Conspecific Cues Research Articles

Public information use—are invasive demersal fish species more effective than natives?

Abstract Organisms determine environmental quality using their senses and personal experience (personal information) but can also use byproducts of other individuals’ activities (i.e. public information). The ability to use public information originating from both con- and heterospecifics gives an advantage over individuals relying only on personal information or conspecific cues. The role of public information in invasion ecology is of high concern, as any differences in this aspect between alien and native species may determine the success of the former. Here, we studied 2 pairs of sympatric invasive and native demersal fish species (racer goby Babka gymnotrachelus/European bullhead Cottus gobio; monkey goby Neogobius fluviatilis/gudgeon Gobio gobio) facing 2 types of public cues (associated with antipredatory and foraging behavior). We used them as a model to check if the invaders could use public information from more sources than the natives. Both invaders and the native gudgeon used cues from con- and heterospecifics, exhibiting antipredatory behavior, while the native bullhead failed to recognize such cues from heterospecifics. The monkey goby and both native species were attracted to foraging cues from donors less likely to exert competitive pressure on the observer (i.e. native species rather than potentially more aggressive invaders). On the other hand, the racer goby appeared unable to correctly recognize heterospecific foraging cues. Our results showed that public cues can enable invaders to read threat from a wide range of individuals and to find optimal food patches, which may contribute to their invasion success.

Background predation risk induces anxiety-like behaviour and predator neophobia in zebrafish

Prey face a major challenge in balancing predator avoidance with other essential activities. In environments with high risk, prey may exhibit neophobia (fear of novelty) due to the increased likelihood of novel stimuli being dangerous. The zebrafish, Danio rerio, is an established model organism for many scientific studies. Although spatial and object neophobia in zebrafish have received previous attention, little is known about the role of background risk in inducing neophobia in zebrafish. Here, we present two experiments using zebrafish to explore whether background predation risk can induce anxiety-like behaviour in a novel environment and neophobic responses when exposed to a novel odour. Over five days, we repeatedly exposed zebrafish to either high background risk in the form of chemical alarm cues (i.e., injured conspecific cues that indicate a predator attack) or a low-risk water control stimulus. In Experiment 1, when tested in a novel tank, zebrafish exposed to high predation risk displayed anxiety-like responses (reduced activity and increased bottom time spent) compared to their low-risk counterparts. Moreover, high-risk individuals showed reduced intra-session habituation to the novel tank compared to low-risk individuals. In Experiment 2, high-risk individuals exhibited fear responses toward a novel odour, unlike low-risk individuals. These results reveal that short-term repeated exposures to high risk can induce anxiety-like behaviour and predator odour neophobia in zebrafish.

Conspecific cues and breeding territory selection in Whinchat on abandoned fields

Many bird species use social information to guide territory selection. Different species in different habitats may use both pre-breeding and post-breeding conspecific cues. Abandoned agricultural fields are of particular interest for studies of conspecific attraction because the ephemeral nature of the habitat suggests territory search just before breeding, but high predation pressure suggests the use of performance-based conspecific cues. We investigated whether post-breeding or pre-breeding social cues affect Whinchat (Saxicola rubetra) abundance at the territorial scale during a two-year experiment in abandoned fields. We assigned 27 experimental plots (3.14 ha) to one of three treatments: post-breeding treatment, pre-breeding treatment and silent control. We conducted playback experiments with fledgling calls (evidence of past reproductive success) during the post-breeding period and male songs (evidence of conspecific presence) during the pre-breeding period. We estimated the difference in Whinchat abundance in two consecutive years and tested whether this value differed between treatment and control plots. We observed a slight increase (0.67 ± 0.29 pairs per plot) in Whinchat abundance in the post-breeding treatment plots and no significant changes in the pre-breeding (−0.22 ± 0.32 pairs per plot) and control (−0.22 ± 0.22 pairs per plot) plots. Our results suggest that Whinchats do not use conspecific acoustic cues during the pre-breeding period and provide limited evidence for the use of fledgling calls as conspecific cues in the post-breeding period.

Mice integrate conspecific and contextual information in forming social episodic-like memories under spontaneous recognition task conditions

The ability to remember unique past events (episodic memory) may be an evolutionarily conserved function, with accumulating evidence of episodic-(like) memory processing in rodents. In humans, it likely contributes to successful complex social networking. Rodents, arguably the most used laboratory models, are also rather social animals. However, many behavioural paradigms are devoid of sociality, and commonly-used social spontaneous recognition tasks (SRTs) are open to non-episodic strategies based upon familiarity. We address this gap by developing new SRT variants. Here, in object-in-context SRTs, we asked if context could be specified by the presence/absence of either a conspecific (experiment 1) or an additional local object (experiment 2). We show that mice readily used the conspecific as contextual information to distinguish unique episodes in memory. In contrast, no coherent behavioural response emerged when an additional object was used as a potential context specifier. Further, in a new social conspecific-in-context SRT (experiment 3) where environment-based change was the context specifier, mice preferably explored a more recently-seen familiar conspecific associated with contextual mismatch, over a less recently-seen familiar conspecific presented in the same context. The results argue that, in incidental SRT conditions, mice readily incorporate conspecific cue information into episodic-like memory. Thus, the tasks offer different ways to assess and further understand the mechanisms at work in social episodic-like memory processing.

The indirect influence of potential mates on survival and reproduction of Tyrophagus curvipenis (Acari: Acaridae).

The social-sexual environment is well known for its influence on the survival of organisms by modulating their reproductive output. However, whether it affects survival indirectly through a variety of cues without physical contact and its influence relative to direct interaction remain largely unknown. In this study, we investigated both the indirect and direct influences of the social-sexual environment on the survival and reproduction of the mite Tyrophagus curvipenis (Acari: Acaridae). The results demonstrated no apparent influence of conspecific cues on the survival of mites, but the survival and reproduction of mated female mites significantly changed, with the females mated with males having a significantly shortened lifespan and increased lifetime fecundity. For males, no significant difference was observed across treatments in their survival and lifespan. These findings indicate that direct interaction with the opposite sex has a much more profound influence on mites than indirect interaction and highlight the urgent need to expand research on how conspecific cues modulate the performance of organisms with more species to clarify their impacts across taxa.

Sub-lethal effects of the insecticide, imidacloprid, on the responses of damselfly larvae to chemosensory cues indicating predation risk

Insecticides, including the widely used neonicotinoids, can affect both pest and non-target species. In addition to lethal effects, these insecticides at sub-lethal levels may cause disruption to sensory perception and processing leading to behavioural impairments. In this laboratory experiment, we investigated the effects of a 10-day exposure to the neonicotinoid insecticide, imidacloprid, on the behaviour of larvae of the damselfly, Lestes congener. In tests of baseline activity, imidacloprid concentrations of 1.0 and 10.0 μg/L caused significant reductions in foraging behaviour. Moreover, in response to chemical cues that indicate a potential risk to the larvae, imidacloprid caused the loss of an appropriate antipredator response (reduced foraging) depending on the concentration and duration of exposure. Imidacloprid at 0.1 μg/L caused the loss of responses toward the odour of a beetle (Dytiscus spp.) predator after 10 days of exposure, whereas 1.0 μg/L caused lost responses toward both the predator odour and injured conspecific cues (i.e., alarm cues) and after only 2 days of exposure. However, at 10.0 μg/L, larvae responded appropriately to both cues throughout the duration of the study, suggesting compensatory responses to imidacloprid at higher concentrations. Hence, the lack of appropriate responses at 1.0 μg/L likely resulted from a cognitive impairment rather than chemical alteration of these important chemosensory cues. In the natural environment, such effects will likely cause decreased survivorship in predator encounters. Hence, imidacloprid exposure, even at low concentrations, could have adverse consequences for chemosensory ecology of this damselfly species.

Conspecific cues mediate habitat selection and reproductive performance in a haplodiploid spider mite

Abstract Selection of a suitable habitat by animals before settlement is critical for their survival and reproduction. In silk-spinning arthropods like spider mites, denser webs offer protection from predation and serve as a dispersal mode. Settling in habitats with the presence of conspecifics and silk webs can benefit the habitat-searching females. Silk and conspecifics usually coexist, but their distinct effects on female colonization have received little attention. In this study, we used a haplodiploid spider mite, Tetranychus ludeni Zacher (Acari: Tetranychidae), to examine the impact of conspecific cues, including cues from ovipositing conspecifics and silk, on habitat selection and subsequent reproductive performance of females. Results show that females significantly preferred habitats with cues from neighboring conspecifics and silk and neighboring conspecifics induced additive effect to that of silk on habitat selection. Conspecific cues did not boost female reproduction but facilitated females laying larger eggs that were more likely to be fertilized and to develop into daughters. When given a choice between silk-covered and clean habitats, females preferred silk-covered habitats, laid a similar number of eggs with similar size, but produced more daughters, suggesting that T. ludeni females can adjust the size threshold for fertilization in response to the current social environment. Knowledge of this study improves our understanding of spider mite habitat selection and post-settlement reproductive performance behaviors.

Predator metamorphosis and its consequence for prey risk assessment.

Living with a diverse array of predators provides a significant challenge for prey to learn and retain information about each predator they encounter. Consequently, some prey respond to novel predators because they have previous experience with a perceptually similar predator species, a phenomenon known as generalization of predator recognition. However, it remains unknown whether prey can generalize learned responses across ontogenetic stages of predators. Using wood frog tadpole (Lithobates sylvaticus) prey, we conducted two experiments to explore the extent of predator generalization of different life stages of two different predators: (1) predacious diving beetles (Dytiscus sp.) and (2) tiger salamanders (Ambystoma mavortium). In both experiments, we used chemical alarm cues (i.e., injured conspecific cues) to condition tadpoles to recognize the odor of either the larval or adult stage of the predator as risky. One day later, we tested tadpoles with either the larval or adult predator odor to determine whether they generalized their learned responses to the other life stages of the predator. Tadpoles generalized between larval and adult beetle odors but failed to generalize between larval and adult salamander odors. These results suggest that the odor of some predator species changes during metamorphosis to an extent that reduces their recognisability by prey. This "predator identity reset" increases the number of threats to which prey need to attend.

Neurobiology of Pathogen Avoidance and Mate Choice: Current and Future Directions.

Animals are under constant threat of parasitic infection. This has influenced the evolution of social behaviour and has strong implications for sexual selection and mate choice. Animals assess the infection status of conspecifics based on various sensory cues, with odours/chemical signals and the olfactory system playing a particularly important role. The detection of chemical cues and subsequent processing of the infection threat that they pose facilitates the expression of disgust, fear, anxiety, and adaptive avoidance behaviours. In this selective review, drawing primarily from rodent studies, the neurobiological mechanisms underlying the detection and assessment of infection status and their relations to mate choice are briefly considered. Firstly, we offer a brief overview of the aspects of mate choice that are relevant to pathogen avoidance. Then, we specifically focus on the olfactory detection of and responses to conspecific cues of parasitic infection, followed by a brief overview of the neurobiological systems underlying the elicitation of disgust and the expression of avoidance of the pathogen threat. Throughout, we focus on current findings and provide suggestions for future directions and research.

The habitat preferences of Idiosepius pygmaeus and their use of conspecific cues

AbstractThe two‐toned pygmy squid (Idiosepius pygmaeus, Steenstrup, 1881) is a small, tropical cephalopod that inhabits seagrass meadows and is known to attach to blades of seagrass using a specialised adhesive organ. A global decline in seagrass habitat due to anthropogenic disturbances may threaten the species that rely on seagrass meadows for shelter, foraging and other crucial activities. It is unclear if I. pygmaeus can utilise alternative habitats in the absence of seagrass. Here, we test the effect of habitat type, material and composition type, and the presence of conspecifics on the settlement preferences of I. pygmaeus. Individuals each underwent three separate experiments: (1) testing the preference between their known habitat, Zostera muelleri subsp. Capricorni and potential substitute, Sargassum, (2) testing the preference to attach to a natural or artificial structure of similar shape and size, and (3) testing the preference of identical habitats, one with a conspecific adhered to and one without. We found that I. pygmaeus did not have a strong preference for either Zostera or Sargassum. However, a strong preference was found for attachment to the natural structure over the artificial one. There was also strong evidence for the use of conspecific cues in habitat choice, with 75% of individuals selecting the habitat that contained a conspecific. As habitat loss is the leading cause of species extinction, the knowledge of habitat preferences for I. pygmaeus is vital in order to assess their risk of population decline. The findings of this study suggest that I. pygmaeus could utilise an alternative habitat in the presence of seagrass meadow reduction, which is under threat from human activity.

Transcriptionally defined amygdala subpopulations play distinct roles in innate social behaviors

Social behaviors are innate and supported by dedicated neural circuits, but the molecular identities of these circuits and how they are established developmentally and shaped by experience remain unclear. Here we show that medial amygdala (MeA) cells originating from two embryonically parcellated developmental lineages have distinct response patterns and functions in social behavior in male mice. MeA cells expressing the transcription factor Foxp2 (MeAFoxp2) are specialized for processing male conspecific cues and are essential for adult inter-male aggression. By contrast, MeA cells derived from the Dbx1 lineage (MeADbx1) respond broadly to social cues, respond strongly during ejaculation and are not essential for male aggression. Furthermore, MeAFoxp2 and MeADbx1 cells show differential anatomical and functional connectivity. Altogether, our results suggest a developmentally hardwired aggression circuit at the MeA level and a lineage-based circuit organization by which a cell’s embryonic transcription factor profile determines its social information representation and behavioral relevance during adulthood.

Response to competing conspecific cues depends on social context in the honey bee Apis mellifera

Response to competing conspecific cues depends on social context in the honey bee Apis mellifera

Perception of con- and heterospecific injury cues in tadpoles of dendrobatid, ranid and bufonid frogs (Anura)

Predator-prey interactions are vital for organismal survival. They shape anti-predator mechanisms and often depend on sensory abilities. Tadpoles use chemical cues, such as injury cues (alarm cues), to assess predation risks and modify their life-history, morphology, and behaviours accordingly. However, the prevalence of chemically mediated anti-predator responses in species with distinct ecological niches (e.g. within phytotelmata) remains unknown, hindering our understanding of the ecological significance and evolution of alarm substances. Therefore, our study aimed to investigate chemically mediated anti-predator responses in tadpoles of two Neotropical poison dart frogs, Ranitomeya sirensis and Epipedobates anthonyi (and compare their responses to two Palearctic model organisms, Rana temporaria and Bufo bufo, which are known to utilise alarm substances). Through behavioural bioassays, we exposed predator-naïve tadpoles to extracts of each species (i.e. con- and heterospecific cues), including water as a control (i.e. five treatments per species). We assessed changes in their activity before and after stimulus introduction. Our results show that E. anthonyi did not respond to any of the stimuli, whereas R. sirensis displayed increased activity levels exclusively in response to conspecific cues, but not to heterospecific cues. With this, our findings suggest a specialized recognition system in R. sirensis, potentially directed at conspecific competitors but likely unrelated to anti-predator mechanisms. In contrast, E. anthonyi may be insensitive to injury cues or utilize alternative sensory modalities to respond to acute predation events. This study sheds light on the chemical alarm response system of Neotropical poison dart frog tadpoles, providing foundational understanding of how dendrobatids react to injury cues. It prompts questions about the ecological significance and evolutionary implications of chemical communication in species facing extreme resource limitation during development and underscores the importance of comparative research for understanding chemical communication in diverse aquatic ecosystems.

Induction of larval settlement in crown-of-thorns starfish is not mediated by conspecific cues

Population irruptions of crown-of-thorns starfish (COTS; Acanthaster spp.) remain a major cause of coral reef degradation throughout the Pacific and Indian Oceans and are inherently modulated by larval settlement and recruitment success. Gregarious larval settlement, as exhibited by many other ecologically important marine invertebrates, can catalyse population growth and replenishment. However, whether conspecific cues induce or influence the settlement of COTS larvae remains a critical information gap. This experimental study examined the induction of COTS settlement in response to a range of conspecific cues associated with early- and late-stage herbivorous juveniles, corallivorous juveniles and adults. Competent COTS larvae were generally not induced to settle by the presence of conspecifics or cues associated with conspecifics, while the settlement success of COTS in the presence of coralline algae was not inhibited or enhanced by adding conspecific conditioned seawater. Rather than being reinforced by gregarious settlement, the recruitment of COTS populations appears dependent on associative settlement cues (i.e., coralline algae and/or associated microbial communities) signalling suitable benthic habitat.

Trait-Specific Indirect Effects Underlie Variation in the Response of Spiders to Cannibalistic Social Partners.

AbstractIn cannibalistic species, selection to avoid conspecifics may stem from the need to avoid being eaten or to avoid competition. Individuals may thus use conspecific cues to modulate their behavior to such threats. Yet the nature of variation for such cues remains elusive. Here, we use a half-sib/full-sib design to evaluate the contribution of (indirect) genetic or environmental effects to the behavioral response of the cannibalistic wolf spider Lycosa fasciiventris (Dufour, 1835) toward conspecific cues. Spiders showed variation in relative occupancy time, activity, and velocity on patches with or without conspecific cues, but direct genetic variance was found only for occupancy time. These three traits were correlated and could be lumped in a principal component: spiders spending more time in patches with conspecific cues moved less and more slowly in those areas. Genetic and/or environmental components of carapace width and weight loss in the social partner, which may reflect the quality and/or quantity of cues produced, were significantly correlated with this principal component, with larger partners causing focal individuals to move more slowly. Therefore, environmental and genetic trait variation in social partners may maintain trait diversity in focal individuals, even in the absence of direct genetic variation.

Assessment of predation risk through conspecific cues by anuran larvae

Accurate assessment of predation risk is critical for prey survival during predator–prey interactions. Prey can assess predation risk by the presence of cues dropped by predators themselves, but they can also gather information about risk level through cues released by other prey, avoiding the hazard of being in close proximity to predators. In this study, we examine the ability of anuran larvae (Pelobates cultripes) to detect predation risk indirectly when they are in contact with conspecifics that have been recently exposed to chemical stimuli from natural predators (larvae of aquatic beetles). In a first experiment, we confirmed that larvae exposed to predator cues exhibited innate defensive behavior, indicating that they perceived the risk of predation and, thus, could potentially act as risk indicators for naïve conspecifics. In a second experiment, we observed that unexposed larvae paired with a startled conspecific adjusted their antipredator behavior, presumably by mirroring conspecifics’ behavior and/or using chemical cues from their partners as a risk information source. This cognitive ability of tadpoles to assess predation risk through conspecific cues might play an important role in their interaction with predators, facilitating the early detection of potential threats to elicit appropriate antipredator responses and increase the chances of survival.

Emigration patterns of motile cryptofauna and their implications for trophic functioning in coral reefs.

Patterns of movement of marine species can reflect strategies of reproduction and dispersal, species' interactions, trophodynamics, and susceptibility to change, and thus critically inform how we manage populations and ecosystems. On coral reefs, the density and diversity of metazoan taxa are greatest in dead coral and rubble, which are suggested to fuel food webs from the bottom up. Yet, biomass and secondary productivity in rubble is predominantly available in some of the smallest individuals, limiting how accessible this energy is to higher trophic levels. We address the bioavailability of motile coral reef cryptofauna based on small-scale patterns of emigration in rubble. We deployed modified RUbble Biodiversity Samplers (RUBS) and emergence traps in a shallow rubble patch at Heron Island, Great Barrier Reef, to detect community-level differences in the directional influx of motile cryptofauna under five habitat accessibility regimes. The mean density (0.13-4.5 ind cm-3) and biomass (0.14-5.2 mg cm-3) of cryptofauna were high and varied depending on microhabitat accessibility. Emergent zooplankton represented a distinct community (dominated by the Appendicularia and Calanoida) with the lowest density and biomass, indicating constraints on nocturnal resource availability. Mean cryptofauna density and biomass were greatest when interstitial access within rubble was blocked, driven by the rapid proliferation of small harpacticoid copepods from the rubble surface, leading to trophic simplification. Individuals with high biomass (e.g., decapods, gobies, and echinoderms) were greatest when interstitial access within rubble was unrestricted. Treatments with a closed rubble surface did not differ from those completely open, suggesting that top-down predation does not diminish rubble-derived resources. Our results show that conspecific cues and species' interactions (e.g., competition and predation) within rubble are most critical in shaping ecological outcomes within the cryptobiome. These findings have implications for prey accessibility through trophic and community size structuring in rubble, which may become increasingly relevant as benthic reef complexity shifts in the Anthropocene.

Conspecific scent marks may influence underground site selection by a fossorial reptile

Conspecific cues often provide social information on habitat quality that is considered when deciding to settle at a specific site. The type of sensory cues useful for this will depend on the environment. For amphisbaenians, reptiles adapted to an underground life with highly reduced sight, chemoreception is especially useful to recognize conspecifics. Here, we first analyzed the lipophilic compounds from precloacal gland secretions of the amphisbaenian Blanus cinereus, showing that there were sex- and size-related variations in the proportions of the three major compounds. Then, we tested in the laboratory whether there was an underground site selection based on conspecific chemical cues (substrate scent marks) in two different contexts. In loose substrates, both male and female amphisbaenians tended to choose first the scent-marked substrates more often when the individual that produced the scent, independently of its sex, was relatively larger than the focal individual. In contrast, inside semi-permanent galleries, males, but not females, chose the scent-marked gallery more often when the scent donor, independently of its sex, was relatively smaller. These results suggest that the proportions of compounds in scent marks may allow amphisbaenians to estimate the body size of the producer and that this information affects their site selection decisions. However, the different substrate-dependent responses suggest a different meaning and usefulness of scent marks depending on the context.Significance statementThe presence of your conspecific in a site may indicate that this is a “quality” site to live in. If you are blind and live underground, smell is one of the best options for detecting conspecifics and assessing how good are your surroundings. Here, we test whether a blind amphisbaenian reptile that spends its life buried in sandy substrates uses conspecific chemical stimuli to choose where to settle. We found that this decision is influenced by the microhabitat type, sex, and the size difference between the individual that sniffs and the producer of the scent. Amphisbaenians seem to detect and assess conspecific traits based on the differences in compounds in their odors. Therefore, using conspecific scent to assess habitat quality may help fossorial animals to live underground.

The role of donor and receiver size in the response to public cues in Hart’s rivulus, Anablepsoides hartii

Abstract Aquatic prey use chemical alarm cues as public information sources to optimize behavioural decisions. Recent studies suggest that the contextual value of these cues is shaped by their source, the size of the donor relative to the receiver, and the size of the receiver itself. Here, we exposed Hart’s rivulus (Anablepsoides hartii) to conspecific or heterospecific alarm cues from donors that were either smaller or larger than the mean focal rivulus size. Smaller rivulus reduced foraging in response to conspecific and heterospecific cues, regardless of donor size. However, larger rivulus exhibited no reduction in foraging towards small conspecific cues and increased foraging towards small heterospecific cues. Additionally, while conspecific donors elicited strong predator avoidance, rivulus exhibited stronger responses to large vs. small heterospecific cues. Our results demonstrate that the value of alarm cues is shaped by the interacting effects of receiver size and the size and species of cue donors.

Alarm cues and alarmed conspecifics: neural activity during social learning from different cues in Trinidadian guppies.

Learning to respond appropriately to novel dangers is often essential to survival and success, but carries risks. Learning about novel threats from others (social learning) can reduce these risks. Many species, including the Trinidadian guppy (Poecilia reticulata), respond defensively to both conspecific chemical alarm cues and conspecific anti-predator behaviours, and in other fish such social information can lead to a learned aversion to novel threats. However, relatively little is known about the neural substrates underlying social learning and the degree to which different forms of learning share similar neural mechanisms. Here, we explored the neural substrates mediating social learning of novel threats from two different conspecific cues (i.e. social cue-based threat learning). We first demonstrated that guppies rapidly learn about threats paired with either alarm cues or with conspecific threat responses (demonstration). Then, focusing on acquisition rather than recall, we discovered that phospho-S6 expression, a marker of neural activity, was elevated in guppies during learning from alarm cues in the putative homologue of the mammalian lateral septum and the preoptic area. Surprisingly, these changes in neural activity were not observed in fish learning from conspecific demonstration. Together, these results implicate forebrain areas in social learning about threat but raise the possibility that circuits contribute to such learning in a stimulus-specific manner.