Animal cognition and culture mediate predator-prey interactions.

Predator-prey ecology and the study of animal cognition and culture have emerged as independent disciplines. Research combining these disciplines suggests that both animal cognition and culture can shape the outcomes of predator-prey interactions and their influence on ecosystems. We review the growing body of work that weaves animal cognition or culture into predator-prey ecology, and argue that both cognition and culture are significant but poorly understood mechanisms mediating how predators structure ecosystems. We present a framework exploring how previous experiences with the predation process creates feedback loops that alter the predation sequence. Cognitive and cultural predator-prey ecology offers ecologists new lenses through which to understand species interactions, their ecological consequences, and novel methods to conserve wildlife in a changing world.

Savviness of prey to introduced predators.

The prey naivety hypothesis posits that prey are vulnerable to introduced predators because many generations in slow gradual coevolution are needed for appropriate avoidance responses to develop. It predicts that prey will be more responsive to native than introduced predators and less responsive to introduced predators that differ substantially from native predators and from those newly established. To test these predictions, we conducted a global meta-analysis of studies that measured the wariness responses of small mammals to the scent of sympatric mammalian mesopredators. We identified 26 studies that met our selection criteria. These studies comprised 134 experiments reporting on the responses of 36 small mammal species to the scent of six introduced mesopredators and 12 native mesopredators. For each introduced mesopredator, we measured their phylogenetic and functional distance to local native mesopredators and the number of years sympatric with their prey. We used predator and prey body mass as a measure of predation risk. Globally, small mammals were similarly wary of the scent of native and introduced mesopredators; phylogenetic and functional distance between introduced mesopredators and closest native mesopredators had no effect on wariness; and wariness was unrelated to the number of prey generations, or years, since first contact with introduced mesopredators. Small mammal wariness was associated with predator-prey body mass ratio, regardless of the nativity. The one thing animals do not seem to recognize is whether their predators are native.

La hipótesis de la ingenuidad de la presa plantea que ésta es vulnerable a los depredadores introducidos porque se requiere que muchas generaciones atraviesen una coevolución lenta y gradual para que se desarrollen las respuestas de evasión adecuadas. La hipótesis supone que la presa será más sensible a los depredadores introducidos que difieren notoriamente de los nativos y de aquellos recién establecidos. Realizamos un metaanálisis global de estudios que midieron las respuestas cautelosas de mamíferos pequeños ante el rastro de meso depredadores simpátricos para probar estas suposiciones. Identificamos 26 estudios que cumplieron con nuestro criterio de selección. Estos estudios estuvieron conformados por 134 experimentos que reportaban las respuestas de 36 especies de mamíferos pequeños ante el rastro de seis meso depredadores introducidos y 12 nativos. Medimos la distancia funcional y filogenética entre cada meso depredador introducido y los meso depredadores locales nativos y el número de años simpátricos con su presa. Usamos la masa corporal del depredador y la presa como medida del riesgo de depredación. A nivel mundial, los mamíferos pequeños compartieron la cautela ante el rastro de los meso depredadores nativos e introducidos; la distancia funcional y la filogenética entre los meso depredadores introducidos y el meso depredador nativo más cercano no tuvieron efecto sobre la cautela; y la cautela no estuvo relacionada con el número de generaciones de la presa, o años, desde el primer contacto con los meso depredadores introducidos. La cautela de los mamíferos pequeños estuvo asociada con las proporciones de masa corporal entre el depredador y la presa, sin importar el origen. Lo único que los animales parecen no reconocer es si el depredador es nativo o no.

AnimalTraits - a curated animal trait database for body mass, metabolic rate and brain size.

Trait databases have become important resources for large-scale comparative studies in ecology and evolution. Here we introduce the AnimalTraits database, a curated database of body mass, metabolic rate and brain size, in standardised units, for terrestrial animals. The database has broad taxonomic breadth, including tetrapods, arthropods, molluscs and annelids from almost 2000 species and 1000 genera. All data recorded in the database are sourced from their original empirical publication, and the original metrics and measurements are included with each record. This allows for subsequent data transformations as required. We have included rich metadata to allow users to filter the dataset. The additional R scripts we provide will assist researchers with aggregating standardised observations into species-level trait values. Our goals are to provide this resource without restrictions, to keep the AnimalTraits database current, and to grow the number of relevant traits in the future.

Welcome to the Pyrocene: Animal survival in the age of megafire.

Planet Earth is entering the age of megafire, pushing ecosystems to their limits and beyond. While fire causes mortality of animals across vast portions of the globe, scientists are only beginning to consider fire as an evolutionary force in animal ecology. Here, we generate a series of hypotheses regarding animal responses to fire by adopting insights from the predator-prey literature. Fire is a lethal threat; thus, there is likely strong selection for animals to recognize the olfactory, auditory, and visual cues of fire, and deploy fire avoidance behaviours that maximize survival probability. If fire defences are costly, it follows that intraspecific variation in fire avoidance behaviours should correspond with variation in fire behaviour and regimes. Species and populations inhabiting ecosystems that rarely experience fire may lack these traits, placing 'fire naive' populations and species at enhanced extinction risk as the distribution of fire extends into new ecosystem types. We outline a research agenda to understand behavioural responses to fire and to identify conservation interventions that could be used to overcome fire naivety.

Red fox viromes in urban and rural landscapes.

The Red fox (Vulpes vulpes) has established large populations in Australia's urban and rural areas since its introduction following European settlement. The cryptic and highly adaptable nature of foxes allows them to invade cities and live among humans whilst remaining largely unnoticed. Urban living and access to anthropogenic food resources also influence fox ecology. Urban foxes grow larger, live at higher densities, and are more social than their rural counterparts. These ecological changes in urban red foxes are likely to impact the pathogens that they harbour, and foxes could pose a disease risk to humans and other species that share these urban spaces. To investigate this possibility, we used a meta-transcriptomic approach to characterise the virome of urban and rural foxes across the Greater Sydney region in Australia. Urban and rural foxes differed significantly in virome composition, with rural foxes harbouring a greater abundance of viruses compared to their urban counterparts. We identified ten potentially novel vertebrate-associated viruses in both urban and rural foxes, some of which are related to viruses associated with disease in domestic species and humans. These included members of the Astroviridae, Picobirnaviridae, Hepeviridae, and Picornaviridae as well as rabbit haemorrhagic disease virus-2. This study sheds light on the viruses carried by urban and rural foxes and emphasises the need for greater genomic surveillance of foxes and other invasive species at the human-wildlife interface.

Context and trade-offs characterize real-world threat detection systems: A review and comprehensive framework to improve research practice and resolve the translational crisis.

A better understanding of context in decision-making-that is, the internal and external conditions that modulate decisions-is required to help bridge the gap between natural behaviors that evolved by natural selection and more arbitrary laboratory models of anxiety and fear. Because anxiety and fear are mechanisms evolved to manage threats from predators and other exigencies, the large behavioral, ecological and evolutionary literature on predation risk is useful for re-framing experimental research on human anxiety-related disorders. We review the trade-offs that are commonly made during antipredator decision-making in wild animals along with the context under which the behavior is performed and measured, and highlight their relevance for focused laboratory models of fear and anxiety. We then develop an integrative mechanistic model of decision-making under risk which, when applied to laboratory and field settings, should improve studies of the biological basis of normal and pathological anxiety and may therefore improve translational outcomes.

Publisher Correction: Open Science principles for accelerating trait-based science across the Tree of Life.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Open Science principles for accelerating trait-based science across the Tree of Life.

Synthesizing trait observations and knowledge across the Tree of Life remains a grand challenge for biodiversity science. Species traits are widely used in ecological and evolutionary science, and new data and methods have proliferated rapidly. Yet accessing and integrating disparate data sources remains a considerable challenge, slowing progress toward a global synthesis to integrate trait data across organisms. Trait science needs a vision for achieving global integration across all organisms. Here, we outline how the adoption of key Open Science principles-open data, open source and open methods-is transforming trait science, increasing transparency, democratizing access and accelerating global synthesis. To enhance widespread adoption of these principles, we introduce the Open Traits Network (OTN), a global, decentralized community welcoming all researchers and institutions pursuing the collaborative goal of standardizing and integrating trait data across organisms. We demonstrate how adherence to Open Science principles is key to the OTN community and outline five activities that can accelerate the synthesis of trait data across the Tree of Life, thereby facilitating rapid advances to address scientific inquiries and environmental issues. Lessons learned along the path to a global synthesis of trait data will provide a framework for addressing similarly complex data science and informatics challenges.

The Extended Genotype: Microbially Mediated Olfactory Communication.

Microbes are now known to influence inter- and intraspecific olfactory signaling systems. They do so by producing metabolites that function as odorants. A unique attribute of such odorants is that they arise as a product of microbial-host interactions. These interactions need not be mutualistic, and indeed can be antagonistic. We develop an integrated ecoevolutionary model to explore microbially mediated olfactory communication and a process model that illustrates the various ways that microbial products might contribute to odorants. This novel approach generates testable predictions, including that selection to incorporate microbial products should be a common feature of infochemicals that communicate identity but not those that communicate fitness or quality. Microbes extend an individual's genotype, but also enhance vulnerability to environmental change.

Australian native mammals recognize and respond to alien predators: a meta-analysis.

Prey naiveté is a failure to recognize novel predators and thought to cause exaggerated impacts of alien predators on native wildlife. Yet there is equivocal evidence in the literature for native prey naiveté towards aliens. To address this, we conducted a meta-analysis of Australian mammal responses to native and alien predators. Australia has the world's worst record of extinction and declines of native mammals, largely owing to two alien predators introduced more than 150 years ago: the feral cat, Felis catus, and European red fox, Vulpes vulpes Analysis of 94 responses to predator cues shows that Australian mammals consistently recognize alien foxes as a predation threat, possibly because of thousands of years of experience with another canid predator, the dingo, Canis lupus dingo We also found recognition responses towards cats; however, in four of the seven studies available, these responses were of risk-taking behaviour rather than antipredator behaviour. Our results suggest that a simple failure to recognize alien predators is not behind the ongoing exaggerated impacts of alien predators in Australia. Instead, our results highlight an urgent need to better understand the appropriateness of antipredator responses in prey towards alien predators in order to understand native prey vulnerability.

Predicting Predator Recognition in a Changing World.

Through natural as well as anthropogenic processes, prey can lose historically important predators and gain novel ones. Both predator gain and loss frequently have deleterious consequences. While numerous hypotheses explain the response of individuals to novel and familiar predators, we lack a unifying conceptual model that predicts the fate of prey following the introduction of a novel or a familiar (reintroduced) predator. Using the concept of eco-evolutionary experience, we create a new framework that allows us to predict whether prey will recognize and be able to discriminate predator cues from non-predator cues and, moreover, the likely persistence outcomes for 11 different predator-prey interaction scenarios. This framework generates useful and testable predictions for ecologists, conservation scientists, and decision-makers.

Novel predators emit novel cues: a mechanism for prey naivety towards alien predators.

Detecting enemies is crucial for survival and a trait that develops over an evolutionary timeframe. Introduced species disrupt coevolved systems of communication and detection in their new ranges, often leading to devastating impacts. The classic example is prey naivety towards alien predators, whereby prey fail to recognise a new predator. Yet exactly why native prey fail to recognise alien predators remains puzzling. Naivety theory predicts that it is because novel predators emit novel cues. Distantly related animals have distinct evolutionary histories, physiologies and ecologies, predicting they will emit different cues. Yet it also possible that all predators emit similar cues because they are carnivorous. We investigate whether odour cues differ between placental and marsupial carnivores in Australia, where native prey experienced only marsupial mammal predation until ~4000 years ago. We compared volatile chemical profiles of urine, scats and bedding from four placental and three marsupial predators. Chemical profiles showed little overlap between placental and marsupial carnivores across all odour types, suggesting that cue novelty is a plausible mechanism for prey naivety towards alien predators. Our results also suggest a role for olfactory cues to complement visual appearance and vocalisations as biologically meaningful ways to differentiate species.

Does Historical Coexistence with Dingoes Explain Current Avoidance of Domestic Dogs? Island Bandicoots Are Naïve to Dogs, unlike Their Mainland Counterparts.

Introduced predators have a global reputation for causing declines and extinctions of native species. Native prey naiveté towards novel predators is thought to be a key reason for predator impacts. However, naiveté is not necessarily forever: where coexistence establishes, it is likely that naiveté will be reduced through adaptation, and the once alien predator will eventually become recognised by prey. For example, native marsupial bandicoots in Sydney avoid backyards with domestic dogs (C. lupus familiaris), but not domestic cats (Felis catus), even though cats and dogs were both introduced about 200 years ago (Carthey and Banks 2012). The authors attributed bandicoots' recognition of dogs to long-term exposure to a close relative of dogs, dingoes that arrived in Australia 4000 years ago. Here, we test a prediction of this hypothesis by taking the study to Tasmania, where dingoes have never been present but where domestic dogs also arrived about 200 years ago. We use a similar survey design to that of Carthey and Banks (2012): asking Hobart residents to report on pet-ownership, bandicoot sightings and scats within their backyards, as well as an array of yard characteristic control variables. We predicted that if long term experience with dingoes enabled mainland bandicoots to recognise domestic dogs, then Tasmanian bandicoots, which are inexperienced with dingoes, would not recognise domestic dogs. Our results indicate that Tasmanian bandicoots are naïve to both dogs and cats after only 200 years of coexistence, supporting our hypothesis and the notion that naiveté in native prey towards alien predators (as observed on the mainland) may eventually be overcome.

Foraging in groups affects giving-up densities: solo foragers quit sooner.

The giving-up density framework is an elegant and widely adopted mathematical approach to measuring animals' foraging decisions at non-replenishing artificial resource patches. Under this framework, an animal should "give up" when the benefits of foraging are outweighed by the costs (e.g., predation risk, energetic, and/or missed opportunity costs). However, animals of many species may forage in groups, and group size is expected to alter perceived predation risk and hence influence quitting decisions. Yet, most giving-up density studies assume either that individuals forage alone or that giving-up densities are not affected by group foraging. For animals that forage both alone and in groups, differences in giving-up densities due to group foraging rather than experimental variables may substantially alter interpretation. However, no research to date has directly investigated how group foraging affects the giving-up density. We used remote-sensing cameras to identify instances of group foraging in two species of Rattus across three giving-up density experiments to determine whether group foraging influences giving-up densities. Both Rattus species have been observed to vary between foraging alone and in groups. In all three experiments, solo foragers left higher giving-up densities on average than did group foragers. This result has important implications for studies using giving-up densities to investigate perceived risk, the energetic costs of searching, handling time, digestion, and missed opportunity costs, particularly if groups of animals are more likely to experience certain experimental treatments. It is critically important that future giving-up density studies consider the effects of group foraging.

Naïveté in novel ecological interactions: lessons from theory and experimental evidence.

The invasion of alien species into areas beyond their native ranges is having profound effects on ecosystems around the world. In particular, novel alien predators are causing rapid extinctions or declines in many native prey species, and these impacts are generally attributed to ecological naïveté or the failure to recognise a novel enemy and respond appropriately due to a lack of experience. Despite a large body of research concerning the recognition of alien predation risk by native prey, the literature lacks an extensive review of naïveté theory that specifically asks how naïveté between novel pairings of alien predators and native prey disrupts our classical understanding of predator-prey ecological theory. Here we critically review both classic and current theory relating to predator-prey interactions between both predators and prey with shared evolutionary histories, and those that are ecologically 'mismatched' through the outcomes of biological invasions. The review is structured around the multiple levels of naïveté framework of Banks & Dickman (2007), and concepts and examples are discussed as they relate to each stage in the process from failure to recognise a novel predator (Level 1 naïveté), through to appropriate (Level 2) and effective (Level 3) antipredator responses. We discuss the relative contributions of recognition, cue types and the implied risk of cues used by novel alien and familiar native predators, to the probability that prey will recognise a novel predator. We then cover the antipredator response types available to prey and the factors that predict whether these responses will be appropriate or effective against novel alien and familiar native predators. In general, the level of naïveté of native prey can be predicted by the degree of novelty (in terms of appearance, behaviour or habitat use) of the alien predator compared to native predators with which prey are experienced. Appearance in this sense includes cue types, spatial distribution and implied risk of cues, whilst behaviour and habitat use include hunting modes and the habitat domain of the predator. Finally, we discuss whether the antipredator response can occur without recognition per se, for example in the case of morphological defences, and then consider a potential extension of the multiple levels of naïveté framework. The review concludes with recommendations for the design and execution of naïveté experiments incorporating the key concepts and issues covered here. This review aims to critique and combine classic ideas about predator-prey interactions with current naïveté theory, to further develop the multiple levels of naïveté framework, and to suggest the most fruitful avenues for future research.

Competitive naïveté between a highly successful invader and a functionally similar native species.

Naïveté can occur within any novel antagonistic interaction, and competitive forces play a fundamental role in shaping community structure, yet competitive naïveté has received very little attention in the literature to date. Naïveté towards a novel competitor is unlikely to result in immediate mortality, but could potentially affect access to resources and hence population growth and survival. In cases where only one species (either native or alien) remains naïve to the other, the species that recognizes the other will gain advantage, with implications for both the persistence of the native species and the establishment and spread of the invasive. The invasive black rat (Rattus rattus) has spread throughout many coastal areas of Australia, and competes with the native bush rat (Rattus fuscipes) wherever they coexist. As these rats have now been interacting for approximately 200 years, and multi-species rodent communities generally maintain their structure through olfactory communication, our aim was to determine whether these two very closely related species recognize one another's odors and use them to mediate their interactions. We used remote-sensing cameras deployed in single- and mixed-species sites to record the behavioral responses of each species to conspecific, heterospecific and control odors. Black rats investigated bush rat odors but not vice versa, suggesting that bush rats may remain naïve towards their new competitor. Highly successful invaders such as black rats may possess traits such as broad recognition templates and rapid learning capabilities that contribute to their ongoing success in invading new environments.

When does an alien become a native species? A vulnerable native mammal recognizes and responds to its long-term alien predator.

The impact of alien predators on native prey populations is often attributed to prey naiveté towards a novel threat. Yet evolutionary theory predicts that alien predators cannot remain eternally novel; prey species must either become extinct or learn and adapt to the new threat. As local enemies lose their naiveté and coexistence becomes possible, an introduced species must eventually become 'native'. But when exactly does an alien become a native species? The dingo (Canis lupus dingo) was introduced to Australia about 4000 years ago, yet its native status remains disputed. To determine whether a vulnerable native mammal (Perameles nasuta) recognizes the close relative of the dingo, the domestic dog (Canis lupus familiaris), we surveyed local residents to determine levels of bandicoot visitation to yards with and without resident dogs. Bandicoots in this area regularly emerge from bushland to forage in residential yards at night, leaving behind tell-tale deep, conical diggings in lawns and garden beds. These diggings were less likely to appear at all, and appeared less frequently and in smaller quantities in yards with dogs than in yards with either resident cats (Felis catus) or no pets. Most dogs were kept indoors at night, meaning that bandicoots were not simply chased out of the yards or killed before they could leave diggings, but rather they recognized the threat posed by dogs and avoided those yards. Native Australian mammals have had thousands of years experience with wild dingoes, which are very closely related to domestic dogs. Our study suggests that these bandicoots may no longer be naïve towards dogs. We argue that the logical criterion for determining native status of a long-term alien species must be once its native enemies are no longer naïve.

Negotiating a noisy, information-rich environment in search of cryptic prey: olfactory predators need patchiness in prey cues.

1. Olfactory predator search processes differ fundamentally to those based on vision, particularly when odour cues are deposited rather than airborne or emanating from a point source. When searching for visually cryptic prey that may have moved some distance from a deposited odour cue, cue context and spatial variability are the most likely sources of information about prey location available to an olfactory predator. 2. We tested whether the house mouse (Mus domesticus), a model olfactory predator, would use cue context and spatial variability when searching for buried food items; specifically, we tested the effect of varying cue patchiness, odour strength, and cue-prey association on mouse foraging success. 3. Within mouse- and predator-proof enclosures, we created grids of 100 sand-filled Petri dishes and buried peanut pieces in a set number of these patches to represent visually cryptic 'prey'. By adding peanut oil to selected dishes, we varied the spatial distribution of prey odour relative to the distribution of prey patches in each grid, to reflect different levels of cue patchiness (Experiment 1), odour strength (Experiment 2) and cue-prey association (Experiment 3). We measured the overnight foraging success of individual mice (percentage of searched patches containing prey), as well as their foraging activity (percentage of patches searched), and prey survival (percentage of unsearched prey patches). 4. Mouse foraging success was highest where odour cues were patchy rather than uniform (Experiment 1), and where cues were tightly associated with prey location, rather than randomly or uniformly distributed (Experiment 3). However, when cues at prey patches were ten times stronger than a uniformly distributed weak background odour, mice did not improve their foraging success over that experienced when cues were of uniform strength and distribution (Experiment 2). 5. These results suggest that spatial variability and cue context are important means by which olfactory predators can use deposited odour cues to locate visually cryptic prey. They also indicate that chemical crypsis can disrupt these search processes as effectively as background matching in visually based predator-prey systems.