Alternative prey can change model–mimic dynamics between parasitism and mutualism

Classical (conventional) Müllerian mimicry theory predicts that two (or more) defended prey sharing the same signal always benefit each other despite the fact that one species can be more toxic than the other. The quasi‐Batesian (unconventional) mimicry theory, instead, predicts that the less defended partner of the mimetic relationship may act as a parasite of the signal, causing a fitness loss to the model. Here we clarify the conditions for parasitic or mutualistic relationships between aposematic prey, and build a model to examine the hypothesis that the availability of alternative prey is crucial to Müllerian and quasi‐Batesian mimicry. Our model is based on optimal behaviour of the predator. We ask if and when it is in the interest of the predator to learn to avoid certain species as prey when there is alternative (cryptic) prey available. Our model clearly shows that the role of alternative prey must be taken into consideration when studying model–mimic dynamics. When food is scarce it pays for the predator to test the models and mimics, whereas if food is abundant predators should leave the mimics and models untouched even if the mimics are quite edible. Dynamics of the mimicry tend to be classically Müllerian if mimics are well defended, while quasi‐Batesian dynamics are more likely when they are relatively edible. However, there is significant overlap: in extreme cases mimics can be harmful to models (a quasi‐Batesian case) even if the species are equally toxic. A crucial parameter explaining this overlap is the search efficiency with which indiscriminating vs. discriminating predators find cryptic prey. Quasi‐Batesian mimicry becomes much more likely if discrimination increases the efficiency with which the specialized predator finds cryptic prey, while the opposite case tends to predict Müllerian mimicry. Our model shows that both mutualistic and parasitic relationship between model and mimic are possible and the availability of alternative prey can easily alter this relationship.     

Reduced performance of prey targeting in pit vipers with contralaterally occluded infrared and visual senses

Both visual and infrared (IR) senses are utilized in prey targeting by pit vipers. Visual and IR inputs project to the contralateral optic tectum where they activate both multimodal and bimodal neurons. A series of ocular and pit organ occlusion experiments using the short-tailed pit viper (Gloydius brevicaudus) were conducted to investigate the role of visual and IR information during prey targeting. Compared with unoccluded controls, snakes with either both eyes or pit organs occluded performed more poorly in hunting prey although such subjects still captured prey on 75% of trials. Subjects with one eye and one pit occluded on the same side of the face performed as well as those with bilateral occlusion although these subjects showed a significant targeting angle bias toward the unoccluded side. Performance was significantly poorer when only a single eye or pit was available. Interestingly, when one eye and one pit organ were occluded on opposite sides of the face, performance was poorest, the snakes striking prey on no more than half the trials. These results indicate that, visual and infrared information are both effective in prey targeting in this species, although interference between the two modalities occurs if visual and IR information is restricted to opposite sides of the brain.     

Is arthropod predation exclusively satiation‐driven?

Functional response models differ in which factors limit predation (e.g. searching efficiency, prey handling time, digestion) and whether predation behaviour is governed by an internal physiological state (e.g. satiation). There is now much evidence that satiation is a key factor in understanding changes in foraging behaviour, and that many predators are effectively digestion limited. Here, we ask if predation in a predatory arthropod can be explained from satiation-driven behaviour alone, or if behaviour is also influenced by the density of prey other than via the effect of prey ingestion on satiation. To address this question a satiation-based predation model is formulated, for which parameters are estimated on the basis of observations on digestion rate, satiation-related prey searching rate and prey capture behaviour, basically under high prey density conditions. The model predictions are subsequently tested against longer term predation experiments carried out at high and low prey densities. Since satiation can easily be linked with egg production, these tests are carried out both for predation and oviposition.
The predator–prey systems under study consist of females of two predatory mite species ( Neoseiulus barkeri and N. cucumeris ) and the larvae of two thrips species ( Thrips tabaci and Frankliniella occidentalis ) as their prey. For N. barkeri foraging on T. tabaci , the model gives good predictions at both high (4 larvae cm⁻¹) and low (0.1–1 larvae cm⁻²) prey densities. For N. cucumeris foraging on F. occidentalis , the predictions hold at the high prey density, but are too low at low prey densities. Thus our analysis indicates that we cannot fully explain density-dependent predation rates from satiation-driven behaviour alone. Different mechanisms are suggested on how prey density may affect foraging efficiency other than via satiation.     

From pattern to process: identifying predator–prey models from time-series data

Fitting nonlinear models to time-series is a technique of increasing importance in population ecology. In this article, we apply it to assess the importance of predator dependence in the predation process by comparing two alternative models of equal complexity (one with and one without predator dependence) to predator–prey time-series. Stochasticities in such data come from both observation error and process error. We consider how these errors must be taken into account in the fitting process, and we develop eight different model selection criteria. Applying these criteria to laboratory data on simple protozoan and arthropod predator–prey systems shows that little predator dependence is present, with one interesting exception. Field data are more ambiguous (either selection depends on the particular criterion or no significant differences can be detected), and we show that both models fit reasonably well. We conclude that, within our modeling framework, predator dependence is in general insignificant in simple systems in homogeneous environments. Relatively complex systems show significant predator dependence more often than simple ones but the data are also often inconclusive. The analysis of such systems should rely on several models to detect predictions that are sensitive to predator dependence and to direct further research if necessary. Received: July 13, 2000 / Accepted: September 25, 2001     

Background evolution in camouflage systems: A predator-prey/pollinator-flower game

A common predator or anti-predator strategy involves camouflage based on background matching. In some systems, the background is an organism whose fitness is affected by the predator-prey interaction. In these cases, the phenotype of the background species may evolve to affect the degree of background matching in the predator-prey interaction. For example, some flower species (the background) are inhabited by camouflaged ambush predators that attack visiting pollinators. These flowers have a fitness interest in the outcome of the predator-prey interaction because flowers depend on pollinator visitations for reproduction. Therefore, floral colour might evolve relative to predator colour so as to influence the detectability of resident predators. I have created a three-player game, based on Signal Detection Theory, to model the co-evolution of predator and prey/pollinator behavioural strategies with floral colour. This model makes two general predictions: (1) Constraints on predator distributions favour the evolution of flowers that match the predators’ colour because they prevent predators from overexploiting these flowers; (2) factors that produce less discriminating pollinators also favour the evolution of flowers that match the predators’ colour because these pollinators are willing to land on these flowers even if the safety of the flower is in doubt.     

Concealed by conspicuousness: distractive prey markings and backgrounds

High-contrast markings, called distractive or dazzle markings, have been suggested to draw and hold the attention of a viewer, thus hindering detection or recognition of revealing prey characteristics, such as the body outline. We tested this hypothesis in a predation experiment with blue tits (Cyanistes caeruleus) and artificial prey. We also tested whether this idea can be extrapolated to the background appearance and whether high-contrast markings in the background would improve prey concealment. We compared search times for a high-contrast range prey (HC-P) and a low-contrast range prey (LC-P) in a high-contrast range background (HC-B) and a low-contrast range background (LC-B). The HC-P was more difficult to detect in both backgrounds, although it did not match the LC-B. Also, both prey types were more difficult to find in the HC-B than in the LC-B, in spite of the mismatch of the LC-P. In addition, the HC-P was more difficult to detect, in both backgrounds, when compared with a generalist prey, not mismatching either background. Thus, we conclude that distractive prey pattern markings and selection of microhabitats with distractive features may provide an effective way to improve camouflage. Importantly, high-contrast markings, both as part of the prey coloration and in the background, can indeed increase prey concealment.     

Comparison of measurement accuracy between two wrist goniometer systems during pronation and supination.

Pronation and supination have been shown to affect wrist goniometer measurement accuracy. The purpose of this study was to compare differences in measurement accuracy between a commonly used biaxial, single transducer wrist goniometer (System A) and a biaxial, two-transducer wrist goniometer (System B) over a wide range of pronation and supination (P/S) positions. Eight subjects moved their wrist between -40 and 40 degrees of flexion/extension (F/E) and -10 and 20 degrees of radial/ulnar (R/U) deviation in four different P/S positions: 90 degrees pronation; 45 degrees pronation; 0 degrees neutral and 45 degrees supination. System A was prone to more R/U crosstalk than System B and the amount of crosstalk was dependent on the P/S position. F/E crosstalk was present with both goniometer systems and was also shown to be dependent on P/S. When moving from pronation to supination, both systems experienced a similar extension offset error; however R/U offset errors were roughly equal in magnitude but opposite in direction. The calibration position will affect wrist angle measurements and the magnitude and direction of measurement errors. To minimize offset errors, the goniometer systems should be calibrated in the P/S posture most likely to be encountered during measurement. Differences in goniometer design and application accounted for the performance differences.     

Pitcher plant facilitates prey capture in a sympatric congener

Carnivorous plants avoid below-ground competition for nitrogen by utilizing an alternative nitrogen resource—invertebrate prey, but it remains unclear if sympatric carnivorous plants compete for prey resources. The aim of this study was to investigate if exploitative prey-resource competition occurs between the two sympatric pitcher plant species, Nepenthes rafflesiana and N. gracilis in Singapore. We first investigated if prey-resource partitioning occurs between these two species, and then investigated niche shift in N. gracilis by examining its pitcher contents along an in situ gradient of N. rafflesiana interspecific competition. Our results showed clear evidence of resource partitioning between the two species, but contrary to the expectation of competition, proximity to N. rafflesiana pitchers correlated with higher total prey numbers in N. gracilis pitchers. Our multivariate model of prey assemblages further suggested that N. rafflesiana facilitates N. gracilis prey capture, especially in several ant taxa that are trapped by both species. Concurrently, we found strong evidence for intraspecific competition between N. gracilis pitchers, suggesting that prey resources are exhaustible by pitcher-predation. Our results show that resource partitioning can be associated with facilitative interactions, instead of competition as is usually assumed. Facilitation is more typically expected between phylogenetically distant species, but divergences in resource acquisition strategies can permit facilitation between congeners.     

Fewer S‐alleles are maintained in plant populations with sporophytic as opposed to gametophytic self‐incompatibility

Plants use self‐incompatibility to reject pollen bearing alleles in common at the S‐locus. These systems are classified as gametophytic (GSI) if recognition involves haploid pollen or sporophytic (SSI) if recognition involves diploid paternal genotypes. Dominance in SSI systems reduces the number of S‐alleles, but it has not been clear which system should maintain greater diversity when all else is equal. We simulated finite populations to compare the equilibrium number of S‐alleles in populations with either GSI or a co‐dominant SSI system. When population size was constant, SSI systems maintained more S‐alleles than GSI systems. When populations fluctuated in response to an S‐Allee effect, fewer S‐alleles were observed in SSI systems when S‐allele diversity was low, and SSI populations were vulnerable to extinction over a broader range of parameters. Turnover rates at the S‐locus were also faster in SSI populations experiencing strong S‐Allee effects. Given the variable expectations concerning S‐allele diversity in these systems, we reviewed published estimates of S‐allele diversity. GSI populations have significantly more S‐alleles on average than SSI populations (GSI = 25.70 and SSI = 16.80). Dominance likely contributes to this pattern, although the demographic consequences of the S‐Allee effect may be important in populations with fewer than 10 S‐alleles.     

Camouflage in predators

Camouflage – adaptations that prevent detection and/or recognition – is a key example of evolution by natural selection, making it a primary focus in evolutionary ecology and animal behaviour. Most work has focused on camouflage as an anti‐predator adaptation. However, predators also display specific colours, patterns and behaviours that reduce visual detection or recognition to facilitate predation. To date, very little attention has been given to predatory camouflage strategies. Although many of the same principles of camouflage studied in prey translate to predators, differences between the two groups (in motility, relative size, and control over the time and place of predation attempts) may alter selection pressures for certain visual and behavioural traits. This makes many predatory camouflage techniques unique and rarely documented. Recently, new technologies have emerged that provide a greater opportunity to carry out research on natural predator–prey interactions. Here we review work on the camouflage strategies used by pursuit and ambush predators to evade detection and recognition by prey, as well as looking at how work on prey camouflage can be applied to predators in order to understand how and why specific predatory camouflage strategies may have evolved. We highlight that a shift is needed in camouflage research focus, as this field has comparatively neglected camouflage in predators, and offer suggestions for future work that would help to improve our understanding of camouflage.     

The effects of predator learning, forgetting, and recognition errors on the evolution of warning coloration

This paper demonstrates that the specifics of predator avoidance learning, information loss, and recognition errors may heavily influence the evolution of aposematism. I establish a mathematical model of the change in frequency over time of bright individuals of a distasteful prey species. Warning color spreads through green beard selection as reformulated by Guilford (1990); bright colored forms gain an advantage due to their phenotypic resemblance to other bright forms, which have been sampled by the predator. I use a general classical conditioning model to examine gradual predator learning and forgetting, and then consider the extreme of one-trial learning and no forgetting over time that may occur with very toxic prey. The advantage of conspicuous coloration under these latter conditions depends upon its role in lowering a constant probability of the prey being misidentified and thus mistakenly attacked by a predator, a rarely emphasized factor in the evolution of warning coloration. This constant probability of mistaken attacks can also be interpreted as a constant probability that forgetting has occurred (forgetting does not increase with time) or a periodic decision by the predator to resample avoided prey. I show that when predators learn and forget gradually, as under the general classical conditioning model, it is very difficult for aposematic coloration to become established unless bright individuals cross an often high threshold frequency through chance factors. In contrast, the conditions expected with highly toxic prey promote the evolution of warning coloration more easily, by means from the fixation of very bright mutations to the fixation of successive mutations each of which causes a small increase in a prey's conspicuousness. The results therefore predict that aposematic coloration may have evolved in a different manner in different predator and prey systems. They also suggest that it may be extremely difficult for warning coloration to evolve in more mildly toxic or distasteful prey outside of a mimicry system.     

Evolution of trophic transmission in parasites: why add intermediate hosts?

Although multihost complex life cycles (CLCs) are common in several distantly related groups of parasites, their evolution remains poorly understood. In this article, we argue that under particular circumstances, adding a second host to a single-host life cycle is likely to enhance transmission (i.e., reaching the target host). For instance, in several situations, the propagules of a parasite exploiting a predator species will achieve a higher host-finding success by encysting in a prey of the target predator than by other dispersal modes. In such a case, selection should favor the transition from a single- to a two-host life cycle that includes the prey species as an intermediate host. We use an optimality model to explore this idea, and we discuss it in relation to dispersal strategies known among free-living species, especially animal dispersal. The model found that selection favored a complex life cycle only if intermediate hosts were more abundant than definitive hosts. The selective value of a complex life cycle increased with predation rates by definitive hosts on intermediate hosts. In exploring trade-offs between transmission strategies, we found that more costly trade-offs made it more difficult to evolve a CLC while less costly trade-offs between traits could favor a mixed strategy.     

The evolution of traits affecting resource acquisition and predator vulnerability: character displacement under real and apparent competition

This article investigates some simple models of the evolutionary interaction between two prey species that share a common resource and a common predator. Each prey species is characterized by a trait that determines both the rate of resource capture and vulnerability to a predator. In a simple model of a three-species food chain, such traits usually increase in response to an imposed reduction in resource density. When the per capita growth rates of each of two prey species depend linearly on resource density, such traits will change in opposite directions when the two prey come into sympatry. In addition, the ratio of the effect of the predator on prey fitness to the effect of the resource on prey fitness will diverge from the corresponding ratio in a second prey species when those species coexist in sympatry. These simple predictions need not hold under several alternative assumptions, which may be more common in biological systems. Parallel changes in sympatry may occur if the relationship between resource consumption and prey growth is nonlinear, if the prey species have partial overlap in the set of resources used or in the set of predators that consume them, or if prey experience direct intraspecific competition. The responses to a second prey can also differ significantly from those predicted by the simplest model if separate traits affect vulnerability to predators and resource acquisition rate. It is important to determine whether examples of character displacement previously interpreted as responses to competition for resources might also reflect responses to altered predation risks in sympatry.     

Functional convergence of two lysyl-tRNA synthetases with unrelated topologies

Lysyl-tRNA can be synthesized by both a class I (LysRS-I) and a class II (LysRS-II) lysyl-tRNA synthetase. The crystal structure of LysRS-I from Pyrococcus horikoshii at 2.6 A resolution reveals extensive similarity with glutamyl-tRNA synthetase (GluRS). A comparison of the structures of LysRS-I and LysRS-II in complex with lysine shows that both enzymes use similar strategies for substrate recognition within unrelated active site topologies. A docking model based upon the GluRS-tRNA complex suggests how LysRS-I and LysRS-II can recognize the same molecular determinants in tRNALys, as shown by biochemical results, while approaching the acceptor helix of the tRNA from opposite sides.     

Reliance on prey-derived nitrogen by the carnivorous plant Drosera rotundifolia decreases with increasing nitrogen deposition

? Carnivory in plants is presumed to be an adaptation to a low-nutrient environment. Nitrogen (N) from carnivory is expected to become a less important component of the N budget as root N availability increases. ? Here, we investigated the uptake of N via roots versus prey of the carnivorous plant Drosera rotundifolia growing in ombrotrophic bogs along a latitudinal N deposition gradient through Sweden, using a natural abundance stable isotope mass balance technique. ? Drosera rotundifolia plants receiving the lowest level of N deposition obtained a greater proportion of N from prey (57%) than did plants on bogs with higher N deposition (22% at intermediate and 33% at the highest deposition). When adjusted for differences in plant mass, this pattern was also present when considering total prey N uptake (66, 26 and 26 μg prey N per plant at the low, intermediate and high N deposition sites, respectively). The pattern of mass-adjusted root N uptake was opposite to this (47, 75 and 86 μg N per plant). ? Drosera rotundifolia plants in this study switched from reliance on prey N to reliance on root-derived N as a result of increasing N availability from atmospheric N deposition.     

The optimal sampling strategy for unfamiliar prey

Precisely how predators solve the problem of sampling unfamiliar prey types is central to our understanding of the evolution of a variety of antipredator defenses, ranging from Müllerian mimicry to polymorphism. When predators encounter a novel prey item then they must decide whether to take a risk and attack it, thereby gaining a potential meal and valuable information, or avoid such prey altogether. Moreover, if predators initially attack the unfamiliar prey, then at some point(s) they should decide to cease sampling if evidence mounts that the type is on average unprofitable to attack. Here, I cast this problem as a "two-armed bandit," the standard metaphor for exploration-exploitation trade-offs. I assume that as predators encounter and attack unfamiliar prey they use Bayesian inference to update both their beliefs as to the likelihood that individuals of this type are chemically defended, and the probability of seeing the prey type in the future. I concurrently use dynamic programming to identify the critical informational states at which predator should cease sampling. The model explains why predators sample more unprofitable prey before complete rejection when the prey type is common and explains why predators exhibit neophobia when the unfamiliar prey type is perceived to be rare.     

Interaction of translation initiation factor 3 with the 30S ribosomal subunit.

Hydroxyl radical footprinting and directed probing from Fe(II)-derivatized IF3 have been used to map the interaction of IF3 relative to 16S rRNA and tRNA(Met)(f) in the 30S ribosomal subunit. Our results place the two domains of IF3 on opposite sides of the initiator tRNA, with the C domain at the platform interface and the N domain at the E site. The C domain coincides with the location of helix 69 of 23S rRNA, explaining the ability of IF3 to block subunit association. The N domain neighbors proteins S7 and S11 and may interfere with E site tRNA binding. Our model suggests that IF3 influences initiator tRNA selection indirectly.     

State-dependent risk-taking by predators in systems with defended prey

Even defended prey items may contain nutrients that can sustain predators in times of energetic need. Conversely, a well-fed predator might be expected to avoid attacking prey items that have a chance of being defended, particularly if there is an abundance of familiar palatable prey to support it. To further understand the implications of optimal state-dependent foraging behaviour by predators in systems that contain defended prey, I developed a stochastic dynamic programming model. This state-dependent approach formally accounts for the trade-off between avoiding starvation and minimising harm from attacking defended prey. It predicts that the mean attack probability of predators on defended models and their undefended mimics should decline in a sigmoidal fashion with increasing availability of alternative undefended prey, and that the foraging decisions of predators should in general be relatively insensitive to the probability that a potentially defended prey item is indeed defended. Some implications of these predictions are that conspicuous warning signals are more likely to evolve in systems that contain an abundance of alternative undefended prey, and that imperfect mimicry will provide almost complete protection to the mimic when predators are readily supported by alternative food sources. Somewhat surprisingly, increasing the density of nutritious undefended mimics while keeping the densities of all other prey types constant tended to decrease the attack rates of predators on encounter with mimics and their defended models. This increase in dietary conservatism arose because in these cases there would be more prey available to sustain the predator if it ever found itself critically low in energy.     

Obligate mutualism with a predator: Stability and persistence of three-species models

We present a general model for three interacting populations, where one population, called a mutualist, benefits a predator in its interaction with the prey. Biologically, there are four different ways in which the mutualist could benefit the predator: by enhancing prey growth rate, by enhancing the rate of prey capture, by providing an alternative food supply for the predator, and by enhancing the efficiency of utilization of prey, once they are ingested. We discuss examples of each type of interaction. We restrict our model to those situations in which the predator cannot survive on the prey in the absence of the mutualist. Therefore, if mutualism exists, it is obligate for the predator. Other conditions of the model include the dynamics of the prey and the mutualist alone and together in the absence of the predator. Given additional reasonable restrictions on the model, we determine the conditions for persistence, where persistence is defined as the continued existence of all three populations without any of them going extinct. There are two ways in which survival may arise in these models. Under one set of conditions, which is equivalent to the predator being able to invade a prey-mutualist system when rare, persistence will occur for any set of positive critical population sizes. Alternatively, survival will occur if there is an asymptotically stable interior equilibrium. However, the conditions for this are complex, and survival may occur only for initial populations in a limited region around the equilibrium.     

Predator search pattern and the strength of interference through prey depression

We develop a model of predators foraging within a single patch,on prey that become temporarily immune to predation (depressed)after detecting a predator. Interference through prey depressionoccurs because the proportion of vulnerable prey (and henceintake rate) decreases as predator density increases. Predatorsin our model are not forced to move randomly within the patch,as is the case in other similar models, but can avoid areasof depressed prey and so preferentially forage over vulnerableprey. We compare the extent to which different avoidance rules(e.g., move more quickly over depressed prey or turn if approachingdepressed prey) influence the amount of time spent foragingover depressed and vulnerable prey, and how this influencesthe strength of interference. Although based on a different mechanism, our model produces two similar general predictionsto interference models based on direct interactions betweenpredators: the strength of interference increases with (1)increased competitor density and (2) decreased prey encounterrate. This suggests that there are underlying similarities in the nature of interference even when it arises through differentprocesses. Not surprisingly, avoidance of depressed prey cansubstantially reduce the strength of interference comparedwith random foraging. However, we identify the region of themodel's parameter space in which this reduction is particularlylarge and show that the only system for which suitable dataare available, redshank Tringa totanus feeding on Corophium volutator, falls within this region. The model shows that, byadjusting its search path to avoid areas of depressed prey,a predator can substantially reduce the amount of the interferenceit experiences and that this applies over a wide range of parameterspace, including the region occupied by a real system. Thissuggests that behavior-based interference models should consider predator search pattern if they are to accurately predict thestrength of the interference.