Wolf spider predator avoidance tactics and survival in the presence of diet-associated predator cues (Araneae: Lycosidae)

Some prey can distinguish between chemical cues from predators fed different diets. Here we document the first evidence of diet-based chemical discrimination of predators in a terrestrial arthropod and measure the survival value of behavioural responses to predator chemical cues. We tested activity level and avoidance behaviour of the wolf spider, Pardosa milvina, to faeces and silk associated with the predatory wolf spider, Hogna helluo, fed either P. milvina or crickets (Acheta domesticus). We then measured survival of Pardosa in the presence of Hogna when placed on blank paper or paper previously occupied by Hogna fed either crickets or Pardosa. Filter paper previously occupied by Hogna from each diet treatment or a blank control were simultaneously presented to adult female Pardosa among four treatment pairs (N=15/treatment): (1) blank paper/blank paper, (2) Hogna fed crickets/blank, (3) Hogna fed Pardosa /blank and (4) Hogna fed Pardosa / Hogna fed crickets. Cues from Hogna fed either crickets or Pardosa elicited significantly less activity relative to blank controls. Cues from Hogna fed Pardosa elicited a significantly greater reduction in activity than Hogna fed crickets. When given a choice, Pardosa initially chose the blank substrate significantly more often than either substrate with Hogna cues. Spiders survived longer in the presence of cues from either Hogna diet treatment relative to blank paper, but there was no significant effect of predator diet on survival. Results suggest diet-based predator cues elicit different levels of activity in Pardosa that reduce predation in the presence of Hogna. Copyright 2001 The Association for the Study of Animal Behaviour.     

Predicting ecological consequences of marine top predator declines

Recent studies document unprecedented declines in marine top predators that can initiate trophic cascades. Predicting the wider ecological consequences of these declines requires understanding how predators influence communities by inflicting mortality on prey and inducing behavioral modifications (risk effects). Both mechanisms are important in marine communities, and a sole focus on the effects of predator-inflicted mortality might severely underestimate the importance of predators. We outline direct and indirect consequences of marine predator declines and propose an integrated predictive framework that includes risk effects, which appear to be strongest for long-lived prey species and when resources are abundant. We conclude that marine predators should be managed for the maintenance of both density- and risk-driven ecological processes, and not demographic persistence alone.     

Oviposition avoidance of parasitized aphid colonies by the syrphid predator Episyrphus balteatus mediated by different cues

Oviposition decisions made by members of a guild of natural enemies can have evolved to avoid intraguild predation, potentially avoiding the disruption of the extraguild prey control. We have studied the oviposition preference of the aphidophagous predator Episyrphus balteatus De Geer (Diptera: Syrphidae) within colonies of Myzus persicae Sulzer (Hemiptera: Aphididae) in the presence of two developmental stages of the aphid parasitoid Aphidius colemani Viereck (Hymenoptera: Aphidiidae). Results from a greenhouse choice experiment showed that E. balteatus females lay significantly fewer eggs in colonies with mummified aphids than in unparasitized colonies. Colonies of parasitized, but not yet mummified did not contain significantly fewer eggs than colonies with unparasitized aphids. In three no-choice experiments, we assessed stimuli coming from aphid honeydew, from the aphids themselves and also from extracts of the aphid bodies, and all of these stimuli mediate the discrimination of mummified aphids from healthy aphids. To a lesser extent these stimuli also contribute to the discrimination against aphids that are parasitized but not yet mummified. These results suggest that the effects of these two species could be complementary for the control of M. persicae, since the species that acts as an intraguild predator, E. balteatus, avoids ovipositing on aphid colonies parasitized by the intraguild prey, A. colemani.     

Spatial interactions between sympatric carnivores: asymmetric avoidance of an intraguild predator

Interactions between intraguild species that act as both competitors and predator–prey can be especially complex. We studied patterns of space use by the black-footed ferret (Mustela nigripes), a prairie dog (Cynomys spp.) specialist, and the American badger (Taxidea taxus), a larger generalist carnivore that competes for prairie dogs and is known to kill ferrets. We expected that ferrets would spatially avoid badgers because of the risk of predation, that these patterns of avoidance might differ between sexes and age classes, and that the availability of food and space might influence these relationships. We used location data from 60 ferrets and 15 badgers to model the influence of extrinsic factors (prairie dog density and colony size) and intrinsic factors (sex, age) on patterns of space use by ferrets in relation to space use by different sex and age categories of badgers. We documented asymmetric patterns of avoidance of badgers by ferrets based on the sex of both species. Female ferrets avoided adult female badgers, but not male badgers, and male ferrets exhibited less avoidance than female ferrets. Additionally, avoidance decreased with increasing densities of prairie dogs. We suggest that intersexual differences in space use by badgers create varying distributions of predation risk that are perceived by the smaller carnivore (ferrets) and that females respond more sensitively than males to that risk. This work advances understanding about how competing species coexist and suggests that including information on both intrinsic and extrinsic factors might improve our understanding of behavioral interactions between sympatric species.     

Additive effects of predator diversity on pest control caused by few interactions among predator species

1. Studies of the impact of predator diversity on biological pest control have shown idiosyncratic results. This is often assumed to be as a result of differences among systems in the importance of predator–predator interactions such as facilitation and intraguild predation. The frequency of such interactions may be altered by prey availability and structural complexity. A direct assessment of interactions among predators is needed for a better understanding of the mechanisms affecting prey abundance by complex predator communities. 2. In a field cage experiment, the effect of increased predator diversity (single species vs. three‐species assemblage) and the presence of weeds (providing structural complexity) on the biological control of cereal aphids were tested and the mechanisms involved were investigated using molecular gut content analysis. 3. The impact of the three‐predator species assemblages of aphid populations was found to be similar to those of the single‐predator species treatments, and the presence or absence of weeds did not alter the patterns observed. This suggests that both predator facilitation and intraguild predation were absent or weak in this system, or that these interactions had counteracting effects on prey suppression. Molecular gut content analysis of predators provided little evidence for the latter hypothesis: predator facilitation was not detected and intraguild predation occurred at a low frequency. 4. The present study suggests additive effects of predators and, therefore, that predator diversity per se neither strengthens nor weakens the biological control of aphids in this system.     

Competition and intraguild egg predation among freshwater snails: re-examining the mechanism of interspecific interactions

Experimental and field studies suggest that freshwater snail species have negative effects on each other's population growth rates. Because snails share similar diets, these interactions have been interpreted as the result of exploitative competition, but they could also result from intraguild predation. Here we present three experiments aimed at testing the hypothesis that interspecific interactions among three species of freshwater gastropod (Helisoma trivolvis, Physa acuta and Stagnicola elodes) are mediated by intraguild egg predation. Foraging trials, conducted in a laboratory, showed that some snails readily prey on eggs, but the extent of egg predation depended on both the identity of the snail predator and the identity of the egg mass. Of the three species considered, Stagnicola had the largest effect on egg mortality and Physa had no effect on egg mortality. Foraging trials also showed that the eggs of Physa were the most vulnerable to predators and that the eggs of Stagnicola were largely invulnerable. A study conducted in large outdoor mesocosms assessed the occurrence of egg mortality in an environment of more extensive spatial scale and complexity. The results largely mirrored those of the laboratory study, with Stagnicola being the most voracious predator and the eggs of Physa being most vulnerable to predation. The reproductive success of Physa and Stagnicola raised in sympatry and allopatry was assessed in a mesocosm study conducted over three months. Recruitment of both species was depressed in sympatry, but patterns of growth in the survivors suggest contrasting mechanisms of suppression: Physa suppressed Stagnicola via exploitative competition, but Stagnicola suppressed Physa via egg predation. These experiments support the hypothesis that freshwater snail assemblages are structured by strong interspecific interactions and that a rich interplay of egg predation and interspecific competition underlie interactions among the members of this guild.     

Nonantagonistic interactions between the sexes revealed by the ecological consequences of reproductive traits

In addition to the obvious role reproductive traits play in mating-system evolution, reproductive characters can also have critical ecological or life history consequences. In this study we examine the ecological consequences of mating for female cactophilic Drosophila to test different hypotheses about the processes driving divergence in reproductive characters. Comparisons between intra- and interpopulation matings suggest that population differences in mating benefits, namely increased desiccation resistance in mated females, is not solely attributable to either a male or female-specific reproductive trait. Instead, the results indicate that increased desiccation resistance is a product of a male-female postmating-prezygotic interactions. The results underscore that postmating-prezygotic interactions can serve as an arena for the evolution of male characters that confer substantial benefits to females, not just costs arising from sexual conflict. Variation in the relative benefits conferred by mating between intra- and interpopulation matings also suggests that the relationship between speciation and divergence in reproductive characters via male-female interaction will be difficult to predict.     

Chemical defense of toad tadpoles under risk by four predator species

Many organisms use inducible defenses as protection against predators. In animals, inducible defenses may manifest as changes in behavior, morphology, physiology, or life history, and prey species can adjust their defensive responses based on the dangerousness of predators. Analogously, prey may also change the composition and quantity of defensive chemicals when they coexist with different predators, but such predator‐induced plasticity in chemical defenses remains elusive in vertebrates. In this study, we investigated whether tadpoles of the common toad (Bufo bufo) adjust their chemical defenses to predation risk in general and specifically to the presence of different predator species; furthermore, we assessed the adaptive value of the induced defense. We reared tadpoles in the presence or absence of one of four caged predator species in a mesocosm experiment, analyzed the composition and quantity of their bufadienolide toxins, and exposed them to free‐ranging predators. We found that toad tadpoles did not respond to predation risk by upregulating their bufadienolide synthesis. Fishes and newts consumed only a small percentage of toad tadpoles, suggesting that bufadienolides provided protection against vertebrate predators, irrespective of the rearing environment. Backswimmers consumed toad tadpoles regardless of treatment. Dragonfly larvae were the most voracious predators and consumed more predator‐naïve toad tadpoles than tadpoles raised in the presence of dragonfly cues. These results suggest that tadpoles in our experiment had high enough toxin levels for an effective defense against vertebrate predators even in the absence of predator cues. The lack of predator‐induced phenotypic plasticity in bufadienolide synthesis may be due to local adaptation for constantly high chemical defense against fishes in the study population and/or due to the high density of conspecifics.     

The ecological consequences of unpalatable prey: phytoplankton response to nutrient and predator additions

Thermoregulation is thought to be the most important factor influencing habitat selection by terrestrial ectotherms, at least in temperate climates. The cost-benefit model of thermoregulation predicts that ectotherms should invest more in thermoregulation when the costs of doing so are low (when the thermal quality of the habitat is high). However, the extent to which ectotherms vary their thermoregulatory behaviour according to the thermal quality of habitats is currently unknown. We studied the relationship between habitat use and thermoregulation in 53 black rat snakes using temperature-sensitive radio-transmitters. Among the habitats available to black rat snakes, edges had the highest thermal quality, retreat sites and forest were intermediate, and open habitats had the lowest thermal quality. Black rat snakes experienced more favourable body temperatures while in barns (retreat sites) than in edges, and in edges than in forest. During the day, the effectiveness and the extent of thermoregulation by the snakes were equal in barns and forest, but much lower in edges. In fact, black rat snakes selected thermally favourable microhabitats less than their availability while in edges. Therefore, more favourable body temperatures were not necessarily achieved in thermally superior habitats by increased thermoregulation, but simply because favourable temperatures were encountered more often in those habitats. This result is contrary to the central prediction of the cost-benefit model of thermoregulation and we suggest that this model should be modified to put more emphasis on other costs of thermoregulation, such as increased predation risk or lost foraging opportunities.     

Leech predation on juvenile freshwater snails: effects of size,species and substrate

Summary The leechGlossiphonia complanata does not appear to have substantial impact on snail populations, but this may be due to most studies focusing on adult snails rather than juvenile snails. In this study I investigated how predation rates ofG. complanata feeding on newly-hatched and juvenile snails was affected by snail species, snail size, snail density and substrate, in a laboratory experiment. Number of snails eaten increased with increasing density resulting in a type II functional response curve. Predation rates were higher when leeches were feeding onLymnaea emarginata than onPhysa gyrina, whereas there was no significant difference in predation rates when they were feeding onL. emarginata andHelisoma anceps. Sandy substrates and greater snail size resulted in decreased predation rates. Sand reduced movement speed ofG. complanata, which probably reduced encounter rates. Thus, there was a comparatively large effect of leech predation on newly-hatched snails, due to a high probability of encounter and high predation rates, but spatial and temporal refuges probably reduce the importance of leech predation as a structuring force in freshwater snail assemblages.     

Analysing ecological networks of species interactions

Network approaches to ecological questions have been increasingly used, particularly in recent decades. The abstraction of ecological systems – such as communities – through networks of interactions between their components indeed provides a way to summarize this information with single objects. The methodological framework derived from graph theory also provides numerous approaches and measures to analyze these objects and can offer new perspectives on established ecological theories as well as tools to address new challenges. However, prior to using these methods to test ecological hypotheses, it is necessary that we understand, adapt, and use them in ways that both allow us to deliver their full potential and account for their limitations. Here, we attempt to increase the accessibility of network approaches by providing a review of the tools that have been developed so far, with – what we believe to be – their appropriate uses and potential limitations. This is not an exhaustive review of all methods and metrics, but rather, an overview of tools that are robust, informative, and ecologically sound. After providing a brief presentation of species interaction networks and how to build them in order to summarize ecological information of different types, we then classify methods and metrics by the types of ecological questions that they can be used to answer from global to local scales, including methods for hypothesis testing and future perspectives. Specifically, we show how the organization of species interactions in a community yields different network structures (e.g., more or less dense, modular or nested), how different measures can be used to describe and quantify these emerging structures, and how to compare communities based on these differences in structures. Within networks, we illustrate metrics that can be used to describe and compare the functional and dynamic roles of species based on their position in the network and the organization of their interactions as well as associated new methods to test the significance of these results. Lastly, we describe potential fruitful avenues for new methodological developments to address novel ecological questions.     

On the implications of predator avoidance

The question to what extent predators regulate the populations of their food species has a long history of debate, and today top-down control of plankton dynamics still is a major issue in limnology. Over the last decade a fascinating extra dimension of this topic has been revealed. Fish, zooplankton and algae can sense their potential predators through chemical cues and adjust their life style in a flexible way to minimize the risk of being eaten. Although much progress has been made in elucidating the mechanisms involved, the implications of such predation avoidance for the potential of predators to reduce the abundance of their food populations are still poorly understood. Model analyses suggest that predation avoidance leads to more stable food webs in which the effects of nutrient enrichment are more evenly distributed over the trophic levels. In this article it is argued that the cost which predation avoidance usually has in terms of food conditions implies a tricky caveat in interpreting observations on predation rates and nutritional status in natural populations. Prey that sense the presence of predators and aggregates at safe sites where food conditions are poor, may appear starved and actual predation losses may be low. Such observations suggest that food limitation is the dominant force limiting their population development, but although starvation may indeed be the proximate cause of poor growth and reproduction, predation is clearly the ultimate factor involved in this situation. Thus when predation avoidance occurs, standard demographic analyses will tend to underestimate the importance of predators in regulating the dynamics of their prey in the field.     

Winning the biodiversity arms race among freshwater gastropods: competition and coexistence through shell variability and predator avoidance

Explanations for the coexistence of many closely related species in inland waters continue to be generated more than 50 years after Hutchinson’s question: why are there so many kinds of animals? This review focuses on the hypothesis that high species diversity of freshwater gastropods results, in part, from predators maintaining biodiversity across a range of deep- and shallow-water habitats. Invertebrate predators, such as aquatic insects, and leeches consume soft tissue of pulmonate snails by penetrating shells of various shapes and sizes. Crayfish and large prawns chip around the shell aperture to enter thick shells and crush small shells with their mandibles. Crabs use their strong chelae to crush thin and thick shells. Fishes with pharyngeal teeth are major shell-breaking predators that combine with other vertebrate predators such as turtles and wading birds to increase the diversity of gastropod communities by regulating the abundance of dominant species. Although the generalized diets of most freshwater predators preclude tight co-evolutionary patterns of responses, there are combinations of predators that modify gastropod behavior and shell morphology in aquatic assemblages of different ages and depths. This combination of invertebrate and vertebrate predatory impacts led to competitive advantages among individual gastropods with different adaptations: (1) less vulnerable shell morphologies and sizes; (2) predator-avoidance behaviors; or (3) rapid and widespread dispersal with variable life histories. Some individuals develop thicker and/or narrow-opening shells or shells with spines and ridges. Other thin-shelled species crawl out of the water or burrow to lower their risk to shell-breaking or shell-entering predators. Some alter their age at first reproduction and grow rapidly into a size refuge. Fluctuations in water levels and introductions of non-native species can change competitive dominance relationships among gastropods and result in major losses of native species. Many different gastropod predators control species that are human disease vectors. Most snails and their predators provide other ecosystem services such as nutrient cycling and transfer of energy to higher trophic levels. Their persistence and diversity of native species require adaptive management and coordinated study.     

Antipredator behaviour mediated by chemical cues: the role of conspecific alarm signalling and predator labelling in the avoidance response of a marine gastropod

Gastropods represent a challenge in the understanding of alarm signalling. We studied predator avoidance (climbing behaviour) of the marine snail Tegula funebralis in laboratory experiments. Snails were exposed to crude extract of conspecifics, and to water conditioned by actively feeding or non-feeding predatory crabs. Crabs had previously been maintained on different diets, and were accordingly labelled by chemical cues of various origins. Tegula -extract alone released climbing behaviour in May, but not in June. However, during both these months, snails responded to chemical cues from crabs that were actively feeding on Tegula . Crabs labelled by Tegula -diet, and actively feeding on Tegula , also caused more climbing responses compared to crabs labelled by other diets. Chemical cues derived from crabs actively feeding on another snail species, or from non-feeding crabs, did not induce snail climbing no matter the previous feeding history of the predators. When snails received Tegula -extract combined with water conditioned with a non-feeding, Tegula -labelled crab, no climbing occurred. However, when the non-feeding, Tegula -labelled crab was present in the solution of Tegula -extract, moderate climbing responses were obtained. The results imply that climbing responses of T. funebralis are in general caused by the action of a two-component system. This system seems to be a mixture of chemical cues leaking from the tissue of conspecifics when being eaten, and latent conspecific chemicals that are modified in crabs and presumably released with the urine of chemically labelled predators. The modified chemical labels appear to be fully released by crabs when feeding, and moderately released when detecting food. The responses obtained in May with crude extract alone may result from a seasonal change in alarm signalling properties, or a change in behavioural responsiveness of snails exposed to a variable predator regime.     

The origins, fate, and ecological significance of free amino compounds released by freshwater pulmonate snails

The mass-specific accumulation rates (MSAR) of both total (TFAC) and individual free amino compounds (FAC) in conditioned media were measured by HPLC, using the orthophthaldialdehyde (OPA) methods, in the following cases: (a) laboratory-reared freshwater snails (B. glabrata) with chemosterilized shells; (b) Biomphalaria glabrata with non-chemosterilized shells; (c) B. glabrata faeces; (d) isolated shells of B. glabrata; and (e) 10 other species of freshwater gastropods from the Lewes Brooks, East Sussex, U.K. The MSAR values for B. glabrata show that 95% of the TFAC's (predominantly ethanolamine, phosphoserine, and the amino acids leucine, isoleucine, valine, aspartic acid, and glycine/threonine) originated from the snails themselves as the faeces and shells contributed only 5.0 and 0%, respectively. In contrast, epizootic organisms on the shells of all 10 snail species from the Lewes Brooks released significant amounts of FAC with the two smallest species (Planorbis vortex and Planorbis contortus) having the highest MSAR values. The MSAR for isolated B. glabrata mucus was 42.45 micromol x g(-1)h(-1). As 500 mg snails can release 16.67 mg of mucus daily, this could potentially result in the daily loss of 707.5 micromol of FAC. The cost/benefits of mucus secretion and the various anatomical, physiological, biochemical, and ecological mechanisms which allow freshwater snails to recover FAC's lost as a result of a high rate of urine production in their hypotonic environment, are discussed.     

Landscapes of Coexistence for terrestrial carnivores: the ecological consequences of being downgraded from ultimate to penultimate predator by humans

Fear of predation can have major impacts on the behaviour of prey species. Recently the concept of the ecology of fear has been defined and formalised; yet there has been relatively little focus on how these ideas apply to large carnivore species which, although not prey sensu stricto, also experience fear as a result of threats from humans. Large carnivores are likely also subject to a Landscape of Fear similar to that described for prey species. We argue that although fear is generic, ‘human‐caused mortality’ represents a distinct and very important cause of fear for large carnivores, particularly terrestrial large carnivores as their activities overlap with those of humans to a greater degree. We introduce the idea of a ‘Landscape of Coexistence’ for large carnivores to denote a subset of the Landscape of Fear where sufficient areas of low human‐caused mortality risk are present in the landscape for long term coexistence of large carnivores and humans. We then explore aspects of terrestrial large carnivore behavioural ecology that may be best explained by risk of human‐caused mortality, and how the nature of a Landscape of Coexistence for these large carnivores is likely to be shaped by specific factors such as habitat structure, wild and domestic prey base, and human distribution and behaviour. The human characteristics of this Landscape of Coexistence may be as important in determining large carnivore distribution and behavioural ecology as the distribution of resources. Understanding the Landscape of Coexistence for terrestrial large carnivores is therefore important for their biology and conservation throughout large parts of their remaining ranges. Synthesis The Landscape of Fear concept describing the relationship between predator and prey also applies to the relationship between humans and top carnivores. We synthesise current research to introduce the Landscape of Coexistence concept, arguing that top predators respond to the risks of human‐caused mortality through spatiotemporal partitioning of activities to reduce contact with people. The character of the Landscape of Coexistence may be more important than the distribution of resources in determining large carnivore distribution and behavioural ecology in human dominated landscapes. Understanding their behavioural responses to human threats is crucial to successful conservation of large carnivores.