Influence of predator density on nonindependent effects of multiple predator species

Interactions between multiple predator species are frequent in natural communities and can have important implications for shared prey survival. Predator density may be an important component of these interactions between predator species, as the frequency of interactions between species is largely determined by species density. Here we experimentally examine the importance of predator density for interactions between predator species and subsequent impacts on prey. We show that aggressive interactions between the predatory shore crabs Carcinus maenas and Hemigrapsus sanguineus increased with predator density, yet did not increase as fast as negative interactions between conspecifics. At low density, interactions between conspecific and heterospecific predators had similar inhibitory impacts on predator function, whereas conspecific interference was greater than interference from heterospecifics at high predator density. Thus the impact of conspecific interference at high predator density was sufficient in itself that interactions with a second predator species had no additional impact on per capita predation. Spatial and temporal variability in predator density is a ubiquitous characteristic of natural systems that should be considered in studies of multiple predator species.     

Intraguild predation by aphidophagous predators on parasitised aphids: the use of multiple video cameras

A video technique that allows simultaneous behavioural observations of several experimental replicates under field and laboratory conditions is described. The technique was used to analyse predation risk of parasitised aphids in a sugar beet field. The images of 16 black and white video cameras were recorded by a video multiplexer in combination with a time-lapse video recorder. Each camera was weather protected and equipped with a single infrared diode to allow observations during night times. Single leaves carrying aphid mummies only or mummies and unparasitised aphids were monitored. All colonies were exposed to predation and parasitation by the community of natural enemies in the field. Colonies with mummies and unparasitised aphids were visited significantly more often by predators than those without additional aphids. Predators also stayed significantly longer in patches with unparasitised aphids. Although an equal proportion of aphid mummies were destroyed in both treatments, the video analysis showed differences in predator species spectrum between treatments. In patches with aphids, coccinellid and hemipteran predators preyed on mummies, while in patches with only mummies, chrysopids accounted for most of the damage. The decrease in parasitoid survival could be attributed to the increasing number of predator visits in aphid patches and to a lesser extent to the decreasing number of unparasitised aphids (alternative prey). Parasitoid survival in colonies without alternative prey was correlated with the number of predator visits and the time predators spent on a leaf.Continuous video observations gave additional behavioural information for the interpretation of field data. Other prospective research fields for the use of the multi video camera technique are outlined and general advantages and disadvantages are discussed.     

Detecting emergent effects of multiple predator species

When foraging together, multiple predator species that share a single prey often cause prey mortality that cannot be predicted based on knowledge of predation by each species separately. Modeling and managing the effects of multiple predator species depend on accurately assessing these combined effects. Two methods are currently used to experimentally examine combined predation by multiple predator species: the additive and substitutive experimental designs. I simultaneously employed both experimental designs to examine predation by two crab species on shared mussel prey. I show that the two methods yield results that disagree both quantitatively and qualitatively, leading to very different conclusions about the way that predator species combine to affect prey mortality. This discrepancy occurred because the two methods examine complimentary, but not interchangeable questions. I advocate using an experimental design that incorporates both additive and substitutive designs to achieve a more complete understanding of the combined effects of multiple predator species.     

Intraguild predation in biological control: consideration of multiple resource species

Theoretical models of intraguild predation (IGP) predict that IGP decreases the effectiveness of biological control while many empirical studies do not agree with this prediction. In this study, I discuss the importance of explicit consideration of multiple resource species that has been neglected in most theoretical IGP models. In the previous models of IGP, a single resource species represented the pest species. However, there are multiple resource species (e.g., multiple pest species or aggregates of pest and non-pest species) in real systems. This study shows that models with multiple resource species can predict a variety of outcomes including those consistent with the empirical observations. The explicit consideration of resource species is useful for the future development of theories in biological control. Handling Editor: Helen Roy     

Estimating the prevalence and strength of non-independent predator effects

Understanding whether multiple predator species have independent effects on shared prey is critical for understanding community dynamics. We describe the prevalence and strength of non-independence between predators by quantifying the prey’s risk of predation and the degree to which it deviates from the risk predicted from a null model of independent predator effects. Specifically, we document how frequently non-independent effects occur among ten different multiple predator combinations with mayfly larvae as prey. These predator combinations vary both predator density and predator species richness. Overall, the predator effects were non-independent and translated to an average of 27% fewer prey being consumed compared to independent predator effects. Non-independence of this magnitude is likely to have population level consequences for the prey and influence the distribution or prey preference of predators. Closer inspection shows that much of the risk reduction in this system is weak, to the point of being indistinguishable from independent predator effects, while few effects are strong. This pattern of many weak interactions and few strong ones parallels the pattern of interaction strengths documented previously in intertidal communities. Consequently, understanding strong interactors in multiple predator systems may help us understand the importance of a species.     

Does aggregation benefit bark beetles by diluting predation? Links between a group‐colonisation strategy and the absence of emergent multiple predator effects

Abstract. 1. Aggregation in bark beetles (Coleoptera: Scolytidae) aids in mate attraction and resource procurement when colonising well‐defended plants; however, some species colonise primarily poorly defended plants, and intraspecific competition increases mortality. The hypothesis that decreased risk of predation was a potential benefit to aggregation in such circumstances was tested, using the pine engraver, Ips pini (Say) and its two major predators Thanasimus dubius (F.) (Coleoptera: Cleridae) and Platysoma cylindrica (Paykull) (Coleoptera: Histeridae). Both single‐ and multiple‐predator effects, across a range of prey densities, were tested. 2. Both male and female colonisation events increased with herbivore density, in an asymptotic fashion. 3. Predators decreased the number of colonisers in a density‐dependent manner, consistent with a type II functional response. 4. The proportional impact of predators decreased with increased herbivore colonisation densities. These findings indicate that predator dilution may be a viable benefit to aggregation. 5. Total emergence of the herbivore also increased with density, although the net replacement rate during one generation was independent of initial arrival density. This was likely due to larval predation, which negates potential relationships between per capita reproductive success and establishment density. 6. Each predator species decreased I. pini's net replacement rate by approximately 42%, and their combined effect was approximately 70%. 7. Overall, these predators modified their prey's establishment and adult mortality relationships in additive manners. This is somewhat surprising, given the potential for emergent effects due to interactions between multiple predators foraging within a common habitat. The persistence of additivity, rather than risk reduction or enhancement to the prey, may increase the predator‐swamping benefit to aggregation for this herbivore. 8. The effects of these predators are substitutable, and likely exert equivalent selective pressures to mask signals at the whole‐plant level.     

Habitat structural complexity mediates the foraging success of multiple predator species

We investigated the role of freshwater macrophytes as refuge by testing the hypothesis that predators capture fewer prey in more dense and structurally complex habitats. We also tested the hypothesis that habitat structure not only affects the prey-capture success of a single predator in isolation, but also the effectiveness of two predators combined, particularly if it mediates interactions between the predators. We conducted a fully crossed four-factorial laboratory experiment using artificial plants to determine the separate quantitative (density) and qualitative (shape) components of macrophyte structure on the prey-capture success of a predatory damselfly, Ischnura heterosticta tasmanica, and the southern pygmy perch, Nannoperca australis. Contrary to our expectations, macrophyte density had no effect on the prey-capture success of either predator, but both predators were significantly less effective in the structurally complex Myriophyllum analogue than in the structurally simpler Triglochin and Eleocharis analogues. Furthermore, the greater structural complexity of Myriophyllum amplified the impact of the negative interaction between the predators on prey numbers; the habitat use by damselfly larvae in response to the presence of southern pygmy perch meant they captured less prey in Myriophyllum. These results demonstrate habitat structure can influence multiple predator effects, and support the mechanism of increased prey refuge in more structurally complex macrophytes.     

Multiple predator effects result in risk reduction for prey across multiple prey densities

Investigating how prey density influences a prey’s combined predation risk from multiple predator species is critical for understanding the widespread importance of multiple predator effects. We conducted experiments that crossed six treatments consisting of zero, one, or two predator species (hellgrammites, greenside darters, and creek chubs) with three treatments in which we varied the density of mayfly prey. None of the multiple predator effects in our system were independent, and instead, the presence of multiple predator species resulted in risk reduction for the prey across both multiple predator combinations and all three levels of prey density. Risk reduction is likely to have population-level consequences for the prey, resulting in larger prey populations than would be predicted if the effects of multiple predator species were independent. For one of the two multiple predator combinations, the magnitude of risk reduction marginally increased with prey density. As a result, models predicting the combined risk from multiple predator species in this system will sometimes need to account for prey density as a factor influencing per-capita prey death rates.     

Emergent multiple predator effects in an experimental microbial community

Studies on multiple predator effects have typically focused on metazoans. Here we examined the effects of multiple consumers on bacteria. Specifically, we investigated the separate and combined effects of two common bacterivorous ciliates, Colpidium striatum and Paramecium caudatum, on a simple bacterial assemblage. Non-additive multiple predator effects emerged for all bacterial species significantly affected by grazing, where bacterial responses in the two-consumer treatment cannot be predicted by summing the separate effects of the two consumers. Some species showed risk reduction (observed responses less than expected), whereas others showed risk enhancement (observed responses larger than expected). We attributed risk alteration to the interference between the two consumers. Contradictory to theoretical predictions, total bacterial abundance in the two-consumer treatment did not differ from single-consumer treatments and consumer-free controls, due largely to risk reduction and compensatory responses within the bacterial assemblage. Decomposition of particulate organic matter was greater in the two-consumer treatment than the Paramecium single-consumer treatment, but did not differ among other treatments. These results suggest that the presence of multiple consumers may have unexpected impacts on the structure and functioning of bacterial communities.     

Predator diversity and density affect levels of predation upon strongly interactive species in temperate rocky reefs

Indirect effects of predators in the classic trophic cascade theory involve the effects of basal species (e.g. primary producers) mediated by predation upon strongly interactive consumers (e.g. grazers). The diversity and density of predators, and the way in which they interact, determine whether and how the effects of different predators on prey combine. Intraguild predation, for instance, was observed to dampen the effects of predators on prey in many ecosystems. In marine systems, species at high trophic levels are particularly susceptible to extinction (at least functionally). The loss of such species, which is mainly attributed to human activities (mostly fishing), is presently decreasing the diversity of marine predators in many areas of the world. Experimental studies that manipulate predator diversity and investigate the effects of this on strongly interactive consumers (i.e. those potentially capable of causing community-wide effects) in marine systems are scant, especially in the rocky sublittoral. I established an experiment that utilised cage enclosures to test whether the diversity and density of fish predators (two sea breams and two wrasses) would affect predation upon juvenile and adult sea urchins, the most important grazers in Mediterranean sublittoral rocky reefs. Changes in species identity (with sea breams producing major effects) and density of predators affected predation upon sea urchins more than changes in species richness per se. Predation upon adult sea urchins decreased in the presence of multiple predators, probably due to interference competition between sea breams and wrasses. This study suggests that factors that influence both fish predator diversity and density in Mediterranean rocky reefs (e.g. fishing and climate change) may have the potential to affect the predators' ability to control sea urchin population density, with possible repercussions for the whole benthic community structure.     

Non-lethal effects of predation in birds

Predators can affect individual fitness and population and community processes through lethal effects (direct consumption or ‘density’ effects), where prey is consumed, or through non‐lethal effects (trait‐mediated effects or interactions), where behavioural compensation to predation risk occurs, such as animals avoiding areas of high predation risk. Studies of invertebrates, fish and amphibians have shown that non‐lethal effects may be larger than lethal effects in determining the behaviour, condition, density and distribution of animals over a range of trophic levels. Although non‐lethal effects have been well described in the behavioural ecology of birds (and also mammals) within the context of anti‐predation behaviour, their role relative to lethal effects is probably underestimated. Birds show many behavioural and physiological changes to reduce direct mortality from predation and these are likely to have negative effects on other aspects of their fitness and population dynamics, as well as affecting the ecology of their own prey and their predators. As a consequence, the effects of predation in birds are best measured by trade‐offs between maximizing instantaneous survival in the presence of predators and acquiring or maintaining resources for long‐term survival or reproduction. Because avoiding predation imposes foraging costs, and foraging behaviour is relatively easy to measure in birds, the foraging–predation risk trade‐off is probably an effective framework for understanding the importance of non‐lethal effects, and so the population and community effects of predation risk in birds and other animals. Using a trade‐off approach allows us to predict better how changes in predator density will impact on population and community dynamics, and how animals perceive and respond to predation risk, when non‐lethal effects decouple the relationship between predator density and direct mortality rate. The trade‐off approach also allows us to identify where predation risk is structuring communities because of avoidance of predators, even when this results in no observable direct mortality rate.     

The functions of plant feeding in the omnivorous predator Dicyphus hesperus: water places limits on predation

1. Dicyphus hesperus Knight (Heteroptera: Miridae) nymphs were fed from egg hatch to the adult stage on Ephestia kuehniella eggs provided either alone or in combination with tomato leaves or with a supplementary water source. 2. Only 6% of individuals completed nymphal development on a diet of eggs alone. In contrast, a high proportion of nymphs completed development on a diet of eggs when either tomato leaves (97%) or a supplementary water source (88%) were provided. 3. The development times of nymphs given access to leaves were significantly shorter than those of nymphs given access only to supplementary water. 4. Adult female D. hesperus that were given access to tomato leaves prior to feeding trials consumed significantly more eggs in a 4‐h period than females that were dehydrated before trials. Dehydrated females that were allowed access to water for 3 h before trials consumed an intermediate number of eggs. 5. Plant feeding or access to some other water source is required for prey feeding, growth, and development in D. hesperus, and acquisition of water is proposed as a primary function of plant feeding. In addition, D. hesperus derives nutrients from plant feeding that increase the rate of nymphal development, although nymphs cannot complete development when provided only with tomato leaves. 6. Three simple models are presented of feeding behaviour in predatory Heteroptera where the amount of plant feeding either decreases, increases, or is constant as a function of the amount of prey feeding. The models are discussed with reference to the results and the probable multifunctional nature of plant feeding in predatory Heteroptera.     

Diel variation in predator abundance, predation risk and prey distribution in shallow-water estuarine habitats

Predation by visual predators is often affected by light conditions and may therefore exhibit strong diel variation. The dominant predators on grass shrimp, Palaemonetes pugio, are finfish predators that are thought to locate their prey by visual cues. We examined the response of grass shrimp to diel variation in predation risk in the nearshore shallow waters of the Chesapeake Bay. We used diel shoreline seines to assess the relative abundance of predators. We assessed the relative risk of predation with shrimp tethered at refuge (30 cm) and nonrefuge (60 cm) depths. To measure grass shrimp response to predation risk, we used dipnets to monitor habitat use. Four predominantly visual predators dominated the shoreline seine catches, Fundulus heteroclitus, Micropogonias undulatus, Morone americana and Morone saxatilis. Total predator abundance had a diel component, with dramatic nighttime decreases in total abundance, whereas guild composition and relative abundance remained unchanged. Relative predation risk for tethered shrimp exhibited significant time by habitat interaction. During the day, depth negatively affected survivorship of tethered shrimp while at night overall survivorship increased and there was no effect of depth. Shrimp habitats use reflected diel predation risks. Abundances in the near shore were highest during the day with decreased abundances at night. Together, the seine and tethering data highlight the importance for a refuge (e.g., shallow water) from predation during the daytime and a relaxation of predation pressure at night.     

Density-dependent effects of multiple predators sharing a common prey in an endophytic habitat

Multiple predator species feeding on a common prey can lead to higher or lower predation than would be expected by simply combining their individual effects. Such emergent multiple predator effects may be especially prevalent if predators share feeding habitat. Despite the prevalence of endophagous insects, no studies have examined how multiple predators sharing an endophytic habitat affect prey or predator reproduction. We investigated density-dependent predation of Thanasimus dubius (Coleoptera: Cleridae) and Platysoma cylindrica (Coleoptera: Histeridae) on a bark beetle prey, Ips pini (Coleoptera: Scolytidae), in a laboratory assay. I. pini utilize aggregation pheromones to group-colonize and reproduce within the stems of conifers. T. dubius and P. cylindrica exploit these aggregation pheromones to arrive simultaneously with the herbivore. Adult T. dubius prey exophytically, while P. cylindrica adults enter and prey within the bark beetle galleries. Larvae of both predators prey endophytically. We used a multiple regression analysis, which avoids confounding predator composition with density, to examine the effects of varying predator densities alone and in combination on herbivore establishment, herbivore reproduction, and predator reproduction. Predators reduced colonization success by both sexes, and decreased I. pini reproduction on a per male and per female basis. The combined effects of these predators did not enhance or reduce prey establishment or reproduction in unexpected manners, and these predators were entirely substitutable. The herbivores net replacement rate was never reduced significantly below one at prey and predator densities emulating field conditions. Similar numbers of each predator species emerged from the logs, but predator reproduction suffered from high intraspecific interference. The net replacement rate of P. cylindrica was not affected by conspecifics or T. dubius. In contrast, the net replacement rate of T. dubius decreased with the presence of conspecifics or P. cylindrica. Combinations of both predators led to an emergent effect, a slightly increased net replacement rate of T. dubius. This may have been due to predation by larval T. dubius on pupal P. cylindrica, as P. cylindrica develops more rapidly than T. dubius within this shared habitat.     

Sequential predator effects across three life stages of the African tree frog, <Emphasis Type="Italic">Hyperolius spinigularis</Emphasis>

While theoretical studies of the timing of key switch points in complex life cycles such as hatching and metamorphosis have stressed the importance of considering multiple stages, most empirical work has focused on a single life stage. However, the relationship between the fitness components of different life stages may be complex. Ontogenetic switch points such as hatching and metamorphosis do not represent new beginnings—carryover effects across stages can arise when environmental effects on the density and/or traits of early ontogenetic stages subsequently alter mortality or growth in later stages. In this study, I examine the effects of egg- and larval-stage predators on larval performance, size at metamorphosis, and post-metamorphic predation in the African tree frog Hyperolius spinigularis. I monitored the density and survival of arboreal H. spinigularis clutches in the field to estimate how much egg-stage predation reduced the input of tadpoles into the pond. I then conducted experiments to determine: (1) how reductions in initial larval density due to egg predators affect larval survival and mass and age at metamorphosis in the presence and absence of aquatic larval predators, dragonfly larvae, and (2) how differences in mass or age at metamorphosis arising from predation in the embryonic and larval environments affect encounters with post-metamorphic predators, fishing spiders. Reduction in larval densities due to egg predation tended to increase per capita larval survival, decrease larval duration and increase mass at metamorphosis. Larval predators decreased larval survival and had density-dependent effects on larval duration and mass at metamorphosis. The combined effects of embryonic and larval-stage predators increased mass at metamorphosis of survivors by 91%. Larger mass at metamorphosis may have immediate fitness benefits, as larger metamorphs had higher survival in encounters with fishing spiders. Thus, the effects of predators early in ontogeny can alter predation risk even two life stages later.     

Predicting the incidence of mohua predation from the seedfall,mouse, and predator fluctuations in beech forests

Abstract

Predator control will be required to save many mohua (Mohoua ochrocephala) populations from extinction. However, control may be required only in years when stoat (Mustela erminea) densities are high. To manage local stoat populations effectively, a reliable predictor of high risk years is required. We examined whether different levels of beech seedfall and mouse capture rates were related to the levels of mohua predation recorded in the Hawdon Valley, Arthur's Pass National Park, and the Eglinton Valley, Fiordland National Park, between 1989 and 1994. During this period there was only one full beech mast year in each study area during autumn. The full mast seedfall in Hawdon Valley was predominantly of mountain beech (Nothofagus solandri var. cliffortioides) and red beech (N. fused), and in Eglinton Valley it was predominantly silver beech (TV. menziesii). During the following summer, mouse and stoat densities, and the predation rate of adult mohua, all increased considerably. There was very little predation on adult mohua in the summers following poor seedfalls when mouse and predator densities remained low. In 1993, a partial mast did not trigger a mouse or stoat irruption.

We conclude that counts of beech seedfall and indices of mouse density are potential predictors of an impending irruption of key predators. Winter mouse density appeared to be the most reliable indicator, because neither stoats nor mice respond to seedfall alone. A combination of these indicators could be used as a basis for management decisions on whether to undertake stoat control to protect mohua populations in the future. However, more information is required on the seedfall thresholds that may trigger sufficient increases in mouse and stoat numbers and, consequently, bird predation.