Olfactory self-recognition in two species of snake.

Mark tests, in which an animal uses a mirror to locate and examine an otherwise unnoticeable mark on its own body, are commonly used to assess self-recognition, which may have implications for self-awareness. Recently, several olfactory-reliant species have appeared to pass odour-based versions of the mark test, though it has never been attempted in reptiles. We conducted an odour-based mark test on two species of snakes, Eastern gartersnakes and ball pythons, with widely divergent ecologies (i.e. terrestrial foragers that communally brumate versus semi-arboreal ambush predators that do not). We find that gartersnakes, but not ball pythons, pass the test, and a range of control tests suggest this is based on self-recognition. Gartersnakes are more social than ball pythons, supporting recent suggestions that social species are more likely to self-recognize. These results open the door to examination of the ecology of self-recognition, and suggest that this ability may evolve in response to species-specific ecological challenges, some of which may align with complexity of social structures.

Socially-mediated activation in the snake social-decision-making network.

Brain areas important for social perception, social reward, and social behavior - collectively referred to as the social-decision-making network (SDN) - appear to be highly conserved across taxa. These brain areas facilitate a variety of social behaviors such as conspecific approach/avoidance, aggression, mating, parental care, and recognition. Although the SDN has been investigated across taxa, little is known about its functioning in reptiles. Research on the snake SDN may provide important new insights, as snakes have a keen social perceptual system and express a relatively reduced repertoire of social behaviors. Here, we present the results of an experiment in which ball pythons (Python regius) interacted with a same-sex conspecific for one hour and neural activation was investigated through Fos immunoreactivity. Compared to controls, snakes that interacted socially had higher Fos counts in brain areas implicated in social behavior across taxa, such as the medial amygdala, preoptic area, nucleus accumbens, and basolateral amygdala. Additionally, we found differential Fos immunoreactivity in the ventral amygdala, which facilitates communication between social brain areas. In many of these areas, Fos counts differed by sex, which may be due to increased competition between males. Fos counts did not differ in early sensory (i.e., vomeronasal) processing structures. As ball python social systems lack parental care, cooperation, or long-term group living, these results provide valuable insight into the basal functions of the vertebrate social decision-making network.

Bolder together: conformity drives behavioral plasticity in eastern gartersnakes.

Personality traits drive individual differences in behaviour that are consistent across time and context. Personality limits behavioural plasticity, which could lead to maladaptive choices if animals cannot adapt their behavior to changing conditions. Here, we assessed consistency and flexibility in one personality trait, boldness, across non-social and social contexts in eastern gartersnakes (Thamnophis sirtalis sirtalis). Snakes explored a novel open arena either alone or in a pair. Pairs were assigned based on the data from the solo trials, such that each snake was paired once with a bolder and once with a less bold partner. We predicted that snakes would conform when in a social context, displaying plasticity in their personality, and causing boldness scores to converge. We found that snakes were consistent within contexts (solo or paired), but changed their behavior across contexts (from solo to paired). Plasticity in boldness resulted from an interaction between conformity and repeatable individual differences in plasticity. In line with some data on other species, snakes conformed more when they were the less bold partner. Personality reflects a consistent bias in decision-making, but our results highlight that the cognitive processes that drive the expression of personality traits in behavior are flexible and sensitive to social context. We show that both consistency and plasticity combine to shape snake social behavior in ways that are responsive to competition. This pattern of behavior may be particularly beneficial for species in which group-living is seasonal.

Western Hognose Snakes (Heterodon nasicus) Prefer Environmental Enrichment.

The environmental enrichment needs of snakes are often disregarded. Using preference testing, we aimed to shed light on the enrichment preferences of a popular pet species, the western hognose snake (Heterodon nasicus). Snakes' enclosures were divided into enriched and standard sides. The enriched half had substrate for burrowing, interactive stimuli, and a large water dish. The standard half had paper towel substrate and a small water dish. Each side also contained a single shelter. We provided belly heat to create a thermal gradient on one side of the cage. Snakes were observed for 6 days, four times daily. We predicted a preference for enriched conditions and, as snakes are ectothermic, a preference for the warmer side. Snakes were additionally given an exploration assay, to explore whether differences in preference for environmental enrichment interact with boldness levels. We found that hognose snakes preferred enrichment, and the strength of this preference increased over time. Preference for enrichment was stronger when the enriched side was cooler. This may be due to the burrowing tendencies of these snakes. We found no relationship between preference and boldness. These findings emphasise the importance of preference testing in establishing research-informed enrichment opportunities for reptiles.

Functional dissociation along the rostrocaudal axis of Japanese quail hippocampus.

The mammalian hippocampus (Hp) can be functionally segregated along its septotemporal axis, with involvement of dorsal hippocampus (dHp) in spatial memory and ventral hippocampus (vHp) in stress responses and emotional behaviour. In the present study, we investigate comparable functional segregation in proposed homologues within the avian brain. Using Japanese quail (Coturnix Japonica), we report that bilateral lesions of the rostral hippocampus (rHp) produce robust deficits in a spatial Y-maze discrimination (YMD) test while sparing performance during contextual fear conditioning (CFC), comparable to results from lesions to homologous regions in mammals. In contrast, caudal hippocampus (cHp) lesions failed to produce deficits in either CFC or YMD, suggesting that, unlike mammals, both cHp and rHp of birds can support emotional behavior. These observations demonstrate functional segregation along the rostrocaudal axis of the avian Hp that is comparable in part to distinctions seen along the mammalian hippocampal septotemporal axis.

Protocol for inducing hippocampal formation lesions and associated behavioral testing in Japanese quail.

Here, we present a protocol for inducing selective lesions in the hippocampal formation of Japanese quail (Coturnix japonica), coupled with associated behavioral testing. We first describe the surgical procedure for aspiration lesions in Japanese quail. We then detail two well-known hippocampus-dependent behavioral tests adapted to birds-foraging array (FA) and spontaneous object recognition (SOR). This protocol is adapted from those used in mammals and can be used to study the involvement of Japanese quail memory centers in declarative memory. For complete details on the use and execution of this protocol, please refer to Damphousse et al. (2022).

Experience-Dependent Egr1 Expression in the Hippocampus of Japanese Quail.

The hippocampal formation (HF) is a structure critical to navigation and many forms of memory. In mammals, the firing of place cells is widely regarded as the fundamental unit of HF information processing. Supporting homology between the avian and mammalian HF, context-specific patterns of Egr1 have been reported in birds that are comparable to those produced by place cell firing in mammals. Recent electrophysiological data, however, suggest that many avian species lack place cells, potentially undermining the correspondence between Egr1 and place cell-related firing in the avian brain. To clarify this, the current study examines Egr1 expression in Japanese quail under conditions known to elicit only weakly spatially modulated firing patterns and report robust context-dependent Egr1 expression. These data confirm that context-dependent expression of Egr1 is not dependent on precise place fields and provide insight into how these birds are able to perform complex spatial tasks despite lacking mammalian-like place cells.

Behavioral evidence for two distinct memory systems in rats.

Serial reaction time tasks, in which subjects have to match a target to a cue, are used to explore whether non-human animals have multiple memory systems. Predictable sub-sequences embedded in the sequence of cues are responded to faster, demonstrating incidental learning, often considered implicit. Here, we used the serial implicit learning task (SILT) to determine whether rats' memory shows similar effects. In SILT, subjects must nose-poke into a sequence of two lit apertures, S1 and S2. Some S1 are always followed by the same S2, creating predictable sequences (PS). Across groups, we varied the proportion of PS trials, from 10 to 80%, and show that rats with more PS experience do better on them than on unpredictable sequences, and better than rats with less experience. We then introduced test trials in which no S2 was cued. Rats with more PS experience did better on test trials. Finally, we reversed some sequences (from predictable to unpredictable and vice versa) and changed others. We find that rats with more PS experience perseverate on old (now incorrect) responses more than those with less PS experience. Overall, we find a discontinuity in performance as the proportion of PS increases, suggesting a switch in behavioral strategies or memory systems, which we confirm using a Process Dissociation Procedure analysis. Our data suggest that rats have at least two distinct memory systems, one of which appears to be analogous to human implicit memory and is differentially activated by varying the proportion of PS in our task.

Dissociation of spatial and object memory in the hippocampal formation of Japanese quail.

The mammalian temporal cortex can be functionally segregated into regions that encode spatial information and others that are predominantly responsible for object recognition. In the present study, we report comparable functional segregation in the avian brain. Using Japanese quail, we find that bilateral lesions of the hippocampus (Hp) produce robust deficits in performance in a foraging array (FA) spatial memory task, while sparing spontaneous object recognition (SOR). In contrast, lesions to the adjacent area parahippocampalis (APH) compromise both SOR and FA. These observations demonstrate a functional dissociation between Hp and APH that is comparable to the distinctions seen in mammals between the hippocampus and surrounding temporal cortex.

Reaction to novelty as a behavioral assay of recognition memory in homing pigeons and Japanese quail.

Spontaneous novelty preference is apparent in a wide array of animals, including mammals, birds, reptiles, and fish. This provides a powerful behavioral assay to assess whether an animal can recognize a diverse array of stimuli in a common paradigm. Surprisingly, no research has been conducted in birds using novelty approach under conditions comparable to the spontaneous object recognition (SOR) protocols that have become standard across other animals. To correct this, the current study adapts a number of SOR protocols commonly used in mammals to characterize novelty approach in Silver King pigeons and Japanese quail. We show that, in general, both quail and pigeons readily approach novel objects or locations when tested using SOR protocols, although pigeons show a neophilic response under some conditions in which quail do not. Neither quail nor pigeons readily approach objects in novel contexts or novel locations. These data show that SOR can be successfully adapted to birds, allowing for more direct comparison between mammals and birds in tasks of shared ecological relevance.

Taking shortcuts in the study of cognitive maps.

Harten, Katz, Goldshtein, Handel, and Yovel (Science, 369, 194-197, 2020) tracked fruit bats from their first flight and demonstrate that they can perform novel shortcuts both within and from outside their home ranges, fulfilling an important criterion of a cognitive map. Their richly detailed data set could be used to explore more key aspects of spatial cognition.

Follow the straggler: zebrafish use a simple heuristic for collective decision-making.

Animal groups often make decisions sequentially, from the front to the back of the group. In such cases, individuals can use the choices made by earlier ranks, a form of social information, to inform their own choice. The optimal strategy for such decisions has been explored in models which differ on, for example, whether or not agents take into account the sequence of observed choices. The models demonstrate that choices made later in a sequence are more informative, but it is not clear if animals use this information or rely instead on simpler heuristics, such as quorum rules. We show that a simple rule 'copy the last observed choice', gives similar predictions to those of optimal models for most likely sequences. We trained groups of zebrafish to choose one arm of a Y-maze and used them to demonstrate various sequences to naive fish. We show that the naive fish appear to use a simple rule, most often copying the choice of the last demonstrator, which results in near-optimal choices at a fraction of the computational cost.

Pair foraging degrades socially transmitted food preferences in rats.

Following presentation of a novel food odor on the breath of a conspecific, naïve rats will exhibit a preference for that food, a form of learning called social transmission of food preference (STFP). When tested in isolation, STFPs are robust, persisting for up to a month and overcoming prior aversions. This testing protocol, however, does not account for rats' ecology. Rats and other rodents forage in small groups, rather than alone. We allowed rats to forage in pairs and found that, following social foraging, they no longer displayed a food preference, i.e., that STFPs degrade during social foraging. Non-foraging rats exposed to the same foods for the same amount of time in isolation maintained their preferences. We also examined whether individual differences between rats affect STFP. Neither boldness nor sociability predicted initial STFP strength, but bolder rats' preferences degraded more following social foraging. Shyer rats were more likely to eat at the same time as their partner. By tracking rats' interactions during social foraging, we show that they use complex rules to combine their own preferences with socially acquired information about foods in their environment. These results situate STFP within the behavioral ecology of foraging and suggest that individual traits and the interactions between them modulate how social learning is maintained, modified, or lost.

Methods for the effective study of collective behavior in a radial arm maze.

Collective behaviors are observed throughout nature, from bacterial colonies to human societies. Important theoretical breakthroughs have recently been made in understanding why animals produce group behaviors and how they coordinate their activities, build collective structures, and make decisions. However, standardized experimental methods to test these findings have been lacking. Notably, easily and unambiguously determining the membership of a group and the responses of an individual within that group is still a challenge. The radial arm maze is presented here as a new standardized method to investigate collective exploration and decision-making in animal groups. This paradigm gives individuals within animal groups the opportunity to make choices among a set of discrete alternatives, and these choices can easily be tracked over long periods of time. We demonstrate the usefulness of this paradigm by performing a set of refuge-site selection experiments with groups of fish. Using an open-source, robust custom image-processing algorithm, we automatically counted the number of animals in each arm of the maze to identify the majority choice. We also propose a new index to quantify the degree of group cohesion in this context. The radial arm maze paradigm provides an easy way to categorize and quantify the choices made by animals. It makes it possible to readily apply the traditional uses of the radial arm maze with single animals to the study of animal groups. Moreover, it opens up the possibility of studying questions specifically related to collective behaviors.

Social learning and associative processes: A synthesis.

Social learning is often considered different from asocial learning in both its characteristics and mechanisms. I presented pigeons with a concurrent discrimination task in which they received artificial social information, consisting of simple shapes that distributed themselves between two options similarly to how conspecifics might. Subjects in some conditions combined personal information about the two options with this social-like information, but subjects in conditions in which personal information was very reliable ignored the social cues, much like cases in which animals only choose to copy choices of others under certain conditions. I present a modification of a popular associative model of individual learning that can replicate these results, despite not distinguishing between social and asocial cues. The model suggests that the adaptive use of social information does not require the assumption of specifically social learning strategies, but may be driven by the overshadowing of less reliable asocial cues by more reliable social cues. (PsycINFO Database Record

Raising the bar on studying cultural evolution.

Sasaki and Biro (2017, Nature Communications, 8, 15049) show that pairs of pigeons can increase the efficiency of their homing routes over several 'generations' in which pair members are gradually replaced by naïve birds. Their findings show that socially transmitted cumulative alterations of behavior are not unique to humans and suggest a way to examine potential mechanisms of cultural evolution.

'Sociability' affects the intensity of mate-choice copying in female guppies, Poecilia reticulata.

Selecting a quality mate can involve acquiring and accessing large amounts of information; information that can be obtained either independently or socially. One means of learning about mates socially is to attend to other members of one's sex and copy their mate choices. It is possible however that not all individuals of a species benefit equally from, or are equally effective at, copying. We examined whether female guppies copied the mate choices of other females. Then, in a separate context we measured each female's 'sociability': their proclivity to affiliate with other guppies. In the mate-choice copying procedure, 'focal' females chose to spend time near two putative mates. Next, focals observed another (model) female interact with the focal's non-preferred male. Finally, the focal again chose between the same two males. For sociability, we examined the time focal females spent near a trio of other guppies. Females did indeed mate copy: they spent more time with their non-preferred male when a model female had been seen interacting with that male. The effect however was highly variable. Sociability significantly predicted the intensity of mate-choice copying. Results suggest that individuals vary consistently in the types of information they use when making mating decisions.

Behavioural plasticity across social contexts is regulated by the directionality of inter-individual differences.

An individual's behavioural phenotype is a combination of its unique behavioural propensities and its responsiveness to environmental variation, also known as behavioural plasticity. In social species, we must not only explore how individuals respond to variations in the physical environment but also how they react to changes in their social environment. A growing body of work has demonstrated that the behavioural heterogeneity of a group can alter its responsiveness, decision making, and fitness. Whether an individual is more or less extreme than a partner - what we term its 'relative personality' - may also alter individual behavioural responses. We determined exploratory tendencies of individual zebrafish (Danio rerio) and then constructed pairs with varying differences in 'relative personality' to determine the effect of differences between partners on behavioural plasticity. We find that relative personality, but not the magnitude of the difference between partners, is the most important determinant of behavioural plasticity across social treatments. Despite this overall effect, pairs of fish exhibited no predictable leader-follower interactions, suggesting that details of the experimental paradigm may be important in shaping social dynamics.

Collective learning and optimal consensus decisions in social animal groups.

Learning has been studied extensively in the context of isolated individuals. However, many organisms are social and consequently make decisions both individually and as part of a collective. Reaching consensus necessarily means that a single option is chosen by the group, even when there are dissenting opinions. This decision-making process decouples the otherwise direct relationship between animals' preferences and their experiences (the outcomes of decisions). Instead, because an individual's learned preferences influence what others experience, and therefore learn about, collective decisions couple the learning processes between social organisms. This introduces a new, and previously unexplored, dynamical relationship between preference, action, experience and learning. Here we model collective learning within animal groups that make consensus decisions. We reveal how learning as part of a collective results in behavior that is fundamentally different from that learned in isolation, allowing grouping organisms to spontaneously (and indirectly) detect correlations between group members' observations of environmental cues, adjust strategy as a function of changing group size (even if that group size is not known to the individual), and achieve a decision accuracy that is very close to that which is provably optimal, regardless of environmental contingencies. Because these properties make minimal cognitive demands on individuals, collective learning, and the capabilities it affords, may be widespread among group-living organisms. Our work emphasizes the importance and need for theoretical and experimental work that considers the mechanism and consequences of learning in a social context.