Emergence of Holling type III zooplankton functional response: Bringing together field evidence and mathematical modelling

Food-web population models are rather sensitive to parameterization of functional response in predation terms. Theoretical studies predict enhancing of ecosystems’ stability for a functional response of sigmoid type (Holling type III). The choice of a correct type of response is especially important for modelling outcome of grazing control of algal blooms by zooplankton in nutrient-rich ecosystems. Extensive experiments on zooplankton feeding in laboratories show non-sigmoid nature of response for most herbivorous zooplankton species. As a consequence, there is a strong opinion in literature that the implementation of Holling III type grazing in plankton models is biologically meaningless. I argue, however, that such an ‘evident’ claim might be wrong and sigmoid functional responses in real plankton communities would emerge more often than was suggested earlier. Especially, this concerns plankton models without vertical resolution, which ignore heterogeneity in vertical distribution of species. Having conducted extensive literature search of data on zooplankton feeding in situ, I show that vertical heterogeneity in food distribution as well as active food searching behaviour of zooplankton can modify the type of functional response. In particular, the rate of food intake by the whole zooplankton population in the column, as a function of total amount of food, often exhibits a sigmoid behaviour, instead of a non-sigmoid one postulated previously based on laboratory experiments. This conceptual discrepancy is due to the ability of zooplankton to feed mostly in layers with high algal density. I propose a generic model explaining the observed alteration of type between overall and local functional responses. I show that emergence of Holling type III in plankton systems is due to mechanisms different from those well known in the ecological literature (e.g. food search learning, existence of alternative food, refuge for prey).     

Consequences of size structure in the prey for predator-prey dynamics: the composite functional response

1. Current formulations of functional responses assume that the prey is homogeneous and independent of intraspecific processes. Most prey populations consist of different coexisting size classes that often engage in asymmetrical intraspecific interactions, including cannibalism, which can lead to nonlinear interaction effects. This may be important as the size structure with the prey could alter the overall density-dependent predation rates. 2. In a field experiment with damselfly and dragonfly larvae, 16 treatments manipulated the density of a small prey stage, the presence of large conspecific prey and the presence of heterospecific predators. 3. Size structure in the prey (i.e. when both prey stages were present) decreased the impact of the predator on overall prey mortality by 25-48% at mid and high prey densities, possibly due to density-dependent size-structured cannibalism in the prey. The predation rates on small prey stages were determined by the interaction of large prey and predators. Predation rates increased with prey density in the absence of large prey, but predation rates were constant across densities when large conspecifics were present. 4. The functional response for unstructured prey followed a Holling type III model, but the predation rate for size-structured prey was completely different and followed a complex pattern that could not be explained with any standard functional response. 5. Using additional laboratory experiments, a mortality model was developed and parameterized. It showed that the overall prey mortality of size-structured prey can be adequately predicted with a composite functional response model that modelled the individual functional responses of each prey stage separately and accounted for their cannibalistic interaction. 6. Thus, treating a prey population as a homogeneous entity will lead to erroneous predictions in most real-world food webs. However, if we account for the effects of size structure and the intraspecific interactions on functional responses by treating size classes as different functional groups, it is possible to reliably predict the dynamics of size-structured predator-prey systems.     

Predator population size structure alters consumption of prey from epigeic and grazing food webs

Numerous studies have found that predators can suppress prey densities and thereby impact important ecosystem processes such as plant productivity and decomposition. However, prey suppression by spiders can be highly variable. Unlike predators that feed on prey within a single energy channel, spiders often consume prey from asynchronous energy channels, such as grazing (live plant) and epigeic (soil surface) channels. Spiders undergo few life cycle changes and thus appear to be ideally suited to link energy channels, but ontogenetic diet shifts in spiders have received little attention. For example, spider use of different food channels may be highly specialized in different life stages and thus a species may be a multichannel omnivore only when we consider all life stages. Using stable isotopes, we investigated whether wolf spider (Pardosa littoralis, henceforth Pardosa) prey consumption is driven by changes in spider size. Small spiders obtained > 80% of their prey from the epigeic channel, whereas larger spiders used grazing and epigeic prey almost equally. Changes in prey consumption were not driven by changes in prey density, but by changes in prey use by different spider size classes. Thus, because the population size structure of Pardosa changes dramatically over the growing season, changes in spider size may have important implications for the strength of trophic cascades. Our research demonstrates that life history can be an important component of predator diet, which may in turn affect community- and ecosystem-level processes.     

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.     

Bistability and limit cycles in generalist predator–prey dynamics

Since generalist predators feed on a variety of prey species they tend to persist in an ecosystem even if one particular prey species is absent. Predation by generalist predators is typically characterized by a sigmoidal functional response, so that predation pressure for a given prey species is small when the density of that prey is low. Many mathematical models have included a sigmoidal functional response into predator–prey equations and found the dynamics to be more stable than for a Holling type II functional response. However, almost none of these models considers alternative food sources for the generalist predator. In particular, in these models, the generalist predator goes extinct in the absence of the one focal prey. We model the dynamics of a generalist predator with a sigmoidal functional response on one dynamic prey and fixed alternative food source. We find that the system can exhibit up to six steady states, bistability, limit cycles and several global bifurcations.     

The feeding biology of the triclad Phagocata vitta (Dugès): A laboratory study

A series of laboratory experiments investigated the diet and feeding behaviour of Phagocata vitta (Dugès). Its fundamental food niche comprises oligochaetes and chironomid larvae, in order of importance. Other arthropod groups, when wounded, are also eaten.Increasing prey density resulted in the ingestion rate increasing in a type 2 functional response curve, sensu Holling. Group feeding by triclads did not widen the food niche but did result in small triclads being more successful in obtaining a meal.When a range of size classes of prey were offered to various size classes of triclad, small triclads were found to take mainly small prey, whilst other sizes would take prey sizes in proportion to their presence in the mixture.Mucous traps do not appear to have an important role in the feeding biology of the triclad.     

Multichannel feeding by spider functional groups is driven by feeding strategies and resource availability

Multichannel feeding, whereby consumers feed across resource channels such as upon herbivore and detritivore resources, acts to link discrete compartments of a food web with implications for ecosystem functioning and stability. Currently however, we have little understanding which feeding strategies of consumers underlie multichannel feeding. We therefore link spider functional group and resource density‐dependent or density‐independent feeding strategies to multichannel feeding by quantifying not only consumer diet, but also the relative availability of resources. Here we analysed herbivore (green) and detritivore (brown) prey use by spider communities in grasslands, and tested if available prey biomass proportions were linked to observed spider dietary proportions. Different spider functional groups each linked green and brown resource channels, but while green prey were always consumed in proportion to their relative biomass, brown prey were consumed independently of proportion by some functional groups. Additionally, we found greater intraguild predation by cursorial spiders when green resources were relatively scarcer, suggesting green prey was preferred, and needed to be compensated for when rare. Overall, we observed a stronger consumer connection to the green than brown resource channel, yet this green connection was more variable due to greater range in green resource availability across grasslands and density‐dependent consumption on green prey. Consequently, multichannel feeding by spiders was determined by density‐dependent and density‐independent feeding strategies that varied by spider functional group and across resources channels. Our results demonstrate that the role of multichannel feeding by spiders in linking separate food web compartments is a dynamic component of food web structure in these wild grasslands.     

A trait‐based approach reveals the feeding selectivity of a small endangered Mediterranean fish

Functional traits are growing in popularity in modern ecology, but feeding studies remain primarily rooted in a taxonomic‐based perspective. However, consumers do not have any reason to select their prey using a taxonomic criterion, and prey assemblages are variable in space and time, which makes taxon‐based studies assemblage‐specific. To illustrate the benefits of the trait‐based approach to assessing food choice, we studied the feeding ecology of the endangered freshwater fish Barbus meridionalis. We hypothesized that B. meridionalis is a selective predator which food choice depends on several prey morphological and behavioral traits, and thus, its top‐down pressure may lead to changes in the functional composition of in‐stream macroinvertebrate communities. Feeding selectivity was inferred by comparing taxonomic and functional composition (13 traits) between ingested and free‐living potential prey using the Jacob's electivity index. Our results showed that the fish diet was influenced by 10 of the 13 traits tested. Barbus meridionalis preferred prey with a potential size of 5–10 mm, with a medium–high drift tendency, and that drift during daylight. Potential prey with no body flexibility, conical shape, concealment traits (presence of nets and/or cases, or patterned coloration), and high aggregation tendency had a low predation risk. Similarly, surface swimmers and interstitial taxa were low vulnerable to predation. Feeding selectivity altered the functional composition of the macroinvertebrate communities. Fish absence favored taxa with weak aggregation tendency, weak flexibility, and a relatively large size (10–20 mm of potential size). Besides, predatory invertebrates may increase in fish absence. In conclusion, our study shows that the incorporation of the trait‐based approach in diet studies is a promising avenue to improve our mechanistic understanding of predator–prey interactions and to help predict the ecological outcomes of predator invasions and extinctions.     

Warming up the system: higher predator feeding rates but lower energetic efficiencies

Predictions on the consequences of the rapidly increasing atmospheric CO₂ levels and associated climate warming for population dynamics, ecological community structure and ecosystem functioning depend on mechanistic energetic models of temperature effects on populations and their interactions. However, such mechanistic approaches combining warming effects on metabolic (energy loss of organisms) and feeding rates (energy gain by organisms) remain a key, yet elusive, goal. Aiming to fill this void, we studied the metabolic rates and functional responses of three differently sized, predatory ground beetles on one mobile and one more resident prey species across a temperature gradient (5, 10, 15, 20, 25 and 30 °C). Synthesizing metabolic and functional‐response theory, we develop novel mechanistic predictions how predator–prey interaction strengths (i.e., functional responses) should respond to warming. Corroborating prior theory, warming caused strong increases in metabolism and decreases in handling time. Consistent with our novel model, we found increases in predator attack rates on a mobile prey, whereas attack rates on a mostly resident prey remained constant across the temperature gradient. Together, these results provide critically important information that environmental warming generally increases the direct short‐term per capita interaction strengths between predators and their prey as described by functional‐response models. Nevertheless, the several fold stronger increase in metabolism with warming caused decreases in energetic efficiencies (ratio of per capita feeding rate to metabolic rate) for all predator–prey interactions. This implies that warming of natural ecosystems may dampen predator–prey oscillations thus stabilizing their dynamics. The severe long‐term implications; however, include predator starvation due to energetic inefficiency despite abundant resources.     

Microgeographic divergence of functional responses among salamanders under antagonistic selection from apex predators

A predator''s functional response determines predator–prey interactions by describing the relationship between the number of prey available and the number eaten. Its shape and parameters fundamentally govern the dynamic equilibrium of predator–prey interactions and their joint abundances. Yet, estimates of these key parameters generally assume stasis in space and time and ignore the potential for local adaptation to alter feeding responses and the stability of trophic dynamics. Here, we evaluate if functional responses diverge among populations of spotted salamander (Ambystoma maculatum) larvae that face antagonistic selection on feeding strategies based on their own risk of predation. Common garden experiments revealed that spotted salamander from ponds with varying predation risks differed in their functional responses, suggesting an evolutionary response. Applying mechanistic equations, we discovered that the combined changes in attack rates, handling times and shape of the functional response enhanced feeding rate in environments with high densities of gape-limited predators. We suggest how these parameter changes could alter community equilibria and other emergent properties of food webs. Community ecologists might often need to consider how local evolution at fine scales alters key relationships in ways that alter local diversity patterns, food web dynamics, resource gradients and community responses to disturbance.     

斑翅肩花蝽对铁杉球蚜的捕食作用

室内用铁杉球Adelges tsugae Annand(Hemlock woolly adelgids)蚜卵、1～4龄若虫、成虫饲养斑翅肩花蝽Tetraphleps galchanoides Ghauri,研究斑翅肩花蝽对铁杉球蚜Adelges tsugae Annand(Hemlock woolly adelgids)的捕食效应。结果表明,斑翅肩花蝽对铁杉球蚜的捕食功能反应属于HollingⅡ型反应,对球蚜密度的捕食干扰反应可能存在种内的干扰作用。对于同一发育期同一密度猎物,斑翅肩花蝽成虫或若虫在高密度条件下的日均捕食量均显著高于低猎物密度下的日均捕食量;而对于不同发育期不同密度猎物,斑翅肩花蝽在低猎物密度时对测定的铁杉球蚜6个不同虫态无明显选择性;在中、高密度时斑翅肩花蝽对测定的铁杉球蚜的不同虫态表现出明显喜好性差异,若虫最喜好食铁杉球蚜卵和1龄若虫,成虫最喜好食铁杉球蚜4龄若虫和成虫。为评价和利用斑翅肩花蝽对铁杉球蚜防治作用进行了讨论。     

Testing the validity of functional response models using molecular gut content analysis for prey choice in soil predators

Analysis of predator–prey interactions is a core concept of animal ecology, explaining structure and dynamics of animal food webs. Measuring the functional response, i.e. the intake rate of a consumer as a function of prey density, is a powerful method to predict the strength of trophic links and assess motives of prey choice, particularly in arthropod communities. However, due to their reductionist set‐up, functional responses, which are based on laboratory feeding experiments, may not display field conditions, possibly leading to skewed results. Here, we tested the validity of functional responses of centipede predators and their prey by comparing them with empirical gut content data from field‐collected predators. Our predator–prey system included lithobiid and geophilomorph centipedes, abundant and widespread predators of forest soils and their soil‐dwelling prey. First, we calculated the body size‐dependent functional responses of centipedes using a published functional response model in which we included natural prey abundances and animal body masses. This allowed us to calculate relative proportions of specific prey taxa in the centipede diet. In a second step, we screened field‐collected centipedes for DNA of eight abundant soil‐living prey taxa and estimated their body size‐dependent proportion of feeding events. We subsequently compared empirical data for each of the eight prey taxa, on proportional feeding events with functional response‐derived data on prey proportions expected in the gut, showing that both approaches significantly correlate in five out of eight predator–prey links for lithobiid centipedes but only in one case for geophilomorph centipedes. Our findings suggest that purely allometric functional response models, which are based on predator–prey body size ratios are too simple to explain predator–prey interactions in a complex system such as soil. We therefore stress that specific prey traits, such as defence mechanisms, must be considered for accurate predictions.     

Ontogenetic niche shifts and resource partitioning in a subarctic piscivore fish guild

The feeding ecology of three piscivorous fish species (perch (Perca fluviatilis), pike (Esox lucius) and burbot (Lota lota)), was studied in the subarctic Pasvik watercourse (69 °N), northern Norway and Russia. All three species primarily occupied the benthic habitats in the watercourse. Perch and burbot exhibited distinct ontogenetic niche shifts in food resource use, perch changing from a dominance of zooplankton to zoobenthos to fish, and burbot from zoobenthos to fish. Fish prey dominated the diet of all the investigated size-classes of pike, but small-sized pike (<20 cm) were not represented in the sample. Fish prey size was positively related to predator size in all three species. Whitefish (Coregonus lavaretus) was the dominant prey of pike and large-sized burbot and perch. Nine-spined sticklebacks (Pungitius pungitius) was also an important prey and appeared to be a dietary stepping-stone enhancing the transition from invertebrate feeding to consumption of large-sized whitefish prey for all three predators. A cluster analysis separated the different size groups of the three predator species into five functional feeding groups, most of them containing two or all three species. Within these feeding groups, and especially among the piscivorous size-classes, there was a strong and significant interspecific overlap in prey selection, and the dietary similarities between the species were in general much larger than the intraspecific similarities between ontogenetic stages. All three piscivorous species are important top predators in the aquatic food web of the watercourse, and their ontogenetic diet shifts and resource partitioning patterns generate a substantial food web complexity in this subarctic ecosystem.     

草间小黑蛛对棉铃虫幼虫的捕食作用及其模拟模型的研究——Ⅰ.捕食者-单种猎物系统的研究

捕食者-猎物系统中的捕食作用是种群生态学中的一个主要组成成分,它是影响动物种群数量变动的一个重要生物学过程,也是有害动物的控制和益虫利用的重要科学依据。由于近十几年来化学防治引起一系列的问题,因而生物防治日益受到重视,与此相适应,有关捕食者(或寄生物)与猎物(或宿主)之间捕食作用关系的研究自六十年代中期以来也越来越多,本文即为这方面的一项研究报道。     

Incorporating prey refuge in a prey–predator model with a Holling type I functional response: random dynamics and population outbreaks

A prey–predator discrete-time model with a Holling type I functional response is investigated by incorporating a prey refuge. It is shown that a refuge does not always stabilize prey–predator interactions. A prey refuge in some cases produces even more chaotic, random-like dynamics than without a refuge and prey population outbreaks appear. Stability analysis was performed in order to investigate the local stability of fixed points as well as the several local bifurcations they undergo. Numerical simulations such as parametric basins of attraction, bifurcation diagrams, phase plots and largest Lyapunov exponent diagrams are executed in order to illustrate the complex dynamical behavior of the system.     

Trophic-dynamic considerations in relating species diversity to ecosystem resilience

Complexity in the networks of interactions among and between the living and abiotic components forming ecosystems confounds the ability of ecologists to predict the economic consequences of perturbations such as species deletions in nature. Such uncertainty hampers prudent decision making about where and when to invest most intensively in species conservation programmes. Demystifying ecosystem responses to biodiversity alterations may be best achieved through the study of the interactions allowing biotic communities to compensate internally for population changes in terms of contributing to ecosystem function, or their intrinsic functional redundancy. Because individual organisms are the biologically discrete working components of ecosystems and because environmental changes are perceived at the scale of the individual, a mechanistic understanding of functional redundancy will hinge upon understanding how individuals' behaviours influence population dynamics in the complex community setting. Here, I use analytical and graphical modelling to construct a conceptual framework for predicting the conditions under which varying degrees of interspecific functional redundancy can be found in dynamic ecosystems. The framework is founded on principles related to food web successional theory, which provides some evolutionary insights for mechanistically linking functional roles of discrete, interacting organisms with the dynamics of ecosystems because energy is the currency both for ecological fitness and for food web commerce. Net productivity is considered the most contextually relevant ecosystem process variable because of its socioeconomic significance and because it ultimately subsumes all biological processes and interactions. Redundancy relative to productivity is suggested to manifest most directly as compensatory niche shifts among adaptive foragers in exploitation ecosystems, facilitating coexistence and enhancing ecosystem recovery after disturbances which alter species' relative abundances, such as extinctions. The framework further explicates how resource scarcity and environmental stochasticity may constitute 'ecosystem legacies' influencing the emergence of redundancy by shaping the background conditions for foraging behaviour evolution and, consequently, the prevalence of compensatory interactions. Because it generates experimentally testable predictions for a priori hypothesis testing about when and where varying degrees of functional redundancy are likely to be found in food webs, the framework may be useful for advancing toward the reliable knowledge of biodiversity and ecosystem function relations necessary for prudent prioritization of conservation programmes. The theory presented here introduces explanation of how increasing diversity can have a negative influence on ecosystem sustainability by altering the environment for biotic interactions and thereby changing functional compensability among biota--under particular conditions.     

Behavioural and life history effects of predator diet cues during ontogeny in damselfly larvae

A central issue in predator–prey interactions is how predator associated chemical cues affect the behaviour and life history of prey. In this study, we investigated how growth and behaviour during ontogeny of a damselfly larva (Coenagrion hastulatum) in high and low food environments was affected by the diet of a predator (Aeshna juncea). We reared larvae in three different predator treatments; no predator, predator feeding on conspecifics and predator feeding on heterospecifics. We found that, independent of food availability, larvae displayed the strongest anti-predator behaviours where predators consumed prey conspecifics. Interestingly, the effect of predator diet on prey activity was only present early in ontogeny, whereas late in ontogeny no difference in prey activity between treatments could be found. In contrast, the significant effect of predator diet on prey spatial distribution was unaffected by time. Larval size was affected by both food availability and predator diet. Larvae reared in the high food treatment grew larger than larvae in the low food treatment. Mean larval size was smallest in the treatment where predators consumed prey conspecifics, intermediate where predators consumed heterospecifics and largest in the treatment without predators. The difference in mean larval size between treatments is probably an effect of reduced larval feeding, due to behavioural responses to chemical cues associated with predator diet. Our study suggests that anti-predator responses can be specific for certain stages in ontogeny. This finding shows the importance of considering where in its ontogeny a study organism is before results are interpreted and generalisations are made. Furthermore, this finding accentuates the importance of long-term studies and may have implications for how results generated by short-term studies can be used.     

Does Mutual Interference Affect the Feeding Rate of Aphidophagous Coccinellids? A Modeling Perspective

Mutual interference involves direct interactions between individuals of the same species that may alter their foraging success. Larvae of aphidophagous coccinellids typically stay within a patch during their lifetime, displaying remarkable aggregation to their prey. Thus, as larvae are exposed to each other, frequent encounters may affect their foraging success. A study was initiated in order to determine the effect of mutual interference in the coccinellids’ feeding rate. One to four 4^th larval instars of the fourteen-spotted ladybird beetle Propylea quatuordecimpunctata were exposed for 6 hours into plastic containers with different densities of the black bean aphid, Aphis fabae, on potted Vicia faba plants. The data were used to fit a purely prey-dependent Holling type II model and its alternatives which account for interference competition and have thus far been underutilized, i.e. the Beddington-DeAngelis, the Crowley-Martin and a modified Hassell-Varley model. The Crowley-Martin mechanistic model appeared to be slightly better among the competing models. The results showed that although the feeding rate became approximately independent of predator density at high prey density, some predator dependence in the coccinellid’s functional response was observed at the low prey—high predator density combination. It appears that at low prey densities, digestion breaks are negligible so that the predators do waste time interfering with each other, whereas at high prey densities time loss during digestion breaks may fully accommodate the cost of interference, so that the time cost may be negligible.     

The impact of nonlinear functional responses on the long-term evolution of food web structure

We investigate the long-term web structure emerging in evolutionary food web models when different types of functional responses are used. We find that large and complex webs with several trophic layers arise only if the population dynamics is such that it allows predators to focus on their best prey species. This can be achieved using modified Lotka-Volterra or Holling/Beddington functional responses with effective couplings that depend on the predator's efficiency at exploiting the prey, or a ratio-dependent functional response with adaptive foraging. In contrast, if standard Lotka-Volterra or Holling/Beddington functional responses are used, long-term evolution generates webs with almost all species being basal, and with additionally many links between these species. Interestingly, in all cases studied, a large proportion of weak links result naturally from the evolution of the food webs.     

Shape and sources of variations of the functional response of wildfowl: an experiment with mallards, Anas platyrhynchos

Understanding the variations of the functional response of an organism, i.e. the predation rate in relation to prey density, is necessary to understand the interactions between the animal and its food supply. This has received little attention in dabbling ducks so we investigated experimentally the shape of the functional response of mallard feeding on poultry pellets, and assessed the influence of several factors such as the size of food items, sex or individual performance on this functional response. Individual differences in intake rate are of crucial importance in group or gregarious foraging species. We used two approaches of the functional response: 1) the relation between feeding rate (pellets/s) and pellet densities (pellets/m²), and 2) the relationship between instantaneous intake rate (g/s) and biomass density (g/m²). For both approaches, we found that the Type II functional response gave better estimates than a Type I linear functional response but explained only a third of the variance. Our results show that pellet size has a large effect on instantaneous intake rate. The comparison of the functional response parameters suggest that handling time per prey may not reflect the real constraints on intake rate, but that handling time per gram ingested may be more appropriate to integrate the effect of item size in the functional response. We then discuss the possible mechanisms involved. We also found individual variations in the functional response for each of the experiments, with some consistency in the hierarchy regarding feeding efficiency. We did not find any differences between males and females. Our results provide an evaluation of individual variations in intake rate in interference-free conditions, which has rarely been done, and call for more controlled experiments to allow a finer understanding of the mechanisms of food acquisition in dabbling ducks.