Despite decades of research into predator control, predation by exotic predators is the leading c... more Despite decades of research into predator control, predation by exotic predators is the leading cause of reintroduction failure in Australia and New Zealand. A variety of methods are used to deal with the threat of predation, including excluding and controlling predators and improving prey responses. Fenced reserves and islands are becoming increasingly popular reintroduction sites and generally have high reintroduction success. However, in this chapter, we argue that the current emphasis on predator exclusion is short-sighted and does not consider the underlying issue of prey naivety. We call for a new paradigm focusing on improving the ability of prey to co-exist with exotic predators – one that acknowledges behavioural plasticity and natural selection.
ABSTRACT Olfaction plays a central role in the game of evasion and detection in predator-prey int... more ABSTRACT Olfaction plays a central role in the game of evasion and detection in predator-prey interactions. Odours are a necessary consequence of metabolic processes and are also used by both predators and prey as social signals in the form of long-lasting scent marks. Because of their longevity, odours are open to exploitation by predators to help them find their prey, and by prey to avoid being detected. In this chapter we explore evidence for the different ways that odour may be used in predator-prey interactions. We also review the evidence for its use by mammalian carnivores and their prey in Australian systems where there are a suite of native and alien predators and prey that are of conservation significance. We then discuss opportunities and challenges for land managers to exploit odours in order to alter predation outcomes and influence prey behaviour. We finish by highlighting key areas where greater insights are needed into how olfaction ultimately determines the outcome of a predation event, and hence shapes the overall impacts of predation.
SUMMARY 1. Many plants disperse their seeds in waterbodies via hydrochoric transport. Despite a g... more SUMMARY 1. Many plants disperse their seeds in waterbodies via hydrochoric transport. Despite a growing body of research into hydrochory, little is known about the fundamental seed traits that determine floatation ability or hydrochoric transport behaviour more generally. Seeds are transported in fluvial systems in one of three phases: surface transport, within the flow or incorporated in bedload. Seeds are often categorised as buoyant or non-buoyant based on density, with little consideration of the morphological traits that determine how long seeds spend in each transport phase. 2. We investigated the seed traits that best predict time spent floating under laboratory conditions, using sixty species of riparian plants from southeastern Australia. We measured and calculated key physical attributes (length, width, volume, surface area, mass, density, sphericity, roundness and shape category) and categorised seeds according to their primary dispersal modes (water/wind, vertebrate , adhesion, ants and unassisted). 3. We used Cox's proportional hazards modelling to reveal that seed density and volume : surface area ratio were the physical traits that best predicted time spent floating. Volume : surface area ratio represents both seed size and shape, as it increases with size and sphericity. Our results showed that denser, larger and/or more spherical seeds (i.e. higher volume : surface area ratio) were poor floa-ters. They are therefore more likely to be transported in subsurface flow or as bedload. 4. We combined our data with geomorphic models of sediment transport in flow to develop a bio-physical process model of how hydrological forces and seed physical traits determine hydrochorous seed transport behaviour in rivers. The model describes how surface tension, buoyancy and flow velocity act on seed density and volume : surface area ratio to characterise time spent floating. We extrapolate from our data to conceptualise how these traits predict transitions between surface, sub-surface and bedload transport. Hydrochoric seed transport behaviour and deposition are both threshold driven and multidirectional. 5. Our process model is likely to be applicable across a range of different seed types in a range of rivers. It substantially increases our understanding of hydrochoric processes in rivers, lakes and lotic wetlands and will help illuminate the links between seed traits, hydrochoric transport and patterns of riparian vegetation and species composition.
Predation is an important selective force on prey species, but avoiding predators can be costly. ... more Predation is an important selective force on prey species, but avoiding predators can be costly. Efficient decisions on who to avoid (predator recognition) and when (situations with different predation risk) will determine the chances of prey survival. In coevolved predator-prey systems, detection of predator odours generally induces a response in potential prey to reduce predation risk. However, prey may not necessarily respond to odours of predators with which they have no previous experience, as predicted by the prey naïveté hypothesis. In turn, perceived predation risk may also modulate predator recognition and the intensity of antipredator responses. In this study, we investigate the responses of an introduced prey species, the European rabbit (Oryctolagus cuniculus), to odours from coevolved and non-coevolved, sympatric and allopatric predators in situations of high and low numbers of predators in Australia. We used pellet counts to quantify rabbits' use of space on experimental plots treated with predator odours. Rabbit avoidance of plots scented with coevolved predator odours was strongest, but they also responded to non-coevolved, marsupial predators. Predator abundance did not affect predator recognition in rabbits, although responses were more intense in situations where perceived predation risk was low and the intensity of responses decreased over time. Our results suggest that rabbits may have learned to recognize novel marsupial predators after 150 years of exposure in their introduced range.
The giving-up density framework is an elegant and widely adopted mathematical approach to measuri... more 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.
Alien predators have wreaked havoc on isolated endemic and island fauna worldwide, a phenomenon g... more Alien predators have wreaked havoc on isolated endemic and island fauna worldwide, a phenomenon generally attributed to prey naiveté, or a failure to display effective antipredator behaviour due to a lack of experience. While the failure to recognise and/or respond to a novel predator has devastating impacts in the short term after predators are introduced, few studies have asked whether medium to long term experience with alien predators enables native species to overcome their naiveté. In Australia, introduced dogs (Canis lupus familiaris), foxes (Vulpes vulpes) and cats (Felis catus) have caused rapid extinctions and declines in small-medium sized native mammals since they were introduced ~150 years ago. However, native wildlife have had ~4000 years experience with another dog – the dingo (Canis lupus dingo). Native bush rats (Rattus fuscipes) remain common despite predation from these predators. We predicted that prior experience with dingoes would mean that bush rats recognise and respond to dogs, but suspect that hundreds of years experience may not be enough for effective responses to cats and foxes. To test these predictions, we combined the giving-up density (GUD) with analysis of remote camera footage to measure bush rat foraging and behavioural responses to body odour from dogs, foxes, cats and native spotted-tail quolls (Dasyurus maculatus). Bush rats responded strongly to dogs with increased GUDs, increased vigilance and decreased foraging. However, mixed responses to foxes and cats suggest that at least some individuals remain naïve towards these predators. Naiveté is not necessarily forever: alien predators devastate many native prey species, but others may learn or adapt to the new threat.
The invasion of alien species into areas beyond their native ranges is having profound effects on... more 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.
Naïveté can occur within any novel antagonistic interaction, and competitive forces play a fundam... more 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.
The giving-up density (GUD) framework provides a powerful experimental approach with a strong the... more 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.
Many animals use olfaction to find food and avoid predators, and must negotiate environments cont... more 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.
The impact of alien predators on native prey populations is often attributed to prey naiveté towa... more 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.
1. Olfactory predator search processes differ fundamentally to those based on vision, particularl... more 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.
The Giving Up Density (GUD) framework provides a powerful experimental approach, with strong theo... more The Giving Up Density (GUD) framework provides a powerful experimental approach, with strong theoretical underpinning, for quantifying foraging outcomes in heterogeneous landscapes. Since its inception, GUD has been applied successfully to a vast range of foraging species and foraging scenarios. Commonly, but not exclusively, it has been used to quantify patch characteristics associated with predation risk and hence to define the landscape of fear. Here we review the current uses of GUD, and we outline the theoretical and practical benefits as well as the, often forgotten, limitations of the technique. We also present ideas on how GUD experiments can be enhanced by combining the technique with 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 these costs should not be ignored. Incorporating new methods alongside GUD has the potential to offer novel but important insights into the study of foraging behaviour.
The Giving Up Density (GUD) framework provides a powerful experimental approach, with strong theo... more The Giving Up Density (GUD) framework provides a powerful experimental approach, with strong theoretical underpinning, for quantifying foraging outcomes in heterogeneous landscapes. Since its inception, GUD has been applied successfully to a vast range of foraging species and foraging scenarios. Commonly, but not exclusively, it has been used to quantify patch characteristics associated with predation risk and hence to define the landscape of fear. Here we review the current uses of GUD, and we outline the theoretical and practical benefits as well as the, often forgotten, limitations of the technique. We also present ideas on how GUD experiments can be enhanced by combining the technique with 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 these costs should not be ignored. Incorporating new methods alongside GUD has the potential to offer novel but important insights into the study of foraging behaviour.
Despite decades of research into predator control, predation by exotic predators is the leading c... more Despite decades of research into predator control, predation by exotic predators is the leading cause of reintroduction failure in Australia and New Zealand. A variety of methods are used to deal with the threat of predation, including excluding and controlling predators and improving prey responses. Fenced reserves and islands are becoming increasingly popular reintroduction sites and generally have high reintroduction success. However, in this chapter, we argue that the current emphasis on predator exclusion is short-sighted and does not consider the underlying issue of prey naivety. We call for a new paradigm focusing on improving the ability of prey to co-exist with exotic predators – one that acknowledges behavioural plasticity and natural selection.
ABSTRACT Olfaction plays a central role in the game of evasion and detection in predator-prey int... more ABSTRACT Olfaction plays a central role in the game of evasion and detection in predator-prey interactions. Odours are a necessary consequence of metabolic processes and are also used by both predators and prey as social signals in the form of long-lasting scent marks. Because of their longevity, odours are open to exploitation by predators to help them find their prey, and by prey to avoid being detected. In this chapter we explore evidence for the different ways that odour may be used in predator-prey interactions. We also review the evidence for its use by mammalian carnivores and their prey in Australian systems where there are a suite of native and alien predators and prey that are of conservation significance. We then discuss opportunities and challenges for land managers to exploit odours in order to alter predation outcomes and influence prey behaviour. We finish by highlighting key areas where greater insights are needed into how olfaction ultimately determines the outcome of a predation event, and hence shapes the overall impacts of predation.
SUMMARY 1. Many plants disperse their seeds in waterbodies via hydrochoric transport. Despite a g... more SUMMARY 1. Many plants disperse their seeds in waterbodies via hydrochoric transport. Despite a growing body of research into hydrochory, little is known about the fundamental seed traits that determine floatation ability or hydrochoric transport behaviour more generally. Seeds are transported in fluvial systems in one of three phases: surface transport, within the flow or incorporated in bedload. Seeds are often categorised as buoyant or non-buoyant based on density, with little consideration of the morphological traits that determine how long seeds spend in each transport phase. 2. We investigated the seed traits that best predict time spent floating under laboratory conditions, using sixty species of riparian plants from southeastern Australia. We measured and calculated key physical attributes (length, width, volume, surface area, mass, density, sphericity, roundness and shape category) and categorised seeds according to their primary dispersal modes (water/wind, vertebrate , adhesion, ants and unassisted). 3. We used Cox's proportional hazards modelling to reveal that seed density and volume : surface area ratio were the physical traits that best predicted time spent floating. Volume : surface area ratio represents both seed size and shape, as it increases with size and sphericity. Our results showed that denser, larger and/or more spherical seeds (i.e. higher volume : surface area ratio) were poor floa-ters. They are therefore more likely to be transported in subsurface flow or as bedload. 4. We combined our data with geomorphic models of sediment transport in flow to develop a bio-physical process model of how hydrological forces and seed physical traits determine hydrochorous seed transport behaviour in rivers. The model describes how surface tension, buoyancy and flow velocity act on seed density and volume : surface area ratio to characterise time spent floating. We extrapolate from our data to conceptualise how these traits predict transitions between surface, sub-surface and bedload transport. Hydrochoric seed transport behaviour and deposition are both threshold driven and multidirectional. 5. Our process model is likely to be applicable across a range of different seed types in a range of rivers. It substantially increases our understanding of hydrochoric processes in rivers, lakes and lotic wetlands and will help illuminate the links between seed traits, hydrochoric transport and patterns of riparian vegetation and species composition.
Predation is an important selective force on prey species, but avoiding predators can be costly. ... more Predation is an important selective force on prey species, but avoiding predators can be costly. Efficient decisions on who to avoid (predator recognition) and when (situations with different predation risk) will determine the chances of prey survival. In coevolved predator-prey systems, detection of predator odours generally induces a response in potential prey to reduce predation risk. However, prey may not necessarily respond to odours of predators with which they have no previous experience, as predicted by the prey naïveté hypothesis. In turn, perceived predation risk may also modulate predator recognition and the intensity of antipredator responses. In this study, we investigate the responses of an introduced prey species, the European rabbit (Oryctolagus cuniculus), to odours from coevolved and non-coevolved, sympatric and allopatric predators in situations of high and low numbers of predators in Australia. We used pellet counts to quantify rabbits' use of space on experimental plots treated with predator odours. Rabbit avoidance of plots scented with coevolved predator odours was strongest, but they also responded to non-coevolved, marsupial predators. Predator abundance did not affect predator recognition in rabbits, although responses were more intense in situations where perceived predation risk was low and the intensity of responses decreased over time. Our results suggest that rabbits may have learned to recognize novel marsupial predators after 150 years of exposure in their introduced range.
The giving-up density framework is an elegant and widely adopted mathematical approach to measuri... more 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.
Alien predators have wreaked havoc on isolated endemic and island fauna worldwide, a phenomenon g... more Alien predators have wreaked havoc on isolated endemic and island fauna worldwide, a phenomenon generally attributed to prey naiveté, or a failure to display effective antipredator behaviour due to a lack of experience. While the failure to recognise and/or respond to a novel predator has devastating impacts in the short term after predators are introduced, few studies have asked whether medium to long term experience with alien predators enables native species to overcome their naiveté. In Australia, introduced dogs (Canis lupus familiaris), foxes (Vulpes vulpes) and cats (Felis catus) have caused rapid extinctions and declines in small-medium sized native mammals since they were introduced ~150 years ago. However, native wildlife have had ~4000 years experience with another dog – the dingo (Canis lupus dingo). Native bush rats (Rattus fuscipes) remain common despite predation from these predators. We predicted that prior experience with dingoes would mean that bush rats recognise and respond to dogs, but suspect that hundreds of years experience may not be enough for effective responses to cats and foxes. To test these predictions, we combined the giving-up density (GUD) with analysis of remote camera footage to measure bush rat foraging and behavioural responses to body odour from dogs, foxes, cats and native spotted-tail quolls (Dasyurus maculatus). Bush rats responded strongly to dogs with increased GUDs, increased vigilance and decreased foraging. However, mixed responses to foxes and cats suggest that at least some individuals remain naïve towards these predators. Naiveté is not necessarily forever: alien predators devastate many native prey species, but others may learn or adapt to the new threat.
The invasion of alien species into areas beyond their native ranges is having profound effects on... more 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.
Naïveté can occur within any novel antagonistic interaction, and competitive forces play a fundam... more 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.
The giving-up density (GUD) framework provides a powerful experimental approach with a strong the... more 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.
Many animals use olfaction to find food and avoid predators, and must negotiate environments cont... more 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.
The impact of alien predators on native prey populations is often attributed to prey naiveté towa... more 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.
1. Olfactory predator search processes differ fundamentally to those based on vision, particularl... more 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.
The Giving Up Density (GUD) framework provides a powerful experimental approach, with strong theo... more The Giving Up Density (GUD) framework provides a powerful experimental approach, with strong theoretical underpinning, for quantifying foraging outcomes in heterogeneous landscapes. Since its inception, GUD has been applied successfully to a vast range of foraging species and foraging scenarios. Commonly, but not exclusively, it has been used to quantify patch characteristics associated with predation risk and hence to define the landscape of fear. Here we review the current uses of GUD, and we outline the theoretical and practical benefits as well as the, often forgotten, limitations of the technique. We also present ideas on how GUD experiments can be enhanced by combining the technique with 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 these costs should not be ignored. Incorporating new methods alongside GUD has the potential to offer novel but important insights into the study of foraging behaviour.
The Giving Up Density (GUD) framework provides a powerful experimental approach, with strong theo... more The Giving Up Density (GUD) framework provides a powerful experimental approach, with strong theoretical underpinning, for quantifying foraging outcomes in heterogeneous landscapes. Since its inception, GUD has been applied successfully to a vast range of foraging species and foraging scenarios. Commonly, but not exclusively, it has been used to quantify patch characteristics associated with predation risk and hence to define the landscape of fear. Here we review the current uses of GUD, and we outline the theoretical and practical benefits as well as the, often forgotten, limitations of the technique. We also present ideas on how GUD experiments can be enhanced by combining the technique with 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 these costs should not be ignored. Incorporating new methods alongside GUD has the potential to offer novel but important insights into the study of foraging behaviour.
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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.
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.