The effects of opportunistic and intentional predators on the herding behavior of prey

In this article, we study how predator behavior influences the aggregation of prey into herds. Game-theoretic models of herd formation are developed based on different survival probabilities of solitary prey and prey that join the herd and on the predator's preference of what type of prey to search for. For an intentional predator that will only pursue its preferred type of prey, a single herd with no solitaries cannot emerge unless the herd acts as a prey refuge. If neither prey choice provides a refuge, it is shown that an equilibrium always exists where there are both types of prey and the predator does not always search for the same type of prey (i.e., a mixed equilibrium exists). On the other hand, if the predator is opportunistic in that it sometimes shifts to pursue the type of prey that is observed first, there may be a single herd equilibrium that does not act as a prey refuge when there is a high level of opportunistic behavior. For low opportunistic levels, a mixed equilibrium is again the only outcome. The evolutionary stability of each equilibrium is tested to see if it predicts the eventual herding behavior of prey in its corresponding model. Our analysis confirms that both predator and prey preferences (for herd or solitary) have strong effects on why prey aggregate. In particular, in our models, only the opportunistic predator can maintain all prey in a single herd that is under predation risk.     

Fish predators and scavengers of the sea urchin Paracentrotus lividus in protected areas of the north-west Mediterranean Sea

Direct observations of predation on 436 individuals of the sea urchin Paracentrotus lividus (Lamarck) were carried out in infralittoral rocky bottoms (between 5 and 20 m deep) in three Mediterranean marine reserves. The predator guild was composed of six fish species, the sparids Diplodus sargus and D. vulgaris being the main predators, and the labrid Coris julis a major predator of juvenile sea urchins. Four species attempted but failed to open sea urchins. The scavenger guild was most rich in species, with 17 species observed. Predation was size-dependent; the size of predators increased with increasing size of the sea urchins. The presence of two feeding guilds is suggested, one composed of sparids (Diplodus spp.), able to kill juvenile and adult sea urchins, and the other composed of labrids (mainly C. julis), which feed on juvenile sea urchins. To avoid the extension of overgrazed, barren areas created by P. lividus populations, fisheries' regulations should focus on major sea-urchin predators, chiefly D. sargus, D. vulgaris and C. julis. Received: 23 April 1997 / Accepted: 30 May 1997     

Vigilance for predators: detection and dilution effects

Summary Grouped individuals are less vigilant for predators than solitary conspecifics because (1) grouping increases the likelihood of predator detection (detection effect) and (2) grouping makes it less likely that any given individual will be preyed upon (dilution effect). However, many models of vigilance behaviour consider only the detection effect, and the interaction of the two effects has been insufficiently considered. I present two models of vigilance behaviour and test them using data on the vigilance of elk, Cervus elaphus. The first model, based on the detection effect alone, is implicit in many published formulations of the relationship between vigilance and group size. Although it predicts the direction of the relationship between vigilance and group size, it provides a poor explanation of the form of the relationship. The second model incorporates both detection and dilution effects. Regression analysis on this security model indicates that the model provides a good prediction of both the direction and the form of the relationship between vigilance and group size, explaining 69% of the variance in vigilance frequency. The security model demonstrates that both detection and dilution are important in determining the frequency of vigilance behaviour but that the relative importance of these two effects changes across group size, with detection providing relatively less benefit as group size increases. However, even when groups are large, individuals should exhibit at least some vigilance because although dilution alone provides much protection from predation, even a low level of vigilance greatly increases the likelihood that an individual will survive repeated predation attempts.     

The deadly effects of "nonlethal" predators

Nonconsumptive predator effects are widespread and include plasticity as well as general stress responses. Caged predators are often used to estimate nonconsumptive effects, and numerous studies have focused on the larval stages of animals with complex life cycles. However, few of these studies test whether nonconsumptive predator effects, including stress responses, are exclusively sublethal. Nor have they assessed whether these effects extend beyond the larval stage, affecting success during stressful life-history transitions such as metamorphosis. We conducted experiments with larvae of a dragonfly (Leucorrhinia intacta) that exhibits predator-induced plasticity to assess whether the mere presence of predators affects larval survivorship, metamorphosis, and adult body size. Larvae exposed to caged predators with no ability to attack them had higher levels of mortality. In the second experiment, larvae reared with caged predators had higher rates of metamorphic failure, but there was no effect on adult body size. Our results suggest that stress responses induced by exposure to predator cues increase the vulnerability of prey to other mortality factors, and that mere exposure to predators can result in significant increases in mortality.     

Asymmetry in community regulation: effects of predators and productivity

Eutrophication and predator additions and extinctions are occurring in ecosystems worldwide. Although theory predicts that both will strongly alter the distribution of biomass in whole communities, empirical evidence has not been consolidated to quantitatively determine whether these theoretical predictions are generally borne out in real ecosystems. Here we analyze data from two types of trophic cascade studies, predator removals in factorial combination with fertilization and observed productivity gradients, to assess the role of top-down and bottom-up forces in structuring multi-trophic communities and compare results from these analyses to those from an extensive database of trophic cascade studies. We find that herbivore biomass declines and plant biomass increases in the presence of predators, regardless of system productivity. In contrast, while plants are increased by fertilization, this effect does not significantly increase herbivores in either the presence or absence of predators. These patterns are consistent among marine, freshwater, and terrestrial ecosystems and are largely independent of study size and duration. Thus, top-down effects of predation are transferred through more trophic levels than are bottom-up effects of eutrophication, showing strong asymmetry in the direction of control of biomass distribution in communities.     

Linking edge effects and patch size effects: Importance of matrix nest predators

The edge effect is usually considered to be the proximate cause of area sensitivity in forest birds. We tested if birds nesting in large patches are less vulnerable to the edge effect using a simple model that assumes an increase in patch size reduces the probability of a matrix predator moving to the core areas of forest and that larger perimeter/area ratios result in a higher number of matrix predators per unit of area. The probability of a nest being successful decreased asymptotically with an increase in either the patch penetration distance of predators or predator density, but those effects were reduced when patch size was increased. Large patches have a lower probability of being affected by an Allee effect and they can function as sink habitats only if penetration distance and predator density are largely increased. However, the transition from an Allee effect to a sink condition occurs with a small increase in penetration distance and predator density. Since birds nesting in large patches are less vulnerable to an increase in matrix predator populations, persistence of bird populations may be possible by increasing the size of habitat patches that can act as source populations.     

Consequences for predators of rescue and Allee effects on prey

The size of a population can be augmented by enriching the carrying capacity of its limiting resource, or by subsidising the renewal of the resource. The well known ‘paradox of enrichment’ models the first case, in which enrichment can force consumers and their limiting resource into destabilising limit cycles, whereas impoverishment stabilises the dynamics. In this paper we model the case of resource subsidy, where the resource is a limiting prey to predators. In contrast to enrichment, the system is stabilised by an influx of prey in the form of a rescue effect, and destabilised by an outflux of prey in the form of an Allee effect. Limit cycles are not sustained by the Allee effect; instead both populations collapse to zero over a large region of the predator-prey phase plane. The catastrophic extinction of prey requires the presence of both an Allee effect on prey and a predator with a type II functional response, though neither needs to contribute a large impact to prey dynamics. The novel implication is that consumers exaggerate the impact of Allee effects on a renewing resource. Conversely, an Allee effect in the form of a cull of resource, even of small value, can trigger local extinction of resource-dependent consumers.     

Consumptive and nonconsumptive effects of predators on metacommunities of competing prey

Although predators affect prey both via consumption and by changing prey migration behavior, the interplay between these two effects is rarely incorporated into spatial models of predator-prey dynamics and competition among prey. We develop a model where generalist predators have consumptive effects (i.e., altering the likelihood of local prey extinction) as well as nonconsumptive effects (altering the likelihood of colonization) on spatially separated prey populations (metapopulations). We then extend this model to explore the effects of predators on competition among prey. We find that generalist predators can promote persistence of prey metapopulations by promoting prey colonization, but predators can also hasten system-wide extinction by either increasing local extinction or reducing prey migration. By altering rates of prey migration, predators in one location can exert remote control over prey dynamics in another location via predator-mediated changes in prey flux. Thus, the effect of predators may extend well beyond the proportion of patches they visit. In the context of prey metacommunities, predator-mediated shifts in prey migration and mortality can shift the competition-colonization trade-off among competing prey, leading to changes in the prey community as well as changes in the susceptibility of prey species to habitat loss. Consequently, native prey communities may be susceptible to invasion not only by exotic prey species that experience reduced amounts of mortality from resident predators, but also by exotic prey species that exhibit strong dispersal in response to generalist native predators. Ultimately, our work suggests that the consumptive and nonconsumptive effects of generalist predators may have strong, yet potentially cryptic, effects on competing prey capable of mediating coexistence, fostering invasion, and interacting with anthropogenic habitat alteration.     

Bottom-up effects of plant genotype on aphids, ants, and predators

Theory predicts that bottom-up ecological forces can affect community dynamics, but whether this extends to the effects of heritable plant variation on tritrophic communities is poorly understood. In a field experiment, I contrasted the effects of plant genotype (28 genotypes; 1064 plants), aphid density, and the presence/absence of mutualistic ants in affecting the per capita population growth of a specialist aphid herbivore, as well as the effects of plant genotype on the third trophic level. Plant genotype strongly affected aphid population growth rate, explaining 29% of the total variation in growth rate, whereas aphid density and ant-aphid interactions explained substantially less variation (< 2%) in aphid population growth rate. Plant genotype also had direct and indirect effects on the third trophic level, affecting the abundance of aphid-tending ants and the richness of predators. Multiple regression identified several heritable plant traits that explained 49% of the variation in aphid growth rate and 30% of the variation in ant abundance among plant genotypes. These bottom-up effects of plant genotype on tritrophic interactions were independent of the effects of either initial aphid density or the presence/absence of mutualistic ants. This study shows that plant genotype can be one of the most important ecological factors shaping tritrophic communities.     

Consequences of stage-structured predators: cannibalism, behavioral effects, and trophic cascades

Cannibalistic and asymmetrical behavioral interactions between stages are common within stage-structured predator populations. Such direct interactions between predator stages can result in density- and trait-mediated indirect interactions between a predator and its prey. A set of structured predator-prey models is used to explore how such indirect interactions affect the dynamics and structure of communities. Analyses of the separate and combined effects of stage-structured cannibalism and behavior-mediated avoidance of cannibals under different ecological scenarios show that both cannibalism and behavioral avoidance of cannibalism can result in short- and long-term positive indirect connections between predator stages and the prey, including "apparent mutualism." These positive interactions alter the strength of trophic cascades such that the system's dynamics are determined by the interaction between bottom-up and top-down effects. Contrary to the expectation of simpler models, enrichment increases both predator and prey abundance in systems with cannibalism or behavioral avoidance of cannibalism. The effect of behavioral avoidance of cannibalism, however, depends on how strongly it affects the maturation rate of the predator. Behavioral interactions between predator stages reduce the short-term positive effect of cannibalism on the prey density, but can enhance its positive long-term effects. Both interaction types reduce the destabilizing effect of enrichment. These results suggest that inconsistencies between data and simple models can be resolved by accounting for stage-structured interactions within and among species.     

Minimizing predation risk in a landscape of multiple predators: effects on the spatial distribution of African ungulates

Studies that focus on single predator-prey interactions can be inadequate for understanding antipredator responses in multi-predator systems. Yet there is still a general lack of information about the strategies of prey to minimize predation risk from multiple predators at the landscape level. Here we examined the distribution of seven African ungulate species in the fenced Karongwe Game Reserve (KGR), South Africa, as a function of predation risk from all large carnivore species (lion, leopard, cheetah, African wild dog, and spotted hyena). Using observed kill data, we generated ungulate-specific predictions of relative predation risk and of riskiness of habitats. To determine how ungulates minimize predation risk at the landscape level, we explicitly tested five hypotheses consisting of strategies that reduce the probability of encountering predators, and the probability of being killed. All ungulate species avoided risky habitats, and most selected safer habitats, thus reducing their probability of being killed. To reduce the probability of encountering predators, most of the smaller prey species (impala, warthog, waterbuck, kudu) avoided the space use of all predators, while the larger species (wildebeest, zebra, giraffe) only avoided areas where lion and leopard space use were high. The strength of avoidance for the space use of predators generally did not correspond to the relative predation threat from those predators. Instead, ungulates used a simpler behavioral rule of avoiding the activity areas of sit-and-pursue predators (lion and leopard), but not those of cursorial predators (cheetah and African wild dog). In general, selection and avoidance of habitats was stronger than avoidance of the predator activity areas. We expect similar decision rules to drive the distribution pattern of ungulates in other African savannas and in other multi-predator systems, especially where predators differ in their hunting modes.     

Tidal regime dictates the cascading consumptive and nonconsumptive effects of multiple predators on a marsh plant

Prey perception of predators can dictate how prey behaviorally balance the need to avoid being eaten with the need to consume resources, and this perception and consequent behavior can be strongly influenced by physical processes. Physical factors, however, can also alter the density and diversity of predators that pursue prey. Thus, it remains uncertain to what extent variable risk perception and antipredator behavior vs. variation in predator consumption of prey underlie prey-resource dynamics and give rise to large-scale patterns in natural systems. In an experimental food web where tidal inundation of marsh controls which predators access prey, crab and conch (predators) influenced the survivorship and antipredator behavior of snails (prey) irrespective of whether tidal inundation occurred on a diurnal or mixed semidiurnal schedule. Specifically, cues of either predator caused snails to ascend marsh leaves; snail survivorship was reduced more by unrestrained crabs than by unrestrained conchs; and snail survivorship was lowest with multiple predators than with any single predator despite interference. In contrast to these tidally consistent direct consumptive and nonconsumptive effects, indirect predator effects differed with tidal regime: snail grazing of marsh leaves in the presence of predators increased in the diurnal tide but decreased in the mixed semidiurnal tidal schedule, overwhelming the differences in snail density that resulted from direct predation. In addition, results suggest that snails may increase their foraging to compensate for stress-induced metabolic demand in the presence of predator cues. Patterns from natural marshes spanning a tidal inundation gradient (from diurnal to mixed semidiurnal tides) across 400 km of coastline were consistent with experimental results: despite minimal spatial variation in densities of predators, snails, abiotic stressors, and marsh productivity, snail grazing on marsh plants increased and plant biomass decreased on shorelines exposed to a diurnal tide. Because both the field and experimental results can be explained by tidal-induced variation in risk perception and snail behavior rather than by changes in snail density, this study reinforces the importance of nonconsumptive predator effects in complex natural systems and at large spatial scales.     

New effects of Roundup on amphibians: predators reduce herbicide mortality; herbicides induce antipredator morphology

The use of pesticides is important for growing crops and protecting human health by reducing the prevalence of targeted pest species. However, less attention is given to the potential unintended effects on nontarget species, including taxonomic groups that are of current conservation concern. One issue raised in recent years is the potential for pesticides to become more lethal in the presence of predatory cues, a phenomenon observed thus far only in the laboratory. A second issue is whether pesticides can induce unintended trait changes in nontarget species, particularly trait changes that might mimic adaptive responses to natural environmental stressors. Using outdoor mesocosms, I created simple wetland communities containing leaf litter, algae, zooplankton, and three species of tadpoles (wood frogs [Rana sylvatica or Lithobates sylvaticus], leopard frogs [R. pipiens or L. pipiens], and American toads [Bufo americanus or Anaxyrus americanus]). I exposed the communities to a factorial combination of environmentally relevant herbicide concentrations (0, 1, 2, or 3 mg acid equivalents [a.e.]/L of Roundup Original MAX) crossed with three predator-cue treatments (no predators, adult newts [Notophthalmus viridescens], or larval dragonflies [Anax junius]). Without predator cues, mortality rates from Roundup were consistent with past studies. Combined with cues from the most risky predator (i.e., dragonflies), Roundup became less lethal (in direct contrast to past laboratory studies). This reduction in mortality was likely caused by the herbicide stratifying in the water column and predator cues scaring the tadpoles down to the benthos where herbicide concentrations were lower. Even more striking was the discovery that Roundup induced morphological changes in the tadpoles. In wood frog and leopard frog tadpoles, Roundup induced relatively deeper tails in the same direction and of the same magnitude as the adaptive changes induced by dragonfly cues. To my knowledge, this is the first study to show that a pesticide can induce morphological changes in a vertebrate. Moreover, the data suggest that the herbicide might be activating the tadpoles' developmental pathways used for antipredator responses. Collectively, these discoveries suggest that the world's most widely applied herbicide may have much further-reaching effects on nontarget species than previous considered.     

Heavier birds react faster to predators: individual differences in the detection of stalking and ambush predators

The relationship between body mass and reactions speed in response to a predatory threat is poorly understood. Theory predicts that different vigilance patterns are optimal for the detection of different predator types. We suggest that birds of different individual state might also differ in their speed of response dependent upon predator type. We used laboratory trials of wild caught chaffinches (Fringilla coelebs) to determine how between individual differences in chaffinch behaviour and state correlate with latency to react to a ground predator model (domestic cat), thus providing a comparison with previous work in the same model system using aerial predator models. In experiment 1, we observed chaffinch responses to a moving cat model, simulating a stalking predator. In experiment 2, we used a camouflaged cat model simulating an ambush predator. Both experiments show evidence suggesting heavier individuals (which previous literature has linked to impaired flight performance) responded more quickly to the model cat. Heavier individuals also had shorter interscan intervals. In contrast to a previous study, both experiments found individuals with a higher intake rate were not faster at responding to the cat model. In addition, individuals in experiment 1 that head turned more while scanning were slower to respond to the stalking cat model. Our work suggests that although heavier individuals may have impaired escape performance they appear to show behavioural compensation by allocating more attention to anti-predator behaviour and by modifying their interscan intervals, resulting in faster response times to a ground predator. We suggest more experiments investigating response time to different predatory types and explicitly manipulating state to elucidate cause and effect.     

Understanding determinants of home range behaviour of feral cats as introduced apex predators in insular ecosystems: a spatial approach

The introduced feral cat (Felis catus) is a widespread generalist with flexible social behaviour and an apex predator without major interspecific competitors in insular ecosystems that evolved in the absence of predators. Mechanistic definitions consider an animal’s home range to be the spatial expression of a cognitive map that is kept up-to-date with the status of critical resources that contribute to animal fitness. We assumed there are two major determinants structuring the home range of cats as apex predators in insular ecosystems: the distribution of critical food resources and conspecific distribution. We hypothesized that cats structure their home ranges by optimizing the use of staple critical food resources and that as a consequence of the presence of rich resources cats tend to socialise, aggregate and share space. We carried out spatial analyses using location data for feral cats tracked using lightweight GPS collars in conjunction with the suitability value of rabbit patches and their associated ownership costs for cats within a New Zealand braided-river environment. Cat home ranges and spatial distribution, especially for females, were related to the inclusion of rabbit patches within home ranges with higher mean value than the average of neighbourhood patches in the landscape. Cats showed solitary behaviour but tolerance to conspecific presence by sharing high-use areas and high-value rabbit patches, mostly at different times, resulting in occasional encounters among males and females. Home range size and patterns of spatial overlap were dependant on sex and season. Solitary spacing patterns as consequence of innate preferences together with resource constraints may regulate feral cat population densities.     

Pyrrolizidine alkaloids on three trophic levels – evidence for toxic and deterrent effects on phytophages and predators

Summary. Pyrrolizidine alkaloids (PAs) present a model system in the investigation of tritrophic interactions mediated by plant secondary compounds. However, their toxicity for insect herbivores has never been experimentally proven. Here, we demonstrate the toxic effects of a PA on growth and survival of the eri silk moth Philosamia ricini. In a feeding experiment, larvae of this generalist herbivore fed with an artificial PA diet gained weight significantly slower than control animals, and died as pupae. We suggest that derivatives of the ingested PA N-oxide damage developmental functions during metamorphosis. A tracer test with [¹⁴C]senecionine N-oxide revealed that the caterpillars lack adaptations that would prevent conversion of the chemical into the pro-toxic free base. In contrast, the PA adapted leaf beetle Longitarsus anchusae accumulates PAs as N-oxides. We tested the purpose of sequestration in this species as defence against predators. Through a series of prey choice experiments with three carabid predator species, chemically non-protected bark beetle pupae were chosen almost uniformly over L. anchusae pupae. In a following choice test with one of these predators, artificially PA-treated mealworm segments deterred the predator from feeding. Overall the study corroborates the immediate toxic effect of PAs on non-adapted herbivores and the protective effect that adapted insects may gain by sequestering them. It thereby underlines the potential for PAs to play a central role in multitrophic interactions between plants, phytophages and their predators.     

Additive effects of vertebrate predators on insects in a Puerto Rican coffee plantation.

A variety of studies have established the value of shaded coffee plantations as habitat for birds. While the value of birds as biological controls in coffee has received some attention, the interactions between birds and other predators of insects have not been tested. We used exclosures to examine the effects of vertebrate predators on the arthropods associated with coffee, in particular the coffee leafminer (Leucoptera coffeella) and the flatid planthopper Petrusa epilepsis, in a shaded coffee plantation in Puerto Rico. We used a 2 x 2 factorial design with four treatments: exclusion of birds, lizards, birds and lizards, and control (no exclusion). Abundance of insects > 5 mm increased when birds or both birds and lizards were removed. Birds and lizards had an additive effect for insects < 5 mm and for all insects combined. Coffee leafminers showed a weak response to removal of predators while planthopper abundance increased significantly in the absence of avian predators. Arthropod predators and parasitoids did not differ significantly between treatments. Our findings suggest that vertebrate insectivores have an additive effect on insects in coffee and may help control abundances of some coffee pests. Equally important, we present evidence suggesting that they do not interfere with other known natural enemies of coffee pests.     

The good and the bad stopover: behaviours of migrant reed warblers at two contrasting sites

Successful migration for passerine birds depends largely on the quality of stopover habitats, but we still lack complete knowledge of how migrants search for habitats en route and how they behave when landing at poor quality stopover sites. We compared the distance of exploratory movements and stopover durations of the reed warbler Acrocephalus scirpaceus, a reedbed habitat specialist, released at suitable (reed bed) and unsuitable (sand dune) stopover sites. Birds tape-lured during nocturnal migration to a sand dune were captured, radio-tagged, released and tracked at two sites of contrasting habitat quality. Lean birds were found to move further in the dunes (max. 300 m) than in reeds (max. 200 m), whereas ‘fat’ individuals at both sites remained stationary. Birds spent just 1 day in the dunes and up to 13 days in the reeds. Our results suggest that some nocturnal migrants with restricted diurnal exploratory movements depend on stopover site selection when ceasing nocturnal flight.     

Learning to recognize novel predators under weakly acidic conditions: the effects of reduced pH on acquired predator recognition by juvenile rainbow trout

Summary. Recent studies have demonstrated that under weakly acidic conditions (pH 6.0), many prey fishes, including juvenile rainbow trout (Onchorhynchus mykiss), do not exhibit overt antipredator responses to conspecific chemical alarm cues. In laboratory trials, we investigated the potential effects of reduced pH on the ability of hatchery reared, predator naïve juvenile rainbow trout to acquire the recognition of a novel predator (yellow perch, Perca flavenscens). Initially, we exposed trout to the odour of a predatory yellow perch, buffered to pH 6.0 (weakly acidic) or pH 7.0 (neutral) paired with conspecific skin extracts (also buffered to pH 6.0 or 7.0) or a distilled water control. Juvenile trout exhibited significant increase in antipredator behaviour when exposed to neutral skin extract (pH 7.0). When retested 48 hours later to perch odour alone (pH 7.0), only trout initially conditioned with neutral skin extracts (pairs with either neutral or acidic perch odour) exhibited a learned recognition of perch odour as a predator risk. Those initially exposed to weakly acidic skin extract or the distilled water control did not show a learned response to predator odour. These results demonstrate that the ability to acquire the recognition of novel predators is impaired under weakly acidic conditions, as would occur in natural waterways affected by acidic precipitation.