Predator functional response and prey survival: direct and indirect interactions affecting a marked prey population

1. Predation plays an integral role in many community interactions, with the number of predators and the rate at which they consume prey (i.e. their functional response) determining interaction strengths. Owing to the difficulty of directly observing predation events, attempts to determine the functional response of predators in natural systems are limited. Determining the forms that predator functional responses take in complex systems is important in advancing understanding of community interactions. 2. Prey survival has a direct relationship to the functional response of their predators. We employed this relationship to estimate the functional response for bald eagle Haliaeetus leucocepalus predation of Canada goose Branta canadensis nests. We compared models that incorporated eagle abundance, nest abundance and alternative prey presence to determine the form of the functional response that best predicted intra-annual variation in survival of goose nests. 3. Eagle abundance, nest abundance and the availability of alternative prey were all related to predation rates of goose nests by eagles. There was a sigmoidal relationship between predation rate and prey abundance and prey switching occurred when alternative prey was present. In addition, predation by individual eagles increased as eagle abundance increased. 4. A complex set of interactions among the three species examined in this study determined survival rates of goose nests. Results show that eagle predation had both prey- and predator-dependent components with no support for ratio dependence. In addition, indirect interactions resulting from the availability of alternative prey had an important role in mediating the rate at which eagles depredated nests. As a result, much of the within-season variation in nest survival was due to changing availability of alternative prey consumed by eagles. 5. Empirical relationships drawn from ecological theory can be directly integrated into the estimation process to determine the mechanisms responsible for variation in observed survival rates. The relationship between predator functional response and prey survival offers a flexible and robust method to advance our understanding of predator-prey interactions in many complex natural systems where prey populations are marked and regularly visited.     

Intuition, functional responses and the formulation of predator-prey models when there is a large disparity in the spatial domains of the interacting species

1. The disparity of the spatial domains used by predators and prey is a common feature of many terrestrial avian and mammalian predatory interactions, as predators are typically more mobile and have larger home ranges than their prey. 2. Incorporating these realistic behavioural features requires formulating spatial predator-prey models having local prey mortality due to predation and its spatial aggregation, in order to generate a numerical response at timescales longer than the local prey consumption. Coupling the population dynamics occurring at different spatial scales is far from intuitive, and involves making important behavioural and demographic assumptions. Previous spatial predator-prey models resorted to intuition to derive local functional responses from non-spatial equivalents, and often involve unrealistic biological assumptions that restrict their validity. 3. We propose a hierarchical framework for deriving generic models of spatial predator-prey interactions that explicitly considers the behavioural and demographic processes occurring at different spatial and temporal scales. 4. The proposed framework highlights the circumstances wherein static spatial patterns emerge and can be a stabilizing mechanism of consumer-resource interactions.     

A synthesis of subdisciplines: predator–prey interactions, and biodiversity and ecosystem functioning

The last 15 years has seen parallel surges of interest in two research areas that have rarely intersected: biodiversity and ecosystem functioning (BEF), and multispecies predator–prey interactions (PPI). Research addressing role of biodiversity in ecosystem functioning has focused primarily on single trophic‐level systems, emphasizing additive effects of diversity that manifest through resource partitioning and the sampling effect. Conversely, research addressing predator–prey interactions has focused on two trophic‐level systems, emphasizing indirect and non‐additive interactions among species. Here, we use a suite of consumer‐resource models to organize and synthesize the ways in which consumer species diversity affects the densities of both resources and consumer species. Specifically, we consider sampling effects, resource partitioning, indirect effects caused by intraguild interactions and non‐additive effects. We show that the relationship between consumer diversity and the density of resources and consumer species are broadly similar for systems with one vs. two trophic levels, and that indirect and non‐additive interactions generally do little more than modify the impacts of diversity established by the sampling effect and resource partitioning. The broad similarities between systems with one vs. two trophic levels argue for greater communication between researchers studying BEF, and researchers studying multispecies PPI.     

Prey DNA detection success following digestion by intraguild predators: influence of prey and predator species

Intraguild predation (IGP) has been increasingly recognized as an important interaction in ecological systems over the past two decades, and remarkable insights have been gained into its nature and prevalence. We have developed a technique using molecular gut-content analysis to compare the rate of IGP between closely related species of coccinellid beetles (lady beetles or ladybirds), which had been previously known to prey upon one another. We first developed PCR primers for each of four lady beetle species: Harmonia axyridis, Coccinella septempunctata, Coleomegilla maculata and Propylea quatuordecimpunctata. We next determined the prey DNA detection success over time (DS(50) ) for each combination of interacting species following a meal. We found that DS(50) values varied greatly between predator-prey combinations, ranging from 5.2 to 19.3 h. As a result, general patterns of detection times based upon predator or prey species alone are not discernable. We used the DS(50) values to correct field data to demonstrate the importance of compensation for detection times that are specific to particular predator-prey combinations.     

Scaling up the functional response for spatially heterogeneous systems

Scale transition theory is a framework for predicting regional population dynamics from local process functions and estimates of spatial heterogeneity. Using this framework, we estimated regional scale functional responses for a benthic predator–prey system in the Baltic Sea. Functional responses were based on laboratory experiments or field observations of stomach contents, and prey densities measured at a local scale (0.1 m²) or a regional scale (300 km²). Laboratory data overestimated consumption at high prey densities, whereas predictions based on local scale data tallied closely with consumption observed at the regional scale. The predicted regional functional response was different for increasing and decreasing prey densities, reflecting that predator and prey densities, as well as the covariance between them, exhibit oscillatory dynamics. We conclude that it is important to validate laboratory data with small-scale field observations and that scale transition is a powerful tool for scaling-up process functions in heterogeneous systems.     

Health food versus fast food: the effects of prey quality and mobility on prey selection by a generalist predator and indirect interactions among prey species

1. In order to understand the relative importance of prey quality and mobility in indirect interactions among alternative prey that are mediated by a shared natural enemy, the nutritional quality of two common prey for a generalist insect predator along with the predator's relative preference for these prey was determined. 2. Eggs of the corn earworm Helicoverpa zea (Lepidoptera: Noctuidae) were nutritionally superior to pea aphids Acyrthosiphum pisum (Homoptera: Aphididae) as prey for big‐eyed bugs Geocoris punctipes (Heteroptera: Geocoridae). Big‐eyed bugs survived four times as long when fed corn earworm eggs than when fed pea aphids. Furthermore, only big‐eyed bugs fed corn earworm eggs completed development and reached adulthood. 3. In two separate choice experiments, however, big‐eyed bugs consistently attacked the nutritionally inferior prey, pea aphids, more frequently than the nutritionally superior prey, corn earworm eggs. 4. Prey mobility, not prey nutritional quality, seems to be the most important criterion used by big‐eyed bugs to select prey. Big‐eyed bugs attacked mobile aphids preferentially when given a choice between mobile and immobilised aphids. 5. Prey behaviour also mediated indirect interactions between these two prey species. The presence of mobile pea aphids as alternative prey benefited corn earworms indirectly by reducing the consumption of corn earworm eggs by big‐eyed bugs. The presence of immobilised pea aphids, however, did not benefit corn earworms indirectly because the consumption of corn earworm eggs by big‐eyed bugs was not reduced when they were present. 6. These results suggest that the prey preferences of generalist insect predators mediate indirect interactions among prey species and ultimately affect the population dynamics of the predator and prey species. Understanding the prey preferences of generalist insect predators is essential to predict accurately the efficacy of these insects as biological control agents.     

Predator diversity and the functioning of ecosystems: the role of intraguild predation in dampening trophic cascades

Single trophic‐level studies of the relationship between biodiversity and ecosystem functioning highlight the importance of mechanisms such as resource partitioning, facilitation, and sampling effect. In a multi‐trophic context, trophic interactions such as intraguild predation may also be an important mediator of this relationship. Using a salt‐marsh food web, we investigated the interactive effects of predator species richness (one to three species) and trophic composition (strict predators, intraguild predators, or a mixture of the two) on ecosystem functions such as prey suppression and primary production via trophic cascades. We found that the trophic composition of the predator assemblage determined the impact of increasing predator species richness on the occurrence of trophic cascades. In addition, increasing the proportion of intraguild predator species present diminished herbivore suppression and reduced primary productivity. Therefore, trophic composition of the predator assemblage can play an important role in determining the nature of the relationship between predator diversity and ecosystem function.     

Indirect effects between shared prey: Predictions for

Suppression of a target prey by a predator can depend on its surrounding community, including the presence of nontarget, alternative prey. Basic theoretical models of two prey species that interact only via a shared predator predict that adding an alternative prey should increase predator numbers and ultimately lower target pest densities as compared to when the target pest is the only prey. While this is an alluring prediction, it does not explain the numerous responses empirically observed. To better understand and predict the indirect interactions produced by shared predation, we explore how additional prey species affect three broad ecological mechanisms, the predator's reproductive, movement, and functional responses. Specifically, we review current theoretical models of shared predation by focusing on these mechanisms, and make testable predictions about the effects of shared predation. We find that target predation is likely to be higher in the two prey system because of predator reproduction, especially when: predators are prey limited, alternative or total prey density is high, or alternative prey are available over time. Target predation may also be greater because of predator movement, but only under certain movement rules and spatial distributions. Predator foraging behavior is most likely to cause lower target predation in the two-prey system, when per capita predation is limited by something other than prey availability. It is clear from this review that no single theoretical generalization will accurately predict community-level effects for every system. However, we can provide testable hypotheses for future empirical and theoretical investigations of indirect interactions and help enhance their potential use in biological control.     

Macroscopic prey remains in the winter diet of foxes Vulpes vulpes in rural Britain

• 1 The winter diet of foxes Vulpes vulpes was quantified in seven landscape types in Britain, using faecal samples from 87 sites.
• 2 Medium‐sized mammals (0.1–5.0 kg) were consistently the most important prey group in arable and pastural landscapes, occurring in 44–72% of scats and comprising 50–75% of the mass of prey ingested. Birds and small mammals (< 0.1 kg) were important secondary prey groups.
• 3 Small mammals were the most frequently recorded prey group in marginal upland (42% of scats) and upland landscapes (75%), followed by large mammals (33% and 23%, respectively). In terms of mass ingested, small mammals (38%) and large mammals (52%) were the most important prey groups in these landscapes.
• 4 In all landscapes, field voles Microtus agrestis, lagomorphs, sheep/deer and passerines/galliforms dominated their respective prey groupings.

     

Studies on functional response and prey selection using zooplankton in the anostracan Chirocephalus diaphanus Prevost, 1803

Freshwater cladocerans and rotifers were used as prey to study functional response and prey selection by adult females of Chirocephalus diaphanus under laboratory conditions. For functional response studies, we offered three rotifer species (Brachionus calyciflorus, B. patulus and Euchlanis dilatata) and three cladoceran species (Alona rectangula, Ceriodaphnia dubia and Moina macrocopa) at various densities ranging from 0.5 to 16 ind. ml^–1. We found increased zooplankton consumption with increasing prey density but beyond 4 ind ml^–1 cladocerans and 8 ind. ml^–1 rotifers, the number of animals eaten plateaued. In general, C. diaphanus consumed fewer large prey (cladocerans) and many more smaller zooplankton (rotifers). For prey selection experiments, we used B. calyciflrous, B. patulus, C. dubia and M. macrocopa, offered at the ratio of two rotifers: one cladoceran and at three prey densities (total zooplankton numbers: 3, 6 and 12 ind. ml^–1). Prey selectivity patterns followed the functional response trends. In general, regardless of prey types, with an increase in the available zooplankton, there was an increase in the number of prey consumed. At any given prey density, C. diaphanus consumed higher numbers of rotifers than cladocerans. Among the prey offered, B. patulus and M. macrocopa were positively selected. Results are discussed in light of possible control of zooplankton by anostracans in temporary ponds.     

Species on the menu of a generalist predator, the eastern red bat (Lasiurus borealis): using a molecular approach to detect arthropod prey

One of the most difficult interactions to observe in nature is the relationship between a predator and its prey. When direct observations are impossible, we rely on morphological classification of prey remains, although this is particularly challenging among generalist predators whose faeces contain mixed and degraded prey fragments. In this investigation, we used a polymerase chain reaction and sequence-based technique to identify prey fragments in the guano of the generalist insectivore, the eastern red bat ( Lasiurus borealis ), and evaluate several hypotheses about prey selection and prey defences. The interaction between bats and insects is of significant evolutionary interest because of the adaptive nature of insect hearing against echolocation. However, measuring the successes of predator tactics or particular prey defences is limited because we cannot normally identify these digested prey fragments beyond order or family. Using a molecular approach, we recovered sequences from 89% of the fragments tested, and through comparison to a reference database of sequences, we were able to identify 127 different species of prey. Our results indicate that despite the robust jaws of L. borealis , most prey taxa were softer-bodied Lepidoptera. Surprisingly, more than 60% of the prey species were tympanate, with ears thought to afford protection against these echolocating bats. Moths of the family Arctiidae, which employ multiple defensive strategies, were not detected as a significant dietary component. Our results provide an unprecedented level of detail for the study of predator–prey relationships in bats and demonstrate the advantages which molecular tools can provide in investigations of complex ecological systems and food-web relationships.     

Allometric scaling enhances stability in complex food webs

Classic local stability theory predicts that complex ecological networks are unstable and are unlikely to persist despite empiricists' abundant documentation of such complexity in nature. This contradiction has puzzled biologists for decades. While some have explored how stability may be achieved in small modules of a few interacting species, rigorous demonstrations of how large complex and ecologically realistic networks dynamically persist remain scarce and inadequately understood. Here, we help fill this void by combining structural models of complex food webs with nonlinear bioenergetic models of population dynamics parameterized by biological rates that are allometrically scaled to populations' average body masses. Increasing predator–prey body mass ratios increase population persistence up to a saturation level that is reached by invertebrate and ectotherm vertebrate predators when being 10 or 100 times larger than their prey respectively. These values are corroborated by empirical predator–prey body mass ratios from a global data base. Moreover, negative effects of diversity (i.e. species richness) on stability (i.e. population persistence) become neutral or positive relationships at these empirical ratios. These results demonstrate that the predator–prey body mass ratios found in nature may be key to enabling persistence of populations in complex food webs and stabilizing the diversity of natural ecosystems.     

Dampening prey cycle overrides the impact of climate change on predator population dynamics: a long‐term demographic study on tawny owls

Predicting the dynamics of animal populations with different life histories requires careful understanding of demographic responses to multifaceted aspects of global changes, such as climate and trophic interactions. Continent‐scale dampening of vole population cycles, keystone herbivores in many ecosystems, has been recently documented across Europe. However, its impact on guilds of vole‐eating predators remains unknown. To quantify this impact, we used a 27‐year study of an avian predator (tawny owl) and its main prey (field vole) collected in Kielder Forest (UK) where vole dynamics shifted from a high‐ to a low‐amplitude fluctuation regime in the mid‐1990s. We measured the functional responses of four demographic rates to changes in prey dynamics and winter climate, characterized by wintertime North Atlantic Oscillation (wNAO). First‐year and adult survival were positively affected by vole density in autumn but relatively insensitive to wNAO. The probability of breeding and number of fledglings were higher in years with high spring vole densities and negative wNAO (i.e. colder and drier winters). These functional responses were incorporated into a stochastic population model. The size of the predator population was projected under scenarios combining prey dynamics and winter climate to test whether climate buffers or alternatively magnifies the impact of changes in prey dynamics. We found the observed dampening vole cycles, characterized by low spring densities, drastically reduced the breeding probability of predators. Our results illustrate that (i) change in trophic interactions can override direct climate change effect; and (ii) the demographic resilience entailed by longevity and the occurrence of a floater stage may be insufficient to buffer hypothesized environmental changes. Ultimately, dampened prey cycles would drive our owl local population towards extinction, with winter climate regimes only altering persistence time. These results suggest that other vole‐eating predators are likely to be threatened by dampening vole cycles throughout Europe.     

The dynamics of prey choice in fish: the importance of prey size and satiation

Over a number of decades the process of prey choice has been investigated using fishes as model predators. Using fishes for the model has allowed the proximate factors that determine how a mobile predator finds and chooses to eat the prey encountered within a variable 3‐D environment to be estimated. During prey choice a number of constraints exist, in particular most fish predators will eat their prey whole thus their jaws and gut create functional limitations once a prey has been attacked. By considering the relationship between the size of the prey and the predator's feeding apparatus and feeding motivation this study explores the link between mechanistic studies and theoretical, optimal foraging based predictions. How the prediction of prey choices made by the fish following prey encounter can be reconciled with what is likely to be found in the fish's stomach is discussed. This study uses a progression of empirical examples to illustrate how the limits of functional constraints and prey choice at different stages of motivation to feed can be taken into account to improve predictions of predator prey choice.     

Predation of Colorado potato beetle eggs by a polyphagous ladybeetle in the presence of alternate prey: potential impact on resistance evolution

The influence of prey choice on the predation of a target prey item by a polyphagous insect predator was investigated in field plot studies. The target prey consisted of eggs of the Colorado potato beetle (CPB), Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae), and the predator was the 12‐spotted ladybeetle, Coleomegilla maculata Lengi (Coleoptera: Coccinellidae). Eggs of the European corn borer (ECB), Ostrinia nubilalis Hübner (Lepidoptera: Pyralidae), and nymphs and adults of the green peach aphid, Myzus persicae Sulzer (Homoptera: Aphididae), comprised the alternative prey choices. The objectives of these studies were to: (1) examine predation in a multiprey scenario likely to occur in an agroecosystem, and (2) use the data to simulate the impact of predator‐induced mortality on the evolution of resistance to Bt‐transgenic plants in the target herbivore. Simulations of the rate of resistance evolution were carried out using a deterministic genetic model. Experiments were performed using potato field plots planted in a manner reflecting a 25% or 50% non‐transgenic refuge. CPB eggs were infested so as to mimic the densities of resistant and susceptible populations that might occur in commercial Bt‐transgenic plantings. Densities of predators and alternate prey species were chosen to represent those that might typically occur in potato crops in the eastern USA. Simulation results indicated that when ECB eggs were present, predation on CPB eggs either became inversely spatially density‐dependent, or increased significantly in a density‐dependent manner. When aphids were present, predation became positively density‐dependent. Model simulations predicted that ECB egg presence is beneficial, in that resistance was delayed by up to 40 pest generations (as compared to the scenario with CPB as the only prey), while aphid presence accelerated resistance evolution by 18 generations. Results suggest that resistance management strategies should take into account the composition of prey species available to generalist predators typically present, so as to best delay pest adaptation to Bt‐toxins.     

The anatomy of predator-prey dynamics in a changing climate

Humans are increasingly influencing global climate and regional predator assemblages, yet a mechanistic understanding of how climate and predation interact to affect fluctuations in prey populations is currently lacking. Here we develop a modelling framework to explore the effects of different predation strategies on the response of age-structured prey populations to a changing climate. We show that predation acts in opposition to temporal correlation in climatic conditions to suppress prey population fluctuations. Ambush predators such as lions are shown to be more effective at suppressing fluctuations in their prey than cursorial predators such as wolves, which chase down prey over long distances, because they are more effective predators on prime-aged adults. We model climate as a Markov process and explore the consequences of future changes in climatic autocorrelation for population dynamics. We show that the presence of healthy predator populations will be particularly important in dampening prey population fluctuations if temporal correlation in climatic conditions increases in the future.     

Tracking the role of alternative prey in soybean aphid predation by Orius insidiosus: a molecular approach

The soybean aphid, Aphis glycines (Hemiptera: Aphididae), is a pest of soybeans in Asia, and in recent years has caused extensive damage to soybeans in North America. Within these agroecosystems, generalist predators form an important component of the assemblage of natural enemies, and can exert significant pressure on prey populations. These food webs are complex and molecular gut-content analyses offer nondisruptive approaches for examining trophic linkages in the field. We describe the development of a molecular detection system to examine the feeding behaviour of Orius insidiosus (Hemiptera: Anthocoridae) upon soybean aphids, an alternative prey item, Neohydatothrips variabilis (Thysanoptera: Thripidae), and an intraguild prey species, Harmonia axyridis (Coleoptera: Coccinellidae). Specific primer pairs were designed to target prey and were used to examine key trophic connections within this soybean food web. In total, 32% of O. insidiosus were found to have preyed upon A. glycines, but disproportionately high consumption occurred early in the season, when aphid densities were low. The intensity of early season predation indicates that O. insidiosus are important biological control agents of A. glycines, although data suggest that N. variabilis constitute a significant proportion of the diet of these generalist predators. No Orius were found to contain DNA of H. axyridis, suggesting intraguild predation upon these important late-season predators during 2005 was low. In their entirety, these results implicate O. insidiosus as a valuable natural enemy of A. glycines in this soybean agroecosystem.     

Modulation of microbial predator-prey dynamics by phosphorus availability: growth patterns and survival strategies of bacterial phylogenetic clades

We simultaneously studied the impact of top-down (protistan grazing) and bottom-up (phosphorus availability) factors on the numbers and biomasses of bacteria from various phylogenetic lineages, and on their growth and activity parameters in the oligo-mesotrophic Piburger See, Austria. Enhanced grazing resulted in decreased proportions of bacteria with high nucleic acid content (high-NA bacteria) and lower detection rates by FISH. There was a change in the composition of the bacterial assemblage, whereby Betaproteobacteria were heavily grazed while Alphaproteobacteria and Cytophaga-Flavobacterium-Bacteroides were less affected by predators. Changes in bacterial assemblage composition were also apparent in the treatments enriched with phosphorus, and even more pronounced in the incubations in dialysis tubes (allowing relatively free nutrient exchange). Here, Betaproteobacteria became dominant and appeared to act as successful opportunistic competitors for nutrients. In contrast, Actinobacteria did not respond to surplus phosphorus by population growth, and, moreover, maintained their small size, which resulted in a very low biomass contribution. In addition, significant relationships between high-NA bacteria and several bacterial phylogenetic clades were found, indicating an enhanced activity status. By combining several single-cell methods, new insight is gained into the competitive abilities of freshwater bacteria from a variety of phylogenetic lineages under contrasting sets of bottom-up and top-down constraints.