (Bolhuis et al., 2004). | Chickens trained on 20 reversals using non-spatial stimuli showed reduced errors across trials (Bacon et al. 1962). Chickens performed comparably to carrion crows in a reversal learning experiment, i.e., they did not differ in the number of trials until learning criterion reached, suggesting similar levels of behavioural flexibility (Wascher et al. 2021). Learning (discriminative, reversal, spatial learning) was not correlated across tasks, though learning speed in reversal tasks correlated with individual variation in exploration in an age-dependent manner, in young and adult junglefowl. Specifically, more explorative chicks more quickly learned the reversal task compared to less explorative ones, while the opposite pattern was found in adult females (not assayed in adult males). There were also sex differences in learning speed in chicks, with females learning faster than males (Zidar et al. 2018). Serial reversal learning: white leghorn chickens were tested on a successive reversal learning task, using a spatial task with two reversals, and performed comparably (i.e., total errors) to guinea fowl. Chickens were outperformed (i.e., made more errors) than several other bird species including myna, pigeon, double yellow-headed parrot, and Himalayan magpie, as well as several mammals including capuchin and squirrel monkeys (Gossette 2016). Rapid reversal learning: chicks were able to peck once at unpalatable blue or green crumbs, on a blue or green background, before being exposed to palatable crumbs of the same colour on the same background. Latency to peck was higher for contrasting prey, indicating stronger avoidance learning, however, the learning the reversal was slower than contrasting with matching prey. These findings suggest that rapid reversal of avoidance response is influenced by contrast between a prey item and its background (Roper 1994). | Studies of carp specifically could not be found, but there are several studies of zebrafish (Danio rerio) that report reversal learning. Zebrafish are capable of learning an operant response (approaching a sensor) to receive food, then learning an alternative response (approaching a different sensor) while inhibiting the original operant response, thus demonstrating they are capable of “ reversal learning between discrete operant responses” (Kuroda et al. 2017). Parker et al. (2012) also report that zebrafish are capable of “(a) distinguishing between two colours when reinforced with food (b) reinforcement of previously unreinforced alternative results in reversal of the discrimination” and intra-dimensional shift (new discrimination between a set of two novel colours). This finding is supported by Colwill et al. (2005) who found that zebrafish were capable of two-choice colour discrimination and subsequent reversal as well. However, evidence from Roy et al. (2019) suggests that the conditioned stimulus may affect reversal learning performance in some populations (e.g. some wild fish only responded to red cues rather than those of other colours) and report that, in their task, domesticated zebrafish showed no reversal learning ability. There is no reason to believe that the ability to reverse previous learning is limited only to zebrafish within the cyprinid family. | Studies of salmon specifically could not be found, but rainbow trout (Oncorhychus mykiss) can reverse previous associative learning. For example, trout bred for low stress reactivity are “markedly slower than reactive HR fish in altering their food seeking behaviour in response to relocated food” (Ruiz-Gomez et al. 2011). There’s no reason to believe that the ability to reverse previous learning is limited only to rainbow trout within the salmonid family. | Several early studies have tested reversal learning in octopus (Boycott & Young, 1957; Young, 1962; Mackintosh, 1964; Mackintosh & Mackintosh, 1963; 1964). These studies suggest that octopuses have strong reversal learning capacities and can successfully perform in serial reversal tasks whereby stimuli are reversed multiple times (i.e., up to four times). Evidence for serial reversal learning is mixed. Notice that the test procedures in these early studies involved pre-training on the positive stimulus after reversal, strong negative reinforcement on incorrect choices (i.e., electric shock), and potential secondary cueing by the experimenter (i.e., octopuses could see the experimenter). Such procedures can cause detrimental effects to the animal’s ability to learn and create extraneous variables, making it challenging to interpret the results. A more recent study (Bublitz et al., 2017) that accounted for these potential drawbacks demonstrated that some octopuses could solve a reversal learning task but only 50 % of the sample (n = 4) successfully reached the learning criterion (80% correct choices) in the first reversal learning phase. For this reason, the RP rating is listed as 'likely yes' instead of 'yes'. Moreover, only one octopus showed serial reversal learning, completing a total of four reversals, and showing progressive improvement (i.e., decreased errors to reach learning criterion the more reversals it experienced). | No studies on reversal learning found in Penaeidae, however one study successfully used a reversal learning procedure to train freshwater shrimp (Macrobrachium acanthurus) to visually discriminate stimuli and make a choice in a Y maze between a punished and non-punished side (Ventura & Mattei 1977). A high level of performance was displayed during the final three sessions with 92% correct choices. As Penaeid shrimp also live in an environment in which flexible discrimination learning is useful, it is possible that they would also display this behaviour. | In one study crabs were trained to press a lever to obtain a food reward (Abramson & Feinman 1990). Once they had learned the task, the contingency associated with the lever was reversed and crabs quickly learned to switch to the correct lever. | In a place learning experiment (using only reward), some crayfish displayed single trial reversal learning (Tierney et al. 2018). However, a study from 1967 (Capretta and Rea) suggests that crayfish lack the ability of reversal learning in a spatial choice task. They used punishment as part of the protocol and this could explain the different results between the two studies. | Raine & Chittka (2012) tested whether rapid learning interferes with the acquisition of new information using a reversal learning paradigm. Bumblebees (Bombus terrestris) were trained to associate yellow with a floral reward. Subsequently the association between colour and reward was reversed, meaning bees then had to learn to visit blue flowers. They demonstrated that individual bumblebees that were fast to learn yellow as a predictor of reward were also quick to reverse this association (Raine & Chittka, 2012). | Adult fruit flies are capable of simple reversal learning with nociceptive stimuli in as little as one trial. Larval fruit flies have been shown to exhibit reversal learning in response to non-nociceptive stimuli. However, these studies do not necessarily demonstrate serial reversal learning (McCurdy et al. 2021; Shuai et al. 2011; Tully and Quinn, 1985; Wu et al. 2012; Guo and Guo, 2005; Ren et al. 2012; Mancini et al. 2019" | No studies on reversal learning in lepidopteran larvae, but a study on adult monarch butterflies showed that they were able to shift away from feeding from yellow flowers containing a sucrose solution (and which they displayed an innate preference for) when the sucrose was substituted with a salt solution (Rodrigues et al. 2010). In a subsequent test, the sucrose reward was offered again in place of salt and butterflies were able to switch back to feeding from the sucrose paired flowers (Rodrigues et al. 2010). Similarly, in a different study pipevine swallowtail butterflies readily shifted their foraging behaviour when the colour of the rewarding flower was changed (Weiss 1997). It is ecologically plausible that the larvae would be able to reverse leaning in a similar way to the adult. | ||||||||||||||
28 | Reverse reward test | The reverse reward test, where a choice is presented between two different food quantities, and the subject is rewarded with the non-chosen item, has been tested in mammals (e.g primates) (Albiach-Serrano and Call 2014) and fish (Danisman et al. 2010). To our knowledge, it does not appear to have been tested in chickens or closely related species. | Several early studies have tested reversal learning in octopus (Boycott & Young, 1957; Young, 1962; Mackintosh, 1964; Mackintosh & Mackintosh, 1963; 1964). These studies suggest that octopuses have strong reversal learning capacities and can successfully perform in serial reversal tasks whereby stimuli are reversed multiple times (i.e., up to four times). Evidence for serial reversal learning is mixed. Notice that the test procedures in these early studies involved pre-training on the positive stimulus after reversal, strong negative reinforcement on incorrect choices (i.e., electric shock), and potential secondary cueing by the experimenter (i.e., octopuses could see the experimenter). Such procedures can cause detrimental effects to the animal’s ability to learn and create extraneous variables, making it challenging to interpret the results. A more recent study (Bublitz et al., 2017) that accounted for these potential drawbacks demonstrated that some octopuses could solve a reversal learning task but only 50 % of the sample (n = 4) successfully reached the learning criterion (80% correct choices) in the first reversal learning phase. For this reason, the RP rating is listed as 'likely yes' instead of 'yes'. Moreover, only one octopus showed serial reversal learning, completing a total of four reversals, and showing progressive improvement (i.e., decreased errors to reach learning criterion the more reversals it experienced). | |||||||||||||||||||||||
29 | Shared intentionality | Unknown: no published literature in octopuses. However, the day octopus, Octopus cyanea, have been observed cooperatively hunting with various fish species including peacock grouper, Cephalopholis argus, brown-marbled grouper, Epinephelus fuscoguttatus, gold-saddle goatfish, Parupeneus cyclotomus, and coral trout, Plectropomus leopardus. The underlying mechanisms that drive this type of coordination remains to be tested. Mechanisms responsible for cooperation vary in complexity and can include chemical regualtion, visual signals, andmeshing psychological states (i.e., shared intentionality). | ||||||||||||||||||||||||
30 | Social learning | During the test phase there was a match or mismatch between location and the flavoured food eaten by the sow. Match piglets showed more behaviour towards, and a higher consumption from, the feeder where the sow was eating, while this was not true for mismatch piglets, suggesting a role of both local and stimulus enhancement. Observation, participation, local and stimulus enhancement thus all seem important for piglets to learn from the sow (Bolhuis et al., 2011). | Chickens can learn new behaviours and about new environments or events from observing conspecifics (Nicol and Pope 1994; Marino 2017). For example, feather plucking (a negative behaviour) has been found to develop and increase in chick groups when chicks showing higher feather plucking frequencies are introduced, compared with control groups (Zeltner et al. 2000). Using an inanimate chicken model, pullets that had observed a trained demonstrator piercing the membrane and consuming blood (the task) from the chicken model performed this cannibalism task better than those without the demonstrator, though control (without demonstrator) birds could also learn the task (Cloutier et al. 2002). Chicks learned a detour task more quickly if the goal included two interacting chicks (opposed to two chicks that could not interact due to a barrier), suggesting chicks respond to social interactions of conspecifics (Regolin et al. 1994). Chickens can learn food or location preferences of conspecifics from observing a demonstrator (e.g., hen or older chick). For instance, observer hens were more likely to follow hens that they had previously observed successfully obtaining food, over those that they had not seen obtain food (Wichman 2018), indicating both sensitivity to the foraging abilities of conspecifics and flexibility to learn selectively (Freire 2020). Chickens sometimes synchronise behaviour, likely due to social influences (Eklund and Jensen 2011). | Bajer et al. (2010) investigated the ability of common carp (Cyprinus carpio) to learn the location of newly introduced food in a lake and found that the speed and precision the carp displayed in this task was facilitated by social learning. In a set of laboratory experiments, Lovén Wallerius et al. (2020) determined that, compared with control groups, common carp individuals with direct or social experience of catch-and-release angling expressed significantly elevated hook avoidance behavior during a short-term vulnerability assessment hours after a catch-and-release experience. Then, in a subsequent trial within days after the threat exposure, fish with direct hooking experience and fish with only social hooking experience were both more cautious towards bait in the presence of a sham rig (i.e., a hookless rig with bait) than when only exposed to bait without a rig (Lovén Wallerius et al., 2020). These results indicate that the combined influence of direct and social experience of catch-and-release angling induced a hook avoidance behavior in common carp (Lovén Wallerius et al., 2020). Chen & Zeng (2022) examined the relationship between vulnerability to angling and social learning in juvenile crucian carp (Carassius auratus) under laboratory conditions and demonstrated that plasticity in the vulnerability of crucian carp to angling was related to previous individual angling experience but not to visual social learning. European minnows (Phoxinus phoxinus), a related cyprinid, have also been shown to increase the frequency of flight responses after observing the flight response of conspecifics in a neighboring tank that had been threatened by a predator (Magurran & Higham 1988). Similarly, Reebs (2000) found that naive golden shiners (Notemigonus crysoleucas; a related cyprinid), could be trained to make daily migrations to a food site by following trained demonstrator conspecifics. | Brown & Laland (2002) investigated whether the darting motion of juvenile Atlantic salmon (Salmo salar) sends a message to other fish that food is available, and whether this cue could be utilised by naive fish to learn to forage on novel prey items. Brown & Laland (2002) found that 100% of the S. salar individuals that paired with pretrained demonstrators learned to accept the novel prey and the naive fish paired with equally naive individuals performed worse (50%) than the individuals learning in isolation (73%), a finding they interpreted as “social inhibition”. Social learning of foraging has also been reported in hatchery-reared juvenile chum salmon (Oncorhynchus keta; Ryer & Olla 1991). Sundstrom & Johnsson (2001) also found an increase in foraging performance, when in visual contact with another feeding conspecific in wild but not in hatchery-reared, brown trout (S. trutta), suggesting that the conditions under which hatchery fish are raised may diminish their ability to exploit social cues. Similar to this, Brown & Laland (2001) wrote a review paper to outline methods and findings that suggest how social learning protocols could realistically be applied on a large scale to enhance the viability of hatchery fish, including multiple species of salmonids, prior to their release into the wild. Vilhunen et al. (2004) demonstrated that the social learning of predator recognition in Arctic charr (Salvelinus alpinus) required a low experienced (“demonstrator”) to naïve (“observer”) fish ratio and this suggested that using social learning procedures in training fish for reintroduction programs could provide considerable advantages. Lastly, White & Gowan (2014) showed that adult brook trout (Salvelinus fontinalis) use social learning to quickly develop search images for novel prey (meal worms). | Social learning has been reported in the common octopus, Octopus vulgaris. In a 1992 study, naïve octopuses were able to solve a colour discrimination task by first observing a conspecific demonstrator solve the same task (Fiorito & Scotto 1992). It should be noted that these findings have not been replicated and the study has since been criticised for lacking controls to distinguish whether the octopuses were learning through observation or alternative mechanisms (Biederman & Davey 1993). Interestingly, studies on cuttlefish have demomnstrated that learning does not improve by observing conspecifics (Boal et al. 2000; Huang & Chiao 2013). The 1992 findings in octopus have also led to a debate about the function of social learning because it was traditionally thought to be an adaptive trait of social living. It has since been suggested that mechanisms such as perception, attention, and motivation might facilitate the capacity for social learning (Lefebvre & Giraldeau 1996; Heyes 2012). As such, the capacity for social learning in octopuses is theoretically plausible, however, additional experiments are needed to corroborate the original findings. | The shrimp Alpheus lottini, of the order Decapoda and family Alpheidae (not Penaeidae) learns from crab “appeasement patterns ... before the shrimp is accepted on the coral by the crab” (Vannini, 1985). A similar behavior might be displayed by Penaeidae shrimps but evidence is not available, and because the crab/shrimp relationship highlighted here is fairly unique, I have not made inferences based on this single study. | Not been demonstrated explicitly, but crayfish (Procambarus clarkii) are able to recognize and remember conspecifics to allow for a stable dominance hierarchy, suggesting they are sensitive to social information which they retain (Jiménez-Morales et al. 2018). One study found that “crayfish are sensitive to reflection, even the partial reflection present in an ordinary glass tank, and that responses of crayfish to a reflective environment depend on prior socialization” (Drodz et al., 2006). | Social insects make elaborate use of simple mechanisms to achieve seemingly complex behavior and may thus provide a unique resource to discover the basic cognitive elements required for culture, i.e., group-specific behaviors that spread from “innovators” to others in the group via social learning. They first explored whether bumblebees (Bombus terrestris) can learn a nonnatural object manipulation task by using string pulling to access a reward that was presented out of reach. Only a small minority “innovated” and solved the task spontaneously, but most bees were able to learn to pull a string when trained in a stepwise manner. In addition, naïve bees learnt the task by observing a trained demonstrator from a distance. Learning the behavior relied on a combination of simple associative mechanisms and trial-and-error learning and did not require “insight”: naïve bees failed a “coiled-string experiment,” in which they did not receive instant visual feedback of the target moving closer when tugging on the string. In cultural diffusion experiments, the skill spread rapidly from a single knowledgeable individual to the majority of a colony’s foragers. They observed that there were several sequential sets (“generations”) of learners, so that previously naïve observers could first acquire the technique by interacting with skilled individuals and, subsequently, themselves become demonstrators for the next “generation” of learners, so that the longevity of the skill in the population could outlast the lives of informed foragers. This suggests that, so long as animals have a basic toolkit of associative and motor learning processes, the key ingredients for the cultural spread of unusual skills are already in place and do not require sophisticated cognition (Alem et al., 2016). | |||||||||||||||||
31 | Socio-spatial cognition | In the holeboard task, measures of cognitive performance are independent of the speed of negotiating the test apparatus. The holeboard is an open field arena with 16 locations (holes, or buckets in the present study) which may contain bait. The study investigated whether pigs are able to acquire a complex spatial holeboard discrimination task (4 of 16 holes baited) and whether mixing stress affects performance in this task. All pigs rapidly reduced the number of re-visits to baited holes (working memory) and to unbaited holes (reference memory). Mixing stress did not affect performance (Arts et al. 2009). | Range use is related to how quickly chickens learn to associate a T-maze arm with a food reward, with differences between adult laying hens housed indoors only (which perform poorly), indoor-preferring or out-door preferring birds (Campbell et al. 2018). In free-range male chickens, low-ranging chickens were quicker and made fewer errors when locating four food-rewarded cups (from eight cup selection) within a squared arena using visual cues placed on the walls, than high-ranging chickens (Ferreira et al. 2019). Broiler chickens can learn to locate a T-maze food-reward arm (Li et al. 2019) however they struggle when the task becomes more complex, like discriminating food quality in a Y-maze arena (Buckley et al. 2011) potentially due to impact of prolonged hunger. Individual exploration behaviour influences performance in T-maze task (finding conspecifics), those with low exploratory behaviour did not leave the start box (Nordquist et al. 2011). Faster spatial learners also show more visits to the range (i.e., individual-level performance correlation) (Campbell et al. 2018). Improved performance on detour task across trials, indicating learning, for example, chicks show higher performance in trial two even after 24-hour delay between trials (Regolin and Rose 1999). The development of spatial cognition is influenced by environment. For example, chicks reared with perch access or elevated structures showed higher performance in detour task than those reared without (Norman et al. 2019). Similarly, meat chickens reared with straw bale access showed higher performance when learning to avoid pecking inedible food stimuli on a coloured background than those without (Tahamtani et al. 2018). | Few studies on carp could be found but multiple species of carp do shoal and school together. For example, juvenile bighead carp tend to form a single large shoal while silver carp tend to form shoals of 2–3 individuals (Ghosal et al., 2016). As well, zebrafish (Danio rerio), a closely related cyprinid, shoal and school (Miller & Gerlai, 2012). Specifically, shoaling can be induced in zebrafish by the presentation of conspecifics and this causes a robust shoaling response under most experimental conditions (e.g. Saverino & Gerlai, 2008; Miller et al., 2012). Additionally, zebrafish reared in enriched tanks have been shown to solve a maze to access conspecifics significantly faster than fish reared in a barren environment (DePasquale et al., 2016). | Schooling (i.e. coordinated swimming group), shoaling (i.e. loosely organized group), and other forms of aggregative behaviour are well known in salmonids as a form of predator defence as well, this collective behaviour has been suggested to play a role in orientation and navigation during homing (Dittman & Quinn, 1996; Berdahl et al., 2016b). To participate in schooling or shoaling behaviors, fishes are likely exerting socio-spatial cognition (e.g. spatially mapping others; reviewed by Larsson (2012)). As well, Salvanes et al. (2013) subjected juvenile Atlantic salmon that had been reared in either an enriched environment or a barren environment to a maze task with conspecifics as a reward. In comparison to the fish reared in the impoverished tanks, the fish reared in the enriched tanks had increased neural plasticity in the telencephalon and had a superior spatial learning ability, allowing the fish to correctly solve a maze to locate conspecifics more efficiently and with less mistakes (Salvanes et al., 2013). Thus, the enriched Atlantic salmon juveniles spatially mapped out where the other fish were located in the maze quickly. Similarly, rainbow trout juveniles reared in an enriched environment were able to solve a maze to access conspecifics faster than fish reared in a barren environment (Bergendahl et a., 2016). | Unknown: but octopuses do have sophisticated spatial learning abilities (Mather 1991a, 1991b, Forsythe & Hanlon 1997). Whether such spatial cognition is coupled with social information such as the location of conspecifics or other animals remains to be exprimentally tested. Nevertheless, navigation studies demonstrate that octopuses take different foraging paths across consectuive days (Mather 1991a, Forsythe & Hanlon 1997). This suggests that they can remember the distribution of prey in a spatial context to avid revisiting depleted areas (Mather 1991a, Forsythe & Hanlon 1997). | Bumblebees (Bombus terrestris) move about their environments by flying and by walking. Most experimental studies have addressed navigation during foraging flights, but they presented our experimental bees with the challenge of learning to navigate while walking as they must do in nature within topographically complex spaces containing their nests. They trained bumblebee workers to navigate complex, nine-channel, mazes in the absence of specific visual, chemical or textural cues. They successfully navigated through complex multi-turn mazes (stereotypical “rat mazes”) with several dead-ends by memorizing the entire sequence of appropriate turns, and their choice of correct first turn on entering the maze. Thus, their observed proficiencies indicated that the individual bumblebees had each memorized the maze by learning motor sequences which were not linked to visual, chemical or textural stimuli, and that their memories were triggered by contextual cues associated with the bees’ positions in a sequence. Our findings have implications on natural ambulatory activities inside and outside the colony, and even in practical use as vectors of biological control agents (Mirwan & Kevan, 2015). | |||||||||||||||||||
32 | Symbolic representation of the world | Research indicates chickens may have a capacity to miss (in a cognitive sense) a resource lacking in their environment, i.e., a mental representation of missing resources, which can influence decision-making. It remains open as to whether such representations trigger processes that allow chickens to experience the resource absence (Freire 2020). | Unknown: no published literature found | |||||||||||||||||||||||
33 | Temporal/ spatial discounting | Performance on the incremental learning task improved across sessions; however, none of the three pigs performing the time estimation task progressed beyond the training stage and only one demonstrated increasing performance across sessions. It appeared that the physical requirements of the TRD lever press (i.e., maintaining a press) were difficult to perform (Ferguson et al., 2009). | Hens trained to peck differently coloured lights in return for a reward following different durations showed a preference for pecking the key with an interval of 6 seconds but access to food for 22 seconds, rather than one with 2 second interval and food access for 3 seconds (Abeyesinghe et al. 2005). Chicks trained to associate colour cues with delayed rewards and in social foraging tasks were tested in their intertemporal choices, with the finding that food variance impacted on temporal discounting. Specifically, chicks trained using a pseudo-competition social condition and variable food condition, chose the large, delayed reward less frequently than chicks trained in isolated social condition, with constant food condition (Mizuyama et al. 2016). | Self-control means choosing a large delayed reward over a small immediate reward; impulsiveness is its opposite. Foraging honeybees (Apis mellifera) have high metabolic rates; the metabolic hypothesis would predict little self-control in bees. But foraging bees work for the longterm good of their hive, conditions that seem to require self-control. In three experiments, we gave bees the choice between (1) a sweeter delayed reward and a less sweet immediate reward and (2) a large delayed reward and a small immediate reward. Bees showed much self-control, inconsistent with the metabolic hypothesis (Cheng et al., 2002). | ||||||||||||||||||||||
34 | Theory of mind | An experiment at the University of Bristol found that one out of ten pigs was possibly able to understand what other pigs can see. That pig observed another pig which had view of a maze in which food was being hidden and trailed that pig through the maze to the food. The other pigs involved in the experiment did not (Held et al., 2005). For example, pigs appear to be able to use ‘what’ and ‘where’ information about more and less-preferred food to organise their foraging behaviour. It may thus be possible to take the next step and ask whether this important domestic species can also use ‘when’ information (Held et al., 2005). | Unknown: no published literature but see perspective taking. | |||||||||||||||||||||||
35 | Tool use | Two individuals, adult females, used the sticks or bark, using a rowing motion, during the final stage of nest building. The third individual, an adult male, attempted to use a stick to dig with. Stick and branch manipulation was observed in other contexts, but not for digging. The observation suggests the hypothesis that the observed use of stick to dig with could have been socially learned through vertical transmission (mother-daughter) as well as horizontal transmission (female-male) (Root-Bernstein et al., 2019). | The ability to use (and in some species, make) tools has been found across a number of animals, including birds, such as corvids, parrots, woodpecker finches, egyptian vultures and herons, most frequently in foraging contexts (e.g. Emery and Clayton, 2009; Ruxton and Hansell, 2010). However, to our knowledge, there does not appear to be published reports of tool-use (experimental or observational) in chickens or closely related species. There does not appear to be published evidence of reports/ observations or aims to test tool-use in chickens or closely related species. | Unknown. No studies of carp or the closely related cyprinid, zebrafish (Danio rerio), could be found. Examples exist for cichlids, wrasse, and whitetail majors (as well as archerfish, gouramis, and triggerfish, if the manipulation of water is considered the use of a tool), however it is unlikely that there is physical, ecological, or behavioural homology between species who exhibit tool use and salmonids or cyprinids. That being said, Brown (2012) highlights “constraints of the current working definition of tool use in fishes” that may hinder our ability to identify tool use in these species. They summarize these constraints: “fishes lack grasping limbs and operate underwater where there are clear constraints with respect to the physics of tool use that differ dramatically from the terrestrial environment.” | Unknown. No studies of salmonids could be found. Examples exist for cichlids, wrasse, and whitetail majors (as well as archerfish, gouramis, and triggerfish, if the manipulation of water is considered the use of a tool), however it is unlikely that there is physical, ecological, or behavioural homology between species who exhibit tool use and salmonids. That being said, Brown (2012) highlights “constraints of the current working definition of tool use in fishes” that may hinder our ability to identify tool use in these species. They summarize these constraints: “fishes lack grasping limbs and operate underwater where there are clear constraints with respect to the physics of tool use that differ dramatically from the terrestrial environment.” | Octopuses use tools for defence. Several species of octopus (e.g. Amphioctopus marginatus, Octopus joubini, O. digueti, O. tetricus, O. vulgaris) have been observed transporting objects such as coconut shells (Finn et al. 2009), bivalve and conch shells, as well as plastic and glass bottles, using these objects as mobile dens to protect themselves from potential predators. Octopuses have also been observed collecting shells and stones with their suckered arms to create a protective armour (Jeffs & Brownlow 2017). It has also been suggested that octopuses use tools to aid in foraging. Similiar to some species of cetaceans, octopuses have been observed using water as a tool - jetting water from their funnel to extract food remains from bivalve shells that would otherwise be unobtainable (Boycott 1954). There have also been some reports of octopuses propping open bivalves with different objects during foraging (Lane 1960; Thorpe 1964; reviewed in Mann & Patterson 2013). However, quantitative evidence for this appears to be absent. | The crab Tiarinia cornigera uses algae to decorate its shell and it changes the amount of algae used for decorating depending on age and presence or absence of competitors and predators (Thamnh et al, 2005). Spider crabs of the Majidae family were found to do the same (Wicksten 1992). Several species of crabs use other marine organisms or pieces of these, to decorate themselves and increase camouflage. Pagurus pollicaris uses anemones and shells for protecting itself from predators and positions them to ensure the carapace is balanced in weight (Brooks et al. 1989). However, it is unlikely that these behaviours are displayed by the swimming family Portunidae. Boxing crabs hold sea anemones in their claws for defence. Guinot, D., Doumenc, D., & Chintiroglou, C. C. (1995). A review of the carrying behaviour in brachyuran crabs, with additional information on the symbioses with sea anemones. Raffles Bulletin of Zoology 43 377-416. See also: Mann, J., & Patterson, E. (2013). Tool use by aquatic animals. Philosophical Transactions Of The Royal Society B: Biological Sciences, 368(1630), 20120424-20120424. doi: 10.1098/rstb.2012.0424 | They explored bees’ behavioral flexibility in a task that required transporting a small ball to a defined location to gain a reward. Bees were pretrained to know the correct location of the ball. Subsequently, to obtain a reward, bees had to move a displaced ball to the defined location. Bees that observed demonstration of the technique from a live or model demonstrator learned the task more efficiently than did bees observing a “ghost” demonstration (ball moved via magnet) or without demonstration. Instead of copying demonstrators moving balls over long distances, observers solved the task more efficiently, using the ball positioned closest to the target, even if it was of a different color than the one previously observed. Such unprecedented cognitive flexibility hints that entirely novel behaviors could emerge relatively swiftly in species whose lifestyle demands advanced learning abilities, should relevant ecological pressures arise (Loukola et al., 2017). | ||||||||||||||||||
36 | Transitive inference | According to this review from 2008, it can be found in chimpanzees, squirrel monkeys, rats, pigeons, pinyon jays, scrub jays, hooded crows and fish - however in pigs it wasn’t apparently even studied (Vasconcelos, 2008). BUT: Reasoning/ Inference: Establishment of an association between a visible and an imagined event (Nawroth et al 2015): The subjects as a group were able to use direct and indirect visual cues. However, over the course of the experiment, the performance dropped to chance level when indirect information was provided. A final experiment (N = 3) provided preliminary results for pigs’ use of indirect auditory information to infer the location of a reward. We conclude that pigs at a very young age are able to make decisions based on indirect information in the visual domain, whereas their performance in the use of indirect auditory information warrants further investigation (Nawroth and von Borell, 2015). | Adult chicken research indicates they show the ability for transitive inference, such as if A > B and B > C, then A > C (Hogue et al. 1996; Forkman 2000). For instance, using social information about dominance to inform decisions. Specifically, after observing a dominant being defeated or defeating a stranger, or two strangers establishing dominance before being introduced to the strangers, the bystander used this information to inform their behavioural strategies, i.e., initiating attacks (Hogue et al. 1996). However, this study did not rule out that hens may use observations of the interaction to gauge a stranger’s fighting potential (Freire 2020). In a later study, chicks were trained to associate a food reward with pecking one of two stimuli, then presented with a series of stimuli-pairs to establish a hierarchy illustrating which item results in a reward (A > B > C > D > E). In the test, B and D were presented for the first time, with equal prior reward/ non-reward experience, and chicks could correctly peck the B from trial 1, indicating an inference between B and D from previous pairs (B > C, C > D) (Daisley et al. 2010). Lower-ranked chickens show higher performance at transitive inference reasoning than higher-ranked individuals (Daisley et al. 2021). | Unknown. No studies of carp or the closely related cyprinid, zebrafish, could be found. Other studies have found that cichlids (specifically Astatotilapia burtoni: Grosenick et al. 2007, and Julidochromis transcriptus: Hotta et al. 2015) and cleaner wrasse (Labroides dimidiatus: Hotta et al. 2020) are capable of transitive inference in the context of determining social dominance and client-reward interactions, respectively. Though these fish are in different orders and so are unlikely to share homology with carp, they are included because the authors of these studies suggest a role of sociality in the evolution of transitive inference among fishes. Social behaviour in carp varies by lifestage, so it is possible that transitive inference would be adaptive for these species at certain times of life (e.g. during shoaling among young carp, etc.). | One study of brook trout (Salvelinus fontinalis) found that young of the year (<1 year old, 7 replicate subjects) were capable of transitive inference in the context of assessing conspecific social rank within a 5-fish hierarchy (White & Gowan 2013). Studies of different salmonid species or lifestages are not available. Other studies have found that cichlids (specifically Astatotilapia burtoni: Grosenick et al. 2007, and Julidochromis transcriptus: Hotta et al. 2015) and cleaner wrasse (Labroides dimidiatus: Hotta et al. 2020) are capable of transitive inference in the context of determining social dominance and client-reward interactions, respectively. Though these fish are in different orders and so are unlikely to share homology with salmon, they are included because the authors of these studies suggest a role of sociality in the evolution of transitive inference among fishes. Social behaviour in salmon varies by lifestage, so it is possible that transitive inference would be adaptive for salmonids at certain times of life (e.g. during juvenile salmonid lifestages or reproduction, etc.). | Unknown. No published literature on transitive inference, a form of inferential reasoning, in octopus or any other cephalopod. However, two-spot octopuses can distinguish between a combination of objects and learn to choose an odd-shaped object in a sequence. Importantly, octopuses can transfer this learning and choose another odd stimulus in a new sequence (Boal 1991), a cogntive process that is described as generalization learning. Generalization learning allows an individual to respond to a variety of challenges, especially when faced with new information and is thought to be a potential precursor of inferential reasoning. | They asked whether honeybees, Apis mellifera, could solve a transitive inference problem. Individual free-flying bees were conditioned with four overlapping premise pairs of five visual patterns in a multiple discrimination task (A+ vs. B-, B+ vs. C-, C+ vs. D-, D+ vs. E-, where + and - indicate sucrose reward or absence of it, respectively). They were then tested with the nonadjacent pairs A vs. E and B vs. D. Preference of B to D is consistent with the use of the implicit hierarchy A > B > C > D > E. Equal choice of B and D supports choice based on the associative strength of the stimuli. The bees' choice was determined by their memory constraints: experience with the last premise pair (D+ vs. E-) predominated. In the tests, bees preferred A to E and chose equally B and D. An analysis of the performance in terms of a reward/penalty ratio showed that B had a higher associative strength than D. Thus, bees do not establish transitive inferences but, rather, guide their choices by the joint action of a recency effect and the associative strength of the stimuli. The former supports choice of D, whereas the latter supports choice of B, thus determining equal choice of B and D in the tests (Benard & Giurfa, 2004). | |||||||||||||||||||
37 | Uncertainty monitoring | A study with pigeons suggests they do not show a capacity for metamemory, i.e. they are not self-reflective in being able to monitor and respond flexibly to uncertain states, potentially as it is difficult to demonstrate experimentally because it is difficult for these birds to use (Inman and Shettleworth 1999). Common ravens were presented with a foraging task (3 containers) where they could observe food being hidden, infer its location using visual or auditory cues, or given no information. They behaved similarly to capuchin monkeys, but not like great apes or macaques, in checking inside at least one tube on every trial, though typically only once inside the baited tube, if they had observed it being baited or visually inferred the food’s location (Lambert and Osvath 2020). It does not appear to be tested in chickens or closely related species, or very comprehensively in birds, while being fairly widely tested in primates, including humans (Smith et al. 2003). | Unknown. No studies of carp or the closely related cyprinid, zebrafish (Danio rerio) could be found. | Unknown. No studies of salmonids could be found. | No published literature on octopuses or any other cephalopod. Thus, no information on whether cephalopods have abilities such as metacognition or metamemory. | No information for Penaeidae. Paper on uncertainty monitoring for the species Paratya australiensisis, of Unknownthe Decapod order, but of a different family (Atyidae). “Conditioned shrimp showed a long delay before making a choice between Gambusia scented water (a predator) and tap water but chose an arm at random” (Bool et al, 2011). Possible that the family Penaeidae would display a similar behavior. | In the spider crab Microphrys Bicornutus (family Mithracidae) the uncertainty of a given act was reduced by knowledge of the previous act (by the other animal) anywhere from 31% up to 81% (Eastabrook and Hazlett 1974). | “[In a T-maze test]..crayfish spent longer in the vicinity of a previously open exit compared to a closed exit (Tierney and Andrews, 2013). The longer wait could be interpreted as a type of uncertainty monitoring. | Here they show that honeybees (Apis mellifera) can adaptively alter their behavior in a choice test in response to trial difficulty. Bees preferentially opt out of difficult trials and by doing so, improve their success rate. They discuss whether this choice involves assessing degree of uncertainty (considered a definition of basic metacognition) or whether this task might be solved by associative mechanisms. They propose a hypothesis for how uncertainty might be processed within the known circuitry of the insect brain to frame the concept of uncertainty as a topic for neurobiological analysis (Perry & Barron, 2013). | |||||||||||||||||
38 | Hedonic Proxies | |||||||||||||||||||||||||
39 | Anxiety-like behavior | Anxiety is a physio-psychological state anticipating an imminent threat. In social mammals it is behaviorally expressed via displacement activities and buffered viaaffiliation. Anxiety research on domestic pigs (Sus scrofa) has mostly focused on abnormal/stereotypic behavior associated with intensive farming. They investigated how anxiety is expressed and modulated in semi-free ranging pigs, in natural habitats. The results show, anxiety behavior in pigs was socially buffered. Intriguingly, anxiety behavior was expressed significantly more by bystanders than opponents, which suggests that pigs may be able to anticipate imminent threats. By highlighting how anxiety is managed under extensive farming, this study contributes to the understanding of pig welfare and biology (Norscia et al., 2021). | Using the tonic immobility paradigm (i.e., catatonic response to restraint), chickens show learned helplessness (i.e., unresponsiveness when cannot escape uncontrollable stressors) attentional shifts. Specifically, when observing eyespots, chickens in a learned helplessness condition took longer to recover motion than control birds but did so faster if an unaffected conspecific was present. Learned helplessness research suggests attentional shifts are associated with anxiety and depression-like states (Rodd et al., 1997). | It is difficult to distinguish anxiety from fear in many behavioural assays of animals, since they are so tightly linked in terms of physiological modulation. But given that cyprinids have fairly well-established fear-like behaviours and responses to relevant, fear-inducing stimuli, it is likely that they also exhibit anxiety-like behaviours in response to perceived threats. A few reports of anxiety-like behaviour in carp do exist (e.g. Todorova et al. 2015, Yalsuyi et al. 2021), but the majority of anxiety-like behaviours have been studied in the closely related cyprinid, zebrafish (Danio rerio). Zebrafish exhibit anxiety-like behaviours that have been experimentally exploited in now standardized behavioural assays such as the novel tank and light-dark preference tests (e.g. Maximino et al. 2010, Cachat et al. 2011, Stewart et al. 2012). Zebrafish are used as a model of anxiety for drug testing (e.g. Stewart et al. 2011) and neurological investigations (e.g. Chakravarty et al. 2013). Their exhibition of anxiety behaviours is well-established in the literature (e.g. Maximino et al. 2010, Cachat et al. 2011, Stewart et al. 2012, Jesuthasan 2012, Kalueff et al. 2013). | Reports of fear in salmonids occur in the scientific record as early as 1961 (e.g. Geller & Brady 1961). According to Chandroo et al. (2004), “Fear in fish has been characterised through branchial responses, alarm pheromone-initiated responses and aversive behavioural reactions.” Several fear-like behaviours have been identified during exposure to threats, such as freezing (e.g. Demuth et al. 2017), escape responses (e.g. frantic and rapid swimming behaviors and sometimes collisions into the sides of the tanks; e.g. Jackson & Brown 2011, Nilsson et al., 2019), and accelerations in response to sudden movements in the environment (e.g. Colson et al. 2015). These are just a few illustrative behavioural examples of many, and more are reviewed by Chandroo et al. (2004). The fear response in salmonids can also mediate learning: for example, fear conditioning is a common experimental paradigm (e.g. Yue et al. 2004, Demuth et al. 2017). Further, in tetrapods, the fear response is typically mediated by the amygdala and hypothalamus. Fish do have a hypothalamus (e.g. Lohr & Hammerschmidt 2011), but they do not possess an amygdala; instead, they have a putatively analogous telencephalic brain region that appears to serve a similar function (dorsomedial telencephalon: e.g. Portavella et al. 2002). | Likely yes: octopuses, as well as other cephalopods (cuttlefish and squid), exhibit a range of stress or anxiety-like behaviours, particularly when kept in captivity. Autophagy, a form of self-cannibalism, which involves the animal eating their own arms, is commonly observed in octopuses when they are stressed*. Agitated swimming behaviours have been observed in stressed cuttelfish, whereby they repeatedly strike their head with the sides of the aquarium tank (Sherril et al. 2000). Agitated bobbing has been observed in both octopus and cuttlefish, whereby the head is moved from side to side or moved up and down (octopus: Boyle 1983; cuttlefish: pers. obs.). Stress-induced inking has been reported after shipping and handling of animals (Oestmann et al. 1997; Moltschaniwskyj et al. 2007; Bennett & Toll 2011). Following a rise in ammonia concentration, cuttlefish have been observed reaching over their dorsal mantle and performing a scratching-like behaviour. This is a behavioural indicator of stress or anxiety and can lead to skin damage. For octopuses, repetitive movements in one location such as performing swimming motions while attached to a tank wall can be a sign of stress (Fiorito et al. 2015). Moreover, reluctance to interact with humans should be a cause for concern as it deviates from an animal that is relaxed and habituated, thus reluctance to interact can be an indicator of stress or anxiety. *Note that Budelmann (1998) states stress contributes to autophagy but is not the primary cause. | In addition to the physiological information provided below, one study has found behavioural evidence of fear/anxiety like responses in caridean shrimp. It is possible that Penaediae shrimp would behave in the same way to the threatening stimulus used. Shrimp were exposed to a daily threatening net chasing treatment and both species tested displayed behavioural responses which are consistent with anxiety/fear-like behaviour. One shrimp species (Neocaridina denticulata ssp.) displayed more thigmotaxis (wall hugging) behaviour, whilst the other species (Palaemon pacificus) demonstrated greater escape responses (Takahashi 2022). It is difficult to differentiate between anxiety and fear responses in crustaceans. Here I report results that could also fall in the above category of ‘Fear like behavior’: a) L. vannamei: “Shrimp were stressed by transfer, chasing, and confinement and the responses were analyzed at several intervals. Lactate levels in hemolymph increased from 10 to 30 min, glucose increased at 60 min, and both returned to baseline levels by 240 min” (Aparicio-Simon et al 2010). b) An increase in glucose levels in penaeid shrimp hemolymph is a well-known stress response to a short term stressor, such as repeated sampling (Mercier et al 2006 , referencing Racotta and Palacios, 1998). c) Stressed shrimp from plastic tanks showed higher concentrations of glucose in hemolymph and higher concentrations of total lipids (Mercier et al 2006 and 2009). | The crab Carcinus maenas reacts to handling stress with an increase in oxygen consumption, haemolymph glucose and haemolymph L-lactate which is related to the magnitude of the stress (Wilson et al 2021). The crab C. pagurus showed an increase in blood glucose, total protein, and hemolymph density after transported in water when compared to transport in air, suggesting the first method is more stressful and that anxiety results in a change in hemolymph makeup (Lorenzon et al 2008). The same results were found for shore crabs that received a mild electric shock (Elwood and Adams 2015). These physiological results don’t necessarily indicate anxiety however one study on a shore crab from the Grapsidae family found that anxiety-like behaviour was significantly decreased by a high dose of fluoxetine (Hamilton et al. 2016). | Fossat et al (2014) demonstrated that after exposure to stress, crayfish (Procambarus clarkii) sustainably avoided illuminated arms of an aquatic maze. This behavior was abolished by the injection of the anxiolytic drug benzodiazepine. Additionally a study by Bacqué-Cazenave et al., (2017) found that potentially stressful social interactions to form a dominance hierarchy induced a level of anxiety-like behaviour in fight-losers which correlated with the stress intensity experienced during the interaction. Finally, Kamada & Nagayama (2021) found that “electrical shocks appeared to elicit serotonin-mediated anxiety since electrical shocks had no effect on mianserin-injected dominant animals. Serotonin of low concentrations mediated anxiety and stimulated forgetting of the winner effect. | Using the best criteria currently agreed on for assessing animal emotions, i.e., a suite of changes in physiology, behavior, and especially cognitive biases, they have shown that agitated bees display a negative emotional state. Although their results do not allow us to make any claims about the presence of negative subjective feelings in honeybees, they call into question how we identify emotions in any nonhuman animal. It is logically inconsistent to claim that the presence of pessimistic cognitive biases should be taken as confirmation that dogs or rats are anxious but to deny the same conclusion in the case of honeybees (Bateson et al., 2011). | Fruit flies avoid light areas and edges of arenas (e.g., more protected areas) and gamma-oryzanol, which is an anti-anxiety drug in vertebrates, reduces their anxiety-like light avoidance behaviors. However, other vertebrate anxiolytics did not have the same effect, so more research will be necessary. (Neckameyer & Nieto-Romero, 2015), (Araujo et al 2021), (Ramos-Hryb et al, 2021) | |||||||||||||||
40 | Associative learning from pain | Despite thousands of years of domestication (Giuffra et al., 2000), the pig is among the least examined of the mammalian species held by man, in terms of knowledge about causes and indicators of pain, which remain a challenge for the veterinary profession (Viñuela-Fernández et al., 2007). | Lame and sound broilers, selected from commercial flocks, were trained to discriminate between different coloured feeds, one of which contained carprofen. The two feeds were then offered simultaneously and the birds were allowed to select their own diet from the two feeds. In a second study, in which only one concentration of analgesic was used, lame birds selected significantly more drugged feed than sound birds, and that as the severity of the lameness increased, lame birds consumed a significantly higher proportion of the drugged feed vs the normal feed, indicating some associative learning (Danbury et al. 2000). | No studies of carp specifically could be found, but goldfish (Carassius auratus), a closely related cyprinid, can be classically conditioned using a noxious stimulus (a response that is modulated by anesthetic: e.g. Yoshida & Hirano 2010), learn to avoid areas that predict shock (e.g. Dunlop et al. 2006), can perform instrumental responses to avoid shock (e.g. escape responses become directed to particular locations in a shuttlebox: Gallon 1972), can be trace conditioned in response to an electric shock (e.g. Overmeier & Savage 1974, Vargas et al. 2009).), and can learn to jump over a hurdle to modify a conditioned stimulus (CS: lights that must either match or not), in order for this CS to predict no shock rather than shock (Zerbolio & Royalty 1983). There is no particular reason to expect that these are species-specific responses that would not be possible for cyprinids more generally. | No studies of Atlantic salmon specifically could be found, but rainbow trout (Oncorhynchus mykiss), a closely related salmonid, can learn to avoid areas that predict shock (e.g. Dunlop et al. 2006) and can be trace conditioned in response to a food reward given after a 3.4s delay post-presentation of a light stimulus (Nordgreen et al. 2010). There is no particular reason to expect that these are species-specific responses that would not be possible for salmonids more generally. | Octopuses are sophisticated learners and many traditional experiments have demonstrated that they can learn via negative reinforcement (e.g., electric shock, Boycott & Young 1957; Sutherland 1957; Young 1962; Mackintosh & Mackintosh 1963; Mackintosh 1964). More recent expeirments have shown that injured octopuses (injected with acetic acid) avoid chambers they associate witt the injury (Crook 2020). | One study found that shore crabs showed rapid discrimination between simultaneously presented shelters when one was consistently associated with an electric shock (Magee & Elwood 2013). However, in a subsequent similar experiment using sequential presentation of the shelters, the same authors found that crabs did not discriminate between the two shelters (Magee & Elwood 2016). | Despite their common use as model organisms in scientific experiments, pain and suffering in insects remains controversial and poorly understood. Here they explore potential pain experience in honeybees (Apis mellifera) by testing the self-administration of an analgesic drug. Foragers were subjected to two different types of injuries: (i) a clip that applied continuous pressure to one leg and (ii) amputation of one tarsus. The bees were given a choice between two feeders, one offering pure sucrose solution, the other sucrose solution plus morphine. They found that sustained pinching had no effect on the amount of morphine consumed, and hence is unlikely to be experienced as painful. The amputated bees did not shift their relative preference towards the analgesic either, but consumed more morphine and more solution in total compared to intact controls. While our data do not provide evidence for the self-administration of morphine in response to pain, they suggest that injured bees increase their overall food intake, presumably to meet the increased energy requirements for an immune response caused by wounding. They conclude that further experiments are required to gain insights into potential pain-like states in honeybees and other insects (Groening et al., 2017). One study found that honeybees were able to learn the association of a coloured light to avoid an electric shock (Kirkerud et al., 2017). Although it is not known whether the electric shock caused pain, it was certainly aversive demonstrated by the bees learning the task. | Adult fruit flies learn odor-shock associations in T-maze tests, and are above to avoid the odor that predicts shocks 95% of the time. They retain the association for at least 24 hours. Third instar fruit fly larvae are also capable of associative learning with pain. There are also widespread examples of operant conditioning, reversal learning, and trace conditioning with painful stimuli in adult fruit flies. Tully and Quinn, 1985; Quinn et al. 1974, Aceves-Piña and Quinn 1979; Khurana et al. 2012, Brembs, 2011; Brembs and Heisenberg, 2000; Heisenberg et al. 2001, Dylla et al. 2017; Galili et al. 2014; Shuai et al. 2011, Grover et al. 2022, McCurdy et al. 2021; Shuai et al. 2011; Tully and Quinn, 1985; Wu et al. 2012, Guo and Guo, 2005, Ren et al. 2012 | |||||||||||||||||
41 | Boredom-like behavior | It is known from several experiments that deprivation can originally lead to rise of plasma corticosteroid levels. But stereotypic behaviour such as chain-nibbling in pigs during food deprivation reduces the hormone levels considerably. As a result of these experiments it was concluded that circulating ACTH and corticosteroid levels are not sensitive to chronic stress (which boredom is considered to be). An essential characteristic of boredom in evaluating welfare is that it directly refers to the mental state of the animal and therefore directly implies suffering (Wemelsfelder, 1985). | The housing of broiler chickens in a relatively constant environment throughout their lifetime raises the question of whether the chickens’ well-being is compromised by boredom. After an initial period of exploration, chickens will habituate to stimuli in their housing environment that have no perceived positive or detrimental effects. In the absence of new sources of novelty, the environment becomes highly predictable and the chickens may no longer be stimulated to perform exploratory behaviour. If so, the lack of novelty may be associated with impaired brain development and boredom (Renner and Rosenzweig, 1987). | No studies of carp or any other fish species could be found. However, preliminary unpublished data from Lavery & Mason suggest that zebrafish housed long-term in barren tanks may be less anxious in the novel tank diving and light-dark preference tests than their counterparts housed with highly preferred environmental enrichment, possibly due to a lack of stimulation in their home tanks. Experimental work on zebrafish boredom is likely forthcoming in the next few years. Although there appears to be a growing interest in animal boredom, which is a potentially underappreciated welfare risk (e.g. Burn, 2017; Meagher, 2018; Fife-Cook & Franks, 2019), definitive experimental data is currently lacking in fish. | No studies of salmonids or any other related fish species could be found. Although there appears to be a growing interest in animal boredom, which is a potentially underappreciated welfare risk (e.g. Burn, 2017; Meagher, 2018; Fife-Cook & Franks, 2019), definitive experimental data is currently lacking in fish. | Lean yes: boredom-like behaviour in animals has been described as repetitive route tracing, constant attempts to break out of confinement, as well as destructive behaviour. Boredom-like behaviour has been described in cephalopods. Anderson (2005) described a bored octopus showed restless and destructive behaviour. Specifically, the octopus repeatedly attacked the tank by scratching the glass, aggressively moved rocks, would bite through nylon ties that held the water filter together and blew gravel around her tank. I have witnessed similiar behaviour in octopuses over my 12 years of working with cephalopods. Environmental enrichment is important for octopuses, it keeps them occupied and stimulated and thus less destructive activities are observed as well as less attempts to escape (Mather & Anderson 2007). Enrichement has also shown to be beneficial for common cuttlefish, Sepia officinalis. Providing environmental enrichment for cuttlefish results in increased learning ability (Dickel et al. 2000). | ||||||||||||||||||||
42 | Concept of death | Nothing found specifically about pigs, but Dr. Susan Monso wrote a nice review about this topic and I am just leaving it here, as I think it is important for the topic in general: contrary to what is often assumed by animal ethicists, the concept of death should not be viewed in binary terms. Possessing a concept of death is not an all-or-nothing matter but rather something that is subject to gradation. This becomes clear once we consider the case of human children, who do not acquire a concept of death over-night. In fact, the scientific consensus is that it takes them an average of 10 years to fully master the concept of death (Kenyon 2001), but we credit them with some understanding of death before they reach this stage. If we accept a gradation in the case of human children, we should also accept it in the case of animals. However, when animal ethicists describe the concept of death in terms as demanding as the understanding of “the possibility of the impossibility of one’s being” (Rollin 2015, p. 52; following Heidegger, [1927]1996), they are using as benchmark the (educated) adult human concept of death. This sets the stage in a biased way, and it is also to a certain extent arbitrary. This is because human adults’ concept of death is also limited (Monsó, 2022). | Nothing found specifically about chicken, but Dr. Susan Monso wrote a nice review about this topic and I am just leaving it here, as I think it is important for the topic in general. | Unknown: no published literature. The concept of death would be difficult to study as octopuses do not form strong social bonds with conspecifics and thus it would not be possible to investigate their reactions or behaviours surrounding the death of another. To study concept of death, one must distinguish whether an octopus can simply discriminate between dead or alive beings or whether they have a more complex conceptual understanding. A starting point would be to investigate a rudimentary concept of death: animal understands that death makes an individual non-functional and that its non-functional state is permanent. | ||||||||||||||||||||||
43 | Curiosity-like behavior | The only interesting paper I found was about curiosity in Zoo animals, but it doesn’t involve pigs (Glickman and Sroges, 1964). Another paper from Byrne 2013, is a general approach to think and maybe identify curiosity in animals (Byrne, 2013). | No studies of carp could be found. However, experimental work shows that simple neophilia (a simple form of curiosity) exists in two closely related species. For example, European minnows (Phoxinus phoxinus) have a strong propensity to inspect novel objects (Murphy & Pitcher, 1991) and when given the opportunity, zebrafish (Danio rerio) will readily inspect new spaces (Graham et al., 2018). These examples only show simple neophilia in these species rather than intrinsic information seeking (a higher-order of curiosity). Preliminary unpublished data from Franks, Gaffney, et al. represents the first research explicitly investigating curiosity in fish and suggests that in addition to being neophilic, zebrafish may also seek out specific information for their own sake (i.e. a higher order of curiosity). Thus, experimental work on zebrafish curiosity is likely forthcoming in the next few years. Note: though a form of curiosity, neophilia is simply the motivation to approach novelty, which can also be driven by the desire to avoid under-stimulation (Burn, 2017) rather than a proactive desire to gain information for its own sake. As such, it is important to distinguish simple neophilia from intrinsic information seeking, which can be considered a higher-order form of curiosity and has been associated with positive well-being in humans and other animals (Kashdan & Steger, 2007; Franks & Higgins, 2012). | Lean yes: no published literature on whether octopuses value non-instrumental information: information that reduces uncertainty about future events but cannot be used functionally to increase reward. Preferences for this type of information have been linked to human curiosity - an intrinsic desire to 'know'. However, octopuses are known for their play behaviour and show exploratory behaviour towards both natural and experimental objects, which has been likened to 'curiosity' (Mather 1994; Mather & Anderson 1999; Kuba et al. 2003; Kuba & Byrne 2006). | ||||||||||||||||||||||
44 | Depression-like behavior | Severely depressed pigs differ from robust pigs in several physiological parameters that may be important for gas euthanasia. Several causal factors could contribute to creating the depressed state, including disease, injury and underdevelopment. In this study, pigs classified as depressed or not did not differ in behavioural and physiological responses associated with efficiacy or distress when euthanized. However, with a small sample size, euthanasia of depressed pigs took longer and resulted in differences for distress indicators (Sadler et al., 2014). | Isolation from social companions in domestic fowl chicken, produced a robust distress vocalizations (DVoc) response in vehicle chicks. The rate of DVocs declined over the first 30 min of the test session to approximately 50% of the initial response rate and remained relatively stable thereafter. At the 5 min block, both chlordiazepoxide and imipramine attenuated DVocs. At the 20min block and beyond, however, where vocalization rates had declined, imipramine enhanced DVoc rates. During this same time period, chlordiazepoxide did not generally alter DVoc rates from that of isolated chicks (Sufka et al., 2006). When looking more closely at the pattern of DVoc rates over time and the differential effects of chlordiazepoxide and imipramine on DVoc rates, however, we suggest that this stress response may be better characterized as three distinct phases we describe as (i) an anxiety-like state, (ii) a transitional phase and (iii) a depressive-like state (Sufka et al., 2006). | No reports of depression-like behaviour could be found for carp, though they are behaviourally affected by antidepressants like fluoxetine (e.g. Orjes 2015). However, the closely related cyprinid, zebrafish (Danio rerio) is widely used as a model of human depressive disorders (e.g. Nguyen et al. 2014, Fonseka et al. 2016, Pittman & Piato 2017, de Abreu et al. 2018). | Shapouri (2020) has characterized a depression-like state in juvenile Atlantic salmon that can be reversed by treatment with busiprone. Further, behavioural inhibition typical of animal models of depression-like states has been observed in salmonids and “co-occurs with reduced neural plasticity and neuroendocrine alterations akin to brain remodeling seen in depression-like states in mammals” (Johansen et al. 2020). | Unknown: no reports of depression-like behaviour in octopuses. However, research on common cuttlefish, Sepia officinalis, has demonstrated that subjects exposed to environmentally relevant concentrations of antidepressants (i.e., fluoxetine) show cryptic and biochemical responses (Poi et al. 2014). Specifically, exposed subjects showed altered camouflage behaviours (i.e., less efficient at camouflage) and increased frequency of sand digging behaviours, which might make them more visible to predators. Moreover, fluoxetine appeared to influence dopaminergic activity. | Forced-swim tests reveal 'depression like' immobility in fruit flies. Vertebrate antidepressants (psilocybin, citalopram) reduced immobility in a fly strain genetically altered to have increased depression. Additional stressors (starvation, sleep deprivation) can also induce immobility in the forced swim test; the vertebrate antidepressant gamma-oryzanol reduced immobility in the flies under these conditions (Neckameyer & Nieto-Romero 2015), (Araujo et al, 2021). | |||||||||||||||||||
45 | Disgust-like behavior | It is not fully disgust, but in this study pigs kept in fresh air from weaning until test were generally less active and spent less time at the centre of the open field if the test was carried out in an ammoniated atmosphere rather than fresh air; this suggests that they found ammonia aversive (Jones et al., 2000). | Social learning in domestic fowl chicken to avoid food is likely to depend on the balance of selective pressures varying as a function of the toxicity and frequency of encounter of potential poisons, and on the likelihood of social interaction during or after a harmful encounter. It is noteworthy, then, that day-old chicks avoid pecking at an aversive stimulus after observing the disgust responses of another chick (Johnston et al. 1998). | |||||||||||||||||||||||
46 | Displacement behavior | The aim of the present study was to investigate whether straw provision in pigs increases positive welfare, and precisely, positive emotions, or decreases negative welfare, including negative emotions, or both. Concerning agonistic behaviour frequency and duration, as well as displacement activities frequency and duration, all were significantly lower in the straw session than in the control session (Marcet-Rius et al., 2019). | While pecking is a natural behaviour in chickens, e.g., of food, gently during allopreening or aggressively to demonstrate dominance, excessive feather pecking is a significant issue of concern in the chicken farming industry (Ferreira et al. 2021). It is multifaceted, for instance, (Jung and Knierim 2018) found 62 factors affecting the risk of feather plucking developing in a flock. For example, as a redirected foraging behaviour (Newberry et al. 2007), displacement behaviour (Zimmerman et al. 2000), or as a means of coping with stress, including pain, fear, and social stress (Cronin and Glatz 2021). Other displacement behaviours include stereotypic pacing (Zimmerman et al. 2000) or pecking at an empty feeder, with eight-week-old broiler breeders spending 50% of their time doing so (van Krimpen and de Jong 2014) likely relating to hunger and/or boredom. | There is evidence to suggest that pacific white shrimp are more susceptible to stress during pre- and post-moult phases (Wajsbrot et al. 1990) and one study found that the same species exhibit additional antennae wipes during the post-moult phase, which the authors suggest could be a reflection of stress (Bardera et al. 2019). | Bumblebees (Bombus terrestris) are believed to minimize travel distance and time while seeking foraging resources, and to memorize landmarks and return to forage patches visited earlier. Given these abilities, if a worker is displaced, will it switch to a new forage resource close by or will it navigate back to the original forage patch? To address this question they collected 210 Bombus vosnesenskii workers from an ornamental Spirea patch, marked them with numbered tags, transported them in a cooler, and released them at seven distances, from 1.5 km to 16 km, in each of two directions. Each worker that returned to the Spirea patch was recaptured, and re-released at its first release location. Over 8 observation days, 54 workers from 11 release locations returned to the Spirea patch. Of these, 16 were recaptured twice, 13 three times, 5 four times and 1 five times. Nine workers returned from release distances ≥10 km, including one from 16 km, despite the presence of multiple rewarding resources between the release location and the Spirea patch. Returns were rapid—three workers released up to 5 km away were recaptured within 4 h, while a worker from 13 km returned within 30 h of release. Wind direction, wind speed, and release direction had significant (P < 0.05) impacts on release-to-recapture-times. Also, workers returned significantly (P < 0.001) more quickly during subsequent trips compared to their first return. These findings highlight the ability of displaced bumble bee workers to travel long distances, and to navigate back to familiar forage patches (Rao et al., 2019). | |||||||||||||||||||||
47 | Effects on exploratory behavior from pain | Kluivers-Poodt and colleagues demonstrated an increase in pain specific behaviors (i.e. tail wagging, stiffness, and huddled up posture) immediately post- castration. These behaviors can be decreased when piglets receive analgesics such as meloxicam prior to castration (Kluivers-Poodt et al., 2013) | Hens were presented with drinking water ranging in temperature from 20 to 45°C, and their behaviour was investigated before and after partial beak amputation. Amputation resulted in significant behavioural changes with reductions in environmental pecking, beak wiping and head shaking. Pecking at water presented at 45°C, and drinking at all temperatures, were also reduced after amputation. These behavioural changes are interpreted as instances of guarding behaviour and hyperalgesia which persisted for 6 weeks, at least 3 weeks after the beak had healed. They provide evidence for possible chronic pain in birds following partial beak amputation (Gentle et al. 1990). | No studies of carp could be found, but some relevant ones exist for the closely related cyprinid, zebrafish (Danio rerio). After a painful procedure (fin clipping, PIT tagging, or injection with acetic acid), Deakin et al. (2019a) analyzed the “complexity of movement patterns” via the fractal dimension (FD) of zebrafish 3D swimming trajectories. The FD did not differ between sham-handled and undisturbed controls, but was reduced in complexity in treated groups. Further, the FD of fish injected with different concentrations of acetic acid decreased in complexity with increasing acid strength. A similar study by Deakin et al. (2019b) used automated recording to examine tank exploratory behaviour after a painful procedure (fin clipping, PIT tagging, or injection with acetic acid), finding that fin clipped and acid injected fish explored significantly less than untreated controls and sham-handled fish. | No studies of Atlantic of Pacific salmon could be found. In the closely related salmonid, rainbow trout (Oncorhychus mykiss) Sneddon et al. (2003) found that untreated fish exhibited neophobia when presented with a novel object: “a classic fear response”, moving away from the object and experiencing an increased opercular beat rate in its presence. In contrast, noxiously stimulated trout spent most of their time in close proximity to the novel object and showed no additional increase in respiration rate to novel object presentation. Importantly, noxiously stimulated fish experienced neophobia at almost normal levels when treated with morphine. | Likely yes: octopuses have been observed withdrawing and reducing exploratory behaviour when exposed to noxious stimuli. Specifically, octopuses moved to the top of their tank after exposure to hermit crabs with stinging anemones on their shells (Ross 1971). Other research shows that octopuses avoid places where they previously experienced a negative stimulus, even if they are free from pain in the current moment (Crook 2020). | Despite their common use as model organisms in scientific experiments, pain and suffering in insects remains controversial and poorly understood. Here they explore potential pain experience in honeybees (Apis mellifera) by testing the self-administration of an analgesic drug. Foragers were subjected to two different types of injuries: (i) a clip that applied continuous pressure to one leg and (ii) amputation of one tarsus. The bees were given a choice between two feeders, one offering pure sucrose solution, the other sucrose solution plus morphine. They found that sustained pinching had no effect on the amount of morphine consumed, and hence is unlikely to be experienced as painful. The amputated bees did not shift their relative preference towards the analgesic either, but consumed more morphine and more solution in total compared to intact controls. While our data do not provide evidence for the self-administration of morphine in response to pain, they suggest that injured bees increase their overall food intake, presumably to meet the increased energy requirements for an immune response caused by wounding. They conclude that further experiments are required to gain insights into potential pain-like states in honeybees and other insects (Groening et al., 2017). | |||||||||||||||||||
48 | Embarrassment-like behavior | |||||||||||||||||||||||||
49 | Emotional contagion | During anticipation of the aversive event, naive pigs tended to show more tail low. During the aversive event, naive pigs tended to defecate more, while they played more during the rewarding event. These results suggest that pigs might be sensitive to emotional contagion, which could have implications for the welfare of group-housed pigs (Reimert et al., 2013). | Chicks appear to be aware of conspecific affective states, as well as their own, such as showing a higher stress response when conspecifics are handled roughly then handled gently (Nakamori et al. 2013). Hens show behavioural and physiological responses to their chicks’ mild distress (Joanne L. Edgar et al. 2012). However, outside of the mother-offspring bond, one study found no evidence that hens show emotional empathy when observing adult conspecifics. Specifically, “despite showing signs of distress in response to an aversive stimulus directed at themselves… observer hens showed no behavioural or physiological responses to mild distress of a familiar adult conspecific” (Edgar et al. 2012), Further studies however, have found "the co-occurrence of socially-mediated behavioural and physiological arousal and contagion; component features of emotional contagion in 9 week old unrelated domestic chicks (Edagar & Nicol 2018). | No studies for carp could be found. However, recent evidence in zebrafish (Danio rerio), a closely related cyprinid, has shown that emotional contagion may extend to the fish taxon. For instance, Oliveira et al. (2017) and Silva et al. (2019) registered the behavioral changes triggered in zebrafish when visually exposed to antipredator behaviors of other conspecifics. These displays induced antipredator reactions in observers similar to those of demonstrators (e.g., freezing, increased swimming speed, diving to the bottom) and observers also showed increases in cortisol levels (Oliveira et al., 2017). The responses of zebrafish were also influenced by familiarity and they responded more strongly when observing a distressed familiar fish than when observing an unfamiliar demonstrator (Silva et al., 2019). Most recently, Lombana et al. (2021) found that Citalopram (an anti-anxiety medication) administration consistently reduced behavioral anxiety of a treated individual zebrafish, in the form of reduced geotaxis, and this behavioral pattern readily generalized to untreated zebrafish subjects. It was found that the transfer of emotional contagion was directional in zebrafish, whereby the treated individual influenced untreated subjects, but not vice-versa (Lombana et al., 2021). | ||||||||||||||||||||||
50 | Emotional reactions to learning | During anticipation of the aversive event, naive pigs tended to show more tail low. During the aversive event, naive pigs tended to defecate more, while they played more during the rewarding event. These results suggest that pigs might be sensitive to emotional contagion, which could have implications for the welfare of group-housed pigs (Reimert et al., 2013). | One study exxamined frustration-related repsonses of chickens during discrimination learning tasks (Khune et al. 2013). They found that " different discrimination-learning tasks appear to call upon the occurrence of frustration-related behaviours to a different extent. The frequency and duration of particular species-typical frustration-related behaviours differs within discriminatory learning and among individuals". | Lean yes: during anticipation of a negative event octopuses tended to cower away. Specifically, octopuses ceased to attack hermit crabs that had a stinging anemone on their shell. They approached cautiously after an initial attack and when their arm came into contact with the anemone, they would pull it away quickly. After 24 hrs of exposure, the octopus would shrink away and move to the top of the tank when the hermit crab approached (Ross 1971). There is no published literature demonstrating whether octopuses show emotion in response to a positive event. | ||||||||||||||||||||||
51 | Envy-like behavior | |||||||||||||||||||||||||
52 | Exhaustion-like behavior | When pigs are stress-challenged during transport, unloading and presentation for slaughter there are a number of visual indicators. Open mouth breathing (dyspnea) is a behavioural sign of acute exercise challenge and reflects increased oxygen demand of exercise in the normally sedentary pig. Early signs of fatigued pigs are muscle tremors and a reluctance to move. Although comprehensive data is lacking, it appears that further excitement or exercise demands to a fatigued or exercise stressed pig result in a more severe compromise of the individual, marked by voluntary recumbency, dyspnea, alternating irregular blanched and reddened areas on the skin, increased body temperature and the development of acute metabolic acidosis (Benjamin, 2005). Half the animals were transported in their social groups (unmixed condition) and half were transported with groups of previously unfamiliar pigs mixed together (mixed condition). Behaviour was recorded, a general activity index scored and saliva samples taken at different stages of the journey for analysis ofcortisol. Pigs spent most of their time standing in both conditions. The journey was very rough (as revealed by characterization with an accelerometer) and in the unmixed condition the pigs appeared to stand to reduce travel sickness. In contrast, in the mixed condition, this preference for standing seemed to be due to fighting which stressed and exhausted the animals (the general activity index was three times the unmixed condition). Levels of salivary cortisol were higher in the mixed condition at the beginning, middle and end of the journey (Bradshaw et al., 1996). | Heat stress and exhaustion is one of the top causes of chicken death. For those new to backyard chicken farming, it is important you learn to recognize the signs of this serious condition and how to keep your chickens cool and hydrated. Chicks, especially, need extra attention to help them remain healthy. For a flock of laying hens, knowing how to prevent heat exhaustion and treat a chicken suffering heat exhaustion is important to preserving their health and the health of their eggs. Once your chicks are old enough to move outdoors, remain vigilant for signs of heat stroke, especially if it’s mid to late summer. Heat stress comes on quickly so it is important to watch them closely. Even older birds need supervision during the hot summer months (Dayyani and Bakhtiari, 2013). Laying hens are susceptible to heat exhaustion. Water is the main content of an egg. Laying eggs requires a lot of fluids so keeping your hens hydrated and comfortable is important (Boissy et al., 2007). | A few studies have used carp to investigate the physiological consequences of exhaustion and have focused on prolonged swimming to the point of exhaustion. As with salmonids, the methods used to exercise carp to exhaustion include chasing them (e.g. Cyprinus carpio, Knudsen & Jensen, 1998; Carassius auratus and Ctenopharyngodon idellus, Fu et al., 2009), putting them in swim chambers (e.g. C. carpio, Hallman et al., 2008; Hypophthalmichthys molitrix; Ke et al., 2012; Mylopharyngodon piceus; Pang et al., 2016), and angling them (e.g. C. carpio, Rapp et al., 2012). Exhaustive exercise results in glycogen depletion and lactic acid accumulation (Knudsen & Jensen, 1998). | The vast majority of studies investigating the physiological consequences of exhaustion have used rainbow trout (Oncorhynchus mykiss) and have focused on prolonged swimming to the point of exhaustion (Milligan, 1996). The most commonly used method to exercise rainbow trout to exhaustion is to chase them around a tank for a fixed period of time (5-10min) (e.g. McDonald et al., 1998; Milligan et al., 2000). Another method is to exercise salmonids to exhaustion is by forcing them to swim against a current in a swim tunnel until they are no longer able to maintain their position (35-40min) (e.g. O. tshawytscha, Gallaugher et al., 2001; O. nerka and O. kisutch, Lee et al., 2003). A third method used to exhaust salmonids is angling them at the end of a hook and line (1-2 min) (e.g. O. kisutch, Farrell et al. 2001; Salvelinus fontinalis, Brownscomb et al., 2017). Each method of exhaustive exercise results in similar types of metabolic and acid-base disturbances in salmonids including glycogen depletion and lactic acid accumulation that may take several hours to restore and recover from (Parkhouse et al., 1988; Kieffer, 2000). Atlantic salmon (Salmo salar) have also been shown to reach exhaustion faster with high density loads of salmon lice (Lepeophtheirus salmonis) during swim tests (Bui et al., 2016). Exhaustion behavior has been used as a term to describe the clinical signs of an outbreak of piscine orthoreoviruses (PRVs) in farmed Atlantic salmon and rainbow trout (Adamek et al., 2019). | Likely yes: octopuses and other cephalopods often enter a period of fasting during breeding (Hanlon & Messenger 2018). During this time, individuals will catabolise their own body proteins. As such, reproductive periods are shortly followed by death for many species. In dumpling squid, research shows that mating effects physical performance post-copulation, suggesting that squid experience exhaustion-like behaviour after mating (Franklin et al. 2012). Outside of mating, energetics research demonstrates that locomotion is much more costly for cephalopods than fishes (O'Dor 2002). For octopuses, Octopus vulgaris, who are often observed 'walking' across substrate, the cost of walking has been compared with the cost of jet-propelled swimming in squid (Wells et al. 1983). These early experiments showed that octopuses were reluctant to keep moving after one hour on a 'treadmill' at 0.34km, despite exposure to electric shocks. This suggests that octopuses experienced exhaustion-like behaviour. Moreover, after an hr of forced walking, octopuses appeared pale and flaccid and were breathing deeply and rapidly (Wells et al. 1983). | Physical and behavioural exhaustion has been demonstrated in the whiteleg shrimp (Litopenaeus vannamei). The escape response (tail-flipping) was repeatedly elicited by prodding shrimp with a stick until no further response was recorded (Robles-Romo et al. 2016). Shrimp reached fatigue after 31 tail flips, which corresponded with a 75% reduction in abdominal muscle arginine phosphate level and an 18% reduction in adenylic energy charge. They also found a 5x increase in hemolymph lactate level and a 2.7x increase in glutathione peroxidase. Levels recovered after 1 hour. | One study found that a sublethal exposure to cadmium caused initial hyperactivity in Procambarus clarkii, which subsequently “exhausted” their hyperactive response (Misra et al. 1996). Another study measured tail flipping behaviour to exhaustion in Cherax destructor (family Parastacidae) (Baldwin et al. 1999). | One study looked at whistling behaviour (thought to be a defensive mechanism) of walnut sphinx caterpillar in the Bombycoidea superfamily and found that some caterpillars regurgitated after prolonged predator attacks, which the authors suggest may be due to exhaustion or stress (Bura et al. 2011). | |||||||||||||||||
53 | Fear-like behavior | They measured brain neurotransmitters in pigs classified as fearful-nonfearful under stressful handling.Stressful handling alters the 5-HT system in the hippocampus and the amygdala. There was no difference between fearful and non-fearful pigs under non-stressful handling. The 5-HT pathway is activated in the hippocampus under stressful handling only in fearful pigs. In conclusion, the existence of an underlying biological trait - possibly fearfulness - may be involved in the pig's response toward stressful challenges, and the serotonergic system seems to play a central role in this response. Highest concentrations of NA were found in the hypothalamus. The concentration of DA and its metabolites DOPAC and HVA were found to be highest in the amygdala and hypothalamus. The ratio DOPAC/DA and HVA/DA was highest in the PFC (Arroyo et al., 2016). | Hens can “learn to avoid being frightened”. For example, 15 hens were presented with a two-compartment shuttle box, each containing a balloon. The birds were given a fright by rapidly inflating the balloon in front of one compartment and a small signal (light) was displayed 20 seconds before inflating. All hens learned quickly to move to the second compartment before the balloon was inflated i.e., they paired the stimulus (light) with the response (balloon inflating). Their fear responses, such as alarm calls, reduced over subsequent trials, indicating “are not simply acting reflexly when they get a fright” (Duncan and Petherick 1991). Maternal effects can have a buffering effect on chick fearfulness (Freire, 2020). For example, hens increased vocalisations and walking, while they decreased preening, when their chicks were threatened (e.g., a cue, such a light or sound, indicating a puff of air would be delivered), though only when the chicks were naive to the cue suggesting the hens’ response is not driven only by the chick’s behaviour (Edgar et al. 2013). Juvenile red junglefowl that were more fearful in a tonic immobility test (both as juveniles and adults) were quicker to change their responses to a previously unrewarded stimulus once it became unrewarded, i.e., a measure of behavioural flexibility (Zidar et al., 2017). Red junglefowl score higher than white leghorn chickens on measures of fearfulness and take longer to feed in a “fear of humans” test, suggesting low fearfulness may be a result of domestication (Campler et al. 2009). | A few studies of fear in carp exist, largely focused on the cyprinid-conserved escape responses observed in response to conspecific alarm pheromones (e.g. Stabell et al. 2010). However, a significant number of studies have investigated fear behaviour in two closely related cyprinids: goldfish (Carassius auratus) and zebrafish (Danio rerio). Both species exhibit a range of fear-related behaviours such as freezing, zig-zagging, “erratic” movement, and tightened shoaling (e.g. Kalueff et al. 2013). The fear response in cyprinids can also mediate learning: for example, zebrafish exhibit place avoidance learning from exposure to conspecific alarm pheromones (e.g. Maximino et al. 2018), active avoidance of electric shock in a shuttlebox (e.g. Xu et al. 2007), and contextual fear conditioning (Kenney et al. 2017). These are just a few illustrative examples of many in the published literature on zebrafish and goldfish. Further, in tetrapods, the fear response is typically mediated by the amygdala and hypothalamus. Fish do have a hypothalamus (e.g. Lohr & Hammerschmidt 2011), but they do not possess an amygdala; instead, they have a putatively analogous telencephalic brain region that appears to serve a similar function (dorsomedial telencephalon: e.g. Portavella et al. 2002). | Reports of fear in salmonids occur in the scientific record as early as 1961 (e.g. Geller & Brady 1961). According to Chandroo et al. (2004), “Fear in fish has been characterised through branchial responses, alarm pheromone-initiated responses and aversive behavioural reactions.” Several fear-like behaviours have been identified during exposure to threats, such as freezing (e.g. Demuth et al. 2017), escape responses (e.g. frantic and rapid swimming behaviors and sometimes collisions into the sides of the tanks; e.g. Jackson & Brown 2011, Nilsson et al., 2019), and accelerations in response to sudden movements in the environment (e.g. Colson et al. 2015). These are just a few illustrative behavioural examples of many, and more are reviewed by Chandroo et al. (2004). The fear response in salmonids can also mediate learning: for example, fear conditioning is a common experimental paradigm (e.g. Yue et al. 2004, Demuth et al. 2017). Further, in tetrapods, the fear response is typically mediated by the amygdala and hypothalamus. Fish do have a hypothalamus (e.g. Lohr & Hammerschmidt 2011), but they do not possess an amygdala; instead, they have a putatively analogous telencephalic brain region that appears to serve a similar function (dorsomedial telencephalon: e.g. Portavella et al. 2002). | Octopuses perform a range of behaviours that are indicative of fear. If octopuses spend an extended amount of time in a defensive posture i.e., arms curled over the body, this is an indication that the animal is fearful or threatened (Fiorito et al. 2015). Inking is a defensive response in cephalopods, so inking should be an indcator that the animal perceives a threat or is stressed. Notice that inking does not necessarily result from the animal receiving a presumed noxious stimulus like an electric shock. Thus, absence of inking should not be interpreted as an absence of fear, anxiety or distress. Intramantle inking has been reported as a post-transport stress behaviour in Octopus bimaculoides (Bennett & Toll 2011). Inking is an alarm signal and can cause stress to neighbouring conspecifics. All cephalopods use expulsion of water from the mantle via the siphon during breathing and locomotion, and this is particularly noticeable in the jetting escape reaction, which occurs when an octopus feels threatened and is attempting to escape. Zarella et al (2015) report that Octopus vulgaris possess a range of genes that increase or decrease in expression in response to fear conditioning (learned fear) and in response to social interaction (innate fear)* (incl. stathmin, tyrosine hydroxylase, dopamine transporter, octopressin cephalotocin). *Should be considered a welfare issue if farmed octopus are housed together. | In addition to the physiological information provided below, one study has found behavioural evidence of fear/anxiety like responses in caridean shrimp. It is possible that Penaediae shrimp would behave in the same way to the threatening stimulus used. Shrimp were exposed to a daily threatening net chasing treatment and both species tested displayed behavioural responses which are consistent with anxiety/fear-like behaviour. One shrimp species (Neocaridina denticulata ssp.) displayed more thigmotaxis (wall hugging) behaviour, whilst the other species (Palaemon pacificus) demonstrated greater escape responses (Takahashi 2022). It is difficult to differentiate between anxiety and fear responses in crustaceans. Here I report results that could also fall in the above category of ‘Fear like behavior’: a) L. vannamei: “Shrimp were stressed by transfer, chasing, and confinement and the responses were analyzed at several intervals. Lactate levels in hemolymph increased from 10 to 30 min, glucose increased at 60 min, and both returned to baseline levels by 240 min” (Aparicio-Simon et al 2010). b) An increase in glucose levels in penaeid shrimp hemolymph is a well-known stress response to a short term stressor, such as repeated sampling (Mercier et al 2006 , referencing Racotta and Palacios, 1998). c) Stressed shrimp from plastic tanks showed higher concentrations of glucose in hemolymph and higher concentrations of total lipids (Mercier et al 2006 and 2009). L. vannamei: “Shrimp showed a pause in heart rate with a sensory stimulus which was likely perceived as threatening (tail pinching)” (Weineck et al, 2018). | The crab Carcinus maenas reacts to handling stress with an increase in oxygen consumption, haemolymph glucose and haemolymph L-lactate which is related the magnitude of the stress (Wilson et al 2021). In another study, the same species were found to choose a normally not preferred shelter (with light) in order to avoid an electric shock (Magee and Elwood, 2013). A study found that the mud crab (Panopeus herbstii) in presence of predators, presents less behavioral variability even when other important factors such as hunger were accounted for (Toscano et al, 2014). The mud crab, Panopeus herbsti reduces its activity levels and increases its refuge use in the presence of predator cues, suggesting that choice of refuge is the consequence of fear (Belgrad et al, 2016). | Although not specifically stated as fear-like behaviour, crayfish seek shelter for moulting in the presence of a fish predator (Hartman & O’Neill 1999). Additionally, crayfish altered several types of resource-use decision-making in the presence of predatory odours, suggesting that they “respond to multiple aspects of a predatory threat” (Wood & Moore 2019). One study also found physiological indicators of handling stress in Astacus leptodatylgrus (family Astacidae) (Gulec & Asku 2012). A study used fear cues in rusty crayfish to examine the decisions they made when given a choice of accessing a burrow in the presence of a fear-inducing odour (MacKay et al. 2021). | One study on the fear behaviour of the african honey bee found that "when balancing food quality against multiple threats (sweeter food corresponding to higher danger), colonies exhibited greater fear than individuals. Colonies decreased foraging at low and high danger patches. Individuals exhibited less fear and only decreased visits to the high danger patch" (Tan et al. 2013). | Drosophila displayed "responses to repetitive visual threat stimuli which may express an internal state exhibiting canonical emotion primitives, possibly analogous to fear in mammals" (Gibson et al. 2015). | |||||||||||||||
54 | Flexible self-protective behavior | Available scientific information about wallowing was systematically described in relation to 10 so-called weighting categories identified in semantic modelling (pain and illness, survival/heat stress, fitness, stress, aggression, abnormal behaviour, frustration, natural behaviour, preferences and demand). The welfare importance of wallowing was assessed by tentatively comparing it to several other welfare attributes, such as food, foraging substrate, social contact and non-castration. This leads to the suggestion that wallowing is important for pig welfare because of its multifaceted nature and hence, could count as self-protective behaviour (Bracke, 2011; Bracke and Spoolder, 2011). | The beak notonly serves to grasp and manipulate food items, but is also used to manipulate non-food objects in nesting and exploration, drinking, and preening. It is also used as a weapon in defensive and aggressive encounters. At the end of the beak is a specialized cluster of highly sensitive mechanoreceptors, called the bill tip organ, which allows chickens to make fine tactile discriminations (Gentle and Breward 1986). Needless to say, damage to the beak is intensely painful, as partially debeaked chickens show asignificant increase in guarding behavior, i.e., tucking the bill under the wing, and diminished use of the bill for pecking and preening after the procedure. These pain-related behaviors may continue for months (Duncan et al. 1989). | One study of common carp (Cyprinius carpio) shows that when their lips are injected with 5% or 10% acetic acid (as compared to a sham, saline-injected control group of fish), 2 of the 5 study fish exhibited “anomalous” behaviours including rubbing their lips on the tank walls and swimming off balance/losing equilibrium (Reilly et al. 2008). The study also demonstrates that these behaviours decreased in prevalence with time post-injection. Studies of a closely related species, zebrafish (Danio rerio), suggest that injection in the tail with 1% acetic acid causes similarly anomalous behaviours like tail-beating (Maximino 2011). However, Reilly et al. (2008) do not observe anomalous behaviours when zebrafish are injected with 5% or 10% acetic acid in their lips. | To date, there exist no studies of Atlantic or Pacific salmon examining self-protective or “anomalous” behaviours in response to noxious stimuli. However, two studies of very closely related rainbow trout (Oncorhynchus mykiss) indicate that, when their lips are injected with 5% or 10% acetic acid (as compared to a sham, saline-injected control group of fish), they rock side to side on the bottom of the tank and rub their lips in the gravel substrate (Reilly et al. 2008, Sneddon 2003). However, Newby & Stevens (2008) did not observe any of these “anomalous” rocking/rubbing behaviours in a similar study of rainbow trout that attempted to replicate Sneddon (2003)’s findings, and a study from Mettam et al. (2011) expected to see anomalous behaviours in response to acetic acid injection decrease after administration of an analgesic, but report no anomalous behaviours whatsoever. | There is strong evidence of wound-grooming and guarding in octopuses. Alupay et al. (2014) reported that algae octopus, Abdopus aculeatus, ink and jet at the onset of injury to an arm and immediately groom their wound. 4/5 of the injured octopuses responded with induced autotomy (i.e. voluntary amputation) of the injured arm. For e.g. injured octopuses held the wound site in their beak for approx. 10 mins and kept the injured area close to their body; 3 subjects wrapped their uninjured arms around the injured arm. Control sham-treated subjects (n = 4) did not show grooming or guarding behaviour. Another study (Polglase et al. 1983) on the lesser octopus (n = 12), Eledone cirrhosa, found that injured octopuses tended to their wound sites by stroking the tip of an arm across the injury. However, this study did not report whether control sham-treated subjects were included. A recent study (Crook 2020) found that Bock's pygmy octopuses, Octopus bocki, injected with acetic acid groom the site by stripping away some of the skin as if to scrape away the noxious stimuli. Several studies on different octopus species suggest that subjects exhibit self-protective behaviour when exposed to hermit crabs that have stinging anemones on their shells (Polimanti 1910; Boycott 1954; Ross 1971; Hand 1975; McClean 1983; Brooks 1988). However, it's difficult to determine whether such behaviours are enforced through negative reinforcement or involve centralised representation of the location of the injury that induces centralised self-protective behaviour. Note that common octopuses, Octopus vulgaris, show reflexive withdrawal in response to noxious stimuli without reference to the brain (Hague et al. 2013). Self-protective behaviour has also been reported anecdotally (I. Gleadall, cited in Andres et al. 2013, reports observed wound-tending behaviour in octopuses that had received surges to the optic capsule or cranium; G. Fiorito reported that octopuses guard sites of injury post-surgery). | Like some other decapod species, penaeid shrimp possess “characteristic setal brushes on the first cheliped for cleaning the chemotactile antennular flagella” (Bauer 1981) and grooming behaviour has been extensively documented in caridean shrimp, which serves to prevent fouling of the body (Bauer 1975; 1977; 1978; 1979). One study on Hawaiian river shrimp (Caridea: family – Palaemonidae) found that the grooming time budget was 24.7%, indicating the importance of the behaviour for maintenance and protection from disease. Diarte-Plata et al. (2012) investigated the response of Macrobrachium americanum shrimp (family: Palaemonidae) to eyestalk ablation and found that the majority of shrimp rubbed the wounded eyestalk. A study on the rockpool prawn (Palaemonide) found that noxious stimuli elicited a targeted antennal grooming and rubbing response, which was inhibited by benzocaine (anaesthetic) (Barr et al. 2008). However, the one study on a Penaeid species Puri & Faulkes (2010) failed to find evidence of a change in grooming or rubbing in response to the same noxious stimuli. | Shore crabs which had a claw twisted off (as is common practice in some fisheries) seemingly held their remaining claw over the wound during interactions with conspecifics and were less likely to engage in competitive interactions (McCambridge et al. 2016). The same species use their claws to wipe or rub the mouthparts, when brushed with acetic acid (Elwood et al. 2017). Again, in shore crabs formalin injection into the claw resulted in flexion, extension, shaking and rubbing of the affected claw in the 1-3 min after injection (Dyuizen et al. 2012). Disorientation and aggressiveness increased in Callinetctes arcuatus following unilateral eyestalk ablation (Vargas-Téllez et al. 2021). | One study found that grooming increased following ablation and cauterisation marking techniques in white-clawed crayfish (McFarlane et al. 2019). One study failed to find evidence of self protective behaviour to extreme PH in Procambarus clarkii (Puri & Faulkes 2010). However, in this research, the effect of an inflow of water "conditioned" by the presence of crayfish in head tanks on the behavior of solitary male crayfish was observed. | Some worker honeybees respond to major disturbances of the colony by flying around the assailant and possibly stinging; they are a subset of the bees involved in colony defense. These defenders have an open-ended age distribution similar to that of foragers, but defensive behavior is initiated at a younger age than foraging is. Behavioral and genetic evidence shows that defenders and foragers are distinct groups of older workers. Behaviorally, defenders have less worn wings than foragers, suggesting less flight activity. Genetically, defenders differ in allozyme frequencies, demonstrating different subfamily composition from foragers in the same colony. They also differ in allozyme frequencies from guards in the same colony, providing further evidence for division of labor associated with colony defense. They use this information to develop a model for honey bee colony defense involving at least two distinct groups of workers and they propose that the non-guard defenders be called “soldiers”, due to their important role in colony defense (Breed et al., 1990, 2004). As there are also some genetic differences in defender bees, and they are defending the whole nest, so not sure I would count this as flexible self-protective behavior, then again we know from (Loukola et al., 2017) that unprecedented cognitive flexibility can occur swiftly in bumblebees. | No studies on flexible self-protective behaviour found in bombycidae. In a study on the defensive response of larval Manduca sexta the authors noted that following a noxious mechanical poke “in some of these cases, the animal later brought its head slowly up to the wound and displayed grooming-like behavior for several seconds, with its open mouthparts repeatedly contacting the wound” (Walters et al. 2001). As Manduca sexta are in the superfamily Bombycoidea, it is possible that the silkworm with a similar anatomy is also capable of displaying wound-grooming behaviour. | |||||||||||||||
55 | Friendship-like behavior | The effects of familiarity and relatedness on agonistic pair relationships (dyads) in different pen regions (pen area or trough area) were studied in 16 groups of newly mixed domestic pigs of similar weight (9 pigs per group) at an age of 12 weeks. The agonistic interactions (AI) within 124 familiar (related) and 452 unfamiliar (related and unrelated) dyads were continuously recorded for 3 days (10 h daily) after mixing. Whereas pigs, both in dyads familiar and unfamiliar to each other, showed the same frequency of AI in the trough area, unfamiliar dyads exhibited significantly more AI in the pen area than familiar dyads. The relatedness of unfamiliar dyads had apparently no influence on AI. It is discussed that, besides establishing a dominance hierarchy, pigs react aggressively on strange subjects. Furthermore, the results are briefly discussed with reference to dominance and resource usage in pigs (Ewbank and Meese, 1971). In this study they conclude, socio-positive behaviours were more prevalent than socio-negative behaviours overall, supporting that positive social interactions may be an important but overlooked aspect of social life. Groups of littermates did not show more positive social behaviour than mixed groups, but they did show less mounting behaviour and seemed less affected by the stress caused by weaning (Camerlink et al., 2021). | No studies on carp could be found. However, affiliative behaviors in zebrafish (Danio rerio), a closely related cyprinid, have been described and are typically measured through group cohesion and coordination of swimming movements (Miller & Gerlai, 2012). Prolonged exposure to chronic stress has been linked with low levels of group cohesion in zebrafish (Saszik & Smith, 2018) and manual tank cleaning has been shown to increase stress and decrease the group cohesion and coordination of zebrafish (Powell et al., 2021). As well, access to a free-choice exploration opportunity is associated with high levels of shoal cohesion and coordination in zebrafish (Graham et al., 2018). | |||||||||||||||||||||||
56 | Guilt-like behavior | |||||||||||||||||||||||||
57 | Helping behavior | Some pigs are also more socially motivated than others (Hemsworth et al., 2011), but whether these pigs are more prosocial remains to be investigated, according to a review by (Rault, 2019). There is one study on helping behaviour in the warthog, during cooperative breeding strategies (White & Cameron 2011). | Nicol and Pope (1994) trained chicks that one of two differently coloured foods was palatable, while the other was not, with the mother hen being trained on the reverse colour combination. The hen showed increased food pecking, ground pecking and scratching when observing chicks pecking from the food that she had learned was unpalatable. These findings suggest hens adjust their behaviour flexibly depending on context, in this case, in assisting chicks learn what is safe to peck (Nicol and Pope 1994). Helping behaviour has been observed in other bird species, such as cooperative breeders. For example, in long-tailed tits, the degree of helping behaviour was influenced by nest predation and during shorter breeding seasons (Hatchwell et al. 2013). There is evidence of cooperative courtship in male turkeys, even unrelated males (Krakauer 2005). The author suggests that "Subordinate (helper) males do not themselves reproduce, but their indirect fitness as calculated by Hamilton's rule more than offsets the cost of helping). | There are no reports of octopuses helping conspecifics and reports are unlikely because octopuses do not live in social groups and do not form strong social bonds with conspecifics. There are reports of the day octopus, Octopus cyanea, cooperatively hunting with various fish species. However, this cannot yet be labelled as 'helping' without further investigation into the mechanisms behind the collaboration. | There is evidence of large male fiddler crabs (family Ocypodidae) assisting their smaller neighbours to defend their territories when potentially threatened by intruders (Bolton et al. 2011). However, due to their swimming nomadic nature, the social behaviour of Portunidae is likely to be different to Ocypodidae. | There is evidence of mother-offspring recognition and kin preferential helping behaviour in Orconectes limosus, with mothers offering extended protection to juveniles from cannibalism and predation (Mathews 2011). There is no evidence of helping behaviour in non-kin. | Social insect colonies represent distinct units of selection. Most individuals evolve by kin selection and forgo individual reproduction. Instead, they display altruistic food sharing, nest maintenance and self-sacrificial colony defence. Recently, altruistic self-removal of diseased worker ants from their colony was described as another important kin-selected behaviour. Here, they report corroborated experimental evidence from honey bee foragers and theoretical analyses. They challenged honeybee foragers with prolonged CO2 narcosis or by feeding with the cytostatic drug hydroxyurea. Both treatments resulted in increased mortality but also caused the surviving foragers to abandon their social function and remove themselves from their colony, resulting in altruistic suicide. A simple model suggests that altruistic self-removal by sick social insect workers to prevent disease transmission is expected under most biologically plausible conditions. The combined theoretical and empirical support for altruistic self-removal suggests that it may be another important kin-selected behaviour and a potentially widespread mechanism of social immunity (Rueppell et al., 2010). | |||||||||||||||||||
58 | Hyperalgesia | Review about pig pain describes hyperalgesia: increased pain due to stimulation of damaged tissue by a stimulus that would normally be perceived as painful. The stimulation would normally be painful, but it is felt as more painful than it would be if the tissues were not damaged. It is a clinical sign of peripheral and central sensitisation (Steagall et al., 2021). Models of inflammatory hyperalgesia have been applied to pig skin to determine the occurrence of local sensitisation. Irradiation of the skin with UVB- light resulted in a decrease in response latencies, suggesting that the porcine inflammatory response is homologous with the process observed in humans. In conclusion the study suggests that behavioural recordings are a valid tool for the assessment of thermal hyperalgesia following UV-B inflammation in porcine skin, but they were not capable of providing a clear indication of the development of mechanical hyperalgesia (Di Giminiani et al., 2014). | Recent research in this laboratory has identified a biological model in which morphine produced a hyperalgesic response to a noxious thermal stimulus. Morphine effects, however, were examined at only one injection-to-test interval (10 min). Because a single injection-to-test interval is relatively uninformative, the present research was designed to more fully characterize this morphine hyperalgesic effect. In Experiment 1, 15-day-old White Leghorn cockerels were placed on a hot plate (59°C) in 10 min after injection of morphine (1.25, 2.5, 5.0, 10.0 mg/ml/kg) or the distilled water vehicle (1 ml/kg). Latency to perform a jump response or attainment of a 90-sec no-jump criterion were recorded. Experiment 2 examined morphine effects (2.5 mg/ml/kg) on hot plate jump latencies at various injection-to-test intervals (10, 30, 60, and 240 min). Morphine produced a dose-dependent hyperalgesic response. Temporal characteristics of morphine effects were evident as a U-shaped function. The dose and temporal characteristics of morphine-induced hyperalgesia in White Leghorn cockerels are similar to the dose and temporal characteristics of morphine-induced analgesia typically seen in other species (Sufka and Hughes 1990). | No studies for carp or other cyprinids could be found. In contrast, some evidence suggests that zebrafish (Danio rerio), a closely related cyprinid, can exhibit stress-induced analgesia after exposure to acute stressors that is reversed by treatment with naloxone (Thomson et al. 2020). Whether stress-induced analgesia is present after exposure to chronic stress remains to be investigated. | There is strong and high-quality evidence that octopuses (especially O. vulgaris) possess sensory neurons (afferent) that experience sensitisation and spontaneously activate after re-exposure to noxious stimuli. Studies that focused on neural firing in response to noxious stimuli or tissue damage have shown that Abdopus aculeatus and Octopus bocki response by decreasing their sensory treshold in response to subsequent stimuli to injured arms and nearby arms. The results also demonstrate that octopuses show increased sensitiation on injured arms and nearby arms (neurons fired only in response to noxious stimuli following arm removal) as well as whole-body responses for 24 hrs following injury (Aluplay et al. 2014; Perez et al. 20176). Similar findings were found in squid. Squid (Doryteuthis pealeii also known as Loligo pealeii) showed neural sensitisation across the whole body (not just site of injury) (Crook et al. 2013) as well as behavioural sensitisation (increased escape response) following injury. Similarly, bobtail squid, Euprymna scolopes show sensitisation of peripheral nerves after a crush injury (Howard et al. 2019). Interestingly, neural excitability is sustained for the lifetime of the squid if they received injuries early in life (Howard et al. 2019). | Hyperalgesia occurs in response to injury in adult fruit flies. The mechanism is very well described (Khuong et al 2019), (He et al, 2022). | No studies on hyperalgesia found in bombycidae. However, there are studies on nociceptive sensitisation in the Manduca sexta caterpillar making it likely that other species of lepidopteran larvae also exhibit hyperalgesia. In the studies on Manduca sexta, a reduced threshold and increased sensitivity to mechanical and thermal noxious stimuli was found after repeated stimulation to either the abdomen or proleg (Walters et al. 2001; McMackin et al. 2016; Adamo & MacMillan 2019; Mukherjee & Trimmer 2019), which lasted up to 19 hours (McMackin et al. 2016). The authors of several articles liken the response to allodynia or hyperalgesia (McMackin et al. 2016; Adamo & MacMillan 2019). | |||||||||||||||||||
59 | Jealousy-like behavior | From personal experience working with pigs, I have definitely encountered something like jealousy-like behaviour. It might well be something like attention seeking behavior from certain animals, but there response was definitely stronger, when I paid more attention to certain individuals, compared to other individuals. Thus, I would call it jealousy-like and not just attention seeking. | ||||||||||||||||||||||||
60 | Joy-like behavior | I was surprised to no find a study about this, as I have experienced joyful behavior in pigs and there are many documentaries with this topic (simple google search about joy in pigs). | No studies of carp or any other related fish species could be found. However, Graham et al. (2018) showed that when zebrafish, a closely related cyprinid, are housed in naturalistic environments, they engage in heightened shoaling behavior (i.e. protracted bouts of tight group cohesion and increased behavioral synchrony). As well, koi (Cyprinus rubrofuscus), another closely related cyprinid, have been shown to seek out tactile contact with humans (Fife-Cook & Franks, 2021). These behaviors may yield insights for future work on positive emotion, includng joy, in fish (Franks et al., 2018b). | No studies of salmonids or any other related fish species could be found. However, Fagen (2017) has suggested that some jumping behavior seen in Atlantic salmon (Salmo salar) may represent a form of locomotor play and Burghardt (2005) has reported on anecdotal observations of possible instances of locomotor play in juvenile Coho salmon (Oncorhynchus kisutch). Although not defined as joy, in humans at least, play is associated with intensely positive emotional experiences like joy and amusement (Franks et al., 2018a). | Lean yes: octopuses in the wild and in captivity exhibit play, which might be indicative of joy-like behaviour. For e.g., individuals manipulate different objects (i.e., plastic balls, bottles, pieces of Lego, shells). In captivity, octopuses have been observed passing objects from arm to arm, squirt the items to the far end of their tank (using water from their siphon) and wait for the water from the outlet pipe to float the objects back towards them (Mather & Anderson 1999). Some researchers have observed octopuses head bobbing when interested in stimuli, a behaviour that has been described as increased arousal (Borrelli et al. 2006) and might be indicative of a postively valanced experience. | |||||||||||||||||||||
61 | Liking-wanting dissociation | No studies for carp could be found. However, a number of papers demonstrate that zebrafish (Danio rerio), a closely related cyrprinid, readily respond to addictive drugs and represent an important animal model for studying the pharmacological effects of drugs of abuse (e.g. Klee et al., 2011; Stewart et al., 2011). In particular, zebrafish have been used to evaluate the rewarding properties of nicotine (e.g. Kedikian et al., 2013; Faillace et al., 2018) and ethanol (e.g. Collier et al., 2014; Tran et al., 2015). Additionally, exposure to cocaine has been shown to increase dopamine in the mesolimbic structures of the zebrafish brain (e.g. Darland et al., 2012; Barreto-Valer et al., 2013). Although zebrafish have been used to investigate addiction, more research is needed into the liking, wanting and incentive-sensitization of zebrafish. | The effect of caffeine was assessed on Vespa orientalis hornets maintained either in sealed breeding boxes or as entire colonies free to forage, and also on Apis mellifera bees within their hives. In a number of instances the hornets were also used to study the effect of various bodily extracts of queen hornets and of the following xanthines: Purine; hypoxanthine; uric acid; theophylline; and theobromine. The studied materials were found to exert an effect on three categories of activities: (1) Motor motility, flight, and construction; (2) sensory response to light, noise, irritability, orientation; and (3) physiological changes in appetite, copulation, oviposition, hibernation, resistance to cold, and longevity. Up to a point the produced effects were reversible. Throughout the period of experimentation the test insects did not show signs of tolerance or addiction towards caffeine (Ishay & Paniry, 1979). | |||||||||||||||||||||||
62 | Loneliness-like behavior | (Sadler and Weiss, 1975) conceptualised loneliness as perceived social isolation, which he described as a gnawing, chronic disease without redeeming features. Pigs in modern farming practice may be exposed to a number of stressors, including social stressors such as mixing or isolation. This may potentially affect both cognitive abilities and stress physiology of the animals. They tested the hypothesis that overnight social isolation in pigs impairs performance in a cognitive holeboard (HB) task (Experiment 1) and the Pig Gambling Task (PGT) (Experiment 2), a decision-making task inspired by the Iowa Gambling Task. In addition, they tested the effect of overnight social isolation on salivary cortisol levels. The effects of overnight social isolation on performance in this task were assessed once, when the pigs were 25 weeks old. Salivary cortisol was measured from samples collected 15 min after the start of isolation and at the end of the isolation period and compared to baseline values collected before the start of social isolation. Our results did not confirm the hypothesis that isolation impaired HB performance and decision-making in the PGT. Unexpectedly, overnight social isolation decreased cortisol levels below baseline values, an effect that was not associated with changes in performance of the behavioral tasks. They hypothesized that the housing and testing conditions may have prepared the animals to cope efficiently with stress (van der Staay et al., 2016). In this paper loneliness is not proven beyond doubt. It states that cognitive and physiological stress is not worsening after 1 night of social isolation, but during the isolation phase they could hear and smell the other pigs. | Separation from conspecifics in chicks elicits high rates of distress vocalizations (DVoc) that decline over the course of the 2h isolation experience. Both (Lehr, 1989) and (Panksepp et al., 1991) describe the initially higher rate of DVoc as a ‘protest’ phase and the subsequent lower rate as either a ‘resignation’ (Lehr, 1989) or ‘despair’ (Panksepp et al., 1991) phase (Sufka et al., 2006). Domestic fowl chicken in one group were isolated from one through 70 days of age; the other group were raised normally. During isolation, four patterns shown by the normal birds were shown by the isolated birds. However, systematic delay in the behaviour was noted among the isolated group. At 70 days of age the isolated birds were assembled together; immediate and intense interactions took place involving all of the birds. Full social organization was apparent within several days. It was concluded that social behaviours occurred during isolation in the absence of stimulation from other birds and that isolation does not prevent later social organization (Ratner, 1965). | Operational definitions of loneliness in fish have yet to be determined and thus, further research is needed. However, there has been some work done on the impacts social isolation has on some fish species. Although social isolation in fishes has not yet been linked to loneliness, Kittilsen (2013) suggests social contact could elicit positive emotional states in social fish species and negative feelings, such as loneliness, could serve to restore social contact if an individual fish has been separated from its group. No studies of carp could be found. However, a number of studies on lab bred zebrafish (Danio rerio), a closely related cyprinid, have shown that social isolation decreases thigmotactic behaviour and serotonin in the brain (Shams et al., 2015), decreases neuronal density and neural net formation in the forebrain (von Krogh et al., 2010), and causes rapid fluctuations in monamine levels in the brain and cortisol in the plasma (Shams et al., 2017). Whole brain mapping has also revealed that the brains of non-social individuals in normal populations (termed “loner fish”) are different from the brains of fish that are non-social due to being raised in isolation ( termed “lonely fish”; Tunbak et al., 2020). Daniel & Bhat (2022) have also shown that social isolation causes stress in wild zebrafish. | Operational definitions of loneliness in fish have yet to be determined and thus, further research is needed. However, there has been some work done on the impacts social isolation has on some fish species. Although social isolation in fishes has not yet been linked to loneliness, Kittilsen (2013) suggests social contact could elicit positive emotional states in social fish species and negative feelings, such as loneliness, could serve to restore social contact if an individual fish has been separated from its group. No studies of salmonids or any other related fish species could be found. However, Øverli et al. (2006) found that social isolation increases the cortisol levels and modifies the feeding and agnostic patterns of rainbow trout (Oncorhynchus mykiss). Social isolation has also been shown to reduce the level of serotonin metabolite while increasing cell proliferation in O. mykiss (Sørensen et al., 2012). Sloman & Baron (2010) found that social isolation during development had a significant effect on both physiological and behavioural traits in developing O. mykiss. For example, the O. mykiss embryos and larvae raised in social isolation had lower oxygen consumption and sodium uptake rates combined with higher ammonia excretion rates and after hatch, juvenile fish raised in social isolation from fertilisation were slower to respond to their own mirror image (Sloman & Baron, 2010). | They have demonstrated that pronounced changes in gene expression, correlated with social isolation, take place in ant workers of T. nylanderi workers. These changes may have adverse effects on the ants as they indicate suppression of the immune system, lower resistance to other stressors, interference with food intake and digestion, and a possible increase in circulating juvenile hormone. Such changes might contribute to a shortened lifespan in isolated workers, as detected for this and other ants. We found moderate changes in social interactions following isolation: ant workers were less inclined to contact their adult nestmates, while increasing the durations of contacts with brood. The reduction in self-grooming with ongoing isolation should reduce the removal of pathogens from the cuticle and, in combination with downregulation of immune genes, might make isolated workers more prone to infection. Future studies should examine how behavioural and physiological immunity variables interact and analyse the behavioural responses to isolation in more depth. Such studies should also include physiological and neurobiological factors. Only such multifaceted examinations can help us to reach a firm conclusion regarding the comprehensive effects of isolation in social species (Scharf et al., 2021). | ||||||||||||||||||||
63 | Love-like behavior | Nothing found, all papers fit more the friendship like behaviour, e.g., (Murphy et al., 2014; Puppe, 1998). | Whether invertebrates exhibit positive emotion–like states and what mechanisms underlie such states remain poorly understood. Here they demonstrate that bumblebees exhibit dopamine-dependent positive emotion–like states across behavioral contexts. Their findings present a new opportunity for understanding the fundamental neural elements of emotions and may alter the view of how emotion states affect decision-making in animals (Perry et al., 2016). The adaptive function of emotions is thought to be the integration of information about the environment and body to modulate decisions and behavior (Anderson & Adolphs, 2014). | |||||||||||||||||||||||
64 | Maternal response to offspring distress | The results suggest that responsiveness to piglet distress calling is an innate response, which is not influenced by previous exposure to piglet squeals or previous experience of maternal behaviour. Variation in sow responsiveness post-partum indicates that the sow is capable of responding to distress calls at any time post-partum, but is most receptive to piglet stimuli within the first 2 days post-partum (Hutson et al., 1992). | Hens show behavioural and physiological responses to their chicks’ mild distress (Edgar et al. 2011). Maternal effects can have a buffering effect on chick fearfulness (Freire 2020). For example, hens increased vocalisations and walking, while they decreased preening, when their chicks were threatened (e.g., a cue, such a light or sound, indicating a puff of air would be delivered), though only when the chicks were naive to the cue suggesting the hens’ response is not driven only by the chick’s behaviour (Edgar et al. 2011). | No reports for carp or other cyprinids could be found. However, it is highly unlikely, since many articles report instead that carp and other cyprinids lack parental care, especially post-hatch parental care. | No reports for salmonids could be found. However, it is highly unlikely, since Pacific salmon species are semelparous, with mothers dying immediately post-spawning, and iteroparous Atlantic salmon migrate away from spawning locations while embryos are still incubating in river substrate. Thus for both types of salmon, mothers would either be dead or absent during any instances of offspring distress. | Octopuses do not care for their offspring | There is evidence of parental care in several caridean shrimp species. For example, freshwater shrimp in the Paratyinae family offer extended parental care after hatching (Huguet et al. 2011). Brooding behaviour is also common in the Decapod order, but except for the Dendrobranchiata suborder (Huguet et al. 2011). As Penaeidae shrimp offer no pre-hatching care to their offspring, it is unlikely that they would experience maternal responses to offspring distress. There is also evidence of continuous rather than seasonal breeding in some Penaeid species (da Costa & Fransozo 2004), further supporting the probable lack of maternal response to offspring distress. | The life cycle of the black soldier fly is short with adult females dying shortly after laying eggs. It is therefore unlikely that there is a meternal response to offspring distress (Tomberlin et al. 2002) | The life cycle of the adult silkmoth is short with some females dying shortly after laying eggs (Banno et al. 2010). It is therefore unlikely that they exhibit maternal responses to offspring distress. | |||||||||||||||||
65 | Mourning-like behavior | This is the homepage from a philosopher currently at the Veterinary University Vienna, Dr. Susana Monso, studying animals understanding of death. Nothing specific found, just again a number of videos showing pigs mourn, but no paper about this behaviour in pigs. | ||||||||||||||||||||||||
66 | Panic-like behavior | The frequency of groups of animals exhibiting a panic response was not significantly different in extensive Iberian pigs (29.0%) compared with Iberian pigs raised in intensive conditions (15.8%) (Z=2.2, P=0.14). However, when a panic response was seen on extensive units, it concerned from 50% to 100% of the groups of animals assessed whereas on intensive farms these proportions ranged from 17% to 40%. Although mean frequencies of the panic response did not depend significantly on the rearing system, there were marked differences between extensive and intensive units in the degree to which the animals were fearful of humans. Indeed, when a panic response was seen on an exten- sive unit, from 50% to 100% of the groups of animals assessed displayed a fear response to the observer. On the contrary, this response affected less than half of the pens assessed when seen on an intensive farm (Temple et al., 2011). | Separation-induced distress vocalisations (Dvocs) in chicks are aimed at re- establishing social contact (Gallup and Suarez, 1980) and are at their highest rate during the first 5 min block of the isolation test session. We are uncomfortable using ‘protest’ to describe DVoc behavior as this term suggests a ‘strong disapproval’ of social separation; rather, this appetitively motivated behavioral response is more akin to a panic or fear state elicited by the sudden onset of a stressor (Sufka et al., 2006). Panic indicates intense fear-like response culminating in flying or jumping at the transparent front wall but also blindly to the ceiling or against solid walls. Vocalizations were common both during and after ESB. Attempts to leave the cage often continued after stimulation in contrast to aggressivere sponses that typically stopped promptly with ESB. Long latencies (10-30 sec) and capriciousr epeatability were seen at a few anterior loci with high thresholds (0.3-0.35 mA) (Putkonen, 1973). | Although not explicitly defined, Vøllestad et al. (2004) state that they observed a strong initial panic reaction in crucian carp (Carassius carassius) when the fish were exposed to pike (Esox lucius) odours in the water. Additionally, in the closely related cyprinidae, zebrafish (Danio rerio), erratic movement (defined as swimming associated with fast directional changes, or “zig-zagging”) has been shown to increase in response to the delivery of alarm substance (Speedie & Gerali, 2008), visual stimulation of a predator (i.e. the indian leaf fish, Nandus nandus; Bass & Gerali, 2008), and an animated (moving) image of this predator (Gerali et al., 2009). Although panic behavior is not specifically mentioned, erratic movement may be an example of panic behaviors. | Panic-like behaviors has been described and observed during thermal delousing methods used to remove sea lice from farmed Atlantic salmon (Salmo salar; Gismervik et al., 2019). In laboratory trials, exposing Atlantic salmon to warm water, even for short durations (i.e. 30s in water 34–36°C), caused the fish to exhibit frantic and rapid swimming behaviors, vigorous aversive reactions (headshakes and bursts), and collisions into the sides of the tanks that lead to injuries (Elliot, 1991; Gismervik et al., 2019; Nillson et al., 2019; Moltumyr et al., 2022). As well, hyperoxia-induced gas bubble disease has been shown to induce panic episodes (defined as when the fish jumped away in an erratic and sudden way) in Atlantic salmon (Espmark et al., 2010). Rainbow trout (Oncorhynchus mykiss) have also been shown to exhibit panic episodes (defined as erratic behavior and sudden jumping) when exposed to high percent total gas pressure (TGP%) levels of 115% that have the ability to result in gas bubble disease (Gültepe et al., 2011). | In captivity and in the wild, octopuses have been observed inking or quicky retreating into their dens when startled (Hanlon & Messenger 2018). In captivity, squid and cuttlefish frequently impact the wall of their tanks when startled/panicked, which can damage skin at the distal part of the mantle, this injury is called 'butt-burn' (Fiorito et al. 2015). | ||||||||||||||||||||
67 | Parental care | The complex nursing behavior of the sow appears designed to prevent the more vigorous piglets from monopolizing the milk. Sows give vocal signals which both attract piglets to suckle and synchronize their behavior during nursing episodes. Piglets give loud vocal signals when separated from the sow; calls which vary in intensity and appear to be honest signals of need. Udder massage by piglets may also serve as an honest signal of need. Parent–offspring conflict has been demonstrated experimentally in pigs. Specifically, when given the opportunity to control contact with their piglets, sows nurse less frequently, provide less milk, and lose less weight during lactation than sows that cannot control their level of contact. Because of this interesting natural history and because they are so amenable to experimentation, domestic pigs provide a rich system for testing ideas drawn from resource allocation theory (Drake et al., 2008). | In domestic chickens, the provision of maternal care strongly influences the behavioural development of chicks. Mother hens play an important role in directing their chicks’ behaviour and are able to buffer their chicks’ response to stressors. Chick’s imprint upon their mother, who is key in directing the chicks’ behaviour and in allowing them to develop food preferences. Chicks reared by a mother hen are less fearful and show higher levels of behavioural synchronisation than chicks reared artificially (Edgar et al. 2016). | No reports of parental care in carp or other cyprinids could be found. The only observable characteristic approaching parental investment or care is mate selection by female zebrafish (Danio rerio), a closely related cyprinid. Female zebrafish exhibit mate preferences that are likely related to increases in offspring fitness via male quality (Lavery et al. in prep) and manifest these preferences via control over how many eggs are released in the presence of a given male (Uusi-Heikkilä et al. 2012). | The only reports of parental care or investment for Atlantic and Pacific salmon species involve redd (nest) site selection, construction, and short-term guarding. It appears that female salmon select redd sites based on habitat characteristics that improve their fitness and offspring survival (e.g. Baxter & MacPhail 1999). Females then build their redds by flicking substrate with their tails, which is hypothesized to “clean” gravel of fine sediments that could otherwise block water flow to incubating embryos (e.g. Peterson & Quinn 1996). They also build their redds in shapes that encourage water to wash through areas where embryos are buried (e.g. Sear et al. 2014). Finally, immediately after spawning and embryo burying in the tail of their redds, females will guard redds short-term to prevent other females from disturbing them (e.g. McPhee & Quinn 1998). Otherwise, no reports of parental care exist for salmonids. | While many species of female octopus guard and care for their eggs, there is no evidence of parental care once the eggs hatch. Female octopuses usually fast during egg care and die just as the hatching begins. | There is evidence of parental care in several caridean shrimp species. For example, freshwater shrimp in the Paratyinae family offer extended parental care after hatching (Huguet et al. 2011). Brooding behaviour is also common in the Decapod order, but except for the Dendrobranchiata suborder (Huguet et al. 2011). As Penaeidae shrimp offer no pre-hatching care to their offspring, it is unlikely that they would offer post-hatching care. There is also evidence of continuous rather than seasonal breeding in some Penaeid species (da Costa & Fransozo 2004), further supporting the lack of parental care. | Although there is no evidence of post-spawning parental care in Portunidae, female crabs do carry and transport their eggs prior to spawning. There is evidence that some Brachyura species supply oxygen to the eggs during transport (Ruiz-Tagle et al. 2002; Fernández et al. 2000). This has not been shown in Portunidae, but it is possible that the family also perform the same behaviour as they also transport large numbers of eggs. | Crayfish offer extended maternal care to their offspring and preferentially treat their kin for more than 10 days post-independence (Mathews 2011). Unlike some other crustacean species, crayfish display “relatively complex parental care” (Aquiloni & Gherardi 2008). The females carry the eggs and first two juvenile stages under the abdomen, thereby “safeguarding of hatching by a telson thread that keeps the helpless newborn hatchlings linked to the egg cases on the maternal pleopods and thus prevents them from being lost” (Vogt & Tolley 2004). Mothers exhibit heightened aggression and territoriality from the egg-bearing stage until they tend stage 2 offpring (Figler et al. 1996; Figler et al. 2001). One study monitored the behviour of mothers and third stage juveniles when they were offered the choice of returning to their biological mother, a foster mother, a non-brooding female or a male (Aquiloni & Gherardi 2008). Biological and foster mothers displayed fairly unique behaviour and a “spoon-like telson posture, which seemed to facilitate offspring’s approaches”. | The possibility of extending brood care via the overlapping presence of relatively short lived adults could generate advantages that may have been among the selective forces at the origin of eusociality. In this paper they provide evidence for extended brood care through sib-rearing in the arid-zone allodapine bee, Exoneurella eremophila. Solitary females of the overwintered generation generally die before all their offspring have become independent. In a relatively high proportion of nests, a newly eclosed female invests in her siblings while producing her own offspring in the maternal nest. The sex ratio of the first offspring produced by the overwintered female is highly female biased, but the overall sex ratio of the brood is unbiased. This finding supports the prediction of Bull's 'insurance by protogyny' model of a female bias in the first-produced offspring as a strategy by the mother to ensure extended brood care (Hogendoorn et al., 2001). | The life cycle of the black soldier fly is short with adult females dying shortly after laying eggs. They therfore do not exhibit parental care (Tomberlin et al. 2002) | The life cycle of the adult silkmoth is short with some females dying shortly after laying eggs (Banno et al. 2010). It is therefore unlikely that they exhibit parental care. | ||||||||||||||
68 | Play behavior | All measures of play, including locomotor, social, and self-handicapping elements, were depressed on the first day after weaning compared to the day before weaning. All measures of play were also significantly lower on the first day after weaning than on subsequent days (Donaldson et al., 2002). | Sparring, also known as play fighting, is reported in some birds, including domestic chickens. According to (Dawson and Siegel 1967) sparring started somewhat later than frolicking, increased at a faster rate and surpassed frolicking when the chicks were 25 days of age. Sparring reached its peak at about 32 days and then declined at approximately the same rate. According to (Baxter et al. 2019) they found that creating space among the broilers was a successful method of stimulating play (largely sparring and frolicking), with play being observed in 93% of videos, however the presence of enrichments did not have an effect on the level of play recorded (P>0.05). There was also no treatment effect on activity levels of broilers in unenriched areas (P>0.05), however levels of overall activity decreased as broilers aged. | No studies of carp could be found. An anecdotal observation of possible play was described in two other cyprinid species, the redeye (Scardinius erythrophthalmus) and the rudd (Leuciscus cephalus), showing that these fish returned over and over for the experience of being thrown out of the water by a human hand and the fish often competed vigorously to be the next one to be thrown (Burghardt, 2005). Burghardt (2005) provides a review of a large body of anecdotal evidence that suggests that play may exist in multiple species of teleost fish. However, further empirical studies involving controlled and systematic observation of fish play behaviors are needed and could follow up on the anecdotal observations outlined by Burghardt (2005). Importantly, the current lack of documented play behavior in fish may not indicate that fish do not play but rather that they are too uncomfortable in the typical housing we provide for them to engage in play (Fife-Cook & Franks, 2019). Thus, further research requires housing fish in environmental and social conditions conducive to a relaxed state (Fife-Cook & Franks, 2019). | It is common for juvenile and adult salmonids to jump into the air from the water, and this behaviour is highly relevant in salmonid net-pen culture and may be related to buoyancy regulation, parasitic infections, or stress (Fagen, 2017). However, Fagen (2017) has suggested that some jumping behavior seen in Atlantic salmon (Salmo salar) may represent a form of locomotor play but calls for additional research. Burghardt (2005) also reports on anecdotal observations of possible instances of locomotor play (not involving jumping) resembling adult redd-digging behavior in juvenile Coho salmon (Oncorhynchus kisutch). Burghardt (2005) provides a review of a large body of anecdotal evidence that suggests that play may exist in multiple species of teleost fish. However, further empirical studies involving controlled and systematic observation of fish play behaviors are needed and could follow up on the anecdotal observations outlined by Burghardt (2005). Importantly, the current lack of documented play behavior in fish may not indicate that fish do not play but rather that they are too uncomfortable in the typical housing we provide for them to engage in play (Fife-Cook & Franks, 2019). Thus, further research requires housing fish in environmental and social conditions conducive to a relaxed state (Fife-Cook & Franks, 2019). | Play behaviour has frequently been reported in octopuses. In captivity, octopuses are eager to explore inanimate objects (e.g., Lego, balls); they carry them around their aquarium tank and pass them from arm to arm (Kuba et al. 2003; Kuba & Byrne 2006). Giant Pacific octopuses, Enteroctopus dofleini, manipulate floating objects (e.g., plastic bottles) by squirting jets of water at the item, sending it to the far end of their aquarium and repeating the behaviour when the object floats back to them (Mather & Anderson, 1999). In the wild, different species have been observed collecting and manipualting different objects such as plastic and glass bottles (Mather 1994). | They explored bees’ behavioral flexibility in a task that required transporting a small ball to a defined location to gain a reward. Bees were pretrained to know the correct location of the ball. Subsequently, to obtain a reward, bees had to move a displaced ball to the defined location. Bees that observed demonstration of the technique from a live or model demonstrator learned the task more efficiently than did bees observing a “ghost” demonstration (ball moved via magnet) or without demonstration. Instead of copying demonstrators moving balls over long distances, observers solved the task more efficiently, using the ball positioned closest to the target, even if it was of a different color than the one previously observed. Such unprecedented cognitive flexibility hints that entirely novel behaviors could emerge relatively swiftly in species whose lifestyle demands advanced learning abilities, should relevant ecological pressures arise (Loukola et al., 2017). | |||||||||||||||||||
69 | Play vocalization | Vocalisations are a potential indicator of emotional valence as they can reflect the internal state of the caller. They experimentally manipulated valence, using positive and negative cognitive bias trials, to quantify changes in pig vocalisations. They found that grunts were shorter in positive trials than in negative trials. Interestingly, they did not find differences in the other measured acoustic parameters between the positive and negative contexts as reported in previous studies (Friel et al., 2019). | In other words, chicken vocalisations related to positive emotions in reward situations seem to be rhythmic, short vocalisations, which can have variable F0 and rhythms. However, more research on how the different vocalisation parameters are influenced by valence is needed (Laurijs et al. 2021). Nevertheless, nothing has been researched directly about play vocalization. | FishSounds.net (Looby et al., 2022) presents a compilation of acoustic recordings and published information on sound production across all extant fish species globally. Although many families of bony fishes possess sound-generating organs and vocalize (signal acoustically) in various behavioural contexts including distress situations, agonistic interactions, courtship or to maintain group cohesion (see Looby et al., 2022); it remains challenging to demonstrate the signal function experimentally and thus, our knowledge of fish sound communication is very limited. To date, no vocalizations related to play behavior or any related positive affective states (e.g. joy) have been recorded/documented in any fish species and thus, further investigations are needed. | FishSounds.net (Looby et al., 2022) presents a compilation of acoustic recordings and published information on sound production across all extant fish species globally. Although many families of bony fishes possess sound-generating organs and vocalize (signal acoustically) in various behavioural contexts including distress situations, agonistic interactions, courtship or to maintain group cohesion (see Looby et al., 2022); it remains challenging to demonstrate the signal function experimentally and thus, our knowledge of fish sound communication is very limited. To date, no vocalizations related to play behavior or any related positive affective states (e.g. joy) have been recorded/documented in any fish species and thus, further investigations are needed. | There are no reports of octopus or any other cephalopods using vocalizations or auditory signals. | ||||||||||||||||||||
70 | Pride-like behavior | |||||||||||||||||||||||||
71 | Prioritizes pain response in relevant context | Suckling by piglets led to increases in prolactin and somatotropin in the sow. Failed nursing attemps, which did not result in milk ejection, also led to elevations of prolactin and somatotropin, suggesting that massage of the udder is sufficient and milk ejection is not necessary for these hormonal changes to occur. Prior treatment with the opioid antagonist, naloxone, blocked the nursing-induced increases in prolactin and somatotropin. Tail-flick latencies of the sows were significantly elevated after a nursing, suggesting reduced pain sensitivity. This was blocked by naloxone, suggesting that nursing directly increases endogenous opioid activity (Rushen et al., 1993). | Endogenous analgesia induced by changes in motivation has been identified in the chicken in previous studies but either the motivational changes were difficult to interpret or the motivation was unpredictable. Experimental sodium urate (SU) arthritis of the ankle joint resulted in pain-coping behaviour (one-legged standing or sitting) for a 2-h period in non-food-deprived birds without access to food. Complete analgesia or marked hypoalgesia was observed in birds which had been food deprived overnight and given access to food immediately after SU injection. This analgesia seen during feeding behaviour in the food-deprived bird could be completely reversed by intravenous injection of naloxone. These results demonstrate that feeding motivation can totally suppress, in some animals, the severe tonic pain of SU arthritis and that this analgesia may be opioid mediated (Wylie and Gentle 1998). | No studies of carp specifically could be found, but for zebrafish (Danio rerio), a closely related cyprinid, Deakin et al. (2019) argue that a “failure to avoid the top half of the tank by 10% Acid [injected] fish could be due to the severity of the pain being so great that it took priority over normal anti predatory or anxiety behaviour”. | No studies of Atlantic salmon specifically could be found. However, rainbow trout (Oncorhynchus mykiss), a closely related salmonid, treated with acetic acid have an impaired neophobic response and fail to express typical neophobic novel object avoidance, an effect that disappears when fish are given an analgesic at the same time as an acetic acid injection (Sneddon et al. 2003). Further, noxiously stimulated trout do not show antipredator responses in the presence of predator cues, suggesting that they prioritize pain (Ashley et al. 2009). Similarly, the same study found that when kept in a familiar group, dominant fish are much less aggressive, suggesting a behavioural impairment in response to noxious stimulation. But in an unfamiliar group, no reduction of aggression was observed, suggesting that “maintaining dominance status took priority over showing signs of pain”. | Recent research shows that octopuses, Octopus bocki, can learn to prioritize pain by avoiding chambers they once preferred but now associate with injury. Instead injured octopuses selectively enter chambers where they can access a local anaesthetic (i.e., lidocaine), which silences activity in pathways connecting the site of injury on the arm to the brain (Crook 2020). This research suggests that octopuses can prioritize pain over 'preferred place'. However, there is no other direct evidence of motivation trade-offs that balance potential pain against other motivations (i.e., food, shelter, mates) in octopus or any other cephalopods. | A study on the effect of eyestalk ablation on Litopenaeus vannamei shrimp found that the onset of feeding following ablation (with no anesthetic) was delayed by up to 30 minutes (Taylor et al. 2004), suggesting they were prioritizing the “pain” response over feeding. When shrimp were given an anesthetic they immediately responded when food was provided, resuming normal feeding. | Small repeated electric shocks were delivered to shore crabs inside a dark shelter within a test arena (Magee & Elwood 2016). Although crabs showed no avoidance of the shelter during the trials or subsequently, they often emerged from the shelter during a trial to avoid further shock. | Despite their common use as model organisms in scientific experiments, pain and suffering in insects remains controversial and poorly understood. Here they explore potential pain experience in honeybees (Apis mellifera) by testing the self-administration of an analgesic drug. Foragers were subjected to two different types of injuries: (i) a clip that applied continuous pressure to one leg and (ii) amputation of one tarsus. The bees were given a choice between two feeders, one offering pure sucrose solution, the other sucrose solution plus morphine. They found that sustained pinching had no effect on the amount of morphine consumed, and hence is unlikely to be experienced as painful. The amputated bees did not shift their relative preference towards the analgesic either, but consumed more morphine and more solution in total compared to intact controls. While our data do not provide evidence for the self-administration of morphine in response to pain, they suggest that injured bees increase their overall food intake, presumably to meet the increased energy requirements for an immune response caused by wounding. They conclude that further experiments are required to gain insights into potential pain-like states in honeybees and other insects (Groening et al., 2017). | |||||||||||||||||
72 | PTSD-like behavior | The issue with pig studies is that most are done on pigs who are slaughtered within 6 months to 2 years. So PTSD is difficult to prove. The paper below deals with most parameters, I would deam important to get something like PTSD-like behavior. The welfare of transported pigs can be compromised both by physical and psychological stresses. The animals' responses can be assessed using records of mortality and trauma, physiological and behavioural observations and, to some degree, by measurements of meat quality since this can reflect the animals' physiological state at death. These assessments may, therefore, be used as measures of animal welfare. During transport pigs show weight loss, increased circulating concentrations of catecholamines, cortisol and creatine phosphokinase (CPK), and an increase in heart rate and packed cell volume; sometimes there is evidence of dehydration. Increased levels of dark, firm, dry (DFD)meat after long transport reflect muscle glycogen depletion and possibly indicate some element of fatigue. There is experimental evidence that transport is aversive to pigs, which may be partially due to the fact that they become travel sick. Mortality in transport has ranged from < 0.1 to > 1.0 per cent in different European countries. Mortality is higher in more stress-susceptible breeds and at higher ambient temperatures. It is increased in pigs fed within 4h of transport, at higher stocking densities and after longer journeys at ambient temperatures greater than 10°C. Pigs may be fasted long enough before slaughter to prejudice their welfare through hunger. Long fasts may also reduce muscle glycogen levels and cause fatigue. Fighting between unfamiliar animals which have been mixed during the marketing procedure is also stressful, however, longer transport may actually reduce this problem by allowing animals to get used to one another under conditions in which it is difficult to fight (Yu et al., 2020). | No studies of carp could be found. However, in zebrafish (Danio rerio), a closely related cyprinid, models of PTSD are being developed by psychiatric and biomedical researchers. A recent paper suggests that their behavioural model of PTSD “successfully recapitulates lasting behavioral and endocrine symptoms of clinical stress-related disorders, but also implicates changes in neuroglia, neuroinflammation, apoptosis and epigenetic modulation in long-term effects of stress pathogenesis in vivo” (Yang et al. 2020). Two review papers (Stewart et al. 2014, Caramillo et al. 2015) echo the potential usefulness of zebrafish as a model for PTSD, in the context of drug and treatment development; these suggest that zebrafish are therefore at least capable of exhibiting something akin to PTSD. There is no ecological or evolutionary reason to believe that such a capacity for PTSD would be species-limited to zebrafish. | |||||||||||||||||||||||
73 | Relief learning | In this study, pigs were able to anticipate positive and negative situations. Pigs were kept in a waiting box and cued with tones signaling whether they would be able to go into a room with a bowl of popcorn (positive) or cross a ramp provoking a visual cliff response (negative). When anticipating the negative situation, the proportion of pigs uttering high-frequency vocalizations was significantly higher, pigs turned around more often, and the latency to move was longer after door opening, than when waiting for the positive situation. However, heart rate, heart rate variability and locomotive activity were not influenced by the valence of the situation but differed depending on the phase (waiting, tone, anticipation, and end) of the trial. Although the authors considered the high-pitched vocalization to be the most sensitive parameter of the pigs’ emotional responses, the results demonstrate various behaviors indicative of an emotional response in anticipation of two different events (Imfeld-Mueller et al., 2011). | Relief learning from tonic pain, i.e. pain escape learning, has been tested in humans, rats and fruit flies (Gerber et al., 2014; Yarali et al. 2008), however, does not appear to have been tested in chickens or related species. | No studies of carp could be found. However, also reviewed in the motivational tradeoffs and self-medication sections, unpublished (but briefly described in Sneddon et al. 2014) work on zebrafish suggests that they can learn to seek a location where they can access analgesia when they are exposed to a noxious stimulus. Zebrafish subcutaneously injected with a noxious substance choose a previously unpreferred barren chamber over a preferred enriched one, when analgesia (lidocaine) is dissolved in the barren chamber. This suggests that zebrafish may be capable of learning what mitigates their experience of pain; however, no other published studies could be found to support this suggestion. | There is evidence that octopuses can change their behaviour after a negative event and are capable of relief-learning when painkillers are offered. One crucial study demonstrates that Bock's pygmy octopus, Octopus bocki, injected with acetic acid groom the site of injection by stripping away skin with their beak. Injured octopuses avoid chambers they assoicate with injury and selectively enter chambers where they can access a local anaesthetic (i.e., lidocaine), which silences activity in pathways connecting the site of injury on the arm to the brain (Crook 2020). | Perhaps not as strong as relief learning, but there is evidence to suggest that shrimp (Caridean (family Atyidae), not Penaeidae) learn to adjust their foraging strategy from diurnal to nocturnal in the presence of a predatory fish (Bool et al. 2011). As Penaeid shrimp also live in an environment in which learning is useful, it is possible that they would also display this behaviour. | An electric shock was directed to the crab Carcinus maenas in a dark shelter (its preferred choice) and no shock in a lit shelter (Magee and Elwood, 2013). The crab started to choose the lit area to avoid the shock. | After being given an electric shock when they oriented themselves towards a preferred blue-lit exit, they chose to orient themselves towards a less preferred white-lit exit (Okada et al., 2021). | Associative learning relies on event timing. Fruit flies for example, once trained with an odour that precedes electric shock, subsequently avoid this odour (punishment learning); if, on the other hand the odour follows the shock during training, it is approached later on (relief learning). During training, an odour-induced Ca++ signal and a shock-induced dopaminergic signal converge in the Kenyon cells, synergistically activating a Ca++-calmodulin-sensitive adenylate cyclase, which likely leads to the synaptic plasticity underlying the conditioned avoidance of the odour. In Aplysia (sea slug), the effect of serotonin on the corresponding adenylate cyclase is bi-directionally modulated by Ca++, depending on the relative timing of the two inputs. Using a computational approach, they quantitatively explore this biochemical property of the adenylate cyclase and show that it can generate the effect of event timing on associative learning. They overcome the shortage of behavioural data in Aplysia and biochemical data in Drosophila by combining findings from both systems (Yarali et al., 2012). Kirkerud et al. 2017, found that honeybees were able to learn to avoid electric shocks in a walking arena through learning the colour of the light which signalled saftey. The authors suggest this reveals the existence of a relief component in aversive operant conditioning in honeybees. | |||||||||||||||||
74 | Rescue behavior | They documented a case in which an adult female wild boar manipulated wooden logs securing the door mechanism of a cage trap and released two entrapped young wild boars. The whole rescue was fast and particular behaviours were complex and precisely targeted, suggesting profound prosocial tendencies and exceptional problem-solving capacities in wild boar. The rescue behaviour might have been motivated by empathy because the rescuer female exhibited piloerection, a sign of distress, indicating an empathetic emotional state matching or understanding the victims. They discuss this rescue behaviour in the light of possible underlying motivators, including empathy, learning and social facilitation (Masilkova et al., 2021). | Rescue behaviour is rare in birds, though well-documented in rats and ants. One example is Seychelles warbler, where 4 instances of an individual engaging in behaviour aimed to remove sticky seeds from a groupmate were reported as “the first recorded case of rescue behaviour in birds” (Hammers and Brouwer 2017). | |||||||||||||||||||||||
75 | Response modified by painkillers | Castration reduced nursing behavior. The effect was partially reversed by use of local anesthetic. This is evidence that castration is painful during this 3-hour period after castration and show pigs modifiy their response with painkillers (McGlone and Hellman, 1988). | To evaluate analgesic efficacies of morphine and butorphanol in lame broiler chickens. Study design: Double blind, randomized, controlled experimental study. Animals: In study 1, 36 lame and 36 sound chickens. In study 2, 48 lame and 48 sound chickens. Methods: Sound and lame chickens were gait scored and randomly assigned into four groups: sound-drug, sound-placebo, lame-drug, and lame-placebo in study 1. In study 2, an additional lame and sound handling control group was included. Chickens in drug groups were injected with either morphine or butorphanol 2 mg kg (-1) intravenously. Chickens in placebo groups were injected with an equal volume of normal saline. All birds underwent an obstacle course (OC) and latency-to-lie (LTL) test before injection and at 30 minutes and 2 hours after injection, to assess their walking ability and their standing ability. The time taken to finish the OC and the standing time in the LTL test were recorded. Friedman tests with Dunn's correction were used to identify significant differences. Results: Lame chickens finished the OC faster (mean ± standard deviation 36 ± 8 c.f. 69 ± 18 seconds) after the injection of butorphanol. Morphine caused sedation with an increase in time taken to finish the OC, even in sound chickens. In the lame handling control and placebo groups the OC times increased and the LTL times decreased with each observation. Conclusion: Intravenous butorphanol (2 mg kg (-1)) may be analgesic in chickens for up to 2 hours. Morphine caused sedation (Singh et al. 2017). | Carp (Cyprinius carpio, sometimes referred to as koi carp) subjected to electric shock exhibit caudal trunk spasms that decrease in magnitude with increasing doses of tramadol; and this analgesic effect of tramadol is reduced when delivered with naloxone (Chervova & Lapshin 2000). When subjected to surgery, carp show reduced activity, lower position in the water column, and decreased feeding intensity, all of which are mitigated by post-operative intramuscular injection with butorphanol (but not by the NSAID ketoprofen: Harms et al. 2005), and butorphanol also mitigates surgery effects on opercular beat rate (Baker et al. 2013). Similarly, morphine mitigates surgery effects on appetite and, to a lesser degree than butorphanol, opercular beat rate (Baker et al. 2013). In a closely related cyprinid zebrafish (Danio rerio), opioids (buprenorphine and morphine) also mitigate the effects of noxious stimuli on adult and larval behavioural responses (e.g. thermal challenge: Lopez-Luna et al. 2017a, acid injection: Lopez-Luna et al. 2017b, submersion in diluted acetic acid: Steenbergen & Bardine 2014). The NSAID aspirin, when delivered via submersion in water, also mitigates the effects of noxious stimuli on opercular beat rate (fin clipping: Schroeder & Sneddon 2017, acid injection: Lopez-Luna et al. 2017b). And finally, in another closely related cyprinid goldfish (Carassius aurata), morphine increases the nocifensive threshold (an effect that is blocked by concurrent delivery of naloxone: Ehrensing et al. 1982) and mitigates noxious stimulus-induced behavioural changes (e.g. Newby et al. 2009, Nordgreen et al. 2009). | Atlantic salmon (Salmo salar) vaccinated via intraperitoneal injection often develop putatively painful granulomatous peritonitis that can increase their latency to eat and decrease swimming during feeding that change with the severity of the condition; but these effects are not mitigated by intramuscular injection with morphine (Nordgreen et al. 2013). No other studies of Atlantic salmon nor any on Pacific salmon could be found. However, in the closely related salmonid rainbow trout (Oncorhynchus mykiss), morphine reduces opercular beat rate (roughly analogous to ventilation rate) and behavioural responses (anomalous self-protective behaviours and latency to feed) to a noxious stimulus (lip injection with acetic acid: Sneddon 2003). Similarly, demorphin delivered intranasally also reduces rainbow trout sensitivity (measured in terms of the severity of a caudal trunk spasm) to a noxious stimulus (electric shock: Chervova et al. 1994). Lidocaine injected at the site of noxious stimulus application (lip injection with acetic acid) and carprofen (an NSAID) injected intramuscularly also reduce opercular beat rate relative to noxiously-treated fish without analgesia (Mettam et al. 2011), with lidocaine producing the more pronounced response modification. In the novel object test, rainbow trout treated with a noxious stimulus (lip injection with acetic acid) exhibit reduced neophobia, a response that is mitigated by treatment with morphine (Sneddon et al. 2003). However another opioid, buprenorphine, has negligible analgesic effects on rainbow trout responses post noxious stimulus application (lip injection with acetic acid: Mettam et al. 2011, surgery: Grans et al. 2014). | There is some evidence that octopuses can modify their behaviour in response to chemical compounds that affect the nervous system via (1) an endogenous neurotransmitter system and (2) painkillers (e.g., putative local anaesthetics). (1) There is a lot of evidence for the presence of important neurotransmitters and receptors (enkephalin-like peptides, oestrogen, serotonin) that are often associated with nociceptive processes but they have not yet been linked to playing a role in response to noxious stimuli or modulating nociceptive pathways in cephalopods. However, this is due to a lack of studies rather than evidence of absence. (2) There is evidence that octopuses can change their response to noxious stimuli in the presence of painkillers. Specifically, lidocaine and magnesium chloride act as local anaesthetics in octopuses (Abdopus aculeatus, Octopus bocki), with evidence that exposure suppresses activity in the peripheral nervous system (measure by electrodes not behaviour) (Butler-Struben et al. 2018). Another crucial study, which bolsters our RP rating to 'likely yes', links exposure to local anaesthetic to changes in behavioural response to injury. Specifically, Bock's pygmy octopus, O. bocki, injected with acetic acid groom and tend to the site of injection by stripping away skin with their beak. Exposure to lidocaine results in octopuses ceasing any injury-directed grooming behaviour towards the injury site (Crook 2020)*. This suggest that lidocaine attenuates an experience of pain as it appears to silence nerve activity between the site of injury and the brain. Currently, there is no work that focuses on the effects of analgesics, anxiolytics, or anti-depressants in cephalopods. One study found that Octopus bimaculoides respond to a different compound, MDMA, with increases social behaviour (Edsinger & Dölen 2018) but this study was not linked to how exposure to this compound effects decision-making or responses to noxious stimuli. *The design of Crook (2020) deserves a mention. Octopuses were given three chambers to explore. Following exploration, octopuses were injected with acetic acid in their preferred chamber. This resulted in octopuses avoiding their preferred chamber from the point of injection and instead preferring an alternaticve chamber where the local anesthetic was accessible. | Taylor et al. (2004) applied a topical anesthetic during eyestalk ablation in female (Litopenaeus vannamei) shrimp and found that lidocaine treated individuals resumed normal foraging behavior more rapidly and exhibited much less erratic swimming following ablation than untreated individuals. Similarly, Diarte-Plata et al. (2012) performed a similar experiment on Macrobrachium americanum shrimp (family: Palaemonidae) and found that lidocaine treated animals showed a significant reduction in tail flicking behaviour. A study on the rockpool prawn (Palaemonide) found that noxious stimuli elicited a targeted antennal grooming and rubbing response, which was inhibited by benzocaine (anaesthetic) (Barr et al. 2008). | There is evidence of a modified defensive response of the crab Neohelice granulatus (Chasmagnathus granulatus) (family Varunidae) to morphine (Lozada et al. 1988), but the only study found on analgesia in Portunidae (shore crab) found that morphine made crabs less likely to enter a shelter in which they’d previously experienced a shock; instead they displayed reduced general responsiveness (rather than a specific analgesic effect) and the authors conclude that morphine has no pain-reducing effect in crabs but still influences their responsiveness (Barr & Elwood 2011). One study by Minter et al. (2013) found that Alfaxalone was an effective anesthetic for blue cabs when administered intravascularly. | Marbled crayfish exposed to the analgesic Tramadol spent more time in shelters, exhibited a reduced velocity and moved shorter distances (Buřič et al. 2018). There is evidence that the analgesic tramadol has an effect on the stress response of signal crayfish (family: Astacidae) (Lozek et al., 2019). | Despite their common use as model organisms in scientific experiments, pain and suffering in insects remains controversial and poorly understood. Here they explore potential pain experience in honeybees (Apis mellifera) by testing the self-administration of an analgesic drug. Foragers were subjected to two different types of injuries: (i) a clip that applied continuous pressure to one leg and (ii) amputation of one tarsus. The bees were given a choice between two feeders, one offering pure sucrose solution, the other sucrose solution plus morphine. They found that sustained pinching had no effect on the amount of morphine consumed, and hence is unlikely to be experienced as painful. The amputated bees did not shift their relative preference towards the analgesic either, but consumed more morphine and more solution in total compared to intact controls. While our data do not provide evidence for the self-administration of morphine in response to pain, they suggest that injured bees increase their overall food intake, presumably to meet the increased energy requirements for an immune response caused by wounding. They conclude that further experiments are required to gain insights into potential pain-like states in honeybees and other insects (Groening et al., 2017). Changes in responsiveness for the stinging reaction of honeybees fixed in a holder after receiving 3 electrical shocks delivered with 1 min interval, was registered and used as measurement for the effect of 2 μl of different solutions injected. Every shock consisted of a train of pulses of 1 msec each, delivered for 2 sec at a frequency of 100 Hz. Injection of morphine-HCl (50 to 200 n-moles/bee) produced a dose dependent reduction of the honeybee stinging response to the electrical shocks. The morphine dose that produced a 50% inhibition of the response (D50) was 148 n-moles/bee (927 μg/g), i.e., a value far greater than that reported for vertebrates in behavioral test of analgesia. Naloxone 1.1 μg/g produces a significant reduction of morphine D50 effect and at 4–5 μg/g, a full disinhibition. Thus, whereas the D50 of morphine for honeybees is far greater than that for vertebrates, the doses of naloxone that antagonize morphine are similar for bees and vertebrates. Possible explanations of this difference are mentioned. Injections of met-enkephalin, leu-enkephalin, kyotorphin and (D-Ala2) methionine-enkephalinamide, given in doses of 200 n-moles/bee, an amount greater than that of the morphine D50, exhibited no effect on the stinging response (Núñez et al., 1983). | ||||||||||||||||
76 | Reward based learning | In one experiment they examined whether pigs fed by an experimenter learn to associate the rewarding elements of this procedure with the experimenter conducting the procedure (Hemsworth et al., 1996). A lot of other studies done are based on reward learning (Bolhuis et al., 2013, 2004) | Using a place preference conditioning paradigm, chickens quickly associated food with one of two compartments in a box, with low-ranging chickens showing a stronger association (i.e., more resistant to extinction) than high-ranging chickens (Ferreira et al. 2020a). If the reward was social rather than food, high-ranging chickens showed a quicker conditioned preference than low-ranging ones, suggesting that conspecific presence enhances foraging opportunities for high-ranging chickens (Ferreira et al. 2020b). The sound of an automated feeder leads to increased anticipatory responses, including vocalisations, in chickens (Freire 2020). They were more accurate in pecking one of two keys matching the colour of a previously presented light when the reward was greater (4 second access to food) than less generous (1 second access to food) (Poling et al. 1996). Hens with a more reactive coping style outperformed those with a more proactive style on associative learning tests (de Haas et al. 2017). Issues with differentiating behaviour resulting from “true” instrumental learning, compared with other learning mechanisms, due to tendencies across species to approach stimuli that predict rewards. For example, Hershberger’s ‘looking glass’ example, found that four-day old domestic hen chicks were unable to go against their Pavlovian (i.e., classical conditioning) tendencies to approach a food reward dispenser, by walking away from it to for a reward (Hershberger 1986). Note that adult hens are still to be tested. Contrafreeloading occurs when animals prefer to show a behaviour for an outcome (e.g., food reward), then have the outcome freely available. For example, chickens can learn to use operant feeders, and use correlates with increased foraging time, particularly when operant feeders were paired with ad lib feed, suggesting they prefer to ‘work’ for food (Lindberg and Nicol 1994). | Common carp (Cyprinius carpio) can be trained to perform an operant response (operating an underwater trigger in a demand feeder, usually by pushing or pulling) for a food reward (e.g. Wright & Eastcott 1982a). They can also learn to associate an acoustic signal with food availability during operant corresponding (e.g. Wright & Eastcott 1982b). Similarly, goldfish (Carassius aurata), a closely related cyprinid, can be trained to bump a lever for a food reward (e.g. Phelps 2014). Further, carp can solve a spatial task (seeking a hidden food reward) using cue-based and algorithmic strategies (Mesquita et al. 2015). Zebrafish (Danio rerio), a closely related cyprinid, have been the subjects in numerous cognition experiments and their ability to learn based on several different reward types (e.g. food, the sight of conspecifics, addictive drugs) rather than punishers has been well-established in a number of experimental paradigms like conditioned place preference, spatial alternation learning, and spatial discrimination tests (e.g. reviewed by Meshalklina et al. 2017). | Atlantic salmon (Salmo salar) can be trained to perform an operant response (operating an underwater trigger in a demand feeder, usually by pushing or pulling) for a food reward (e.g. Paspatis & Boujard 1996), as can other salmonids (e.g. Branas & Alanara 1994). Salmon can also learn to associate a previously aversive conditioned stimulus (a flashing light) with a food reward such that the conditioned stimulus elicits anticipatory behavior rather than avoidance (Bratland et al. 2010). They also learn in response to a variety of reward types including food, discussed above, and the sight of conspecifics (e.g. Bergendahl et al. 2016). Note that these are just illustrative examples, as there are many other examples of salmonids learning in response to rewards not reviewed here. | There is strong reward based learning evidence in octopuses. Specifically, octopuses can learn through positive reinforcement using food as a reward (Young 1961; Mackintosh & Mackintosh 1963). They can even learn with delayed rewards (i.e., rewards offered 30 seconds after stimuli is presented) (Wells & Young 1968). Reward based learning occurs quickly in octopuses, they can be taught to associate inanimate objects/stimuli with rewards in several trials. This type of learning is processed in the brain (Gutnick et al. 2016; Sanders 1975). | Although no studies have been found in Penaeidae, one article on Macrobrachium acanthurus (Palaemonidae) suggests this shrimp can discriminate punished and non-punished stimuli by making choices in a Y maze (Ventura and Mattel, 1977). As Penaeid shrimp also live in an environment in which flexible discrimination learning is useful, it is possible that they would also display this behaviour. | The crab Carcinus maenas learned to navigate a complex maze over four consecutive weeks using food as a motivator (Davies et al 2019). Crabs showed steady improvement during this conditioning period in both the time taken to find the food and in the number of wrong turns taken. Crabs also clearly remembered the maze as when returned two weeks later but without any food. Similar findings are described by Orlosk et al, (2011) who found that within 6 days of testing, 21 out of 30 crabs (Carcinus maenas) were successfully trained to enter a beam of light to receive food, despite them instinctively seeking shelter from predators in dark areas. When attempting to crack the shells of Littorina littorea, Carcinus meenas crabs learned to use more frequent and higher intensity cracking techniques when a crack formed in the shell (Abby-Kalio 1989). In a study comparing the learning ability of two different species in the Portunidae family, Carcinus Maenus demonstrated a significantly enhanced leaning ability than Callinectes sapidus (Roudez et al. 2008). The green crab (Carcinus Maenus) has also displayed the ability to perform operant conditioning by pressing a lever to receive a food reward (Abramson & Feinman 1990). | Much of the reward based learning literature on crayfish concerns drug-sensitive rewards. Crayfish can learn in spatial or conditioned place preference tasks to self-administer rewarding drugs such as amphetamine (Imeh-Nathaniel et al. 2016; Datta et al. 2018). Crayfish show rapid acquisition of a classical conditioning learning task, when in non-stressed conditions and accessed a small hole to obtain a food reward (Bierbower et al. 2013). In a different study, rusty crayfish were trained to associate a known food cue with a cue from a walleye egg (unknown food cue) (Weisbord et al. 2012). They successfully demonstrated second-order conditioning through associative learning. | Olfactory learning and floral scents are co-adaptive traits in the plant–pollinator relationship. However, how scent relates to cognition and learning in the diverse group of Neotropical stingless bees is largely unknown. Here they evaluated the ability of Melipona eburnea a stingless bee, to be conditioned to scent using the proboscis extension reflex (PER) protocol. Stingless bees did not show PER while harnessed but were able to be PER conditioned to scent when free-to-move in a mini-cage (fmPER). They evaluated the effect of: 1) unconditioned stimulus (US) reward, and 2) previous scent–reward associations on olfactory learning performance. The effect of the unconditioned stimulus reward was not a significant factor in the model on day 2. This indicates that olfactory learning performance can increase via either taste receptors or accumulated experience with the same odor (Amaya-Márquez et al., 2019). | One recent study on associative learning in silkworms has found that one strain of silkworm (c10) was able to associate red coloured paper with food, whilst another strain (p50) showed no discrimination between red and blue paper following training (Takahashi et al. 2021). In another experiment silkworms that were trained to associate an unconditioned stimulus (mulberry leaves) with a conditioned stimulus (odour) during the larval stage retained this association into adulthood, preferring to oviposit in the presence of the conditioned stimulus (compared to an unconditioned control group) (Gámez & León 2020). | |||||||||||||||
77 | Sadness-like behavior | Panksepp (2003) describes a study on humans by Eisenberger et al (2003), were the subjects experienced emotional distress as indicated by substantial blood-flow changes in two key brain areas. One of these areas, the anterior cingulate cortex, has been implicated in generating the aversive experience of physical pain. Eisenberger and colleagues demonstrate that the greater the feeling of social distress, the more this brain area becomes activated. The other brain region, in the prefrontal cortex, showed an opposite pattern of activity, becoming more active when the distress was least. In other words, the two brain areas involved in the distressing feelings of social exclusion responded in opposite ways to the degree of social pain experienced (Eisenberger et al., 2003; Panksepp, 2003). Nothing similar was found for pig. | ||||||||||||||||||||||||
78 | Self-medication | In this review it is stated that pigs are among those animals found to self-medicate, using the plant Punicum granatum (Family Punicaceae), also called pomegranate - where pigs in Mexico sought out the root. Described in a book by Janzen (1978) and McCann (1932) (Huffman, 2003). | Lame and sound broilers, selected from commercial flocks, were trained to discriminate between different coloured feeds, one of which contained carprofen. The two feeds were then offered simultaneously and the birds were allowed to select their own diet from the two feeds. In an initial study to assess the most appropriate concentration of drug, the plasma concentrations of carprofen were linearly related to the birds' dietary intake. The walking ability of lame birds was also significantly improved in a dose-dependent manner and lame birds tended to consume more analgesic than sound birds. In a second study, in which only one concentration of analgesic was used, lame birds selected significantly more drugged feed than sound birds, and that as the severity of the lameness increased, lame birds consumed a significantly higher proportion of the drugged feed (Danbury et al. 2000). | No studies of carp could be found, but many examples exist for a closely related species, zebrafish. In studies of zebrafish conditioned place preference behaviour (usually in the context of studying fish models of addiction), a variety of drugs can be used as reinforcers: e.g. cocaine (e.g. Darland & Dowling 2001), amphetamines (e.g. Ninkovic et al. 2006), morphine (e.g. adults: Lau et al. 2006, larvae: Bretaud et al. 2007), alcohol and nicotine (e.g. Kily et al. 2008). This indicates that zebrafish prefer and seek out areas where they can receive addictive and rewarding substances. In terms of self-medication during an actual health/fitness challenge however, there is limited information. Previously reviewed in the motivational tradeoffs section, one example of zebrafish self-administration of analgesia exists outside the published literature (but is briefly described in Sneddon et al. 2014): zebrafish subcutaneously injected with a noxious substance choose a previously unpreferred barren chamber over a preferred enriched one, when analgesia (lidocaine) is dissolved in the barren chamber. It is unlikely that carp (or indeed salmon) would have fundamentally different abilities from zebrafish, with respect to this type of analgesia self-administration or to conditioned place preference reinforced by rewarding drugs. | No studies of salmonids could be found. In studies of zebrafish conditioned place preference behaviour (usually in the context of studying fish models of addiction), a variety of drugs can be used as reinforcers: e.g. cocaine (e.g. Darland & Dowling 2001), amphetamines (e.g. Ninkovic et al. 2006), morphine (e.g. adults: Lau et al. 2006, larvae: Bretaud et al. 2007), alcohol and nicotine (e.g. Kily et al. 2008). This indicates that zebrafish prefer and seek out areas where they can receive addictive and rewarding substances. In terms of self-medication during an actual health/fitness challenge however, there is limited information. Previously reviewed in the motivational tradeoffs section, one example of zebrafish self-administration of analgesia exists outside the published literature (but is briefly described in Sneddon et al. 2014): zebrafish subcutaneously injected with a noxious substance choose a previously unpreferred barren chamber over a preferred enriched one, when analgesia (lidocaine) is dissolved in the barren chamber. It is unlikely that carp (or indeed salmon) would have fundamentally different abilities from zebrafish, with respect to this type of analgesia self-administration or to conditioned place preference reinforced by rewarding drugs. | Likely yes: one crucial study on Bock's pygmy octopus provides evidence for self-medication behaviour. In Crook's (2020) study, a conditioned place preference paradigm demonstrates that octopuses avoid locations in which pain was experienced and learn to prefer a location in which they experienced pain relief. Importantly, octopuses did not show conditioned preference and thus did not self-medicate in the absence of pain (Crook 2020). | One study found that rusty crayfish alter their feeding strategy (macrophyte consumption) as parasite load increased (MacKay & Moore 2021). However, this is the first step in determining self-medication in crayfish. Another has shown that crayfish are capable of self-administration of amphetamine (Datta et al. 2018). | A complication is that demonstrating such a fitness cost might not always be straight-forward, as the toxicity of a substance may vary not only withdose but also according to the nutritional status of an indi-vidual. Tannic acid is normally harmful when consumed, butlocusts provided with an optimal ratio of protein to carbohydratedid not experience any deleterious effects of consuming tannicacid (Behmer, 2009). In addition, insects may con-sume non-nutritive secondary plant metabolites not to preventinfection, but because the food source in question most closelymatches their nutrient intake target (Behmer, 2009). Both of these factors could make it difficult to definitively establish that prophylactic self-medication is occurring (Abbott, 2014). Diverse animals have evolved an ability to collect antimicrobial compounds from the environment as a means of reducing infection risk. Honeybees battle an extensive assemblage of pathogens with both individual and “social” defenses. They determined if the collection of resins, complex plant secretions with diverse antimicrobial properties, acts as a colony-level immune defense by honeybees. Exposure to extracts from two sources of honeybee propolis (a mixture of resins and wax) led to a significantly lowered expression of two honey bee immune-related genes (hymenoptaecin and AmEater in Brazilian and Minnesota propolis, respectively) and to lowered bacterial loads in the Minnesota (MN) propolis treated colonies. Differences in immune expression were also found across age groups (third-instar larvae, 1-day-old and 7-day-old adults) irrespective of resin treatment. The finding that resins within the nest decrease investment in immune function of 7-day-old bees may have implications for colony health and productivity. This is the first direct evidence that the honey bee nest environment affects immune-gene expression (Simone et al., 2009). | No evidence of self-medication in Bombycidae. However, there is evidence of self-medication in lepidopteran larvae more generally. Parasitised woolly bear (Grammia geneura) and Grammia incorrupta (Arctiidae) caterpillars have been found to self-medicate by ingesting large amounts of the pyrrolizidine alkaloids, plant toxins which increase survivability of the larvae when infected (Singer et al. 2004; Singer et al. 2009; Smilanich et al. 2011). Similarly, African armyworm (Spodoptera exempta) larvae showed plasticity in their diet choice during a baculovirus infection (Povey et al. 2014). Each of these examples however is in a polyphagous caterpillar, so it is not definite that more dietary specific caterpillars, like the silkworm would be capable of flexible feeding decisions in order to self-medicate. | |||||||||||||||||
79 | Sensory-Affective Dissociation | Twenty-four two-week old chicks were first tested to determine which of two mashes, differing either in color or in taste only, was preferred. The main group received a painful leg shock when they ate their preferred food, while the control group were either shocked in the absence of the test food or not shocked. Electric shock proved to be an effective noxious stimulus for changing food preferences based on visual cues but not for those distinguishable by taste alone [Moore and Capretta, 1968]. This shows some sort of sensory affected dissociation as the chickens then avoided the formerly preferred food. | Yes: strong evidence from a recent study on Bock's pygmy octopus, Octopus bocki, demonstrates sensory-affective dissociation. Octopuses were tested using a conditioned place preference paradigm to distinguish between sensory and affective components of pain (Crook 2020). This paradigm used operant learning behaviours to reveal (i) whether octopuses could experience an ongoing negative affective state; and (ii) whether octopuses value an anaesthetic when injured. Results showed that octopuses learned to avoid their preferred chamber after experiencing an injury in the chamber (i.e., an injection of acetic acid in one arm). Moreover, they learned to prefer the chamber where they could receive a local anaesthetic. Finally, this change in chamber preference was dependent on injury as the behaviour was only obserevd in injured octopuses. Sham-treated octopuses, individuals injected with saline solution, did not induce a change in chamber preference. | |||||||||||||||||||||||
80 | Shame-like behavior | |||||||||||||||||||||||||
81 | Social buffering | The effects of familiarity and relatedness on agonistic pair relationships (dyads) in different pen regions (pen area or trough area) were studied in 16 groups of newly mixed domestic pigs of similar weight (9 pigs per group) at an age of 12 weeks. The agonistic interactions (AI) within 124 familiar (related) and 452 unfamiliar (related and unrelated) dyads were continuously recorded for 3 days (10 h daily) after mixing. Whereas pigs, both in dyads familiar and unfamiliar to each other, showed the same frequency of AI in the trough area, unfamiliar dyads exhibited significantly more AI in the pen area than familiar dyads. The relatedness of unfamiliar dyads had apparently no influence on AI. It is discussed that, besides establishing a dominance hierarchy, pigs react aggressively on strange subjects. Furthermore, the results are briefly discussed with reference to dominance and resource usage in pigs (Puppe, 1998). | Maternal effects can have a buffering effect on chick fearfulness (Edgar et al. 2016; Freire 2020). For example, hens increased vocalisations and walking, while they decreased preening, when their chicks were threatened (e.g., a cue, such a light or sound, indicating a puff of air would be delivered), though only when the chicks were naive to the cue suggesting the hens’ response is not driven only by the chick’s behaviour (Edgar et al. 2013). There are individual differences in mother hens in effectiveness as social buffers for chicks (Edgar et al. 2015). | No studies of carp could be found. However, multiple reports of social buffering exist for zebrafish (Danio rerio), a closely related cyprinid. For example, Faustino et al. (2017) found that when zebrafish were exposed to alarm substances, zebrafish that were tested in the presence of other zebrafish (visual or odour) displayed significantly less fear responses and recovered more quickly in comparison to zebrafish that were tested alone. When the effectiveness of each type of cue (visual or odour) was tested, visual cues appeared to be superior to olfactory cues in reducing aversive behaviours and promoting social buffering in zebrafish (Faustino et al., 2017). Similarly, White et al. (2017) found that zebrafish held in a group recovered much more quickly from painful events (White et al., 2017). Social buffering has been correlated with the activation of comparable brain regions in zebrafish and mammals, and thus the mechanisms may be evolutionarily conserved (Oliveira & Faustion, 2017; Faustion et al., 2017). | It is generally accepted that temperate subspecies of honeybees can maintain stable temperatures inside their nests; however, little information is available on the cooling ability of tropical honeybees and the effect of high environmental temperatures on individuals. In this study, they registered temperatures in the brood area of strong- and medium-populated colonies of Africanized honeybees during heatwaves (maximum environmental temperature 44°C) between April and May in the tropical Yucatán Peninsula of México. To evaluate the effect on colonies, they compared the body size of workers produced under high temperatures in the field and siblings produced at stable 34–35 °C laboratory conditions. Their results provide evidence that social buffering of honey bee colonies in tropical thermoregulation disruption during heat waves (Poot-Báez et al., 2020). | |||||||||||||||||||||
82 | Sympathy-like behavior | |||||||||||||||||||||||||
83 | Taste aversion behavior | Taste aversion learning in suckling and weanling pigs suggests taste aversion behaviour does exist in pigs (Houpt et al., 1979). | Chicks respond to disgust responses of conspecifics, specifically avoiding pecking an aversive-tasting bead after observing another chick’s disgust response (Johnston et al. 1998). Several experiments have manipulated the findings indicating that social learning can influence feather plucking in chickens to try to reduce this behaviour (Ferreira et al. 2021). For example, hens exposed to feathers soaked in a bitter solution showed less feather plucking than those exposed to feathers soaked in a sweet solution or control birds (Harlander-Matauschek et al. 2008). In taste aversion test, chickens learned to avoid oleic acid, indicating they can detect oleic acid, so may prefer lipid in feed (Kawabata et al. 2021). Chickens can also be successfully conditioned to avoid a unami solution using this test, suggesting they may perceive unami taste as “salty- and sweet-like taste” (Yoshida et al. 2018). Conditioned taste aversion has also been used to attempt to decrease egg predation (e.g., carrion crows, (Cox et al. 2004)). | Kasumyan & Morsi (1995) determined that carp (Cyprinus carpio) have a taste aversion to a number of amino acids and classic taste substances (i.e. tryptophane, arginine, threonine, methionine, phenylalanine, serine, and valine) in their feed. However, when C. carpio are starved for extended periods of time, they will eventually begin to eat feeds that they initially showed taste aversive to but, the relative taste aversion of the feeds is retained (i.e., phenylalanine containing feed, in spite of longer starvation, was always the last feed to be consumed; Kasumyan & Sidorov, 2010). Goldfish (Carassius auratus), a closely related cyprinid, have been found capable to learn to avoid flavored food particles following injections with lithium chloride for extended periods after learning (Martín et al., 2011). Additionally, when Goldfish were offered pellets containing potentially aversive taste stimuli (quinine or caffeine) or mixtures of aversive and appetitive components (amino acids or food), the quinine and caffeine pellets were rejected at high rates and the mixed pellets were ingested more frequently (Lamb & Finger, 1995). The pellets with mixed components resulted in the goldfish utilizing extended sorting behaviors (i.e. including prolonged periods of rinsing and backwashing) suggesting that goldfish use chemical cues to drive sorting and rejection/ingestion feeding behaviors (Lamb & Finger, 1995). | When ammonium-containing trimethylamine (which occurs in rancid fish meals and oils) was added to the diet of Chinook Salmon (Oncorhynchus tshawytscha) fry, they showed an aversion to the experimental diet and reduced their feed consumption (Hughes, 1991). This effect of trimethylamine may have indicated that the O. tshawytscha fry were sensitive to it as an indicator of the freshness of their feed (Hughes, 1991; 1993). Atlantic salmon (Salmo salar) fed high selenite diets also showed reduced feed intake and growth (i.e., apparent toxicity), potentially due to the odor of the selenite (Berntssen et al., 2017). | Taste aversion learning has not directly been tested in octopuses, but recent research has shown that octopus suckers contain chemotactile receptors, which can be used to discriminate between attractive and aversive substances (van Giesen et al. 2020). Given that octopuses possess these specialised chemosensory cells, are sophisticated learners and can learn via negative reinforcement (e.g., electric shock, Boycott & Young 1957; Sutherland 1957; Young 1962; Mackintosh & Mackintosh 1963; Mackintosh 1964), it is likely that they are capable of learning through conditioned taste aversion. Moreover, evidence of taste aversion learning has been demosmtrated in a cephalopod relative, the cuttlefish, Sepia officinalis, whereby individuals learn to avoid their preferred food after it was made distateful (Darmaillacq et al. 2004). A more divergent molluscan relative, the pond snail Lymnaea stagnalis, was also trained through conditioned taste aversion learning to inhibit feeding behaviour and produce a conditioned fear response (Kita et al. 2011). | A study on the feeding behaviour of Pacific white shrimp found that shrimp spent more time exploring the test arena and less time interacting with the food when they were given a diet that was tainted with 0.07M quinine-HCl (giving a bitter taste) than when they were presented with one tainted with an attractant (Bardera et al. 2020). | The crabs Portunus sebae, P. spinnimanus and P. ordway showed more rapid rejection of luminescent unpalatable ophiuroids than of non-luminescent controls. After five trials, unpalatable luminescent prey were rejected three times as quickly as either unpalatable or palatable non-luminescent controls (Grober 1988). The increased speed of rejection in absence of other conditioning factors could be considered an example of taste aversion behaviour. | The crayfish Procambarus clarkii was fed trout feed and a novel food (chicken) associated with a well-known toxic substance, lithium chloride (LiCl), and food intake was recorded for 10 days. A significant effect of treatment was observed that accounted for the lower chicken intake in the LiCl-treated group, compared with the control groups. LiCl-treated animals had an increased trout feed intake during the entire period. These results indicate that the crayfish may develop a food aversion learning when illness is induced by LiCl (Arzuffi et al., 2000). | It has been observed that if aversive substances are associated with an odor, the above retards learning of this odor when it is subsequently paired with sucrose. It is hypothesized that "bitter substances as well as concentrated saline solutions generate a postingestional malaise in harnessed bees, which do not seem to react in an obvious way to their unpalatable taste" (de Brito Sanchez, 2011). To avoid poisoning and death when toxins are ingested, the body responds with a suite of physiological detoxification mechanisms accompanied by behaviours that in mammals often include vomiting, nausea, and lethargy. Few studies have characterised whether insects exhibit characteristic ‘malaise-like’ behaviours in response to intoxication. Here, we used the honeybee to investigate how intoxication produced by injection or ingestion with three toxins with different pharmacological modes of action quinine, amygdalin, and lithium chloride affected behaviour. We found that toxin-induced changes in behaviour were best characterised by more time spent grooming. Bees also had difficulty performing the righting reflex and exhibited specific toxin-induced behaviours such as abdomen dragging and curling up. The expression of these behaviours also depended on whether a toxin had been injected or ingested. When toxins were ingested, they were least 10 times less concentrated in the haemolymph than in the ingested food, suggesting that their absorption through the gut is strongly regulated. Our data show that bees exhibit changes in behaviour that are characteristic of ‘malaise’ and suggest that physiological signalling of toxicosis is accomplished by multiple post-ingestive pathways in animals (Hurst et al., 2014). | No work has looked officially into taste aversion in BSF; however, BSF have 31 odorant binding proteins (larvae) or 27 (adults; 15 in common across life stages) suggesting the ability to discriminate between many volatile organic compounds. BSF adult females are known to discriminate between feeding substrates when choosing oviposition sites (this study and *) (Sripontan et al. 2017). Because BSF is a filth-feeding fly, results from Drosophila may be less relevant here; HOWEVER, data from Musca domestica (another filth-feeder) suggests taste-aversion in response to certain pesticide baits (Sripontan et al. 2017) | In an experiment on single experience learning in the codling moth Pszczolkowski & Brown (2005) found that neonate larvae were able to develop an aversion to the taste of saccharine by pairing it with foliage of the maidenhair tree (Gingko biloba), which causes illness and mortality if sufficient is consumed. In another experirment food aversion learning has been demonstrated in two polyphagous lepidopteran caterpillars (Dethier 1980). However, as noted by Pszczolkowski & Brown (2005), the “adaptive advantage of food-aversion learning is self-evident…but mono- and oligophagous herbivores should not demonstrate such a type of learning, whereas polyphagous ones should. It is not therefore possible to extrapolate these results and make inferences for the monophagous (Tsuneto et al. 2020) silkworm. Additionally, the domesticated silkworm can only survive by eating mulberry leaves and with human intervention (Banno et al. 2010). It is therefore unlikely that the have retained taste aversion behaviour. | ||||||||||||||
84 | Trace conditioning and pain | No studies of carp could be found, but goldfish (Carassius aurata), a closely related cyprinid, can be trace conditioned in response to an aversive electric shock applied after a 15s delay post-presentation of a light stimulus (Overmeier & Savage 1974, Vargas et al. 2009). There is no particular reason to expect that this is a species-specific response that would not be possible for cyprinids more generally. | No studies of salmon could be found, and no studies using noxious stimuli could be found for salmonids. However, rainbow trout (Oncorhynchus mykiss) can be trace conditioned in response to a food reward given after a 3.4s delay post-presentation of a light stimulus (Nordgreen et al. 2010). There is no particular reason to expect that this is a species-specific response that would not be possible for cyprinids more generally, or that this response would only occur when learning is reinforced with a reward rather than a punisher. | Direct studies that link trace conditioning to pain were not found. However, the relationship between learning and gene expression has been investigated in the octopus. Specifically, some genes (incl. Stathmin: Ovsrm, tyrosine hydroxylase: Ov-TH, dopamine transporter: Ovdat, octopressin: Ov-OP, cephalotocin: Oc-ct) are expressred in response to learned fear (i.e., fear conditioning) and innate fear (i.e., social fear). | Despite their common use as model organisms in scientific experiments, pain and suffering in insects remains controversial and poorly understood. Here they explore potential pain experience in honeybees (Apis mellifera) by testing the self-administration of an analgesic drug. Foragers were subjected to two different types of injuries: (i) a clip that applied continuous pressure to one leg and (ii) amputation of one tarsus. The bees were given a choice between two feeders, one offering pure sucrose solution, the other sucrose solution plus morphine. They found that sustained pinching had no effect on the amount of morphine consumed, and hence is unlikely to be experienced as painful. The amputated bees did not shift their relative preference towards the analgesic either, but consumed more morphine and more solution in total compared to intact controls. While their data do not provide evidence for the self-administration of morphine in response to pain, they suggest that injured bees increase their overall food intake, presumably to meet the increased energy requirements for an immune response caused by wounding. They conclude that further experiments are required to gain insights into potential pain-like states in honeybees and other insects (Groening et al., 2017). | |||||||||||||||||||||
85 | Valuing behavior | One study found that pigs learned to discriminate food rewards of different value and remembered the location of the higher value sources (Held et al. 2005). | One study found that the anticipatory behaviour of laying hens "reflected the perceived value of the rewards, with birds appearing to be more motivated to access the Dusty substrate compared with the food rewards" (McGrath et al. 2016). Latency to access rewards also conveyed the relative value of rewards. Another study suggests that peat is a valued substrate for broiler chickens and that positive memories associated with bathing in peat resulted from it's short term exposure (Vas et al. 2020) | Unknown. No studies of carp or other closely related species could be found. Only one study could be found of banded tetras (Astyanax fasciatus), where the authors trained fish to associate two different colour cues to the same food reward, but with one presented when fish were experiencing higher levels of food deprivation. Fish preferred cues associated with greater food deprivation even though the food rewards were identical (Aw et al. 2009). There’s no ecological reason to believe this tendency would be exclusive to tetras; rather, it is likely that the absence of evidence for valuing behaviour in carp and salmon reflects a lack of research. | Unknown. No studies of salmonids or other closely related species could be found. Only one study could be found of banded tetras (Astyanax fasciatus), where the authors trained fish to associate two different colour cues to the same food reward, but with one presented when fish were experiencing higher levels of food deprivation. Fish preferred cues associated with greater food deprivation even though the food rewards were identical (Aw et al. 2009). There’s no ecological reason to believe this tendency would be exclusive to tetras; rather, it is likely that the absence of evidence for valuing behaviour in carp and salmon reflects a lack of research. | No published literature but octopuses are suitable candidates for this type of research as they do show strong preferences for different foods, places & objects and one species has been shown to use tools. | There is one study on the assessment of resource value during contests in mantis shrimp (Green & Harrison 2020), but these are a different order (Stomatopoda), so not likely to be inferable to Penaeidae. | One study looked at the influence of resource value on the agonistic behaviour of the shore crab (Sneddon et al. 1996). They found that contests increased in intensity when food was present, suggesting that they value the resource. In another study crabs were more persistent during agonisitc encounters in the perceived presence of a sexually receptive female, which could indicate that that they value the opportunity to mate with a receptive female (Smith et al. 1994). | One study has shown that crayfish bury their own exuviae following moulting (Buric et al. 2016). The authors propose that this could be evidence of hoarding or caching, suggesting they place value on the exuviae. It should be noted however that the species of crayfish studied were in the Astacidae family. | There are numerous studies on the ability of bees to select rewards of higher "value". For example, honeybees can distinguish nectars of different quality (Sanderson et al. 2013). | ||||||||||||||||
86 | General Proxies | |||||||||||||||||||||||||
87 | Brain mass | This article shows the differences between the weight of fresh brain mass and fixed brain masses, as well as brain weight according to age class (Minervini et al., 2016). Adult range 107-160 g. Midpoint of range = 134.5g | Domesticated chickens (WL) have a larger brain mass and body mass than their wild progenitor, but whereas body mass has increased by ~85% during domestication, brain mass has only increased by ~15%. This indicates that brain mass has been altered less by selection during domestication than body mass and that in chickens reduced relative brain mass during domestication has mainly been caused by an increase in body mass (Henriksen et al. 2016). An adult chicken brain is double the size of a bobtail quail brain (Charvet and Striedter 2010). A red junglefowl has a brain mass of 2.819 ± 0.200 gram (Olkowicz et al. 2016) There is variation across domestic chicken strains in relative brain size, and in comparison, to related species, such as red junglefowl (Mehlhorn and Caspers 2020). | Relationships between brain mass and age are not well-established for carp. For common carp (Cyprinius carpio), brain mass varies depending on whether they are wild-derived or from a hatchery. Khan et al. (2022) report that wild common carp (age unknown, body mass: 195.16 ± 52.53 g) have brains that weigh 0.45 ± 0.14 g and hatchery common carp (age unknown, body mass: 345±48.68 g) have brains that weigh 0.28 ± 0.047 g. Mid point of range = 0.365 g. Smith et al. (2009) report that wild-caught crucian carp (Carassius carassius) of unknown ages have brains weighing 106.5 ± 14.5 mg. | Relationships between brain mass and age are not well-established for salmonids. Several studies comparing hatchery-reared salmonids with wild, or semi-naturally reared, salmonids have provided mixed evidence for how rearing environment effects brain mass. For example, domesticated rainbow trout (Oncorhynchus mykiss) have been shown to have smaller sizes of several brain structures than wild conspecifics (Marchetti & Nevitt, 2003). Devlin et al (2012) found brain mass to be smaller in domesticated (fast-growing; age 432 days) versus wild-type (slow-growing; age 1139 days) strains of rainbow trout smolts (domesticated: 0.207 ± 0.005 mg; wild: 0.260 ± 0.012 mg). Wiper et al. (2014) reported that adult male Chinook salmon (Oncorhynchus tshawytscha) had a significantly larger absolute total brain mass when they were reared in wild environments (1.21 ± 0.027 g) versus in hatchery environments (1.03 ± 0.019 g). Range = 0.260-1.21 g. Midpoint of range = 0.735 g | The octopus brain is comprised of a series of ganglia (of molluscan origin) configured into lobes that are fused together to form masses (Young 1971; Shigeno et al. 2018). There is a large range in brain mass across the 300 species of octopus because body size varies greatly ranging from the size of an inch to spanning 20 feet wide when arms are spread. | Sayol et al. 2020 reported that Apis mellifera had a brain mass of 3.02mg and the mean brain mass across the species from the Apidae family that were measured was 2.96mg (range: 0.50 - 7.43mg). | Range 0.00042-0.00072 g. Midpoint of range = 0.00057 g. Female and male brain mass scaled hypoallometrically with body mass, but at different rates (F = 7.43, df = 19, p = 0.0134); female brains increased in mass as body size increased, while male brain mass was unaffected by increasing body mass (females: log [brain mass] = 0.51 log [body mass] – 1.07, F = 7.33, df = 10, p = 0.022, R2 = 0.42; males: F = 0.91, df = 9, p = 0.37). Females had increased brain masses compared to males (Table 2; Welch’s t-test, t = 3.72, df = 13.66, p = 0.0024; female mean = 0.58 ± 0.09 mg, range: 0.42 - 0.72 mg; males mean = 0.48 ± 0.03 mg, range = 0.44 – 0.53 mg). - Reference: Barrett M, Godfrey RK, Sterner EJ, Waddell EA, in press. Impacts of development and adult sex on brain cell numbers in the Black Soldier Fly, Hermetia illucens L. (Diptera: Stratiomyidae). Arthropod Structure & Development.Note from MRB: In general, I detest species-average brain mass/volume for insects with a large degree of size polymorphism, like BSF. In the paper, we treat brain mass as a function of body mass. In males, a species average is fine as brain mass is unaffected by body mass, but in females hypoallometric scaling suggests female brain mass is dependent on body mass which can vary outside the range we saw in this paper (and which makes mean a poor representation of the biological reality of BSF female brain masses). Just an FYI. | There have been numerous studies involving the extraction of silkworm brains for mass spectrometry analysis and immunohistochemistry for hormone/molecular/mRNA analysis, but brain mass is not reported. Lepidopteran “larval brain size increases after each molt and brain morphology changes markedly during metamorphosis” Cui et al. (2021) (as shown in the Tobacco Hornworm (Manduca sexta) (Champlin & Truman 1998)). Cui et al. (2021) noted, “as the only fully domesticated insect, the Lepidoptera silkworm Bombyx mori experienced changes in larval brain morphology and certain behaviors during the domestication process”, but brain mass has not been found to be reported in these studies. Nordlander & Edwards 1968 compare the morphology of larval and adult monarch butterfly brains, but again mass is not specified. One study has reported the mean brain mass in adults of 4 species of butterfly as follows: Battus philenor (Papilionidae) – 0.382mg; Danaus plexippus (Nymphalidae) – 0.257mg; Junonia coenia (Nymphalidae) - 0.163mg; Pieris napi (Pieridae) – 0.0663mg (Snell-Rood et al. 2020). | |||||||||||||||||
88 | Brain mass to body mass ratio | (Minervini et al., 2016) looked at the mean value for body and brain weights of each class of age and review the relevant literature on ratios over the years. | The emu, the red junglefowl, and the pigeon, all species representing more basal bird lineages, share lower degree of encephalization, a proportionally smaller telencephalon, small telencephalic and dominant cerebellar neuronal fractions, generally lower neuronal densities, and larger glia/neuron ratios. Therefore, their brains harbor much smaller absolute numbers of neurons than brains of equivalently sized songbirds or parrots. For instance, although a red junglefowl is ∼50-fold heavier than a great tit, both birds have approximately the same number of brain neurons. Remarkably, even in these basal birds, neuronal densities in the pallium are still comparableto those observed in the primate cortex. Thus, high neuronal density in the telencephalon appears characteristic of all birds. This means that neuronal densities in the primate pallium are matched by those of chicken and emu, but surpassed by those of songbirds and parrots (Olkowicz et al. 2016). According to (Racicot et al. 2021) white Leghorn chicken have 3274,17 mg brain mass to 2,14 kg body mass. | Cyprinid body sizes are highly variable, so there are few reports of brain volume or mass standardized to body length or mass (Kotrschal & Palzenberger 1992) - rather they tend to standardize brain region volume to total brain volume. Using values from Khan et al. (2022), the ratio for common carp appears to be between 0.45:195 g (for wild fish) and 0.28:345 g (for hatchery fish). | Measures of relative brain mass/volume are often standardized by dividing the absolute brain mass/volume by the length and/or mass of salmonids. However, ratios are not often reported. For example, Wiper et al. (2014) determined the relative brain mass of adult Chinook salmon by dividing the brain mass by the body mass of the fish (i.e. brain mass/body mass= relative brain mass) and found that Chinook salmon jacks had significantly larger relative brain mass than (2.89 × 10−4 ± 1.25 × 10−5) than hooknose males (1.43 × 10−4 ± 6.70 × 10−6), with jack brains being twice as large as hooknose once corrected for body size. As well, once body size was corrected for, the relative brain mass of hatchery-reared chinook salmon (1.63 × 10−3 ± 9.12 × 10−6) were significantly larger than their wild counterparts (1.28 × 10−4 ± 7.82 × 10−6; Wiper et al., 2014). | Cephalopods (octopus, cuttlefish and squid) have the largest brain to body size ratio of all invertebrates. The ratio is comparable to vertebrates, smaller than the ratio of birds and mammals, but larger than the ratio found in most fish and reptiles. Estimares value taken from Packard 1971 Fig 17 which graphs Log-log plots of brain and body weights in Octopus vulgaris, O. salutii, O. defillipi | As is the case in vertebrates, they found an overall allometric relationship between body size and brain and brain component size, ganglion volume and neuron volume, and number across the five bee species examined. Individual differences in thesemeasures point towards species-specific sensory orcognitive disparities. They found only a weak correlation between head/thorax mass and brain volume within some of the honeybee species investigated. This is probably due to the relatively small differences in body size within those species. However, the brain-body size correlation is much more obvious in bumblebees (B. impatiens). They calculated the brain-head-thorax mass data on a double-logarithmic scale. For the four honeybee species, the slopes of ther esulting regressions are as follows: ln brain mass = 0.65 × ln body mass; R2= 0.92 and ln thoracic ganglion mass = 0.62 × ln body mass; R2 = 0.93; combining all five bee species, the slope is ln brain mass = 0.61 × ln body mass; R2 = 0.93 (Gowda & Gronenberg, 2019). | Across adults, relative brain mass increased non-linearly with decreasing body mass in accordance with Haller’s rule ([Brain:body mass] = 1.23 E-05 [body mass]2 – 0.001 [body mass] + 0.04, F = 7.20, df = 20, p = 0.0143, R2 = 0.61). Body mass data (mean + SD): Adult (37.98 ± 8.15); F only (41.23 ± 8.52); M only (34.44 ± 6.32) (Barrett et al, 2022). Arthropod Structure & Development. Raw data can be used for further analysis, will be available on Dryad following publication. | ||||||||||||||||||
89 | Brain volume | Data on volume sizes of the fundamental brain sections, the allocortical subdivisons, the total brains (mm3) and brain weights (g) of feral pigs from Galapagos island (Kruska and Röhrs, 1974). | To test whether a heavier brain equals a larger brain, compared brain mass to volume in a subset of chicken and red junglefowl brains. “The relative brain region mass was calculated by dividing the mass for each specific region by the total brain mass. Brain volume was found to scale linearly with mass. In all four brain regions, regions with a larger mass had a greater volume, with brain mass explaining 98–100% of the variation when regressed on to brain volume”. This study showed that an increased in brain mass correlated with an increase in volume in chickens (Henriksen et al. 2016). | Common carp (Cyprinius carpio): 384614 mm3, crucian carp (C. carassius): 230623 mm3 (Linden et al. 2001). Note these are in vivo MRI measurements of young carp (~ 12cm long, 40-60g); adult carp can range from 30-60cm long and most teleost fish have indeterminate growth. Whether brain volume increases allometrically with body length is unknown, but highly likely (Brandstatter & Kotrschal 1991). | Peris Tamayo et al. (2020) outline the volumes of five different brain regions of four Arctic charr (Salvelinus alpinus) genetically segregated morphs (i.e. Piscivore, Planktivore, Dwarf, and Abyssal). For example, the Abyssal Arctic charr morph was found to have brain volumes of: 0.10 ± 0.04 (olfactory bulb), 0.37 ± 0.16 (telencephalon), 0.78 ± 0.23 (optic tectum), 0.72 ± 0.30 (cerebellum), 0.17 ± 0.07. (hypothalamus). Kihslinger & Nevitt (2006) found that the absolute olfactory bulb volumes of wild Chinook salmon (Oncorhynchus tshawytscha) brains were approximately 23% larger than those reared in hatchery settings. However, the exact brain volumes were not reported. | Brain volume varies across species; Octopus vulgaris 92.6, O. bimaculatus 49.8, O. defilippi 12. 6, O. dofleini 926.2, O. macropus 66.6, O. salutii 91.6 | Brain volume was studied for Stenopus hispidus of the Stenopodidea family, which belongs to the same order of Penaeidae (the Decapoda) but belongs to a different Suborder. This paper described the brain volume and structure of S. hispidus and reports “The gross brain anatomy is comparable to that of the dendrobranchiata Pacific White Shrimp Penaeus vannamei…although specific neuropils differ in shape and size” (Krieger et al, 2019), making it difficult to make inferences for Penaediae. There is reference to two papers that talk about the anatomy of P. vannamei’s brain but seem to describe the structure and not the volume (Meth et al, 2017). | A study investigated the brain anatomy of both Carcinus maenas and Pagurus Bernardus (Krieger et al. 2012). The mean adult brain width of Cacinus maenas is 2.7 +/- 0.11mm and length is 1.5 +/- 0.18mm, excluding the lateral protocerebum and the optic neuropils. The glomeruli have a mean volume of 230000+/- 30000 µm3. | One study found that brain volume shrinkage occurred during fixation and the amount of shrinking depended on the fixation method used (Nischik & Krieger 2018). This study reports some juvenile brain volumes but they should be used with caution due to fixation shrinkage. | A. florea has a brain volume of 0,60 mm3, A. cerana 0,86 mm3, A. mellifera 1,53 mm3, A. dorsata 1,56 mm3, B. impatiens 1,85 mm3 (Gowda & Gronenberg, 2019). | One study reported the mean brain volume of 42 species of butterfly (range: Satyrium edwardsii = 0.166mm3 to Papilio palamedes = 1.958mm3, Snell-Rood et al. 2020), but no studies have reported brain volume in the Bombycidae family. In a different study, volumetric analysis of the adult Bogong moth brain revealed that the male brain was slightly larger than the female brain 0.188 ± 0.035 mm3 and 0.162 ± 0.005 mm3 (Adden et al.2020). El Jundi et al. (2009) have reconstructed the Manduca sexta brain and report the volume of each neuorphil individually, but not as a whole. | |||||||||||||||
90 | Critical flicker-fusion frequency in Hz | Although there are few studies on CFF in pigs, it has been estimated to be close to the value for cats (70-80Hz) (Rosolen et al. 2005; Rosolen et al. 2008), using the method proposed by Rovamo et al (1999). | Behavioural experiments with domestic chicken using full spectrum light intensities from 0.2-2812 cb m-2 indicate an average flicker-fusion frequency of 19.8 Hz (lowest light intensity) to CFF (critical flicker fusion frequency) of 87.0 Hz at 1375 cd m-2. There was some individual variation as some birds showed CFFs of 90-100 hz (Lisney et al. 2011). Average CFF was ca. 105 Hz in a second study using electroretinograms in hens (Lisney et al. 2012). Another study compared two general methods for assessing CFF in hens (conditional discrimination and two-alternative forced-choice), with both methods showing comparable results, and indicating that hens’ CFF is higher than humans (Railton et al. 2009). | One study found the mean CFF in Salmon was 72Hz (Hanyu & Ali 1964). | One study found the mean CFF in Salmon was 72Hz (Hanyu & Ali 1964). | Mixed: some reports on octopus flicker fusion threshold suggest they have a rate less than 30 Hz (Bullock & Budelmann 1991), but other reports have demonstrated that they have flicker fusion rates of up to 60 Hz (Hamasaki 1968). For comparison humans have a rate of 60 Hz (Gleitman 1992) and chickens have a rate of 87 Hz (Lisney et al. 2011) | Vision across shrimp species’ is variable and the critical flicker fusion frequency depends on the environment and depth of water each species inhabits i.e. whether the eyes are dark-adapted or light adapted. One study reports that a species of snapping shrimp (Alpheus heterochaelis, family: Alpheidae) has the fastest vision of any aquatic animal with a temporal sampling rate of at least 160Hz (Kingston et al. 2020). A study on the Penaeid shrimp species Funchalia villosa (which inhabits relatively shallow waters) has measured a maximum critical flicker fusion frequency of 21 Hz in both light-adapted and dark-adapted conditions (Frank 2003), although it was measured as 24 Hz in one study (Frank 1999). The same study reports a frequency of 25 Hz in the species Sergia filictum (Dendrobranchiata, family: Sergestidae), which lives in deeper waters (Frank 1999). Matsuda & Wilder (2013) have measured differences in temporal resolution between juvenile and sub-adult white-leg shrimp, with sub-adults continuing to respond up to 30 Hz, whereas juveniles were barely responding at 20 Hz. | Closest found is 14Hz for Bathynectes longipes (family Polybiidae) (Frank et al. 2012), however this is a deep sea species so is likely to be different from surface dwelling species. | One study reported a maximum flicker fusion frequency of 50-60 Hz in Cambarus bartonii (Waterman 1961). | Bumblebees (Bombus terrestris) have apposition compound eyes (one on either side of the head) of about 6,000 ommatidia and three small single-lens ocelli on the frons of their head capsule. The surface of the eye is smooth and interommatidial hairs, as in the honeybee, are not developed. Each ommatidium (approx. 26 μm in diameter) is capped by a hexagonal facet and contains in its centre a 3 μm wide, columnar light-perceiving structure known as the rhabdom. Rhabdoms consist of thousands of regularly aligned, fingerlike microvilli, which in their membranes contain the photopigment molecules. Axons from each ommatidium transmit the information of their photic environment to the visual centres of the brain, where behavioural reactions may be initiated. Since bumblebee eyes possess three classes of spectrally different sensitivity peaks in a ratio of 1:1:6 (UV = 353 nm, blue = 430 nm and green = 548 nm) per ommatidium, they use colour vision to find and select flower types that yield pollen and nectar. Ommatidial acceptance angles of at least 3° are used by the bumblebees to discriminate between different flower shapes and sizes, but their ability to detect polarized light appears to be used only for navigational purposes. A flicker fusion frequency of around 110 Hz helps the fast flying bumblebee to avoid obstacles (Meyer-Rochow, 2019) | No studies on FFF in Stratiomyidae. This study tested one Glossina and one Drosophila species (Miall 1978). However there is considerable variation between those two genera (even within Glossina, varies from 85-205 Hz), and I doubt either are representative of Stratiomyidae. Other flies are at >200 (Lucilia; Ruck 1961). One other thing of note is that H. illucens are attracted to the flickering sunlight coming off the wings of conspecific females, at a WBF rate of 100 Hz according to this patent. So FFF should be higher than this threshold. My understanding is that these FFFs are dependent on light intensity. | No studies on flicker-fusion frequency found in bombycidae. There is a study which measures flicker-fusion frequency in other adult lepidopteran families (Chatterjee et al. 2020), but because of the diversity in visual systems and lifestyles between families (i.e. nocturnal or diurnal) and because the study took measurements from adults, it is not possible to make inferences for silkworms or the Bombycidae family generally. | ||||||||||||||
91 | Encephalization quotient | EQ of 2,42 for one day piglets, 0,58 for young adults and 0,38 for adults, in sexually mature individuals it is 0,39, compared to humans with an EQ of 6,62 (Minervini et al., 2016). | There are different methods for calculating EQ. In Vanaraja chickens, Duncan’s encephalization quotient ranged from 5.802 ± 0.514 (male) to 5.944 ± 0.451 (female) on 21st day, decreasing from day 21 to 42, then was 1.346 +- 0.115 (male and 1.444 ± 0.114 (female) on 84th day. Using Cuvier’s EQ, the range was from 35.079 ± 0.288 (male) to 36.531 ± 0.312 (female) on day 21, reduced from day 21 to 42, then from 15.607 ± 0.123 (male) to 16.038c ± 0.125 (male) on day .84”. These two methods were highly correlated (Kumar Panigrahy et al. 2017). | Only one report based on 52 store-bought crucian carp (Carassius carassius: age unknown) reports an EQ of 0.37 (Masai et al. 1983). However, Triki et al. (2021) note that “for endothermic vertebrates, absolute brain size, rather than EQ, has been argued to explain best the interspecific variation in cognitive performance”, citing Deaner et al. (2007), MacLean et al. (2012), and Herculano-Houzel (2017). However, they report the mean intraspecific brain-body regression slope as an alternative to EQ, calculated from 51 species of wild-caught teleost fish (largely comprised of cichlid and seahorse genera): mean slope = 0.46, range = 0.26-0.79. They report an absence of a taxon-level effect on slope within their set of teleost species, which is consistent with findings from Tsuboi et al. (2018). Thus, it is plausible to assume that, in absence of clear, robust reports of salmonid- or cyprinid-specific EQ or intraspecific brain-body slopes, Triki et al. (2021)’s intraspecific brain-body slope values might be applied to salmon and carp for the time being. | No reports of EQ for salmon could be found. However, Triki et al. (2021) note that “for endothermic vertebrates, absolute brain size, rather than EQ, has been argued to explain best the interspecific variation in cognitive performance”, citing Deaner et al. (2007), MacLean et al. (2012), and Herculano-Houzel (2017). However, they report the mean intraspecific brain-body regression slope as an alternative to EQ, calculated from 51 species of wild-caught teleost fish (largely comprised of cichlid and seahorse genera): mean slope = 0.46, range = 0.26-0.79. They report an absence of a taxon-level effect on slope within their set of teleost species, which is consistent with findings from Tsuboi et al. (2018). Thus, it is plausible to assume that, in absence of clear, robust reports of salmonid- or cyprinid-specific EQ or intraspecific brain-body slopes, Triki et al. (2021)’s intraspecific brain-body slope values might be applied to salmon and carp for the time being. | Calculated for a giant octopus weighing 14 kg with brain mass of 70 g. More data required to determine EQ between and across species. | In general, insect brain size follows Haller’s rule. This relationship is verifiable both between species, and within species. However, recent studies have pointed to several exceptions to Haller’s rule. For example, Van der Woude et al. performed an intraspecific comparison between differently sized individuals of the small parasitic wasp Trichogramma evanescens, and showed for the first time an isometric brain–body size relation, so brain size is directly proportional to body size (with the brain occupying 8.2% of the body in this case). Brain size is directly proportional to body size (Carle 2021). | |||||||||||||||||||
92 | Neuron packing density | From the two-dimensional analysis of tissue sections cut at the same thickness, Friede (1954) observed that the glia/neuron ratio in the cerebral cortex of several species increases from frog (with an index of 0.25) to man (averageindex of 1.48 across cortical layers), going in ascending order of brain size through chicken (0.46), mouse (0.36), rabbit (0.43), pig (1.20), cow (1.22), and horse (1.23) (Herculano-Houzel, 2014) | See under total neuron 221x106 in jungle fowl chicken (Olkowicz et al. 2016). | No reports of neuron packing density in the carp or salmon brain could be found. However again, since the teleost brain is capable of adult neurogenesis, with neural proliferation zones in dozens of locations within the brain (e.g. Zupanc et al. 2005, Zupanc 2006, Zupanc 2009), definitive measures of neuronal density are difficult and continuously in flux. Importantly, the teleost brain is capable of remarkable rates of adult neurogenesis, making definitive measures of neuron packing density difficult. In female guppies they found a neuronal density of 9.05 × 10^5. (Marhounov et al., 2019) | No reports of neuron packing density in the carp or salmon brain could be found. However again, since the teleost brain is capable of adult neurogenesis, with neural proliferation zones in dozens of locations within the brain (e.g. Zupanc et al. 2005, Zupanc 2006, Zupanc 2009), definitive measures of neuronal density are difficult and continuously in flux. | Neuron density in the octopus brain varies between the different brain structures. For e.g. the optic lobes (motor centre and part visual analyser) contain 65 million nerve cells in each lobe. The superior frontal and vertical lobes (involved in learning and memory) contain approximately 30 million cells. The vertical lobe (~25 million nerve cells), in particular shows, a tighlty packed pattern because 99% of the cells are tiny interneurons. The inferior frontal and subfrontal lobes contain 6 million nerve cells. The central motor centres contain less that 4 million (less 1% of all the nerve cells in the animal). | Across adults, cell density (nuclei/mg) in the OL and total brain decreased as body mass increased, while CB density remained statistically similar, but trended towards decreasing (Total: [brain cell density] = -9405 [body mass] + 996185, F = 6.23, df = 21, p = 0.021, R2 = 0.23; OL: [OL cell density] = -8300 [body mass] + 872429, F = 5.27, df = 21, p = 0.0322, R2 = 0.20; CB: F = 4.19, df = 21, p = 0.054). Males had more dense brains than females (Table 2; Unpaired t-test: t = 5.66, df = 21, p < 0.0001); this was due to increased cell density in the OL but not the CB (K-W ANOVA: K-W = 30.28, p < 0.0001; Dunn’s MCT, OL: Z = 2.61, p = 0.0181; CB: Z = 1.12, p = 0.52). Reference: Barrett M, Godfrey RK, Sterner EJ, Waddell EA, in press. Impacts of development and adult sex on brain cell numbers in the Black Soldier Fly, Hermetia illucens L. (Diptera: Stratiomyidae). Arthropod Structure & Development. | |||||||||||||||||||
93 | Total neurons | The total number of neocortical neurons is 430 million in the Danish Landrace pig, and approximately 325 million in the mature Gottingen minipig (Jelsing et al., 2006) reflecting the greater size of the Landrace pig brain. Furthermore, the pig has cerebral structures common to other mammalian species and, with relative well-defined cerebral circumvolutions, its brain appears to be comparable to human in terms of anatomy, histology and vascularization (Lind et al., 2007). | A red junglefowl has 220.84 ± 44.50 million total brain neurons. The junglefowl brain has a lower absolute neuron count than brains of similarly sized songbirds and parrots. For instance, despite being 50 times bigger than a great tit, a junglefowl has comparable neuron count. However, the neuronal densities in the pallium of “basel” birds, including junglefowl are similar to those in the primate cortex. This indicates that “neuronal densities (i.e., number of neurons) in the primate pallium are matched by those of chicken and emu but surpassed by those of songbirds and parrots” (Olkowicz et al. 2016). Brain weight, brain volume and encephalization quotient were highly correlated with neuronal size in vanaraja chickens (Kumar Panigrahy et al. 2017). | The teleost brain is capable of adult neurogenesis, with neural proliferation zones in dozens of locations within the brain (e.g. Zupanc et al. 2005, Zupanc 2009). This makes a definitive count of total neurons within the brain difficult, since the number of neurons may be continuously in flux. For example, Zupanc (2009) summarizes: “the continuous production of new cells, together with the longterm persistence of a large portion of them, leads to a permanent growth of the brain and its individual structures... This growth by a net increase in the total number of brain cells is characteristic of at least some, but likely most, of the estimated 30,000 species of teleost fish.” Therefore, reports of total neuron counts for salmon and carp are rare, but Hinsch & Zupanc (2007) report that “By labeling S-phase cells with the thymidine analog 5-bromo-2-deoxyuridine (BrdU), quantitative analysis demonstrated that, on average, 6000 new cells were generated in the entire adult brain within any 30 min period. This corresponds to roughly 0.06% of the total number of brain cells” in an adult zebrafish (Danio rerio, a model cyprinid) brain. As part of their study, Hinsch & Zupanc (2007) report that, for adult zebrafish, the total number of brain cells varied between 0.8 x 107 and 1.3 x 107 (mean: 1.0 x 107 ± S.E.M. 8 x 105). They also report that “approximately 46% of the cells present at 10 days persisted in the adult zebrafish brain” meaning that “at least half of the cells generated in the adult zebrafish brain develop into neurons and are likely to persist for the rest of the fish’s life.” This pattern is reflected in other species of teleosts, for example in adult gymnotiform fish (Apteronotus leptorhynchus) who generate 100 000 new brain cells (corresponding to approximately 0.2% of the total population of cells in the brain) within a period of 2 hours (Zupanc & Horschke 1995). Thus the teleost brain is constantly growing and likely increasing in terms of total number of neurons, and counts are only representative of snapshots through time. | The teleost brain is capable of adult neurogenesis, with neural proliferation zones in dozens of locations within the brain (e.g. Zupanc et al. 2005, Zupanc 2009). This makes a definitive count of total neurons within the brain difficult, since the number of neurons may be continuously in flux. For example, Zupanc (2009) summarizes: “the continuous production of new cells, together with the longterm persistence of a large portion of them, leads to a permanent growth of the brain and its individual structures... This growth by a net increase in the total number of brain cells is characteristic of at least some, but likely most, of the estimated 30,000 species of teleost fish.” Therefore, reports of total neuron counts for salmon and carp are rare, but Hinsch & Zupanc (2007) report that “By labeling S-phase cells with the thymidine analog 5-bromo-2-deoxyuridine (BrdU), quantitative analysis demonstrated that, on average, 6000 new cells were generated in the entire adult brain within any 30 min period. This corresponds to roughly 0.06% of the total number of brain cells” in an adult zebrafish (Danio rerio, a model cyprinid) brain. As part of their study, Hinsch & Zupanc (2007) report that, for adult zebrafish, the total number of brain cells varied between 0.8 x 107 and 1.3 x 107 (mean: 1.0 x 107 ± S.E.M. 8 x 105). They also report that “approximately 46% of the cells present at 10 days persisted in the adult zebrafish brain” meaning that “at least half of the cells generated in the adult zebrafish brain develop into neurons and are likely to persist for the rest of the fish’s life.” This pattern is reflected in other species of teleosts, for example in adult gymnotiform fish (Apteronotus leptorhynchus) who generate 100 000 new brain cells (corresponding to approximately 0.2% of the total population of cells in the brain) within a period of 2 hours (Zupanc & Horschke 1995). Thus the teleost brain is constantly growing and likely increasing in terms of total number of neurons, and counts are only representative of snapshots through time. | The octopus nervous system has approximately 500 million nerve cells, similar in number to that of a dog (approx. 600 million neurons). Approximately two-thirds of these neurons are distributed in their arms (and body). | Estimated to have a similar number to crayfish, although probably fewer. | See table 9.2 in Feinberg, T., & Mallatt, J. (2016). The ancient origins of consciousness. Cambridge: MIT Press. https://books.google.ca/books?hl=en&lr=&id=fIPTCwAAQBAJ&oi=fnd&pg=PR5&dq=Todd+Ancient+origin+of+consciousness&ots=c6jVYS29q0&sig=rvzDnoIVFK5AxAz2XaLmoyZW_94#v=onepage&q=Todd Ancient origin of consciousness&f=false. We could not locate the original source used by Feinberg & Mallat, so we do not know precisely to which crab species or genus this figure refers to. No other academic sources on neuron counts in crabs were found. | Abdominal ganglion + the 6th abdominal ganglion: 700 + ("All five anterior abdominal ganglia have an almost identical number of 600-700 neurons with a similar pattern of distribution" (Kondoh and Hisada 1986). then the 5 Thoracic ganglion (Mulloney and Hall 1990). Then: 1 subesophageal and 1 supraesophageal (CNS) then there are some ganglia in the eye stalks Corning, W., Dyal, J.A., & Willows, A.O.D. (Eds.) (2012). Invertebrate Learning: Volume 2. Arthropods and Gastropod Mollusks. New York, NY: Springer & Plenum Press. https://books.google.ca/books?id=aQLkBwAAQBAJ&pg=PA62&lpg=PA62&dq=Crayfish+neuron+count&source=bl&ots=yjE-9RjFiM&sig=GsTizULBn9PeIUxRESVIEgOntDA&hl=en&sa=X&ved=2ahUKEwjvlPy-47bdAhWLg1QKHePbDfsQ6AEwH3oECA0QAQ#v=onepage&q=Crayfish%20neuron%20count&f=false | A. florea has total neurons 20,442, A. cerana 19,640, A. mellifera 26,882, A. dorsata 27,456, B. impatiens N/A (Gowda & Gronenberg, 2019). A. mellifera (Western honey bee) was estimated to have 613,000 neurons in total. The estimate of total brain cell number for the European honeybee (Apis mellifera; 𝑥¯ ≈ 6.13 × 105, s = 1.28 × 105; electronic supplementary material table S1) was lower than the existing estimate from brain sections ≈ 8.5 × 105 (Godfrey et al 2021). Some bees have as few as around 234,000 and others as much as around 1,180,000, according to estimates in (Menzel et al 2001). | Males had significantly more brain cells than females (Table 1, Figure 2B; Unpaired t-test: t = 2.97, df = 21, p = 0.0074). This difference was due to increased numbers of cells in their optic lobes, but not the central brain region (Table 2, Figure 2B; Brown-Forsythe’s ANOVA: F = 168.4, df = 20.27, p < 0.0001; Dunnett’s T3 MCT, OL: t = 2.91, df = 20.12, p = 0.0171; CB: t = 1.00, df = 17.74, p = 0.55). Males had 321,776 ± 44,636 cells in their optic lobes compared to 257,566 ± 60,579 for females. Adults had 42,462 ± 5,222 cells in the central brain region. Cell number did not scale with brain mass in adults (Supplementary Figure 1; OL: F = 0.40, df = 21, p = 0.54; CB: F = 0.04, p = 0.84; Total: F = 0.39, p = 0.54) (Barrett et al, 2022). | There is information on the mushroom body (e.g. Fukushima & Kanzaki 2009), olfactory neurons (e.g. Namiki & Kanzaki 2019) and descending neurons (Namiki et al. 2018) in the silkmoth brain, but total neuron count is not reported. One study reported that adult silkmoths have approx 100000 times fewer neurons in the brain than humans (Chiba et al. 2010). Based on this, an estimation has been made for the total neurons, but note that this is for adults rather than the larval form. | ||||||||||||||
94 | Working memory load | Housing conditions of pigs did not affect reference memory, but environmental enrichment improved working memory of pigs in a spatial discrimination task. Based on the findings of the study, it is suggested that cognitive functioning of pigs may be impaired under commonly used housing conditions (Bolhuis et al., 2013). In the holeboard task, measures of cognitive performance are independent of the speed of negotiating the test apparatus. The holeboard is an open field arena with 16 locations (holes, or buckets in the present study) which may contain bait. The study investigated whether pigs are able to acquire a complex spatial holeboard discrimination task (4 of 16 holes baited) and whether mixing stress affects performance in this task. All pigs rapidly reduced the number of re-visits to baited holes (working memory) and to unbaited holes (reference memory). Mixing stress did not affect performance. (Arts et al., 2009). | (Nordquist et al. 2011) study supports “high levels of working memory performance and low levels of reference memory in chickens” with high or low fearfulness (i.e., latency to approach familiar human). Using delayed matching to sample test (presenting sample for specific time before removing it and showing selection of stimuli, one being same as sample), chickens can match the stimulus to a sample after a 16 second delay (Nakagawa et al. 2004), comparable to some mammals (Lind et al. 2015). Also, able to remember the trajectory of a hidden imprinting stimulus for 3 minutes, also comparable to mammals (Vallortigara et al. 1998). Less evidence for metacognition in birds than mammals, which may be due to demands on working memory in birds during cognitive tasks, such as matching to sample. | No studies of carp could be found. However, studies of the closely related cyprinid, zebrafish (Danio rerio), show that they can successfully perform a delayed match-to-sample task. They can learn to discriminate between two colours and match-to-sample both simultaneously and with a 3-4 second delay between sample presentation and choice-making (Bloch et al. 2019). Bloch et al. (2019) clarify that “the presence of working memory without the mesencephalic dopamine neurons indicates the convergent evolution of this function in amniotes and teleosts”, but that their delayed match-to-sample task is an example of “operant conditioning in teleosts comparable to that in amniotes”. Importantly, they also note that zebrafish are only capable of the delayed match-to-sample task in a certain setup (e.g. they were successful when the response required “entering a hallway” but not “passing through a window”). Zebrafish are also capable of remembering a novel object after a much more significant delay of 2 hours or more, even when they are exposed to it only once (Lucon-Xiccato & Dadda 2014). Fontana et al. (2021) use the number of alternations in turn-direction in a free-movement pattern (FMP) Y-maze to infer working memory ability (they claim that alternations in turn-direction in the FMP Y-maze are reduced after treatment with memory-impairing drugs): they found that adult (4 month old) zebrafish increase the number of alternations after exposure to mild early life stress as larvae (daily stressors applied over 3 days). Finally, Sovrano et al. (2018) found that zebrafish and goldfish can successfully solve a detour task that requires them to “temporarily abandon the view of the goal-object (a group of conspecifics) to circumvent an obstacle”, suggesting that they possess working memory sufficient to enable their success in the task. It is unlikely that carp would have fundamentally different abilities from zebrafish and goldfish, with respect to working memory. However, it is also not currently possible to distinguish whether fish performance in the tasks outlined above represents the use of working memory or other forms of short-term/delay memory. | No studies of salmonids could be found. However, studies of zebrafish (Danio rerio) show that they can successfully perform a delayed match-to-sample task. They can learn to discriminate between two colours and match-to-sample both simultaneously and with a 3-4 second delay between sample presentation and choice-making (Bloch et al. 2019). Bloch et al. (2019) clarify that “the presence of working memory without the mesencephalic dopamine neurons indicates the convergent evolution of this function in amniotes and teleosts”, but that their delayed match-to-sample task is an example of “operant conditioning in teleosts comparable to that in amniotes”. Importantly, they also note that zebrafish are only capable of the delayed match-to-sample task in a certain setup (e.g. they were successful when the response required “entering a hallway” but not “passing through a window”). Zebrafish are also capable of remembering a novel object after a much more significant delay of 2 hours or more, even when they are exposed to it only once (Lucon-Xiccato & Dadda 2014). Fontana et al. (2021) use the number of alternations in turn-direction in a free-movement pattern (FMP) Y-maze to infer working memory ability (they claim that alternations in turn-direction in the FMP Y-maze are reduced after treatment with memory-impairing drugs): they found that adult (4 month old) zebrafish increase the number of alternations after exposure to mild early life stress as larvae (daily stressors applied over 3 days). Finally, Sovrano et al. (2018) found that zebrafish and goldfish can successfully solve a detour task that requires them to “temporarily abandon the view of the goal-object (a group of conspecifics) to circumvent an obstacle”, suggesting that they possess working memory sufficient to enable their success in the task. It is unlikely that carp (or indeed salmon) would have fundamentally different abilities from zebrafish and goldfish, with respect to working memory. However, it is also not currently possible to distinguish whether fish performance in the tasks outlined above represents the use of working memory or other forms of short-term/delay memory. | A range of classic studies demonstrate that both octopuses and cuttlefish have short- (i.e., working memory) and long-term memory (Sanders & Young 1940; Schiller 1949). The memory trace was reported to last for weeks (Boal 1991; Fiorito & Scotto 1992) to months (Sanders 1970) (reviewed in Borrelli & Fiorito 2008). Octopuses, Octopus vulgaris, can also recall memories in as little as 1h after training trials cease in an avoidance learning task (Sanders & Barlow 1971). However, specific working memory tasks that quantify short-term memory load were not found. A systematic analysis of memory phases, retention and memory consolidation (as well as possible reconsolidation) are still insufficient in octopuses (and other cephalopods) when compared with other taxa. | The crab Neohelice granulata learns where food will be provided and remembers that spot even 24 hours after trials (Klappenbach et al, 2020). Crabs are able to memorize, however there is no information on working memory load in Portunidae. | Both sexes displayed place memory for the exit location and reduced latency to exit during trials 24 h, 48 h, 72 h, and 1 week after initial training trials, suggesting that spatial memories in crayfish are relatively enduring (Tierney and Andrews, 2013). “.. crayfish [have the ability] to learn and remember a location and a motor task. In an experiment carried out by Bierbower et al., (2012) crayfish learnt and remembered how to move their chelipeds through a tight access point which led to a food reward. | They assessed the impact of acute sulfoxaflor exposure on performance in two paradigms that have previously been used to illustrate negative impacts of neonicotinoid pesticides on bee learning and memory. They checked whether acute sulfoxaflor exposure influences (a) olfactory conditioning performance in both bumblebees (Bombus terrestris) and honeybees (Apis mellifera), using a proboscis extension reflex assay, and (b) working memory performance of bumblebees, using a radial-arm maze. They found no evidence to suggest that sulfoxaflor influenced performance in either paradigm. Their results suggest that despite a shared mode of action between sulfoxaflor and neonicotinoid-based insecticides, widely documented effects of neonicotinoids on bee cognition may not be observed with sulfoxaflor, at least at acute exposure regimes (Siviter et al., 2019). Chronic exposure is nonetheless clearly relevant for larval brood, and the same meta-analysis highlighted that exposure as a larva is more likely to have a negative impact on bee learning than adult exposure (Siviter et al., 2018, 2019). | In an experiment which aimed to assess learning and memory through metamorphosis, third instar Manduca sexta (superfamily Bombycoidea) larvae retained a conditioned odor aversion into the fifth instar, but not into adulthood. When fifth instar larvae were trained on the same odor association, the aversion persisted into adulthood (Blakiston et al. 2008). Similarly, in a separate experiment on Grapholita molesta (Lepidoptera Tortricidae), avoidance of the odor ethyl acetate was learned during the larval stage and retained for 72 hours after metamorphosis (Sant’Ana et al. 2021). Pszczolkowski & Brown 2005 used preference induction and aversive conditioning in codling moth larvae and found that larvae retained information for 3 days for aversive conditioning and only 3 hours for preference induction leaning. However, Zhu et al. (2021) used a T-maze apparatus to examine the effect of group/solitary living on the memory of rewards/punishments in fifth instar silkworm larvae. They found no effect of living condition on memory and overall found no change in the preference for the rewarded/punished side of the T-maze, suggesting lack of memory or learning. They were relying on odor cues being paired with the rewarded/punished sides of the maze and it is possible that the odors selected could not be discriminated by the silkworms. | ||||||||||||||||
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