Associational resistance or susceptibility: the indirect interaction between chemically‐defended and non‐defended herbivore prey via a shared predator

Many organisms possess chemical defences against their natural enemies, which render them unpalatable or toxic when attacked or consumed. These chemically‐defended organisms commonly occur in communities with non‐ or less‐defended prey, leading to indirect interactions between prey species, mediated by natural enemies. Although the importance of enemy‐mediated indirect interactions have been well documented (e.g. apparent competition), how the presence of prey chemical defences may affect predation of non‐defended prey in terrestrial communities remains unclear. Here, an experimental approach was used to study the predator‐mediated indirect interaction between a chemically‐defended and non‐defended pest aphid species. Using laboratory‐based mesocosms, aphid community composition was manipulated to include chemically‐defended (CD) aphids Brevicoryne brassicae, non‐defended (ND) aphids Myzus persicae or a mixed assemblage of both species, on Brassica oleracea cabbage plants, in the presence or absence of a shared predator (Chrysoperla carnea larvae). Aphid population growth rates, aphid distributions on host plants and predator growth rates were measured. In single‐species treatments, C. carnea reduced M. persicae population growth rate, but had no significant impact on B. brassicae population growth rate, suggesting B. brassicae chemical defences are effective against C. carnea. Chrysoperla carnea had no significant impact on either aphid species population growth rate in mixed‐species treatments. Myzus persicae (ND) therefore experienced reduced predation in the presence of B. brassicae (CD) through a predator‐mediated indirect effect. Moreover, predator growth rates were significantly higher in the M. persicae‐only treatments than in either the B. brassicae‐only or mixed‐species treatments, suggesting predation was impaired in the presence of B. brassicae (CD). A trait‐mediated indirect interaction is proposed, consistent with associational resistance, in which the predator, upon incidental consumption of chemically‐defended aphids is deterred from feeding, releasing non‐defended aphids from predatory control.     

Did Gause Have a Yeast Infection?

We planned to develop predator–prey models using Paramecium and yeast, but they have not been empirically examined since work by Gause in the 1930s. Therefore, we evaluated if Paramecium aurelia ingests and grows on eight yeasts. Recognising that it ingested yeasts but could not grow, we assessed if it might grow on other yeasts, by empirically parameterising a predator–prey model that relies on ingestion, not growth. Simulations were compared to P. aurelia‐yeast time‐series data, from Gause. We hypothesised that if the model simulated predator–prey dynamics that mimicked the original data, then possibly P. aurelia could grow on yeast; simulations did not mimic the original data. Reviewing works by Gause exposed two issues: experiments were undoubtedly contaminated with bacteria, allowing growth on bacteria, not yeast; and the population cycle data cannot be considered a self‐sustaining time series, as they were manipulated by adding yeast and ciliates. We conclude that past and future work should not rely on this system, for either empirical or theoretical evaluations. Finally, although we show that P. aurelia, P. caudatum, Euplotes patella, and Blepharisma sp. cannot grow on yeast, Tetrahymena pyriformis and Colpidium striatum can; these may provide models to explore predator–prey dynamics.     

Multi-predator effects across life-history stages: non-additivity of egg- and larval-stage predation in an African treefrog

The effects of multiple predators on their prey are frequently non‐additive because of interactions among predators. When prey shift habitats through ontogeny, many of their predators cannot interact directly. However, predators that occur in different habitats or feed on different prey stages may still interact through indirect effects mediated by prey traits and density. We conducted an experiment to evaluate the combined effects of arboreal egg‐stage and aquatic larval‐stage predators of the African treefrog, Hyperolius spinigularis. Egg and larval predator effects were non‐additive – more Hyperolius survived both predators than predicted from their independent effects. Egg‐stage predator effects on aquatic larval density and size and age at hatching reduced the effectiveness of larval‐stage predators by 70%. Our results indicate that density‐ and trait‐mediated indirect interactions can act across life‐stages and habitats, resulting in non‐additive multi‐predator effects.     

Trait‐mediated indirect interactions in a marine intertidal system as quantified by functional responses

Studies of trait‐mediated indirect interactions (TMIIs) typically focus on effects higher predators have on per capita consumption by intermediate consumers of a third, basal prey resource. TMIIs are usually evidenced by changes in feeding rates of intermediate consumers and/or differences in densities of this third species. However, understanding and predicting effects of TMIIs on population stability of such basal species requires examination of the type and magnitude of the functional responses exhibited towards them. Here, in a marine intertidal system consisting of a higher‐order fish predator, the shanny Lipophrys pholis, an intermediate predator, the amphipod Echinogammarus marinus, and a basal prey resource, the isopod Jaera nordmanni, we detected TMIIs, demonstrating the importance of habitat complexity in such interactions, by deriving functional responses and exploring consequences for prey population stability. Echinogammarus marinus reacted to fish predator diet cues by reducing activity, a typical anti‐predator response, but did not alter habitat use. Basal prey, Jaera nordmanni, did not respond to fish diet cues with respect to activity, distribution or aggregation behaviour. Echinogammarus marinus exhibited type II functional responses towards J. nordmanni in simple habitat, but type III functional responses in complex habitat. However, while predator cue decreased the magnitude of the type II functional response in simple habitat, it increased the magnitude of the type III functional response in complex habitat. These findings indicate that, in simple habitats, TMIIs may drive down consumption rates within type II responses, however, this interaction may remain de‐stabilising for prey populations. Conversely, in complex habitats, TMIIs may strengthen regulatory influences of intermediate consumers on prey populations, whilst potentially maintaining prey population stability. We thus highlight that TMIIs can have unexpected and complex ramifications throughout communities, but can be unravelled by considering effects on intermediate predator functional response types and magnitudes. Synthesis Higher‐order predators and habitat complexity can influence behaviour of intermediate species, affecting their consumption of prey through trait‐mediated indirect interactions (TMIIs). However, it is not clear how these factors interact to determine prey population stability. Using functional responses (FRs), relating predator consumption to prey density, we detected TMIIs in a marine system. In simple habitats, TMIIs reduced consumption rates, but FRs remained de‐stabilising for prey populations. In complex habitats, TMIIs strengthened prey regulation with population stabilizing FRs. We thus demonstrate that FRs can assess interactions of environmental and biological cues that result in complex and unexpected outcomes for prey populations.     

The changes in the predatory behavior of the microturbellarian <Emphasis Type="Italic">Stenostomum sphagnetorum</Emphasis> on two species of toxin-secreting ciliates of the genus <Emphasis Type="Italic">Spirostomum</Emphasis>

It is known that the microturbellarian Stenostomum sphagnetorum, a common ciliate predator, is very sensitive against different types of toxins produced by other ciliates for chemical defense, and consequently, it is not able to capture and ingests these ciliates. In particular, when the predator tries to attack one of these toxin-secreting ciliates, it is forced to regurgitate the captured prey in response to the toxin discharged from the ciliates. In this study it is shown that after repeated attacks by S. sphagnetorum against two species of toxic ciliates (Spirostomum ambiguum and Spirostomum teres), the predator acquires a behavior of prey selection that leads to the exclusion of these ciliates among the possible prey and to the distinction between edible and inedible (toxic) ciliates. This learned behavior, which is maintained for days, is lost only after the asexual reproduction of the microturbellarian. In addition, S. sphagnetorum learns to recognize and avoid specimens of S. ambiguum and S. teres artificially deprived of their toxins, strongly suggesting that the toxins are not exclusively associated in the prey recognition of the microturbellarian.     

Evolution of the Dynein Heavy Chain Family in Ciliates

Dynein heavy chains are motor proteins that comprise a large gene family found across eukaryotes. We have investigated this gene family in four ciliate species: Ichthyophthirius, Oxytricha, Paramecium, and Tetrahymena. Ciliates appear to encode more dynein heavy chain genes than most eukaryotes. Phylogenetic comparisons demonstrated that the last common ancestor of the ciliates that were examined expressed at least 14 types of dynein heavy chains with most of the expansion coming from the single‐headed inner arm dyneins. Each of the dyneins most likely performed different functions within the cell.     

Spatial extinction or persistence: landscape‐temperature interactions perturb predator–prey dynamics

Recognising that species interact across a range of spatial scales, we explore how landscape structure interacts with temperature to influence persistence. Specifically, we recognise that few studies indicate thermal shifts as the proximal cause of species extinctions; rather, species interactions exacerbated by temperature result in extinctions. Using microcosm‐based experiments, as models of larger landscape processes, we test hypotheses that would be problematic to address through field work. A text‐book predator–prey system (the ciliates Didinium and Paramecium) was used to compare three landscapes: an unfragmented landscape subjected to uniform temperatures (10, 20, 30°C); a fragmented landscape (potentially hosting metapopulations) subjected to these three temperatures; and a fragmented landscape subjected to a spatial temperature gradient (～ 10 to 30°C) – despite the prevalence of natural temperature ecoclines this is the first time such an analysis has been conducted. Initial thermal response‐analysis (growth, mortality, and movement measured between 10 and 30°C) suggested that as temperature increased, the predator might drive the prey to extinction. Thermal preferences (measured at 5 temperatures between 10 and 30°C), indicated that both predator and prey preferred warmer temperatures, with the predator exhibiting the stronger preference, suggesting that cooler regions might act as a prey‐refuge. The landscape level observations, however, did not entirely support the predictions. First, in the unfragmented landscape, increased temperature led to extinctions, but at the highest temperature (where the predator growth can be reduced) the prey survived. Second, at high temperatures the fragmented landscape failed to host metapopulations that would allow predator–prey persistence. Third, the thermal ecocline did not provide heterogeneity that improved stability; rather it forced both species to occupy a smaller realized space, leading toward extinctions. These findings reveal that temperature‐impacted rates and temperature preferences combine to drive predator–prey dynamics and persistence across landscapes.     

The demographic and life‐history costs of fear: Trait‐mediated effects of threat of predation on Aedes triseriatus

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A Note on the Possible Ecological Significance of Chemotaxis in Certain Ciliated Protozoa1

ABSTRACT. A heat-stable chemoattractant has been isolated from bacterial cultures. This component has a molecular weight in the range of 500–1000 daltons, is produced by both Gram-positive and Gram-negative bacteria, and serves equally well as an attractant for both the bacterial feeding Paramecium and for its natural predator, Didinium. Aspects of the ecological relationship between bacterial feeding ciliates and their ciliate predators are briefly discussed with respect to responses of both predator and prey to such a common chemotactic bacterial factor.     

Prey temporarily escape from predation in the presence of a second prey species

1. Indirect interactions between populations of different prey species mediated by a shared predator population are known to affect prey dynamics. 2. Depending on the temporal and spatial scale, these indirect interactions may result in positive (apparent mutualism), neutral or negative effects (apparent competition) of the prey on each other's densities. Although there is ample evidence for the latter, evidence for apparent mutualism is scarce. 3. The effectiveness of using one species of predator for biological control of more than one pest species depends on the occurrence of such positive or negative effects. 4. We used an experimental system consisting of the two prey species Western flower thrips (Franklineilla occidentalis Pergande) and greenhouse whitefly (Trialeurodes vaporariorum Westwood) and a shared predator, the phytoseiid mite Amblyseius swirskii Athias‐Henriot. We released all three species on the same plant and studied their dynamics and distribution along rows of plants. 5. We expected that the more mobile prey species (thrips) would escape temporarily in the presence of the other prey species (whitefly) by dispersing from plants with the predator. The predator was expected to disperse slower in the presence of two prey species because of the higher availability of food. 6. Evidence was found for slower dispersal of predators and short‐term escape of thrips from predation when whiteflies were present, thus confirming the occurrence of short‐term apparent mutualism. 7. The apparent mutualism resulted in a cascade to the first trophic level: a higher proportion of fruits was damaged by thrips in the presence of whiteflies. 8. We conclude that apparent mutualism can be an important phenomenon in population dynamics, and can significantly affect biological control of pest species that share a natural enemy.     

Feedback between size balance and consumption strongly affects the consequences of hatching phenology in size‐dependent predator–prey interactions

In many size‐dependent predator–prey systems, hatching phenology strongly affects predator–prey interaction outcomes. Early‐hatched predators can easily consume prey when they first interact because they encounter smaller prey. However, this process by itself may be insufficient to explain all predator–prey interaction outcomes over the whole interaction period because the predator–prey size balance changes dynamically throughout their ontogeny. We hypothesized that hatching phenology influences predator–prey interactions via a feedback mechanism between the predator–prey size balance and prey consumption by predators. We experimentally tested this hypothesis in an amphibian predator–prey model system. Frog tadpoles Rana pirica were exposed to a predatory salamander larva Hynobius retardatus that had hatched 5, 12, 19 or 26 days after the frog tadpoles hatched. We investigated how the salamander hatch timing affected the dynamics of prey mortality, size changes of both predator and prey, and their subsequent life history (larval period and size at metamorphosis). The predator–prey size balance favoured earlier hatched salamanders, which just after hatching could successfully consume more frog tadpoles than later hatched salamanders. The early‐hatched salamanders grew rapidly and their accelerated growth enabled them to maintain the predator‐superior size balance; thus, they continued to exert strong predation pressure on the frog tadpoles in the subsequent period. Furthermore, frog tadpoles exposed to the early‐hatched salamanders were larger at metamorphosis and had a longer larval period than other frog tadpoles. These results suggest that feedback between the predator‐superior size balance and prey consumption is a critical mechanism that strongly affects the impacts of early hatching of predators in the short‐term population dynamics and life history of the prey. Because consumption of large nutrient‐rich prey items supports the growth of predators, a similar feedback mechanism may be common and have strong impacts on phenological shifts in size‐dependent trophic relationships.     

Behavioural activity levels and expression of stress proteins under predation risk in two damselfly species

Abstract 1. It has become apparent that predators may strongly decrease prey fitness without direct contact with the prey, as they induce the development of defence systems that limit the availability of energy for growth and reproduction. Recent studies suggest that stress proteins may help prey organisms deal with this stress. The pattern is not general, however, and little is known about species differences in physiological traits in coping with predator stress, and covariation of physiological with other antipredator traits. 2. To explore these issues, we quantified levels of constitutive and fish‐induced stress proteins (Hsp60 and Hsp70) and anti‐predator behaviours in larvae of two damselfly species that differ in lifestyle. Both stress proteins were fixed at higher levels in Erythromma najas, which has a slow lifestyle, than in Lestes sponsa, which has a fast lifestyle. Similarly, anti‐predator behaviours were fixed at safer levels in E. najas than in L. sponsa. 3. These results suggest that stress proteins may be part of anti‐predator syndromes of damselfly larvae, and there may be trait co‐specialisation between stress proteins and behavioural anti‐predator traits. Studies formally testing these hypotheses in more species may prove rewarding in advancing our understanding of the functional integration of physiological anti‐predator traits in relation to the prey’s lifestyle.     

Predatory fish impact on competition between stream insect grazers: a consideration of behaviorally- and density-mediated effects on an apparent coexistence pattern

A manipulative field experiment and theoretical analyses of a simple competition model were used to show how exploitative competition between a caddisfly (Glossosoma sp.) and three mayfly grazers (Ameletus sp., Baetisthermicus and Cinygmula sp.) was mediated by a predatory fish, freshwater sculpin (Cottus nozawae). The field experiment followed a two‐factorial design, with Glossosoma densities (natural vs reduced) and sculpin presence (present vs absent) as treatments. Diet analysis revealed that all four prey species were eaten under the natural condition and the sculpin preferred mayfly grazers to Glossosoma. Our experiment showed that although mayfly densities in the presence of either sculpin or Glossosoma were lower than in the no‐sculpin plus reduced‐Glossosoma treatment, no difference in mayfly densities was found between the following three treatments: sculpin plus natural‐Glossosoma, no‐sculpin plus natural‐Glossosoma, and sculpin plus reduced‐Glossosoma. These results indicated that fish predator produced no effects additive to the competitive operation on the mayfly density, and also that competitive operation of Glossosoma on the mayfly densities produced no additional effects to fish predators. In addition, although the competitive effect of the mayflies on Glossosoma could not be manipulated in isolation, the density of Glossosoma in the presence of sculpin was greater than that in the absence of sculpin in the natural‐Glossosoma treatment. Thus, the densities of these competing grazers either stayed the same or increased in the presence of the fish predator relative to predator‐free treatments. A theoretical model, developed to explain the experimental results here, predicted that the densities of the two competing prey under predation pressure could be simultaneously greater than those under predator absent conditions when the behaviorally‐mediated effects of the predator were strongly operative. Although we were unable to distinguish experimentally the two different effects of predator on the prey competition, the behaviorally‐ and density‐mediated effects, the reality of the behaviorally‐mediated effects in the experiment was discussed.     

Responses of the ciliates <Emphasis Type="Italic">Tetrahymena</Emphasis> and <Emphasis Type="Italic">Paramecium</Emphasis> to external ATP and GTP

The unicellular ciliates Paramecium and Tetrahymena are the simplest eukaryotic cells to show reliable depolarizing responses to micromolar concentrations of external ATP and GTP. Their simplicity allows for combined analysis of swimming behavior, electrophysiology, receptor binding, behavioral mutant and drug screens as well as molecular genetic approaches such as RNAi and gene knockouts experiments. ATP and GTP are depolarizing chemorepellents in both ciliates, producing measurable receptor potentials and Ca²⁺-based action potentials that are correlated with jerking behaviors called avoiding reactions (AR). GTP also causes repetitive continuous ciliary reversals (CCR) and oscillating plateau depolarizations in Paramecium. Both ciliates show high affinity, saturable external binding of ³²P-GTP and ³²P-ATP but GTP does not compete for ATP binding and vice versa. Chemosensory adaptation occurs after continued exposure (15 min) to these ligands, producing a loss of external binding and forward swimming. However, cells adapted to ATP still bind and respond to GTP and GTP-adapted cells still bind and respond to ATP. This, combined with pharmacological analyses, suggests that there are two separate receptor systems: A metabotropic ATP receptor pathway and a different, novel GTP receptor pathway. A Paramecium mutant (ginA) lacks the GTP-induced oscillating depolarizations but does show AR in GTP, unveiling isolated GTP-receptor potentials for study. An ecto-ATPase is also present that may be involved in inactivation of ATP and GTP signals. Gene knockout experiments are currently underway to determine the roles of the ecto-ATPase and a putative 7-transmembrane spanning receptor in these responses.     

Predator density and competition modify the benefits of group formation in a shoaling reef fish

Synthesis Predation risk experienced by individuals living in groups depends on the balance between predator dilution, competition for refuges, and predator interference or synergy. These interactions operate between prey species as well: the benefits of group living decline in the presence of an alternative prey species. We apply a novel model‐fitting approach to data from field experiments to distinguish among competing hypotheses about shifts in predator foraging behavior across a range of predator and prey densities. Our study provides novel analytical tools for analyzing predator foraging behavior and offers insight into the processes driving the dynamics of coral reef fish. Studies of predator foraging behavior typically focus on single prey species and fixed predator densities, ignoring the potential importance of complexities such as predator dilution; predator‐mediated effects of alternative prey; heterospecific competition; or predator–predator interactions. Neglecting the effects of prey density is particularly problematic for prey species that live in mixed species groups, where the beneficial effects of predator dilution may swamp the negative effects of heterospecific competition. Here we use field experiments to investigate how the mortality rates of a shoaling coral reef fish (a wrasse: Thalassoma amblycephalum), change as a result of variation in: 1) conspecific density, 2) density of a predator (a hawkfish: Paracirrhites arcatus), and 3) presence of an alternative prey species that competes for space (a damselfish: Pomacentrus pavo). We quantify changes in prey mortality rates from the predator's perspective, examining the effects of added predators or a second prey species on the predator's functional response. Our analysis highlights a model‐fitting approach that discriminates amongst multiple hypotheses about predator foraging in a community context. Wrasse mortality decreased with increasing conspecific density (i.e. mortality was inversely density‐dependent). The addition of a second predator doubled prey mortality rates, without significantly changing attack rate or handling time – i.e. there was no evidence for predator interference. The presence of a second prey species increased wrasse mortality by 95%; we attribute this increase either to short‐term apparent competition (predator aggregation) or to a decrease in handling time of the predator (e.g. through decreased wrasse vigilance). In this system, 1) prey benefit from intraspecific group living though a reduced predation risk, and 2) the benefit of group living is reduced in the presence of an alternative prey species.     

Guanylyl cyclases in unicellular organisms

Guanylyl cyclases in eukaryotic unicells were biochemically investigated in the ciliates Paramecium and Tetrahymena, in the malaria parasite Plasmodium and in the ameboid Dictyostelium. In ciliates guanylyl cyclase activity is calcium-regulated suggesting a structural kinship to similarly regulated membrane-bound guanylyl cyclases in vertebrates. Yet, cloning of ciliate guanylyl cyclases revealed a novel combination of known modular building blocks. Two cyclase homology domains are inversely arranged in a topology of mammalian adenylyl cyclases, containing two cassettes of six transmembrane spans. In addition the protozoan guanylyl cyclases contain an N-terminal P-type ATPase-like domain. Sequence comparisons indicate a compromised ATPase function. The adopted novel function remains enigmatic to date. The topology of the guanylyl cyclase domain in all protozoans investigated is identical. A recently identified Dictyostelium guanylyl cyclase lacks the N-terminal P-type ATPase domain. The close functional relation of Paramecium guanylyl cyclases to mammalian adenylyl cyclases has been established by heterologous expression, respective point mutations and a series of active mammalian adenylyl cyclase/Paramecium guanylyl cyclase chimeras. The unique structure of protozoan guanylyl cyclases suggests that unexpectedly they do not share a common guanylyl cyclase ancestor with their vertebrate congeners but probably originated from an ancestral mammalian-type adenylyl cyclase.     

Reversed predator–prey cycles are driven by the amplitude of prey oscillations

Ecoevolutionary feedbacks in predator–prey systems have been shown to qualitatively alter predator–prey dynamics. As a striking example, defense–offense coevolution can reverse predator–prey cycles, so predator peaks precede prey peaks rather than vice versa. However, this has only rarely been shown in either model studies or empirical systems. Here, we investigate whether this rarity is a fundamental feature of reversed cycles by exploring under which conditions they should be found. For this, we first identify potential conditions and parameter ranges most likely to result in reversed cycles by developing a new measure, the effective prey biomass, which combines prey biomass with prey and predator traits, and represents the prey biomass as perceived by the predator. We show that predator dynamics always follow the dynamics of the effective prey biomass with a classic ¼‐phase lag. From this key insight, it follows that in reversed cycles (i.e., ¾‐lag), the dynamics of the actual and the effective prey biomass must be in antiphase with each other, that is, the effective prey biomass must be highest when actual prey biomass is lowest, and vice versa. Based on this, we predict that reversed cycles should be found mainly when oscillations in actual prey biomass are small and thus have limited impact on the dynamics of the effective prey biomass, which are mainly driven by trait changes. We then confirm this prediction using numerical simulations of a coevolutionary predator–prey system, varying the amplitude of the oscillations in prey biomass: Reversed cycles are consistently associated with regions of parameter space leading to small‐amplitude prey oscillations, offering a specific and highly testable prediction for conditions under which reversed cycles should occur in natural systems.     

Antagonistic indirect interactions between large and small conspecific prey via a heterospecific predator

Intrapopulation size variation strongly influences ecological interactions because individuals belonging to different size groups have distinct functions. Most demonstrations of the impacts of size variation in trophic systems have focused on size variation in predator species, and the consequences of size variation in prey species are less well understood. We investigated how prey size structure shapes intra‐ and interspecific interactions in experiments with a gape‐limited predator (larvae of the salamander Hynobius retardatus) and its heterospecific prey (frog tadpoles, Rana pirica). We found that large and small tadpole size groups each increased mortality in the other group by intensifying salamander predation; this type of indirect interactions is called apparent competition. The antagonistic impacts on the prey size groups were caused by different size‐specific mechanisms. By consuming small tadpoles, the salamanders grew large enough to consume large tadpoles. The activity of large tadpoles, by increasing the activity of the small tadpoles, may increase the number of encounters with the predator and thus small tadpole mortality. These results suggest that the magnitude of a predator's ecological role, such as whether a top–down trophic cascade is initiated, depends on size variation in its heterospecific prey.     

Eco‐evolutionary feedbacks between prey densities and linkage disequilibrium in the predator maintain diversity

Diversity occurs at multiple scales. Within a single population, there is diversity in genotypes and phenotypes. At a larger scale, within ecological communities, there is diversity in species. A number of studies have investigated how diversity at these two scales influence each other through what has been termed eco‐evolutionary feedbacks. Here we study a three‐species ecological module called apparent competition, in which the predator is evolving in a trait that determines its interaction with two prey species. Unlike previous studies on apparent competition, which employed evolutionary frameworks with very simple genetics, we study an eco‐evolutionary model in which the predator's trait is determined by two recombining diallelic loci, so that its mean and variance can evolve, as well as associations (linkage disequilibrium) between the loci. We ask how eco‐evolutionary feedbacks with these two loci affect the coexistence of the prey species and the maintenance of polymorphisms within the predator species. We uncover a novel eco‐evolutionary feedback between the prey densities and the linkage disequilibrium between the predator's loci. Through a stability analysis, we demonstrate how these feedbacks affect polymorphisms at both loci and, among others, may generate stable cycling.     

Variation of prey responses to cues from a mesopredator and an apex predator

Detection and avoidance of predator cues can be costly, so it is important for prey to balance the benefits of gaining food against the costs of avoiding predators. Balancing these factors becomes more complicated when prey are threatened by more than one type of predator. Hence, the ability to recognize species‐specific predator odours and prioritize behaviours according to the level of risk is essential for survival. We investigated how rock rats, Zyzomys spp. modify their foraging behaviour and giving‐up density (GUD) in the presence of an apex predator, the dingo Canis dingo, a mesopredator, the northern quoll Dasyurus hallucatus, a herbivore, the rock wallaby Petrogale brachyotis as a pungency control and water as a procedural control. Both dingoes and quolls consume rock rats, but because quolls can enter small crevices inhabited by rock rats, they pose a greater threat to rock rats than dingoes. Rock rats demonstrated a stronger avoidance to quoll odour than dingo odour, and no avoidance of the pungency control (rock wallaby) and the procedural control (water). GUD values declined significantly over the duration of the study, but did not differ between odour treatments. Our results support the hypothesis that prey vary behaviour according to perceived predator threat, and show stronger responses to potentially more dangerous predators.