The evolution and ecology of multiple antipredator defences

Prey seldom rely on a single type of antipredator defence, often using multiple defences to avoid predation. In many cases, selection in different contexts may favour the evolution of multiple defences in a prey. However, a prey may use multiple defences to protect itself during a single predator encounter. Such “defence portfolios” that defend prey against a single instance of predation are distributed across and within successive stages of the predation sequence (encounter, detection, identification, approach (attack), subjugation and consumption). We contend that at present, our understanding of defence portfolio evolution is incomplete, and seen from the fragmentary perspective of specific sensory systems (e.g., visual) or specific types of defences (especially aposematism). In this review, we aim to build a comprehensive framework for conceptualizing the evolution of multiple prey defences, beginning with hypotheses for the evolution of multiple defences in general, and defence portfolios in particular. We then examine idealized models of resource trade-offs and functional interactions between traits, along with evidence supporting them. We find that defence portfolios are constrained by resource allocation to other aspects of life history, as well as functional incompatibilities between different defences. We also find that selection is likely to favour combinations of defences that have synergistic effects on predator behaviour and prey survival. Next, we examine specific aspects of prey ecology, genetics and development, and predator cognition that modify the predictions of current hypotheses or introduce competing hypotheses. We outline schema for gathering data on the distribution of prey defences across species and geography, determining how multiple defences are produced, and testing the proximate mechanisms by which multiple prey defences impact predator behaviour. Adopting these approaches will strengthen our understanding of multiple defensive strategies.     

Density-dependent effects of prey defences

In this study, we show that the protective advantage of a defence depends on prey density. For our investigations, we used the predator-prey model system Chaoborus-Daphnia pulex. The prey, D. pulex, forms neckteeth as an inducible defence against chaoborid predators. This morphological response effectively reduces predator attack efficiency, i.e. number of successful attacks divided by total number of attacks. We found that neckteeth-defended prey suffered a distinctly lower predation rate (prey uptake per unit time) at low prey densities. The advantage of this defence decreased with increasing prey density. We expect this pattern to be general when a defence reduces predator success rate, i.e. when a defence reduces encounter rate, probability of detection, probability of attack, or efficiency of attack. In addition, we experimentally simulated the effects of defences which increase predator digestion time by using different sizes of Daphnia with equal vulnerabilities. This type of defence had opposite density-dependent effects: here, the relative advantage of defended prey increased with prey density. We expect this pattern to be general for defences which increase predator handling time, i.e. defences which increase attacking time, eating time, or digestion time. Many defences will have effects on both predator success rate and handling time. For these defences, the predator’s functional response should be decreased over the whole range of prey densities. Received: 15 September 1999 / Accepted: 23 December 1999     

Dynamic state-dependent modelling predicts optimal usage patterns of responsive defences

Chemical defences against predation often involve responses to specific predation events where the prey expels fluids, such as haemolymph or gut contents, which are aversive to the predator. The common link is that each predation attempt that is averted results in an energetic cost and a reduction in the chemical defences of the prey, which might leave the prey vulnerable if the next predation attempt occurs soon afterwards. Since prey appear to be able to control the magnitude of their responses, we should expect them to trade-off the need to repel the current threat against the need to preserve defences against future threats and conserve energy for other essential activities. Here we use dynamic state-dependent models to predict optimal strategies of defence deployment in the juvenile stage of an animal that has to survive to maturation. We explore the importance of resource level, predator density, and the costs of making defences on the magnitude of the responses and optimal age and size at maturation. We predict the patterns of investment and the magnitude of the deployment of defences to potentially multiple attacks over the juvenile period, and show that responses should be smaller when the costs of defences and/or predation risk are higher. The model enables us to predict that animals in which defences benefit the adult stage will employ different strategies than those that do not use the same defences as adults, and thereby experience a smaller reduction in body size as a result of repeated attacks. We also explore the effect of the importance of adult size, and find that the sex and mating system of the prey should also affect defensive strategies. Our work provides the first predictive theory of the adaptive use of responsive defences across taxa.     

Inducible defences and the paradox of enrichment

In order to evaluate the effects of inducible defences on community stability and persistence, we analyzed models of bitrophic and tritrophic food chains that incorporate consumer-induced polymorphisms. These models predict that intra-specific heterogeneity in defence levels resolves the paradox of enrichment for a range of top-down effects that affect consumer death rates and for all possible levels of primary productivity. We show analytically that this stability can be understood in terms of differences in handling times on the different prey types. Our predictions still hold when defences also affect consumer attack rates. The predicted stability occurs in both bitrophic and tritrophic food chains.
Inducible defences may promote population persistence in tritrophic food chains. Here the minimum densities of cycling populations remain bound away from zero, thus decreasing the risk of population extinctions. However, the reverse can be true for the equivalent bitrophic predator–prey model. This shows that theoretical extrapolations from simple to complex communities should be made with caution. Our results show that inducible defences are among the ecological factors that promote stability in multitrophic communities.     

Automimicry and the evolution of discrete prey defences

We consider the neglected question of how secondary defences of prey animals evolve if they are discontinuous in nature, being either present or absent, or expressible over a limited number of levels. We present a novel computer model that evaluates the conditions in which defended mutant prey may (1) fail to rise above nontrivial levels within a population, (2) reach values close to fixation, or (3) find some evolutionarily stable strategy (ESS) frequency between these two situations. Undefended prey that coexist with defended conspecifics are known as automimics. One finding is that automimicry can be an ESS over a range of conditions, but especially when prey are relatively cryptic and secondary defences are very effective at deterring predation. Evolutionarily stable automimicry emerges from the interplay between the direct benefits of costly defences in surviving individual attacks by predators and frequency-dependent benefits conferred on all prey, from a reduction in the rate of attack on all identical-looking prey. When, in contrast, secondary defences have continuous variation, the result is effectively a monomorphic state of defence across the population. Thus the degree and kind of variation that a defence takes has a profound effect on its initial evolution. We discuss the interesting possibility that mixed ESSs may help explain some examples of variation in prey secondary defences.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 87 , 393–402.     

Taste-rejection behaviour by predators can promote variability in prey defences

The evolution and maintenance of toxicity in a prey population is a challenge to evolutionary biologists if the investment in toxin does not benefit the individual. Recent experiments suggest that taste-rejection behaviour enables predators to selectively ingest less toxic individuals, which could stabilize investment in defences. However, we currently do not know if taste rejection of defended prey is accurate across different contexts, and that prey always benefit according to their investment. Using avian predators, we show that the rejection probability does not solely depend on the investment in defence by an individual, but also on the investment by other individuals in the same population. Therefore, taste rejection by predators could lead to destabilization in the investment in defences, and allow variability in prey defences to exist.     

Linking herbivore-induced defences to population dynamics

1. Theoretical studies have shown that inducible defences have the potential to affect population stability and persistence in bi‐ and tritrophic food chains. Experimental studies on such effects of prey defence strategies on the dynamics of predator–prey systems are still rare. We performed replicated population dynamics experiments using the herbivorous rotifer Brachionus calyciflorus and four strains of closely related algae that show different defence responses to this herbivore. 2. We observed herbivore populations to fluctuate at a higher frequency when feeding on small undefended algae. During these fluctuations minimum rotifer densities remained sufficiently high to ensure population persistence in all the replicates. The initial growth of rotifer populations in this treatment coincided with a sharp drop in algal density. Such a suppression of algae by herbivores was not observed in the other treatments, where algae were larger due to induced or permanent defences. In these treatments we observed rotifer population densities to first rise and then decline. The herbivore went extinct in all replicates with large permanently defended algae. The frequency of herbivore extinctions was intermediate when algae had inducible defences. 3. A variety of alternative mechanisms could explain differential herbivore persistence in the different defence treatments. Our analysis showed the density and fraction of highly edible algal particles to better explain herbivore persistence and extinctions than total algal density, the fraction of highly inedible food particles or the accumulation of herbivore waste products or autotoxins. 4. We argue that the rotifers require a minimum fraction and density of edible food particles for maintenance and reproduction. We conjecture that induced defences in algae may thus favour larger zooplankton species such as Daphnia spp. that are less sensitive to shifts in their food size spectrum, relative to smaller zooplankton species, such as rotifers and in this way contributes to the structuring of planktonic communities.     

Behavioural responses to predation may explain shifts in community structure

相似文献   

Benefits,costs and reactivity of inducible defences: an experimental test with rotifers

1. A key aspect of the ecology and evolution of adaptive prey responses to predator risk is the timing by which the former develop a defensive trait in response to inducing signals released by the latter. This property, called reactivity, has been shown to affect population stability and persistence. 2. Theoretically, the minimal predator density required by prey to exhibit induced defences is expected to increase with the effectiveness of the defence and decrease with its cost. Likewise, the time required for the prey population to exhibit an induced defence is expected to increase together with cost. 3. The freshwater rotifers Brachionus calyciflorus and B. havanaensis and their predator Asplanchna brightwelli were used to test the hypothesis that prey species exhibiting defences that offer a larger fitness benefit and lower fitness cost are more reactive to predator signals, in terms of requiring shorter exposure time and lower signal concentration to trigger a morphological defence reaction. 4. Our results showed that both prey species exhibited costly and effective defences after induction by predator infochemicals. Faster reactions were observed at higher levels of predator cues. Nevertheless, the observed relationship between reactivity and benefit/cost of defences did not agree with our expectations. 5. To our knowledge, this is the first study in which the timing of induction of morphological defences is experimentally assessed over a gradient of risk signals. We propose new research directions to disentangle the mechanisms and project the consequences of prey decisions at the morphological level.     

Effects of the presence of a predatory fish and the phenotype of its prey (a shredding shrimp) on leaf litter decomposition

相似文献   

Physical and chemical properties of primary defences in Tenebrio molitor

Prevention and reaction are the foundation for any defence system. In insects, the primary defences against pathogens and parasites limit invasion; the secondary ones (e.g. immune system) act when the cuticle and other primary defences fail. Because investment in both aspects of defence may be costly, they should be regulated in a plastic or variable way in accordance with the risk of infection. The mealworm beetle Tenebrio molitor L. changes cuticle colour and its resistance to fungal infection when subject to high population density, although such resistance is a result of the primary (cuticle) defences rather than the secondary (immunological) ones. The present study tests the hypothesis that the physical and chemical properties of the primary defences in T. molitor change with cuticular darkness. Beetles expressing black phenotypes (or with darker cuticle) have a thicker cuticle, with four well organized layers (epi‐, exo‐, endocuticle and formation zone) and more melanin than tan beetles. The cuticle properties investigated in the present study are likely to be the underlying mechanisms of pathogen resistance in black beetles, including the content of carbonylated proteins, which in black beetles was almost half that of tan beetles after exposure to ultraviolet radiation. It is proposed that, in polyphenic insects (such as mealworm beetles), primary and secondary defences are regulated pleiotropically, with the genes responsible for the expression of one defence having a positive effect on others, whereas, in polymorphic insects, there is no such link and so investment in one defence may impair others.     

Costs and limits of dosage response to predation risk: to what extent can tadpoles invest in anti-predator morphology?

Inducible defences have long been considered as a polyphenism opposing defended and undefended morphs. However, in nature, preys are exposed to various levels of predation risk and scale their investment in defence to actual predation risk. Still, among the traits that are involved in the defence, some are specific to one predator type while others act as a more generalised defence. The existence of defence costs could prevent an individual investing in all these traits simultaneously. In this study, we investigate the impact of an increasing level of predator density (stickleback, Gasterosteus aculeatus) on the expression of morphological inducible defences in tadpoles of Rana dalmatina. In this species, investment in tail length and tail muscle is a stickleback-specific response while increased tail fin depth is a more general defence. As expected, we found a relationship between investment in defence and level of risk through the responses of tail fin depth and tail length. We also found an exponential increase of defence cost, notably expressed by convex decrease of growth and developmental rates. We found a relative independence of investment in the different traits that compose the defence, revealing a high potential for fine tuning the expression of defended phenotypes with respect to local ecological conditions.     

The evolutionary stability of automimicry

Internal defences such as toxins cannot be detected from a distance by a predator, and are likely to be costly to produce and maintain. Populations of well-defended prey may therefore be vulnerable to invasion from rare 'cheater' mutants that do not produce the toxin themselves but obtain some protection from their resemblance to their better defended conspecifics (automimicry). Although it is well established that well-defended and weakly defended morphs may coexist stably in protected dimorphisms, recent theoretical work suggests that such dimorphisms would not be resistant to invasion by novel mutants with defence levels intermediate to those present. Given that most defences (including toxins) are likely to be continuous traits, this implies that automimicry may tend to be a transitory phenomenon, and thus less likely to explain variation in defence levels in nature. In contrast to this, we show that automimicry can also be evolutionarily stable for continuous traits, and that it may evolve under a wide range of conditions. A recently developed geometric method allows us to determine directly from a trade-off curve whether an evolutionarily stable defence dimorphism is at all possible, and to make some qualitative inferences about the ecological conditions that may favour it.     

A field demonstration of the costs and benefits of group living to edible and defended prey

Both theoretical and laboratory research suggests that many prey animals should live in a solitary, dispersed distribution unless they lack repellent defences such as toxins, venoms and stings. Chemically defended prey may, by contrast, benefit substantially from aggregation because spatial localization may cause rapid predator satiation on prey toxins, protecting many individuals from attack. If repellent defences promote aggregation of prey, they also provide opportunities for new social interactions; hence the consequences of defence may be far reaching for the behavioural biology of the animal species. There is an absence of field data to support predictions about the relative costs and benefits of aggregation. We show here for the first time using wild predators that edible, undefended artificial prey do indeed suffer heightened death rates if they are aggregated; whereas chemically defended prey may benefit substantially by grouping. We argue that since many chemical defences are costly to prey, aggregation may be favoured because it makes expensive defences much more effective, and perhaps allows grouped individuals to invest less in chemical defences.     

Frequency-dependent taste-rejection by avian predation may select for defence chemical polymorphisms in aposematic prey

Chemically defended insects advertise their unpalatability to avian predators using conspicuous aposematic coloration that predators learn to avoid. Insects utilize a wide variety of different compounds in their defences, and intraspecific variation in defence chemistry is common. We propose that polymorphisms in insect defence chemicals may be beneficial to insects by increasing survival from avian predators. Birds learn to avoid a colour signal faster when individual prey possesses one of two unpalatable chemicals rather than all prey having the same defence chemical. However, for chemical polymorphisms to evolve within a species, there must be benefits that allow rare chemical morphs to increase in frequency. Using domestic chicks as predators and coloured crumbs for prey, we provide evidence that birds taste and reject proportionally more of the individuals with rare defence chemicals than those with common defence chemicals. This indicates that the way in which birds attack and reject prey could enhance the survival of rare chemical morphs and select for chemical polymorphism in aposematic species. This is the first experiment to demonstrate that predators can directly influence the form taken by prey's chemical defences.     

Density-dependent investment in costly anti-predator defences: an explanation for the weak survival benefit of group living

A central explanation for group living across animal taxa is the reduced rate of attack by predators. However, many field observations show a weak or non-existent effect of group size on per capita mortality rates. Herein we resolve this apparent paradox. We found that Pieris brassicae larvae defended themselves less readily when in groups than when alone, in that they were more reluctant to regurgitate in response to simulated attacks and produced less regurgitant. Furthermore, a simple model demonstrates that this reluctance was sufficient to cancel out the benefit from being in a group. This conditional strategy can be understood in terms of the costs and benefits of defences. For grouped individuals, defence is less often required because attack rates are lower and the costs of defence may be higher due to competition for resources. These phenomena are likely to be widespread in facultatively gregarious species that utilise anti-predator defences.     

Express yourself: bold individuals induce enhanced morphological defences

Organisms display an impressive array of defence strategies in nature. Inducible defences (changes in morphology and/or behaviour within a prey''s lifetime) allow prey to decrease vulnerability to predators and avoid unnecessary costs of expression. Many studies report considerable interindividual variation in the degree to which inducible defences are expressed, yet what underlies this variation is poorly understood. Here, we show that individuals differing in a key personality trait also differ in the magnitude of morphological defence expression. Crucian carp showing risky behaviours (bold individuals) expressed a significantly greater morphological defence response when exposed to a natural enemy when compared with shy individuals. Furthermore, we show that fish of different personality types differ in their behavioural plasticity, with shy fish exhibiting greater absolute plasticity than bold fish. Our data suggest that individuals with bold personalities may be able to compensate for their risk-prone behavioural type by expressing enhanced morphological defences.     

You get what you pay for: reward-specific trade-offs among direct and ant-mediated defences in plants

Plant defences against herbivores include direct defences such as secondary metabolites or physical structures (e.g. trichomes) as well as indirect defences mediated via mutualistic interactions with other organisms including ants. Production of both direct defences and rewards for mutualistic ants may be costly for a plant, and it has been suggested that trade-offs may exist between direct and ant-mediated defences. We have conducted a meta-analysis of 25 studies testing the above hypothesis and found a significant negative correlation between plant allocation to direct and ant-mediated defences. The strength of correlation was similar for across- and within-species comparisons, and for chemical and physical direct defences. However, trade-offs with direct defences were significant only in plants which offered to ants more costly rewards such as food bodies and/or domatia, but not in plants which attracted ants with relatively cheap extrafloral nectaries. Our results therefore support the hypothesis that plant investment in ant-mediated defences may reduce the requirement for direct chemical and physical defences, but only in plants which offer more costly rewards to their bodyguards.     

Behavioural ecology of defence in a risky environment: caterpillars versus ants in a Neotropical savanna

1. Predatory ants may reduce infestation by herbivorous insects, and slow‐moving Lepidopteran larvae are often vulnerable on foliage. We investigate whether caterpillars with morphological or behavioural defences have decreased risk of falling prey to ants, and if defence traits mediate host plant use in ant‐rich cerrado savanna. 2. Caterpillars were surveyed in four cerrado localities in southeast Brazil (70–460 km apart). The efficacy of caterpillar defensive traits against predation by two common ant species (Camponotus crassus, C. renggeri) was assessed through experimental trials using caterpillars of different species and captive ant colonies. 3. Although ant presence can reduce caterpillar infestation, the ants' predatory effects depend on caterpillar defence traits. Shelter construction and morphological defences can prevent ant attacks (primary defence), but once exposed or discovered by ants, caterpillars rely on their size and/or behaviour to survive (secondary defence). 4. Defence efficiency depends on ant identity: C. renggeri was more aggressive and lethal to caterpillars than C. crassus. Caterpillars without morphological defences or inside open shelters were found on plants with decreased ant numbers. No unsheltered caterpillar was found on plants with extrafloral nectaries (EFNs). Caterpillars using EFN‐bearing plants lived in closed shelters or presented morphological defences (hairs, spines), and were less frequently attacked by ants during trials. 5. The efficiency of defences against ants is thus crucial for caterpillar survival and determines host plant use by lepidopterans in cerrado. Our study highlights the effect of EFN‐mediated ant‐plant interactions on host plant use by insect herbivores, emphasizing the importance of a tritrophic viewpoint in risky environments.     

Defence Cheats Can Degrade Protection of Chemically Defended Prey

Many species defend themselves against enemies using repellent chemicals. An important but unanswered question is why investment in chemical defence is often variable within prey populations. One explanation is that some prey benefit by cheating, paying no costs of defence, but gaining a reduced attack rate because of the presence of defended conspecifics. Two important assumptions about predator behaviour must be met to explain cheating as a stable strategy: first, predators increase attack rates as cheats increase in frequency; second, defended prey survive attacks better than non‐defended conspecifics. We lack data from wild predators that evaluate these hypotheses. Here, we examine how changes in the frequency of non‐defended ‘cheats’ affect predation by wild birds on a group of otherwise defended prey. We presented mealworm larvae that were either edible (‘cheats’) or unpalatable (bitter tasting), and varied the proportion of cheats from 0 to 1 by increments of 0.25. We found strong frequency‐dependent effects on the birds' foraging behaviour, with the proportion of prey attacked increasing nonlinearly with the frequency of cheats. We did not, however, observe that birds taste‐rejected defended prey at the site of capture. One explanation is that wild birds may not assess prey palatability at the site of capture, but do this elsewhere. If so, defended and undefended prey may pay high costs of initial attack and relocation away from ecologically favourable locations. Alternatively, defended prey may not be taste‐rejected because with acute time constraints, wild birds do not have time to make fine‐grained decisions during feeding. We discuss the data in relation to the evolutionary ecology of prey defences.