Effects of an infectious fungus, Batrachochytrium dendrobatidis, on amphibian predator-prey interactions

The effects of parasites and pathogens on host behaviors may be particularly important in predator-prey contexts, since few animal behaviors are more crucial for ensuring immediate survival than the avoidance of lethal predators in nature. We examined the effects of an emerging fungal pathogen of amphibians, Batrachochytrium dendrobatidis, on anti-predator behaviors of tadpoles of four frog species. We also investigated whether amphibian predators consumed infected prey, and whether B. dendrobatidis caused differences in predation rates among prey in laboratory feeding trials. We found differences in anti-predator behaviors among larvae of four amphibian species, and show that infected tadpoles of one species (Anaxyrus boreas) were more active and sought refuge more frequently when exposed to predator chemical cues. Salamander predators consumed infected and uninfected tadpoles of three other prey species at similar rates in feeding trials, and predation risk among prey was unaffected by B. dendrobatidis. Collectively, our results show that even sub-lethal exposure to B. dendrobatidis can alter fundamental anti-predator behaviors in some amphibian prey species, and suggest the unexplored possibility that indiscriminate predation between infected and uninfected prey (i.e., non-selective predation) could increase the prevalence of this widely distributed pathogen in amphibian populations. Because one of the most prominent types of predators in many amphibian systems is salamanders, and because salamanders are susceptible to B. dendrobatidis, our work suggests the importance of considering host susceptibility and behavioral changes that could arise from infection in both predators and prey.     

Native predators living in invaded areas: responses of terrestrial amphibian species to an Argentine ant invasion

Predator–prey interactions play a key role in the success and impacts of invasive species. However, the effects of invasive preys on native predators have been poorly studied. Here, we first reviewed hypotheses describing potential relationships between native predators and invasive preys. Second, we examined how an invasive prey, the Argentine ant (Linepithema humile), affected a native terrestrial amphibian community. In the field, we looked at the structure of the amphibian community in invaded versus uninvaded areas and characterized amphibian trophic ecology. The amphibian community sampled seemed to show a species-dependent response in abundance to invasion: adults of the natterjack toad (Bufo calamita), the species demonstrating the highest degree of ant specialization, were less abundant in invaded areas. Although available ant biomass was significantly greater in invaded than in uninvaded areas (only Argentine ants occurred in the former), amphibians consumed relatively fewer ants in invaded areas. In the lab, we quantified amphibian consumption of Argentine ants versus native ants and assessed whether consumption patterns could have been influenced by prior exposure to the invader. The lab experiments corroborated the field results: amphibians preferred native ants over Argentine ants, and prior exposure did not influence consumption. Differences in preference explained why amphibians consumed fewer Argentine ants in spite of their greater relative availability; they might also explain why the most ant-specialized amphibians seemed to avoid invaded areas. Our results suggest the importance to account for predator feeding capacities and dietary ranges to understand the effects of invasive species at higher trophic levels.     

Defensive larval secretions of leaf beetles attract a specialist predator Parasyrphus nigritarsis

1. Noxious larval secretions of leaf beetles, which repel generalist predators, do not deter specialist syrphid fly predators (genus Parasyrphus ). These flies cause considerable mortality to the beetles, but little is known about their foraging behaviour.
2. Larvae of Parasyrphus nigritarsis were attracted to the volatile larval secretions produced by two prey species Phratora vitellinae and Linaeidea aenea. Parasyrphus nigritarsis feeds on both beetles in nature. Phratora vitellinae feeds on willows and utilizes host plant compounds for secretion production, while the alder-feeding L. aenea produces an autogenous secretion.
3. Fly larvae were strongly attracted to pieces of filter paper treated with larval secretion of the beetles. They attempted to feed on them for up to 7 min, and were equally attracted to the secretions of Ph. vitellinae and L. aenea . Fly larvae were also attracted to pure salicyl aldehyde, the main component of the secretion of Ph. vitellinae .
4. Fly larvae searched extensively for prey on leaves that had been damaged by beetle larvae. They also followed trails made with solutions containing faecal matter of prey larvae. They showed no differential preference for Ph. vitellinae or L. aenea , but always rejected larvae of the non-prey leaf beetle Agelastica alni .
5. Beetle secretions thus play an important, but unexpected, role in the feeding behaviour of P. nigritarsis . This predator uses the beetle secretion to locate its prey. The implications of these results for three trophic level interactions are discussed.     

Predaceous diving beetle, Dytiscus sharpi sharpi (Coleoptera: Dytiscidae) larvae avoid cannibalism by recognizing prey

Larvae of diving beetles such as the various Dytiscus species (Coleoptera: Dytiscidae) are carnivorous and usually prey on other aquatic animals. Cannibalism among larvae of Dytiscus sharpi sharpi (Wehncke) was observed to begin when they were starved for more than two days under artificial breeding conditions. However, the 2-day starved larvae did not show cannibalism in the presence of intact, motionless, frozen tadpoles, or frozen shrimps. The beetle larvae attacked and captured intact tadpoles faster (15 sec) than other motionless and frozen tadpoles (120 sec), indicating that prey movement was an important factor in stimulating feeding behavior in larvae. Prey density does not have an effect on larval cannibalism. In cases in which preys are present at lower densities than that of larvae, a group of beetle larvae frequently fed on single prey. This feeding behavior, therefore, provides direct evidence of self-other recognition at the species level. Using two traps in one aquarium that allows the larvae to detect only prey smell, one containing tadpoles and another empty, the beetle larvae were attracted to the trap with tadpoles at high frequency, but not to the empty trap. In another experiment, the beetle larvae were not attracted to the trap containing a beetle larva. These results suggest that the larvae of D. sharpi sharpi are capable of recognizing prey scent, which enables the promotion of foraging behavior and the prevention of cannibalism.     

Prey perception of predation risk: volatile chemical cues mediate non-consumptive effects of a predator on a herbivorous insect

Predators can affect prey in two ways—by reducing their density (consumptive effects) or by changing their behavior, physiology or other phenotypic traits (non-consumptive effects). Understanding the cues and sensory modalities prey use to detect predators is critical for predicting the strength of non-consumptive effects and the outcome of predator–prey encounters. While predator-associated cues have been well studied in aquatic systems, less is known about how terrestrial prey, particularly insect larvae, detect their predators. We evaluated how Colorado potato beetle, Leptinotarsa decemlineata, larvae perceive predation risk by isolating cues from its stink bug predator, the spined soldier bug, Podisus maculiventris. When exposed to male “risk” predators that were surgically manipulated so they could hunt but not kill, beetles reduced feeding 29 % compared to controls. Exposure to risk females caused an intermediate response. Beetles ate 24 % less on leaves pre-exposed to predators compared to leaves never exposed to predators, indicating that tactile and visual cues are not required for the prey’s response. Volatile odor cues from predators reduced beetle feeding by 10 % overall, although male predators caused a stronger reduction than females. Finally, visual cues from the predator had a weak effect on beetle feeding. Because multiple cues appear to be involved in prey perception of risk, and because male and female predators have differential effects, beetle larvae likely experience tremendous variation in the information about risk from their local environment.     

A mechanistic model for interference and Allee effect in the predator population

We present the results of simulations in an individual-based model describing spatial movement and predator-prey interaction within a closed rectangular habitat. Movement of each individual animal is determined by local conditions only, so any collective behavior emerges owing to self-organization. It is shown that the pursuit of prey by predators entails predator interference, manifesting itself at the population level as the dependency of the trophic function (individual ration) on predator abundance. The stabilizing effect of predator interference on the dynamics of a predator-prey system is discussed. Inclusion of prey evasion induces apparent cooperation of predators and further alters the functional response, giving rise to a strong Allee effect, with extinction of the predator population upon dropping below critical numbers. Thus, we propose a simple mechanistic interpretation of important but still poorly understood behavioral phenomena that underlie the functioning of natural trophic systems.     

Using functional response modeling to investigate the effect of temperature on predator feeding rate and energetic efficiency

Temperature is one of the most important environmental parameters influencing all the biological processes and functions of poikilothermic organisms. Although extensive research has been carried out to evaluate the effects of temperature on animal life histories and to determine the upper and lower temperature thresholds as well as the optimal temperatures for survival, development, and reproduction, few studies have investigated links between thermal window, metabolism, and trophic interactions such as predation. We developed models and conducted laboratory experiments to investigate how temperature influences predator-prey interaction strengths (i.e., functional response) using a ladybeetle larva feeding on aphid prey. As predicted by the metabolic theory of ecology, we found that handling time exponentially decreases with warming, but--in contrast with this theory--search rate follows a hump-shaped relationship with temperature. An examination of the model reveals that temperature thresholds for predation depend mainly on search rate, suggesting that predation rate is primarily determined by searching activities and secondly by prey handling. In contrast with prior studies, our model shows that per capita short-term predator-prey interaction strengths and predator energetic efficiency (per capita feeding rate relative to metabolism) generally increase with temperature, reach an optimum, and then decrease at higher temperatures. We conclude that integrating the concept of thermal windows in short- and long-term ecological studies would lead to a better understanding of predator-prey population dynamics at thermal limits and allow better predictions of global warming effects on natural ecosystems.     

Evaluating a predator–prey interaction in the field: the interaction between beetle larvae (predator) and tadpoles (prey)

The larval amphibian community of temporary pond ecosystems has served as a model for studies in community ecology, with a majority of this work being conducted in mesocosms. Recent research has suggested that mesocosms may overestimate ecological effects; therefore, experimental studies conducted under field conditions are required to gauge the results of mesocosm studies. To assess a species interaction under more natural conditions, we conducted a series of field experiments examining the predator–prey interaction between beetle larvae ( Dytiscus sp.; predator) and larval wood frogs Rana sylvatica (prey) in central Pennsylvania, USA. Quantitative sampling of woodland ponds indicated that beetle larvae of the genus Dytiscus were the most common predator of tadpoles. In a field enclosure experiment, dytiscids were effective predators of tadpoles in the pond environment. Moreover, tadpoles avoided areas in a pond containing caged dytiscids, demonstrating that tadpoles recognize the chemical stimuli of predators in complex environments. The results of this study are consistent with data from prior laboratory and mesocosm studies and suggest that these venues can produce reliable interpretations of predator–prey dynamics in this community.     

The interaction between spatial heterogeneity and genetic feedback in laboratory predator-prey systems

Summary A hybrid experimental design combining laboratory populations and computer simulation was used to study the relative influence of spatial heterogeneity, genetic feedback and predator foraging behavior on the stability of predator-prey systems. Houseflies, Musca domestica, maintained in multicellular or single-cell population cages were used as predator feeding on chemical solutions contained in small glass vials. Feeding, mortality and dispersal of the predators occurred within the cages, but reproduction of the predators and prey as well as dispersal of the prey was controlled by a computer program. Genetic change in the prey was determined partially by the computer model which associated chemical solutions with particular genotypes, and partially by the predators, whose foraging behavior influenced the fitness of each genotype. Three treatments were compared: a genetically polymorphic prey population in a spatially homogeneous environment, a monomorphic prey population in a heterogeneous environment, and a polymorphic prey population in a heterogeneous environment. With the parameters used, the latter treatment, involving an interaction between spatial heterogeneity and genetic feedback, was the most stable. Without genetic feedback in the prey, spatial heterogeneity was insufficient to overcome the destabilizing influence of the predator's foraging behavior. Without spatial heterogeneity, genetic feedback was insufficient to overcome the destabilizing effect of preferential feeding by the predators on palatable prey. The prey population evolved sufficient resistance to cause extinction of the predator population. The results support the hypothesis that population regulation by genetic feedback in predator-prey systems is less likely when predators feed preferentially on susceptible prey and that spatial heterogeneity, by decreasing the relative accessibility of susceptible prey and hence altering the predator's foraging strategy, may increase the likelihood of regulation through genetic feedback.     

Explicit model for searching behavior of predator

The authors present an approach for explicit modeling of spatio-temporal dynamics of predator-prey community. This approach is based on a reaction-diffusion-adjection PD (prey dependent) system. Local kinetics of population is determined by logistic reproduction function of prey, constant natural mortality of predator and Holling type 2 trophic function. Searching behavior of predator is described by the advective term in predator balance equation assuming the predator acceleration to be proportional to the prey density gradient. The model was studied with zero-flux boundary conditions. The influence of predator searching activity on the community dynamics, in particular, on the emergence of spatial heterogeneity, has been investigated by linear analysis and numerical simulations. It has been shown how searching activity may effect the persistence of species, stabilizing predator-prey interactions at very low level of pest density. It has been demonstrated that obtaining of such dynamic regimes does not require the use of complex trophic functions.     

Stepping in Elton's footprints: a general scaling model for body masses and trophic levels across ecosystems

Despite growing awareness of the significance of body-size and predator-prey body-mass ratios for the stability of ecological networks, our understanding of their distribution within ecosystems is incomplete. Here, we study the relationships between predator and prey size, body-mass ratios and predator trophic levels using body-mass estimates of 1313 predators (invertebrates, ectotherm and endotherm vertebrates) from 35 food-webs (marine, stream, lake and terrestrial). Across all ecosystem and predator types, except for streams (which appear to have a different size structure in their predator-prey interactions), we find that (1) geometric mean prey mass increases with predator mass with a power-law exponent greater than unity and (2) predator size increases with trophic level. Consistent with our theoretical derivations, we show that the quantitative nature of these relationships implies systematic decreases in predator-prey body-mass ratios with the trophic level of the predator. Thus, predators are, on an average, more similar in size to their prey at the top of food-webs than that closer to the base. These findings contradict the traditional Eltonian paradigm and have implications for our understanding of body-mass constraints on food-web topology, community dynamics and stability.     

食饵庇护所对斑块环境下Leslie-Gower捕食系统的影响

建立了一个显式含有空间庇护所的两斑块Leslie-Gower捕食者-食饵系统。假设只有食饵种群在斑块间以常数迁移率迁移,且在每个斑块上食饵间的迁移比局部捕食者-食饵相互作用发生的时间尺度要快。利用两个时间尺度,可以构建用来描述所有斑块总的食饵和捕食者密度的综合系统。数学分析表明,在一定条件下,存在唯一的正平衡点,并且此平衡点全局稳定。进一步,捕食者的数量随着食饵庇护所数量增加而降低;在一定条件下,食饵的数量随着食饵庇护所数量增加先增加后降低,在足够强的庇护所强度下,两物种出现灭绝。对比以往研究,利用显式含有和隐含空间庇护所的数学模型所得结论不一致,这意味着在研究庇护所对捕食系统种群动态影响时,空间结构可能起着重要作用。     

The effect of spatial heterogeneity on the persistence of predator-prey interactions

The effect of spatially discontinuous environments on predator-prey systems is examined by using a computer simulation model. It is shown that increasing prey dispersal and decreasing predator dispersal do not necessarily have a stabilizing influence on the interaction, as had been concluded by previous workers. The stability of predator-prey interaction depends on the interaction of the dispersal process with normal reproduction and feeding of the predator and prey species.     

Effect of predator density dependent dispersal of prey on stability of a predator-prey system

This work presents a predator-prey Lotka-Volterra model in a two patch environment. The model is a set of four ordinary differential equations that govern the prey and predator population densities on each patch. Predators disperse with constant migration rates, while prey dispersal is predator density-dependent. When the predator density is large, the dispersal of prey is more likely to occur. We assume that prey and predator dispersal is faster than the local predator-prey interaction on each patch. Thus, we take advantage of two time scales in order to reduce the complete model to a system of two equations governing the total prey and predator densities. The stability analysis of the aggregated model shows that a unique strictly positive equilibrium exists. This equilibrium may be stable or unstable. A Hopf bifurcation may occur, leading the equilibrium to be a centre. If the two patches are similar, the predator density dependent dispersal of prey has a stabilizing effect on the predator-prey system.     

The hyal and ventral branchial muscles in caecilian and salamander larvae: Homologies and evolution

Amphibians (Lissamphibia) are characterized by a bi‐phasic life‐cycle that comprises an aquatic larval stage and metamorphosis to the adult. The ancestral aquatic feeding behavior of amphibian larvae is suction feeding. The negative pressure that is needed for ingestion of prey is created by depression of the hyobranchial apparatus as a result of hyobranchial muscle action. Understanding the homologies of hyobranchial muscles in amphibian larvae is a crucial step in understanding the evolution of this important character complex. However, the literature mostly focuses on the adult musculature and terms used for hyal and ventral branchial muscles in different amphibians often do not reflect homologies across lissamphibian orders. Here we describe the hyal and ventral branchial musculature in larvae of caecilians (Gymnophiona) and salamanders (Caudata), including juveniles of two permanently aquatic salamander species. Based on previous alternative terminology schemes, we propose a terminology for the hyal and ventral branchial muscles that reflects the homologies of muscles and that is suited for studies on hyobranchial muscle evolution in amphibians. We present a discussion of the hyal and ventral branchial muscles in larvae of the most recent common ancestor of amphibians (i.e. the ground plan of Lissamphibia). Based on our terminology, the hyal and ventral branchial musculature of caecilians and salamanders comprises the following muscles: m. depressor mandibulae, m. depressor mandibulae posterior, m. hyomandibularis, m. branchiohyoideus externus, m. interhyoideus, m. interhyoideus posterior, m. subarcualis rectus I, m. subarcualis obliquus II, m. subarcualis obliquus III, m. subarcualis rectus II‐IV, and m. transversus ventralis IV. Except for the m. branchiohyoideus externus, all muscles considered herein can be assigned to the ground plan of the Lissamphibia with certainty. The m. branchiohyoideus externus is either apomorphic for the Batrachia (frogs + salamanders) or salamander larvae depending on whether or not a homologous muscle is present in frog tadpoles. J. Morphol., 2011. © 2011 Wiley‐Liss, Inc.     

Prey patchiness, predator survival and fish recruitment

A simple mathematical model is presented for the population dynamics of fish larvae when the main food supply, in this case copepods, is spatially patchy in its distribution. Encounters by an individual predator (larva) with prey patches, and with individual prey within patches, are represented by Poisson processes. It is demonstrated analytically, and confirmed by numerical experiments, that prey patchiness fails to alter mean predator-prey encounter rates from their values for homogeneous prey distributions. Individual variance in encounter rate is, however, much affected. This has significant consequences for the (small) numbers of larvae surviving to metamorphosis and recruitment to the adult fish population.     

带有年龄结构的捕食者-食饵模型研究

研究带有年龄结构的捕食者-食饵模型的渐近行为.本文所研究的模型假定捕食者从幼年阶段到成年阶段的转变率依赖于幼年种群的密度,还假定幼年捕食者捕食食饵.本文最终给出了有年龄结构的捕食者-食饵模型的捕食者持久和灭绝的若干条件.     

Predator–prey interactions: why do larger albatrosses eat bigger squid?

The relationship between predator sizes and prey sizes is well documented for terrestrial but rarely for marine ecosystems. We show that wandering albatrosses, the biggest albatross species, feed on larger cephalopod prey than those consumed by smaller albatrosses (grey-headed and black-browed albatrosses). This reflects differences in timing of breeding, foraging ecology and their feeding methods. Wandering albatrosses breed later in the year, during the austral winter, than smaller albatrosses (therefore catching older squid) and forage most of the year in Antarctic open waters, sub-Antarctic, subtropical and tropical waters, overlapping minimally with the smaller albatrosses' foraging range while breeding. Also, wandering albatrosses mostly scavenge whereas smaller albatrosses feed more on live prey. Prey ecology may also play a key role because many squid species might experience post-spawning mortality during the austral winter, becoming easily available to wandering albatrosses. Spawning in winter can be linked to predator avoidance (i.e. reduction in mortality in winter by avoiding pelagic predators) and would allow squid larvae to develop and take advantage of the high productivity (i.e. Antarctic phytoplankton bloom) in spring and at the beginning of summer. Thus, aspects of prey and predator ecology may combine to generate observed differences in prey size.     

水生生态环境中捕食信息素的生态学效应

捕食信息素是捕食者释放的,能够引发猎物反捕食反应的化学信号。在水生生态系统中,捕食信息素在捕食者和猎物之间信息传递及协同进化过程中发挥着重要的作用,其生态学效应在国际上受到广泛关注。捕食信息素的来源有多种形式,研究中常使用养殖过捕食者的水溶液作为捕食信息素的来源。捕食信息素的作用效果受到捕食者和猎物的种类、信息素的浓度、观察的指标等多方面因素的影响。捕食信息素可以对水生生物的行为、形态和生活史特征等方面造成影响。水生生物通过感知捕食信息素来提前预知潜在的被捕食风险,并作出适应性调整,以降低被捕食的风险。在某些情况下,捕食信息素可以与污染物产生交互作用,从而干扰污染物对水生生物的毒性。对水生环境中捕食信息素的研究现状做了综述,介绍了当前对捕食信息素来源和理化性质等本质问题的认识,总结捕食信息素对水生生物行为、形态和生活史特征的影响,以及捕食信息素对污染物毒性的干扰,并分析了这一研究领域尚存在的困难和今后的研究方向。加强对捕食信息素的研究,将为解析水生环境中捕食者和猎物的生态关系提供新依据。