Importance of consumptive and non-consumptive prey mortality in a coupled predator–prey system

1. Laboratory experiments were completed to identify the mechanisms by which the predatory flatworm, Dugesia tigrina , imposes mortality on its Aedes aegypti and Daphnia magna prey. Feeding trials were completed in glass microcosms which contained one of three – nine densities of small or large individuals of each prey species.
2. Mortality by Dugesia on small and large Aedes followed a type II functional response, whereas the mortality of Daphnia resembled a type III functional response. Prey mortality imposed by Dugesia consisted of consumptive and non-consumptive elements. Non-consumptive mortality occurred when prey individuals trapped in mucus trails subsequently died but were not ingested.
3. Additional experiments were conducted to quantify consumptive (capture followed by ingestion) and non-consumptive mortality (death not followed by ingestion).
4. Consumptive mortality followed a type II functional response for small and large individuals of both prey species, whereas non-consumptive mortality increased with prey density, although the relationships differed with prey species and size. The non-consumptive mortality of large Daphnia increased at an accelerating rate with prey density and exceeded consumptive mortality at intermediate prey abundances. In contrast, non-consumptive mortality of small Aedes and small Daphnia was lower than consumptive mortality and either increased with prey density at a decelerating (small Aedes ) or accelerating (small Daphnia ) rate.
5. These results suggest that the importance of consumptive and non-consumptive mortality to total prey mortality needs to be considered when modelling predator–prey dynamics.     

Temperature effects on chemical signalling in a predator–prey system

SUMMARY 1. We investigated the effect of temperature on chemical signalling in a predator–prey model system (planktivorous fish and Daphnia galeata ). Life-history changes in Daphnia in response to chemical cues (kairomones) derived from fish have become a paradigm for chemically induced anti-predator defences.
2. As temperature can affect both predator and prey, we carried out two experiments to disentangle these effects. In order to test for temperature effects on the predator, we kept prey at a single temperature and exposed them to kairomones from fish exposed to two different temperatures. Daphnia exhibited a higher intrinsic rate of population increase ( r ) when exposed to fish kairomones produced at high rather than low temperature. Assuming a positive correlation between r (because of an earlier maturation and/or increased clutch sizes) and kairomone concentration, our results suggest that kairomone production increases with rising temperature.
3. In the second experiment, to study the influence of temperature on the prey, Daphnia were kept at two different temperatures and exposed to fish kairomones produced at one constant temperature. We found no interaction between the effects of fish kairomone and temperature on Daphnia life history, suggesting that temperature does not directly alter life-history responses to fish kairomones.
4. Our results suggest that temperature influences Daphnia life history through its effects on fish kairomone concentration, but that temperature does not affect the strength of the response of Daphnia to the presence of fish.     

Habitat loss decreases predator–prey ratios in a pine-bark beetle system

Increasing intensity of land use by humans has led to loss of natural habitats, resulting in isolation of remaining habitat fragments. Using a pine-bark beetle ecosystem as a model, we tested the hypothesis that the ratio of abundance of predators to prey should decrease with increasing habitat loss at the landscape scale. We selected ten red pine ( Pinus resinosa ) sites, representing extremes of available habitat within a 2 km radius surrounding each stand. The bark beetle, Ips pini , and its coleopteran predators were sampled using baited multiple funnel traps. Effects of stand isolation were considerable; ratios of predators to prey (mean number of predators/number of prey±SE) were significantly reduced in isolated stands (0.38±0.09) as compared to those with large amounts of surrounding conifer habitat (1.63±0.41). The decline in ratio occurred both because there was: a) a lower abundance of predators (ca 0.5–0.8×) captured in isolated stands; and b) a significantly higher number of prey (ca 2.2×) captured in isolated stands. Isolation or loss of habitat, therefore, differentially affected the two trophic levels, supporting theoretical predictions. Reductions in predator abundance and, presumably, enemy-caused mortality may lead to changes in the population dynamics of their prey species, possibly leading to increased outbreaks as habitat becomes increasingly isolated.     

Allee effect makes possible patchy invasion in a predator–prey system

The dynamics of interacting ecological populations results from the interplay between various deterministic and stochastic factors and this is particularly the case for the phenomenon of biological invasion. Whereas the spread of invasive species via propagation of a population front was shown to appear as a result of deterministic processes, the spread via formation, interaction and movement of separate patches has been recently attributed to the influence of environmental stochasticity. An appropriate understanding of the comparative importance of deterministic and stochastic mechanisms is still lacking, however. In this paper, we show that the patchy invasion appears to be possible also in a fully deterministic predator–prey model as a result of the Allee effect.     

A predator–prey refuge system: Evolutionary stability in ecological systems

A refuge model is developed for a single predator species and either one or two prey species where no predators are present in the prey refuge. An individual’s fitness depends on its strategy choice or ecotype (predators decide which prey species to pursue and prey decide what proportion of their time to spend in the refuge) as well as on the population sizes of all three species. It is shown that, when there is a single prey species with a refuge or two prey species with no refuge compete only indirectly (i.e. there is only apparent competition between prey species), that stable resident systems where all individuals in each species have the same ecotype cannot be destabilized by the introduction of mutant ecotypes that are initially selectively neutral. In game-theoretic terms, this means that stable monomorphic resident systems, with ecotypes given by a Nash equilibrium, are both ecologically and evolutionarily stable. However, we show that this is no longer the case when the two indirectly-competing prey species have a refuge. This illustrates theoretically that two ecological factors, that are separately stabilizing (apparent competition and refuge use), may have a combined destabilizing effect from the evolutionary perspective. These results generalize the concept of an evolutionarily stable strategy (ESS) to models in evolutionary ecology. Several biological examples of predator–prey systems are discussed from this perspective.     

Coupled predator–prey oscillations in a chaotic food web

Coupling of several predator–prey oscillations can generate intriguing patterns of synchronization and chaos. Theory predicts that prey species will fluctuate in phase if predator–prey cycles are coupled through generalist predators, whereas they will fluctuate in anti-phase if predator–prey cycles are coupled through competition between prey species. Here, we investigate predator–prey oscillations in a long-term experiment with a marine plankton community. Wavelet analysis of the species fluctuations reveals two predator–prey cycles that fluctuate largely in anti-phase. The phase angles point at strong competition between the phytoplankton species, but relatively little prey overlap among the zooplankton species. This food web architecture is consistent with the size structure of the plankton community, and generates highly dynamic food webs. Continued alternations in species dominance enable coexistence of the prey species through a non-equilibrium 'killing-the-winner' mechanism, as the system shifts back and forth between the two predator–prey cycles in a chaotic fashion.     

Parasitism in a declining population of snowshoe hares

Prevalence and intensity of six endoparasites were determined in 346 snowshoe hares (Lepus americanus) obtained at Rochester, Alberta, during December-April 1981-1982, the second winter of a cyclic population decline. The data were analyzed for (1) differences among host sex and age classes, and among months and sample sources, and (2) evidence that parasitism was of demographic significance to the hare population. Prevalence and intensity of Obeliscoides cuniculi were consistently highest among adult hares, but rose most sharply from February to March among juveniles. In contrast, prevalence and intensity of Nematodirus triangularis were highest among juveniles; prevalence reached 90-100% by January, whereas intensity continued to rise through April. Prevalence and intensity of both Trichuris leporis and Protostrongylus boughtoni were highest also among juvenile hares; neither parameter exhibited a definite trend over time. Prevalences of Taenia pisiformis (cysticerci) and Eimeria spp. were unrelated to sex, age or month; but Taenia intensity was highest among juveniles, and Eimeria intensity tended to decrease from December to April. Intensities of Nematodirus, Protostrongylus and Eimeria were higher in male hares than in females. Prevalence and intensity were correlated directly in Obeliscoides, Nematodirus, Trichuris and Eimeria. Hares that died during trapping and handling, or from natural predation, had greater intensities of Obeliscoides than did animals killed on purpose. There was no indication, however, that risk of death was increased by the other parasitic infections. Age-related immune responses to parasitism (except Obeliscoides) were evidenced by reduced or stabilized prevalence and/or intensity among older hares. A multiple-regression model predicted depressed body weight with increasing intensities of Nematodirus, Trichuris or Protostrongylus. Other body-condition and reproductive indices were unassociated with parasite intensities. Within the hare population, Obeliscoides, Trichuris, Protostrongylus and Taenia had overdispersed distributions (typical of many endoparasites) that did not differ from a negative binomial. The frequency with which each possible combination of helminth species occurred within individual hares was consistent with the assumption that such infections occurred independently. There was no compelling reason to believe parasitism was a significant factor in the overwinter decline of this population of snowshoe hares.     

Effects of prey dispersal on predator–prey interactions in streams

1. We studied the effect of mesh size (6 and 3 mm) on interactions between brown trout ( Salmo trutta ) and benthic invertebrates in enclosures placed in a stream in southern Sweden. We also compared how different prey exchange rates affected interactions between trout and invertebrates.
2. Trout had strong impacts on some benthic taxa, and different mesh sizes produced different patterns. Trout affected the abundance of 10 of the 21 taxa examined, six in enclosures with 3 mm mesh and six in enclosures with 6 mm mesh. The abundance of nine of the prey taxa was lower in the presence of trout, only leptocerids were more numerous in the presence of trout.
3. Our measurements of prey immigration/emigration, together with trout diet data, suggest that direct consumption by trout, rather than avoidance behaviour by prey, explains most decreases in prey abundance. There was avoidance behaviour by only two of the twenty-one prey taxa, with trout inducing emigration of the mayflies Baetis rhodani and Paraleptophlebia sp.
4. Trout indirectly increased periphyton biomass in both 3 and 6 mm enclosures. The effect of trout on periphyton was probably due to strong effects of trout on the grazer, Baetis rhodani , Heptagenia sp. and Paralepthoplebia sp.
5. Our results suggest that mesh size, through its effects on exchange rates of prey, may affect interactions between predators and prey in running waters, but that the effects of dispersal and predation on invertebrates are taxon specific.     

Multi-behavioral strategies in a predator–prey game: an evolutionary algorithm analysis

Behavioral games between predators and prey often involve two sub-games: 'pre-encounter' games affecting the rate of encounter between predators and prey (e.g. predator–prey space games, Sih 2005 ), and 'post-encounter' games that influence the outcome of encounters (e.g. waiting games at prey refugia, Hugie 2003 , and games of vigilance, Brown et al. 1999 ). Most models, however, focus on only one or the other of these two sub-games.
I investigated a multi-behavioral game between predators and prey that integrated both pre-encounter and post-encounter behaviors. These behaviors included landscape-scale movements by predators and prey, a type of prey vigilance that increases immediately after an encounter and then decays over time ('ratcheting vigilance'), and predator management of prey vigilance. I analyzed the game using a computer-based evolutionary algorithm. This algorithm embedded an individual-based model of ecological interactions within a dynamic adaptive process of mutation and selection. I investigated how evolutionarily stable strategies (ESS) varied with the predators' learning ability, killing efficiency, density and rate of movement. I found that when predators learn prey location, random prey movement can be an ESS. Increased predator killing efficiency reduced prey movement, but only if the rate of predator movement was low. Predators countered ratcheting vigilance by delaying their follow-up attacks; however, this delay was reduced in the presence of additional predators. The interdependence of pre-and post-encounter behaviors revealed by the evolutionary algorithm suggests an intricate co-evolution of multi-behavioral predator–prey behavioral strategies.     

Allometry and selection in a novel predator–prey system: Australian snakes and the invading cane toad

Because many organismal traits vary with body size, interactions between species can be affected by the respective body sizes of the participants. We focus on a novel predator–prey system involving an introduced, highly toxic anuran (the cane toad, Bufo marinus ) and native Australian snakes. The chance of a snake dying after ingesting a toad depends on the size of the snake and the size of the toad, and ultimately reflects the effect of four allometries: (1) physiological tolerance (the rate that physiological tolerance to toad toxin changes with snake size); (2) swallowing ability (the rate that maximal ingestible toad size (i.e. snake head size) increases with snake body size); (3) prey size (the rate that prey size taken by snakes increases with snake head size) and (4) toad toxicity (the rate that toxicity increases with toad size). We measured these allometries, and combined them to estimate the rate at which a snake's resistance changes with toad toxicity. The parotoid glands (and thus, toxicity) of toads increased disproportionately with toad size (i.e. relative to body size, larger toads were more toxic) but simultaneously, head size relative to body size (and thus, maximal ingestible prey size relative to predator size) declined with increasing body size in snakes. Thus, these two allometries tended to cancel each other out. Physiological tolerance to toxins did not vary with snake body size. The end result was that across snake species, mean adult body size did not affect vulnerability. Within species, however, smaller predators were more vulnerable, because the intraspecific rate of decrease in relative head size of snakes was steeper than the rate of increase in toxicity of toads. Thus, toad invasion may cause disproportionate mortality of juvenile snakes, and adults of the sex with smaller mean adult body sizes.     

Actinobacillosis in free-ranging snowshoe hares (Lepus americanus) from Alaska

Actinobacillus capsulatus was isolated from lung, liver, and/or spleen tissue of three snowshoe hares (Lepus americanus) in Alaska. This is the first report of the isolation of this bacterium from free-ranging hares. Actinobacillus capsulatus may have a negative impact on the population density of hares.     

Summer diet selection of snowshoe hares: a test of nutritional hypotheses

We examined summer diet selection by snowshoe hares in the southwestern Yukon, Canada, and attempted to explain how plant qualities such as nutritional content (protein, energy, fiber, water) and defensive compounds affect hare food choice. Male hares were placed in enclosures in natural vegetation areas dominated by shrubs and in both open and closed spruce forests. Each site contained a variety of herbaceous plant species. After 24 h, hares were sacrificed, their stomachs collected, and the contents removed and analyzed. Of the 30 plant species recorded in the enclosures only 10 were identified in the stomach contents of the hares. The summer diet is composed predominantly of five plant species; Lupinus arcticus, Salix spp. Shepherdia canadensis, Betula glandulosa and Festuca altaica. The selection of these species changes between sampling times. Protein, energy and water contents were highest in leaf tissues of most species early in the season, and most species had an increase in fiber through the summer. Protein content consistently explains the largest amount of variation in diet selection, although protein selection is modified by extremely high concentrations of defence compounds. It is likely that hares are not protein limited and are selecting for other plant characteristics correlated with protein content such as energy content. It is significant that hares continue to ingest heavily defended species (e.g. Shepherdia canadensis, B. glandulosa and L. arcticus) when many less defended plants are available to be eaten (e.g. F. altaica, Epilobium latifolium and Anemone parviflora). Our results support the idea that hares are selecting dietary items on the basis of energy content. No single plant species can satisfy all of the hares’ nutritional requirements and the selection patterns may reflect the need to balance many conflicting plant qualities.     

Agricultural farming alters predator–prey interactions in nearby natural habitats

Agricultural farming is a major consumer of global arable lands and has a direct effect on species decline through habitat destruction. However, agricultural endeavours can also evoke indirect threats that will result in behavioural modifications of indigenous species. In a desert ecosystem, where a political border led to a farming dichotomy between intensive cultivates in Israel and intact lands in Jordan, we compared the foraging behaviours and abundances of the red fox and two species of gerbils, close to and distant from farms, and during two moon phases. We estimated fox and gerbil foraging levels by track counts, and measured gerbil time allocation, vigilance and apprehension by the giving-up density method. While foxes were significantly more abundant and active at locations close to farms, gerbils were significantly more abundant and active at locations distant from farms. Moreover, the typical reduction in food consumption during full-moon nights was exhibited only at locations close to farms. These results could suggest that indicators of predation risk, such as illumination intensity or distance to cover, are not universal, and their effectiveness may depend indirectly on anthropogenic activities, such as agricultural farming. The results could also suggest that although intensive agricultural endeavours benefit foxes, they might increase the predatory pressure on gerbils in addition to the already known effects of habitat loss. Therefore, agriculture acts as a double-edged sword by reducing natural habitats, while at the same time changing the predator–prey natural balance.     

Spatial decomposition of predation risk using resource selection functions: an example in a wolf–elk predator–prey system

Predation is a fundamental ecological and evolutionary process that varies in space, and the avoidance of predation risk is of central importance in foraging theory. While there has been a recent growth of approaches to spatially model predation risk, these approaches lack an adequate mechanistic framework that can be applied to real landscapes. In this paper we show how predation risk can be decomposed into encounter and attack stages, and modeled spatially using resource selection functions (RSF) and resource selection probability functions (RSPF). We use this approach to compare the effects of landscape attributes on the relative probability of encounter, the conditional probability of death given encounter, and overall wolf and elk resource selection to test whether predation risk is simply equivalent to location of the predator. We then combine the probability of encounter and conditional probability of death into a spatially explicit function of predation risk following Lima and Dill's reformulation of Holling's functional response. We illustrate this approach in a wolf–elk system in and adjacent to Banff National Park, Alberta, Canada. In this system we found that the odds of elk being encountered by wolves was 1.3 times higher in pine forest and 4.1 times less in grasslands than other habitats. The relative odds of being killed in pine forests, given an encounter, increased by 1.2. Other habitats, such as grasslands, afforded elk reduced odds (4.1 times less) of being encountered and subsequently killed (1.4 times less) by wolves. Our approach illustrates that predation risk is not necessarily equivalent to just where predators are found. We show that landscape attributes can render prey more or less susceptible to predation and effects of landscape features can differ between the encounter and attack stages of predation. We conclude by suggesting applications of our approach to model predator–prey dynamics using spatial predation risk functions in theoretical and applied settings.     

Strategies of aphidophagous predators: lessons for modelling insect predator–prey dynamics

Both theoretical and empirical evidence indicate that in systems where insect predators have longer developmental times than their prey the predators have little impact on the abundance of their prey. In assessing the 'effectiveness' of a predator for biological control one should take into account that selection maximizes predator fitness, not its effctiveness as a biocontrol agent. Therefore, predators that have a long developmental time relative to their prey are unlikely to be the best biocontrol agents. If these results can be generalized to other predator–prey systems, then it is clear that an understanding of predator–prey dynamics can only be achieved by studying predators.