Alexandra J. R. Carthey

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.

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.

A practical guide to avoid giving up on giving-up densities

The giving-up density (GUD) framework provides a powerful experimental approach with a strong theoretical underpinning to quantify foraging outcomes in heterogeneous landscapes. Since its inception, the GUD approach has been applied successfully to a vast range of foraging species and foraging scenarios. However, its application is not simple, as anyone who has tried to use it for the first time might attest. Limitations of the technique were noted at its conception, yet only the artificiality of the patches, the appropriateness of the food resource, and the possibility of multiple visiting foragers were identified. Here we show the current uses of GUD and outline the practical benefits as well as the often overlooked limitations of the technique. We define seven major points that need to be addressed when applying this methodology: (1) the curvilinearity between harvest rate and energy, (2) the energetic state of the forager, (3) the effect of group foraging, (4) food quality and substrate properties, (5) the predictability of the patch, (6) behavioral traits of the forager, and (7) nontarget species. We also suggest how GUD experiments can be enhanced by incorporating complementary methods (such as cameras) to better understand the foraging processes involved in the GUD itself. We conclude that the benefits of using GUD outweigh the costs, but that its limitations should not be ignored. Incorporating new methods when using GUD can potentially offer novel and important insights into the study of foraging behavior.

Risk vs. reward: how predators and prey respond to aging olfactory cues

Many animals use olfaction to find food and avoid predators, and must negotiate environments containing odors of varying compositions, strengths, and ages to distinguish useful cues from background noise. Temporal variation in odor cues (i.e., “freshness”) seems an obvious way that animals could distinguish cues, yet there is little experimental evidence for this phenomenon. Fresh cues provide a more reliable indicator of donor presence than aged cues, but we hypothesize that the benefits of responding to aged cues depend on whether the cue indicates the proximity of a predator or a potential meal. As prey cannot remain eternally risk averse in response to predator odor, we predict that antipredator responses should diminish as predator cues age. In contrast, animals searching for food should investigate aged prey cues if investigation costs are sufficiently low and the potential benefit (a meal) sufficiently high; thus, we predict that predators will maintain interest in aged prey cues. We tested these ideas using free-ranging rats (Rattus spp.) in two separate experiments; firstly assessing giving-up densities in the presence of predator odor, and secondly examining investigation rates of prey odors. As predicted, giving-up densities dropped once predator odor had aged, but investigation rates remained similar for aged and fresh prey odor. Thus, rats used temporal variation in odor cues to evaluate the cost–benefit relationship of responding to predator and prey odors. We suggest that the ecological significance of variable cue age needs more research and should be considered when interpreting behavioral responses to olfactory information.

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.

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.

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.

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.

Naïve, bold, or just hungry? An invasive exotic prey species recognises but does not respond to its predators

Alien species experience both costs and benefits in invaded environments, through naiveté of potential prey species, but also predation pressure from native predators. The question of whether alien prey recognise and respond to native predators has been relatively understudied, despite the hypothesised potential for native predators to provide biotic resistance to invasion. There are two main hypotheses about whether exotic prey should recognise native and exotic predators in their new ranges: (1) naiveté—predicting recognition of evolutionarily familiar predators only, and (2) pre-adaptation—predicting recognition of all predators through a generalist recognition template. With regards to antipredator responses, (3) naïveté theory presumes that exotic prey will respond to the predators they recognise, but we suggest that (4) a bold behavioural syndrome, and/or a high marginal value of food in invaded environments might result in weak or absent responses, even to recognised predators. Here we combine the giving-up density framework with behavioural analysis of remote camera footage to experimentally test these ideas in a disturbed, peri-urban, Australian ecosystem, where alien black rats are predated on by alien dogs, foxes, cats, and native quolls. Black rats recognised dogs and foxes, but appear naïve towards quolls. However, they showed no antipredator responses at all, consistent with a bold behavioural syndrome, elevated predation risk, and/or a high marginal value of food in invaded environments.

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 individuals genotype, but also enhance vulnerability to environmental change.