Effects of alternative prey on predation by small mammals on gypsy moth pupae

Previous work shows that predation by small mammals is a dominant cause of mortality of low-density gypsy moths in North America and that declines in small mammal density result in increases in gypsy moth density. Here we examined whether predation by small mammals is density dependent by way of a type III functional response, and how predation is influenced by alternative prey. First we showed that the preference of predators for gypsy moth pupae was low compared to other experimental prey items, such as mealworm pupae and sunflower seeds. Predation on gypsy moth pupae was characterized by a type II functional response with percent predation highest at the lowest prey densities, whereas the functional response to sunflower seeds was characterized by a type III functional response in which predation increased with increasing prey density. These results suggest that predation by small mammals is unlikely to stabilize low-density gypsy moth populations.     

Body masses,functional responses and predator–prey stability

The stability of ecological communities depends strongly on quantitative characteristics of population interactions (type‐II vs. type‐III functional responses) and the distribution of body masses across species. Until now, these two aspects have almost exclusively been treated separately leaving a substantial gap in our general understanding of food webs. We analysed a large data set of arthropod feeding rates and found that all functional‐response parameters depend on the body masses of predator and prey. Thus, we propose generalised functional responses which predict gradual shifts from type‐II predation of small predators on equally sized prey to type‐III functional‐responses of large predators on small prey. Models including these generalised functional responses predict population dynamics and persistence only depending on predator and prey body masses, and we show that these predictions are strongly supported by empirical data on forest soil food webs. These results help unravelling systematic relationships between quantitative population interactions and large‐scale community patterns.     

Consequences of refuge for the functional response of Dermestes ater (Coleoptera: Dermestidae) to Musca domestica (Diptera: Muscidae)

It is well known that a predator has the potential to regulate a prey population only if the predator responds to increases in prey density and inflicts greater mortality rates. Predators may cause such density-dependent mortality depending on the nature of the functional and numerical responses. Yet, few studies have examined the relationship between the addition of refuges and the characteristic of functional response fits. We investigated whether addition of a refuge changed the type of functional response exhibited by Dermestes ater on Musca domestica, comparing the inherent ability of D. ater to kill houseflies in the absence and in the presence of refuge. An additional laboratory experiment was also carried out to assess handling and searching times exhibited by D. ater. Logistic regression analyses revealed a type III functional response for predator–prey interaction without refuge, and results were described by the random predator equation. The mean number of prey killed did not differ between experimental habitats, indicating that the addition of refuge did not inhibit predation. However, predators that interacted with prey without refuge spent less time searching for prey at higher densities, increasing predatory interaction. We concluded that this interaction may be weak, because data from experiments with refuge fitted poorly to models. However, the high variability and the nonsignificance of the data from the experiment with refuge show the importance of refuge for promoting spatial heterogeneity, which may prevent prey extinction.     

Effect of prey size on attack components of the functional response by Notonecta undulata

The number of encounters per prey, the proportion of encounters resulting in attacks, and the proportion of attacks that were successful were observed while fourth-instar Notonecta undulata nymphs preyed on smaller N. undulata nymphs. While encounters per prey and proportion of encounters resulting in attacks increased with prey size, the proportion of attacks that were successful decreased. The increase in encounter rate per prey was due in part to an increase in the predator's reactive distance to prey as prey size increased. While none of the attack parameters varied significantly with prey density, logarithmic regression of the number of encounters per unit search time on prey density suggested that prey density tends to have a positive effect on encounters per first-instar prey but a negative effect on encounters per second-instar prey. A functional response model is presented that incorporates components of the predator's attack rate as exponential functions of prey density and allows for effects of the time the predator may spend evaluating prey encountered but not attacked and time spent attacking prey not captured. Estimates of the attack parameters derived from the experimental data are used in the model to generate functional response curves for fourth-instar N. undulata preying on first- or second-instar conspecifics. The predicted curve for second-instar prey is typical type II but the curve for firstinstar prey is slightly positively density dependent at low prey densities, i.e., type III.     

Impacts of predation on dynamics of age-structured prey: Allee effects and multi-stability

With a series of mathematical models, we explore impacts of predation on a prey population structured into two age classes, juveniles and adults, assuming generalist, age-specific predators. Predation on any age class is either absent, or represented by types II or III functional responses, in various combinations. We look for Allee effects or more generally for multiple stable steady states in the prey population. One of our key findings is the occurrence of a predator pit (low-density ??refuge?? state of prey induced by predation; the chance of escaping predation thus increases both below and above an intermediate prey density) when only one age class is consumed and predators use a type II functional response ??this scenario is known to occur for an unstructured prey consumed via a type III functional response and can never occur for an unstructured prey consumed via a type II one. In the case where both age classes are consumed by type II generalist predators, an Allee effect occurs frequently, but some parameters give also rise to a predator pit and even three stable equilibria (one extinction equilibrium and two positive ones??Allee effect and predator pit combined). Multiple positive stable equilibria are common if one age class is consumed via a type II functional response and the other via a type III functional response??here, in addition to the behaviours mentioned above one may even observe three stable positive equilibria????double?? predator pit. Some of these results are discussed from the perspective of population management.     

Estimation and testing with overdispersed proportions using the beta-logistic regression model of Heckman and Willis

Methods are presented for modeling dose-related effects in proportion data when extra-binomial variability is a concern. Motivation is taken from experiments in developmental toxicology, where similarity among conceptuses within a litter leads to intralitter correlations and to overdispersion in the observed proportions. Appeal is made to the well-known beta-binomial distribution to represent the overdispersion. From this, an exponential function of the linear predictor is used to model the dose-response relationship. The specification was introduced previously for econometric applications by Heckman and Willis; it induces a form of logistic regression for the mean response, together with a reciprocal biexponential model for the intralitter correlation. Large-sample, likelihood-based methods for estimating and testing the joint proportion-correlation response are studied. A developmental toxicity data set illustrates the methods.     

How can the functional reponse best be determined?

Summary We evaluated three methods for the analysis of functional response data by asking whether a given method could discriminate among functional responses and whether it could accurately identify regions of positive density-dependent predation. We evaluated comparative curve fitting with foraging models, linear least-squares analysis using the angular transformation, and logit analysis. Using data from nature and simulations, we found that the analyses of predation rates with the angular transformation and logit analysis were best at consistently determining the true functional response, i.e. the model used to generate simulated data. These methods also produced the most accurate estimates of the true regions of density dependence. Of these two methods, functional response data best fulfill the assumptions of logit analysis. Angularly transformed predation rates only approximate the assumptions of linear leastsquares analysis for predation rates between 0.1 and 0.9. Lack-of-fit statistics can reveal inadequate fit of a model to a data set where simple regression statistics might erroneously suggest a good match.     

How predation by Podisus nigrispinus is influenced by developmental stage and density of its prey Alabama argillacea

The functional response of a predator to the density of its prey is affected by several factors, including the prey's developmental stage. This study evaluated the functional response of Podisus nigrispinus (Dallas) (Hemiptera: Heteroptera: Pentatomidae) females to fourth instars and pupae of Alabama argillacea (Hübner) (Lepidoptera: Noctuidae), an important pest of cotton (Gossypium hirsutum L., Malvaceae) in Brazil. The prey were exposed to the predator for 12 and 24 h, and in densities of 1, 6, 12, 18, 24, and 30 items per predator female. The predation data were subjected to polynomial regression logistic analysis to determine the type of functional response. Holling and Rogers' equations were used to estimate parameters such as attack rate and handling time. Podisus nigrispinus females showed functional response types II and III by preying on larvae and pupae, respectively. The attack rate and handling time did not differ between the 12 and 24 h exposure times. Predation rate was higher at higher larval and pupal densities; predation was highest at a density of 30 prey items per female, and it was similar at 18 and 24 prey per predator. Understanding the interaction of predators and their food resources helps to optimize biological control strategies. It also helps the decision‐making and the improvement of release techniques of P. nigrispinus in the field.     

The functional response of a predatory plant preying on swarming zooplankton

In a laboratory study, we determined the functional response of the carnivorous aquatic plant Utricularia vulgaris feeding on Polyphemus pediculus, a cladoceran zooplankton that forms swarms. The number of prey eaten increased linearly with prey density up to a density of 35 prey per 125 ml and decreased slightly above this density. Independent estimates of handling time showed that the number eaten was not limited by handling. Thus, we hypothesized that the functional response levelled off because attack rate decreased with increasing density. Direct observations of the predation act at high and low prey densities showed that prey per capita mortality rate was markedly lower at high densities. An analysis of the components of the predation cycle showed that encounter rate and attack probability but not capture success decreased with increasing prey density. We, then, studied the degree of aggregation and the movement behaviour of Polyphemus . The tendency to form swarms increased with density and this was associated with reduced swimming speed and swimming along a more tortuous path. Presence of Utricularia leaves did not influence the spatial distribution and swimming behaviour of Polyphemus . We concluded that the unusual shape of the functional response was due to density dependent prey mortality rates that resulted from a density dependent tendency to form swarms. We, therefore, suggested a modification of Holling's type II functional response model that included density dependent attack rate and this model fitted data significantly better than the original model.     

Time‐to‐kill: measuring attack rates in a heterogenous landscape with multiple prey types

Although spatial heterogeneity of prey and landscapes are known to contribute to variation around predator‐prey functional response models, few studies have quantified these effects. We illustrate a new approach using data from winter movement paths of GPS‐collared wolves in the Rocky Mountains of Canada and time‐to‐event models with competing risks for measuring the effect of prey and landscape characteristics on the time‐to‐kill, which is the reciprocal of attack rate (aN) in a Holling's functional response. We evaluated 13 a priori models representing hypothesized mechanisms influencing attack rates in a heterogeneous landscape with two prey types. Models ranged from variants on Holling's disc equation, including search rate and prey density, to a full model including prey density and patchiness, search rates, satiation, and landscape features, which were measured along the wolf's movement path. Movement rates of wolves while searching explained more of the variation in time‐to‐kill than prey densities. Wolves did not compensate for low prey density by increasing movement rates and there was little evidence that spatial aggregation of prey influenced attack rates in this multi‐prey system. The top model for predicting time‐to‐kill included only search rate and landscape features. Wolves killed prey more quickly in flat terrain, likely due to increased vulnerability from accumulated snow, whereas attack rates were lower when wolves hunted near human‐made features presumably due to human disturbance. Understanding the sources of variation in attack rates provides refinements to functional response models that can lead to more effective predator–prey management in human‐dominated landscapes.     

Functional feeding responses of piscivorous fishes from the northeast US continental shelf

The functional feeding response forms of piscivorous fishes used in multispecies and ecosystem modeling have been questioned because they were mostly conjectural or solely based on laboratory studies. Here, we investigate the functional feeding response of seven species of piscivorous fishes on four species of their prey from the northeast US continental shelf using field data that spans 30 years. Our study confirmed that Holling’s types II and III functional responses are the most common functional responses for piscivorous fishes in this region. However, our analyses also revealed that differences exist between piscivorous fishes’ functional responses, and, therefore, combining functional responses of piscivores is probably not appropriate in multispecies and ecosystem modeling. In the absence of specific predator–prey functional responses, we suggest that, for cruising, actively attacking predators, a type II functional response is slightly preferable; for a sedentary, ambush predator, a type III functional response is slightly preferable; at low prey densities for a generic fish predator, a type III functional response should be used; and at moderate to high prey densities, either should work sufficiently. Because we have shown that the functional response of a particular predator to individual prey species varies, these relationships must be further evaluated as we continue to develop and employ multispecies and ecosystem modeling.     

Functional response of the predators Podisus maculiventris (Say) and Podisus nigrispinus (Dallas) (Het., Pentatomidae) to the beet armyworm, Spodoptera exigua (Hübner) (Lep., Noctuidae): ef fect of temperature

Predation abilities of Podisus maculiventris and Podisus nigrispinus on caterpillars of the beet armyworm, Spodoptera exigua (Hübner), were compared at three different temperatures (18, 23 and 27°C) by performing functional response tests. In both species, predation capacity was a function of temperature and prey density: more prey were captured as temperature and number of prey offered increased. Results indicated that type II and III functional responses provided the best fit to the data obtained for P. nigrispinus at 18 and 23°C, and at 27°C, respectively. However, the data for P. maculiventris showed a better fit to type II at 18°C and to type III at higher temperatures. In both pentatomids the handling time decreased with increasing temperature. At higher temperatures, P. nigrispinus demonstrated greater predation rates than P. maculiventris . The implications of these findings for the control of caterpillar pests in glasshouses are discussed.     

The influence of light level on the functional response of a zooplanktonivorous fish

Summary Light and vision are clearly of significance in foraging behaviour by underyearling common bream [Abramis brama (L.)]. These fish are effective predators at 1.25 Lux but they were also shown to be capable of taking prey, at a reduced rate, at a much lower light intensity (less than 5x10^-3 Lux). In the latter case they may have been using sensory modes other than vision, perhaps involving tactile and/or olfactory stimuli.We investigated the influence of light level on the functional response of bream to Daphnia magna prey. At 1.25 Lux the predator showed a typical type II response. However, the relatively unfavourable conditions in the lower light intensity appear to have been responsible for generating a sigmoid type III functional response. Observations, using infra-red sensitive equipment, suggested a behavioural basis for this result. Thus, the predator's attack rate was not constant, but increased with prey density. The significance of the type III functional response is discussed, both in terms of predator energetics and predator-prey population stability.     

How predator functional responses and Allee effects in prey affect the paradox of enrichment and population collapses

In Rosenzweig-MacArthur models of predator-prey dynamics, Allee effects in prey usually destabilize interior equilibria and can suppress or enhance limit cycles typical of the paradox of enrichment. We re-evaluate these conclusions through a complete classification of a wide range of Allee effects in prey and predator's functional response shapes. We show that abrupt and deterministic system collapses not preceded by fluctuating predator-prey dynamics occur for sufficiently steep type III functional responses and strong Allee effects (with unstable lower equilibrium in prey dynamics). This phenomenon arises as type III functional responses greatly reduce cyclic dynamics and strong Allee effects promote deterministic collapses. These collapses occur with decreasing predator mortality and/or increasing susceptibility of the prey to fall below the threshold Allee density (e.g. due to increased carrying capacity or the Allee threshold itself). On the other hand, weak Allee effects (without unstable equilibrium in prey dynamics) enlarge the range of carrying capacities for which the cycles occur if predators exhibit decelerating functional responses. We discuss the results in the light of conservation strategies, eradication of alien species, and successful introduction of biocontrol agents.     

Long-term variation of link strength in a simple benthic food web

1. The predatory isopod Saduria entomon (L.) and its amphipod prey Monoporeia affinis (Lindstr?m) are key components of the food web in the northern Baltic Sea, together representing 80-90% of the macrobenthic biomass. We use 20 years of stomach content data for Saduria to investigate how diet dynamics affect the stability of the interaction between Saduria and Monoporeia. 2. Consumption of the main prey, Monoporeia, fitted a type III functional response. Consumption rates of the most important alternative prey, mysids, were found to be unrelated to mysid densities but negatively related to the density of Monoporeia. The fit of consumption data to a model that assumes passive prey selection was poor. Thus we conclude that some form of active choice is involved. 3. The effect of consumption of mysids, the alternative prey, on the stability of this system was investigated using a 'one predator-two prey' model with stochastic environmental variation. Analysis of the model suggests that feeding on mysids leads to a decreased extinction risk for the predator, Saduria, and reduced density oscillations for both Saduria and its main prey, Monoporeia.     

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.     

You can’t run but you can hide: refuge use in frog tadpoles elicits density-dependent predation by dragonfly larvae

The potential role of prey refuges in stabilizing predator–prey interactions is of longstanding interest to ecologists, but mechanisms underlying a sigmoidal predator functional response remain to be fully elucidated. Authors have disagreed on whether the stabilizing effect of prey refuges is driven by prey- versus predator-centric mechanisms, but to date few studies have married predator and prey behavioural observations to distinguish between these possibilities. We used a dragonfly nymph–tadpole system to study the effect of a structural refuge (leaf litter) on the predator’s functional response, and paired this with behavioural observations of both predator and prey. Our study confirmed that hyperbolic (type II) functional responses were characteristic of foraging predators when structural cover was low or absent, whereas the functional response was sigmoidal (type III) when prey were provided with sufficient refuge. Prey activity and refuge use were density independent across cover treatments, thereby eliminating a prey-centric mechanism as being the genesis for density-dependent predation. In contrast, the predator’s pursuit length, capture success, and handling time were altered by the amount of structure implying that observed shifts in density-dependent predation likely were related to predator hunting efficiency. Our study advances current theory by revealing that despite fixed-proportion refuge use by prey, presence of a prey refuge can induce density-dependent predation through its effect on predator hunting strategy. Ultimately, responses of predator foraging decisions in response to changes in prey availability and search efficiency may be more important in producing density-dependent predation than the form of prey refuge use.     

Should "handled" prey be considered? Some consequences for functional response, predator-prey dynamics and optimal foraging theory

Predator-prey models consider those prey that are free. They assume that once a prey is captured by a predator it leaves the system. A question arises whether in predator-prey population models the variable describing prey population shall consider only those prey which are free, or both free and handled prey together. In the latter case prey leave the system after they have been handled. The classical Holling type II functional response was derived with respect to free prey. In this article we derive a functional response with respect to prey density which considers also handled prey. This functional response depends on predator density, i.e., it accounts naturally for interference. We study consequences of this functional response for stability of a simple predator-prey model and for optimal foraging theory. We show that, qualitatively, the population dynamics are similar regardless of whether we consider only free or free and handled prey. However, the latter case may change predictions in some other cases. We document this for optimal foraging theory where the functional response which considers both free and handled prey leads to partial preferences which are not observed when only free prey are considered.     

Revisiting the influence of learning in predator functional response,how it can lead to shapes different from type III

Predator/parasitoid functional response is one of the main tools used to study predation behavior, and in assessing the potential of biological control candidates. It is generally accepted that predator learning in prey searching and manipulation can produce the appearance of a type III functional response. Holling proposed that in the presence of alternative prey, at some point the predator would shift the preferred prey, leading to the appearance of a sigmoid function that characterized that functional response. This is supported by the analogy between enzyme kinetics and functional response that Holling used as the basis for developing this theory. However, after several decades, sigmoidal functional responses appear in the absence of alternative prey in most of the biological taxa studied. Here, we propose modeling the effect of learning on the functional response by using the explicit incorporation of learning curves in the parameters of the Holling functional response, the attack rate (a), and the manipulation time (h). We then study how the variation in the parameters of the learning curves causes variations in the shape of the functional response curve. We found that the functional response product of learning can be either type I, II, or III, depending on what parameters act on the organism, and how much it can learn throughout the length of the study. Therefore, the presence of other types of curves should not be automatically associated with the absence of learning. These results are important from an ecological point of view because when type III functional response is associated with learning, it is generally accepted that it can operate as a stabilizing factor in population dynamics. Our results, to the contrary, suggest that depending on how it acts, it may even be destabilizing by generating the appearance of functional responses close to type I.     

A functional response model of a predator population foraging in a patchy habitat

1. Functional response models (e.g. Holling's disc equation) that do not take the spatial distributions of prey and predators into account are likely to produce biased estimates of predation rates. 2. To investigate the consequences of ignoring prey distribution and predator aggregation, a general analytical model of a predator population occupying a patchy environment with a single species of prey is developed. 3. The model includes the density and the spatial distribution of the prey population, the aggregative response of the predators and their mutual interference. 4. The model provides explicit solutions to a number of scenarios that can be independently combined: the prey has an even, random or clumped distribution, and the predators show a convex, sigmoid, linear or no aggregative response. 5. The model is parameterized with data from an acarine predator-prey system consisting of Phytoseiulus persimis and Tetranychus urticae inhabiting greenhouse cucumbers. 6. The model fits empirical data quite well and much better than if prey and predators were assumed to be evenly distributed among patches, or if the predators were distributed independently of the prey. 7. The analyses show that if the predators do not show an aggregative response it will always be an advantage to the prey to adopt a patchy distribution. On the other hand, if the predators are capable of responding to the distribution of prey, then it will be an advantage to the prey to be evenly distributed when its density is low and switch to a more patchy distribution when its density increases. The effect of mutual interference is negligible unless predator density is very high. 8. The model shows that prey patchiness and predator aggregation in combination can change the functional response at the population level from type II to type III, indicating that these factors may contribute to stabilization of predator-prey dynamics.