Temporal partitioning and aggression among foragers: modeling the effects of stochasticity and individual state

In many natural systems, individuals compete with conspecificsand heterospecifics for food and in some cases, individualshave been observed to partition their foraging times or fightover food. In this study, I investigated when it is optimalfor a consumer to partition time and be aggressive. I formulatedan individual-based model of foraging and used game theoryto find evolutionarily stable strategies (ESSs) that maximizethe probability that consumers survive each day and acquiretheir daily food requirements. Consumers choose when to forageand when to behave aggressively during confrontations overfood. Consumers are each associated with a state variable,representing the amount of food eaten, and a dominance ranking, which describes how likely they are to forage and fight forfood. The ESS is sensitive to food abundance, consumer state,and the dominance ranking. When food is abundant, temporalpartitioning is often an ESS where the dominant consumer foragesfirst; however, partitioning is unlikely to be an ESS when food abundance is low. Fights over food are typically avoidedbut may be part of an ESS when food abundance is low, bothconsumers are hungry, or the time available for foraging eachday is drawing to a close. Because the ESS is sensitive toconsumer state, the stochastic nature of finding food often results in considerable variation in observed foraging dynamicsfrom one day to the next, even when consumers adopt the samestate-dependent strategy each day. Results are compared withempirical observations, and I discuss implications for consumercoexistence.     

Decreasing functional responses as a result of adaptive consumer behavior

Summary Several different mechanisms that may produce decreasing functional responses are investigated using models that assume that an optimally foraging consumer is exploiting one or two resources. Decreasing functional responses are associated with situations in which there are costs to resource consumption. If the process of resource acquisition has costs, decreasing functional responses may occur when there is a single homogeneous resource. If the cost is solely a function of the amount of resource ingested, decreasing functional responses on a single resource do not occur. Both types of cost can produce decreasing functional responses when there are two resource types and a trade-off relationship between consumption of one and consumption of the other. Decreasing functional responses seem to be most likely to occur on a food that yields high benefits and costs per unit of foraging time or effort when there is an alternative resource which yields low benefits and costs. Given this type of foraging choice, the functional response is most likely to decrease when the benefits of ingestion increase at a decreasing rate, and the costs of ingestion increase at an increasing rate with amount ingested. An important and unique consequence of decreasing functional responses is the possibility of population cycles in differential equation models of consumer-resource systems with non-reproducing resources; this is illustrated with a simple comsumer-resource model.     

Satiation and the functional response: a test of a new model

Abstract. 1. A model of the functional response to prey density is derived to include the reduction in time available for search, T_s , resulting from predator satiation.
2. For larger prey items predator satiation occurs at each prey capture and T_s is reduced by the attack time and digestive pause of a series of attack cycles. For small prey items predator foraging is continuous at low densities with T_s reduced solely by attack time. At higher densities predator satiation occurs after the capture of several small prey items and T_s is reduced by the attack time and digestive pause of a series of foraging cycles.
3. A comparison of the predicted asymptotic level of prey capture using experimentally estimated parameter values, with the maximum consumption of aphids by larval and adult coccinellids provides a test of the satiation model.
4. The limitation of prey capture by predator satiation is discussed with reference to handling time and the success of coccinellids in biological control.     

Non‐linear feeding functional responses in the Greater Flamingo (Phoenicopterus roseus) predict immediate negative impact of wetland degradation on this flagship species

Accurate knowledge of the functional response of predators to prey density is essential for understanding food web dynamics, to parameterize mechanistic models of animal responses to environmental change, and for designing appropriate conservation measures. Greater flamingos (Phoenicopterus roseus), a flagship species of Mediterranean wetlands, primarily feed on Artemias (Artemia spp.) in commercial salt pans, an industry which may collapse for economic reasons. Flamingos also feed on alternative prey such as Chironomid larvae (e.g., Chironomid spp.) and rice seeds (Oryza sativa). However, the profitability of these food items for flamingos remains unknown. We determined the functional responses of flamingos feeding on Artemias, Chironomids, or rice. Experiments were conducted on 11 captive flamingos. For each food item, we offered different ranges of food densities, up to 13 times natural abundance. Video footage allowed estimating intake rates. Contrary to theoretical predictions for filter feeders, intake rates did not increase linearly with increasing food density (type I). Intake rates rather increased asymptotically with increasing food density (type II) or followed a sigmoid shape (type III). Hence, flamingos were not able to ingest food in direct proportion to their abundance, possibly because of unique bill structure resulting in limited filtering capabilities. Overall, flamingos foraged more efficiently on Artemias. When feeding on Chironomids, birds had lower instantaneous rates of food discovery and required more time to extract food from the sediment and ingest it, than when filtering Artemias from the water column. However, feeding on rice was energetically more profitable for flamingos than feeding on Artemias or Chironomids, explaining their attraction for rice fields. Crucially, we found that food densities required for flamingos to reach asymptotic intake rates are rarely met under natural conditions. This allows us to predict an immediate negative effect of any decrease in prey density upon flamingo foraging performance.     

Cue use affects resource subdivision among three coexisting hummingbird species

Competition for food can influence the coexistence of speciesvia habitat selection, and learned behavior can influence foragingdecisions. I investigated whether learned behavior and competitionact together to influence species interactions between threecoexisting hummingbird species: black-chinned (Archilochusalexandri), blue-throated (Lampornis clemenciae), and magnificent(Eugenes fulgens) hummingbirds. I found that color cue useby individuals affects not only their foraging choices butalso population-level responses to competition. I presented hummingbirds two types of habitats (rich and poor feeders).All birds shared a preference for the rich feeders, but shiftedpreference toward poor feeders in response to competition.I used color cues to manipulate the amount of information availableto birds and examined the effects of two information states(complete or incomplete) on their foraging choices. I examined hummingbirds' preferences for the rich feeders when both competitordensities and information varied. To relate foraging choicesto energetic intake, I also analyzed energy gained during asingle foraging bout. Males of all species exhibited strongpreferences for rich feeders when they foraged with complete information and low competitor densities. Without complete information,the two subordinate species (black-chinned and magnificent)shifted preference away from rich feeders in response to highdensities of the dominant species (blue-throated). Each subordinatespecies shifted in a unique way: black-chinned hummingbirdsreduced foraging efficiency, while magnificent hummingbirdsreduced foraging time. Birds foraging with complete information remained selective on rich feeders even at high competitor densities.Thus, learned information affected competitive interactions(for rich feeders) among these species.     

Gut architecture,digestive constraints and feeding ecology of deposit-feeding and carnivorous polychaetes

Summary We analyze gut architectures of 42 species of marine polychaetes in terms of their anatomically distinct compartments, and quantify differences among guts in terms of ratios of body volume to gut volume, relative compartmental volumes, total gut aspect ratios and compartmental aspect ratios. We use multivariate techniques to classify these polychaetes into 4 groups: carnivores with tubular guts; deposit feeders with tubular guts; deposit feeders with 3 gut compartments; and deposit feeders with 4 or 5 gut compartments. Tubular guts, morphological expressions of plug flow, are common among deposit feeders and may allow relatively rapid ingestion rates and short throughput times. Median gut volume per unit of body volume in deposit feeders (31%) is twice that of carnivores (15%) and ranges up to 83% in one deep-sea species. Deep-sea deposit feeders tend to have relatively larger and longer guts than closely-related nearshore and shelf species. Guts of a number of deep-sea deposit feeders and nearshore and shelf deposit feeders from muddy environments are relatively longer and narrower as body size increases, suggesting that digestive diffusion limitations may be important. Gut volume scales as (body volume)¹ while ingestion rate scales as (body volume)^0.7. If diet and the chemical kinetics of digestion do not change appreciably, throughput time and thus the extent of digestion of given dietary components therefore must increase as a deposit feeder grows. Digestive processing constrainst may be most important in juveniles of species (especially those species with plug-flow guts) that are deposit feeders as adults.     

Remarks on antipredator behavior and food chain dynamics

When consumers feeding on a resource spend time in avoiding high risks of predation, the predator functional response declines with predator density. While this is well established, less attention has been paid to the dependence of the consumer functional response on predator density. Here we show how the separation of behavioral and ecological timescales allows one to determine both responses starting from an explicit behavioral model. Within the general set-up considered in this paper, the two functional responses can tend toward Holling type II responses when consumers react only weakly to predation. Thus, the main characteristics of the standard Rosenzweig-MacArthur tritrophic food chain (logistic resource and Holling type II consumer and predator) remain valid also when consumers have weak antipredator behavior. Moreover, through numerical analysis, we show that in a particular but interesting case pronounced antipredator behaviors stabilize the system.     

Marine subsidies change short‐term foraging activity and habitat utilization of terrestrial lizards

Resource pulses are brief periods of unusually high resource abundance. While population and community responses to resource pulses have been relatively well studied, how individual consumers respond to resource pulses has received less attention. Local consumers are often the first to respond to a resource pulse, and the form and timing of individual responses may influence how the effects of the pulse are transmitted throughout the community. Previous studies in Bahamian food webs have shown that detritivores associated with pulses of seaweed wrack provide an alternative prey source for lizards. When seaweed is abundant, lizards (Anolis sagrei) shift to consuming more marine‐derived prey and increase in density, which has important consequences for other components of the food web. We hypothesized that the diet shift requires individuals to alter their habitat use and foraging activity and that such responses may happen very rapidly. In this study, we used recorded video observations to investigate the immediate responses of lizards to an experimental seaweed pulse. We added seaweed to five treatment plots for comparison with five control plots. Immediately after seaweed addition, lizards decreased average perch height and increased movement rate, but these effects persisted for only 2 days. To explore the short‐term nature of the response, we used our field data to parametrize heuristic Markov chain models of perch height as a function of foraging state. These models suggest a “Synchronized‐satiation Hypothesis,” whereby lizards respond synchronously and feed quickly to satiation in the presence of a subsidy (causing an initial decrease in average perch height) and then return to the relative safety of higher perches. We suggest that the immediate responses of individual consumers to resource pulse events can provide insight into the mechanisms by which these consumers ultimately influence community‐level processes.     

Optimum search speed and activity: a dynamic game in a three-link trophic system

We analysed how a consumer should simultaneously trade-off search speed and time active in a game with predators that optimise their search speed. Both the consumers and the predators are continuously reproducing and maximise fitness by maximising the per capita growth rate. The impact of the predator's presence on consumer behaviour, and the effects of type I and II functional responses on the behaviour of both species are considered. In the analyses, consumers were allowed to co-ordinate activity or behave independently in relation to other consumers. The ESS-analysis of the game ensures that no mutant can invade the system. The independent activity was found to be optimal in all analyses, while the co-ordinated activity was only optimal at full activity where the two activity strategies coincided. The model showed that consumers should change activity to account for predation risk. Activity generally decreased with predation risk. Concerning the energetic aspects, both activity and search speed were important to account for the reproductive output. The functional responses influenced the optimum activity and search speed of consumers and predators. In general, the optimum behaviours showed complex non-linear responses in relation to the resource and the consumer density. A predator type II functional response had profound impacts on the properties of the optima, the stability and presence of alternative strategies. As a result of the optimum behaviours, the realised functional responses of both species became sigmoidal.     

Functional responses of adaptive consumers and community stability with emphasis on the dynamics of plant-herbivore systems

A comparatively recent focus in consumer–resource theory has been the examination of whether adaptive foraging by consumers, manifested through the functional response, can stabilize consumer–resource dynamics. We offer a brief synthesis of progress on this body of theory and identify the conditions likely to lead to stability. We also fill a gap in our understanding by analysing the potential for adaptively foraging herbivores, which are constrained by time available to feed and digestive capacity, to stabilize dynamics in a single-herbivore/two-plant resource system. Because foraging parameters of the adaptive functional response scale allometrically with herbivore body size, we parameterized our model system using published foraging data for an insect, a small mammal and a large mammal spanning four orders of magnitude in body size, and examined numerically the potential for herbivores to stabilize the consumer–resource interactions. We found in general that the herbivore–plant equilibrium will be unstable for all biologically realistic herbivore population densities. The instability arose for two reasons. First, each herbivore exhibited destabilizing adaptive consumer functional responses (i.e. density-independent or inversely density-dependent) whenever they selected a mixed diet. Secondly, the numerical response of herbivores, based on our assumption of density-independent herbivore population growth, results in herbivores reaching densities that enable them to exploit their resource populations to extinction. Our results and those of studies we reviewed indicate that, in general, adaptive consumers are unlikely to stabilize the dynamics of consumer–resource systems solely through the functional response. The implications of this for future work on consumer–resource theory are discussed.     

Predicting and testing functional responses: An example from a tardigrade–nematode system

Numerous studies have empirically measured consumer functional responses or theoretically developed response models, but whether these models can quantitatively predict observed data has hardly been tested. We perform such a test for the terrestrial predator–prey system Macrobiotus richtersi (Tardigrada)–Acrobeloides nanus (Nematoda). For two different size classes of A. nanus, we report a functional response as measured in the laboratory and quantitatively compare it to predictions of three models with different degrees of complexity: (1) the disc equation which does not include satiation effects; (2) the steady-state satiation (SSS) equation which assumes a constant level of predator satiation; and (3) the satiation model which accounts for prey depletion and increasing predator satiation over the course of the experiments. We parameterized these models with data that were measured independently of the functional response experiments. In both prey-size classes, the predictions of the satiation model matched the observations best, and the match came close to that of logistic regressions fitted to the observations. Thus, the parameterized satiation model seems to include the most important determinants of the functional response in our focal system. For understanding functional responses, we need more studies that compare data to independently derived model predictions.     

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).     

Adaptive responses of generalist herbivores to competition: Convergence or divergence

Summary Generalist herbivores are often faced with a choice of eating abundant, low quality foods or rare high quality foods. An adaptive forger in this situation should have mixed responses (Abrams, 1990) to the densities of the two food types. Competition from another generalist herbivore species will generally cause convergence in foraging time allocations when both species are strictly food limited. Competition will usually cause a convergent response in traits determining the relative consumption rates of the two food categories. Divergent responses are possible when consumers are not strictly food limited. Divergent responses are also expected in some other traits related to resource use, such as gut size. Evidence for the predicted responses and implications for plant-herbivore coevolution are discussed.     

When carnivores are “full and lazy”

Are animals usually hungry and busily looking for food, or do they often meet their energetic and other needs in the 24 h of a day? Focusing on carnivores, I provide evidence for the latter scenario. I develop a model that predicts the minimum food abundance at which a carnivore reaches satiation and is released from time constraints. Literature data from five invertebrate and vertebrate species suggest that food abundances experienced in the field often exceed this threshold. A comparison of energetic demands to kill rates also suggests that carnivores often reach satiation: for the 16 bird and mammal species analyzed, this frequency is 88% (average across species). Because pressure of time would likely lead to trade-offs in time allocation and thus to a nonsatiating food consumption, these results suggest that carnivores are often released from time constraints.     

Opposing organizing forces of deposit-feeding marine communities

We contend that a range of phenomena characterizing temperate deposit-feeding communities in low-energy environments is strongly organized by two principal opposing forces: (1) spatially localized inputs of detritus or new recruits, leading to a mosaic of initial patches, with subsequent impacts on spatio-temporal variation of species with limited mobility; and (2) the impact of mobile consumers, which move to spatially localized resources and thereby exert major controls over comparatively larger spatial scales. Surface deposit feeders react differently from deep feeders, in terms of spatio-temporal population change. The two opposing community control forces, combined with responses of deposit feeder functional groups, have potentially different effects on community structure. Mobile consumers, often acting as keystone species, may move to localized patches created by the bottom-up force of food input or by localized recruitment of prey. Their mobility, combined with predicted optimal foraging behavior, would usually produce a spatially homogenizing force, leading to reduced spatial variation in community composition. By contrast, spatially localized inputs of resources, if dominant, would always lead to strong spatial heterogeneity. Dominance of complex space–time variation in detrital enrichment would lead to strong spatio-temporal complexity in macrofauna if the response of recruiting larvae and rapidly growing small invertebrate populations was immediate and keyed to localized food input. The ability of mobile consumers to locate detritus, combined with the spatial distribution and overall input rate of detritus, should determine the balance of surface and deep-feeding deposit feeders. The opposing force approach can be applied to communities generally.     

Experimental Predictions of The Functional Response of A Freshwater Fish

The functional response is the relationship between the feeding rate of an animal and its food density. It is reliant on two basic parameters; the volume searched for prey per unit time (searching rate) and the time taken to consume each prey item (handling time). As fish functional responses can be difficult to determine directly, it may be more feasible to measure their underlying behavioural parameters in controlled conditions and use these to predict the functional response. Here, we tested how accurately a Type II functional response model predicted the observed functional response of roach Rutilus rutilus, a visually foraging fish, and compared it with Type I functional response. Foraging experiments were performed by exposing fish in tank aquaria to a range of food densities, with their response captured using a two‐camera videography system. This system was validated and was able to accurately measure fish behaviour in the aquaria, and enabled estimates of fish reaction distance, swimming speed (from which searching rate was calculated) and handling time to be measured. The parameterised Type II functional response model accurately predicted the observed functional response and was superior to the Type I model. These outputs suggest it will be possible to accurately measure behavioural parameters in other animal species and use these to predict the functional response in situations where it cannot be observed directly.     

Foraging guild membership explains variation in waterbird responses to the hydrological regime of an arid‐region flood‐pulse river in Namibia

1. Little is known about hydrological influences on tropical waterbird communities. We used a 16‐year data set (1991–2007) of waterbird censuses, together with a classification of observed species into foraging guilds, to explore the relationships between natural variations in flow regime, foraging guild and the community composition of waterbirds at the Okavango River in the Caprivi Strip of north‐eastern Namibia, southern Africa. 2. We addressed three hypotheses to explain variation in waterbird community composition: (i) exploitation (birds move towards resource‐rich patches to exploit periods of high food abundance); (ii) escapism (declines in regional habitat quality force birds to aggregate in perennial waterbodies); and (iii) interaction (bird assemblages are dominated by intra‐ and interspecific interactions, such as flock formation for breeding or moulting, that can be explained better by life history demands or competition than by resource availability). 3. Waterbirds in different foraging guilds responded strongly but at different periods to changes in the hydrological environment, creating a complex but predictable successional pattern in community composition through time. Deep‐water feeders responded fastest (abundance peaking 2 months post‐flood), followed by shallow‐water feeders (4 months) and emergent vegetation feeders (7 months). Species that forage on short vegetation or in mud showed a bimodal response with peaks in abundance at 3 and 8 months post‐flood. 4. Our results indicated a strong effect of the local flow regime and hence supported the exploitation hypothesis. The foraging guild approach allowed us to identify clear patterns in a highly complex ecosystem and shows considerable promise as an analytical tool for similar data sets. Our results further suggest that while the entire bird community will be affected by hydrological alterations such as impoundments, water extraction and climate change, deep‐water feeders may be one of the most vulnerable groups.     

Evolutionary branching and long-term coexistence of cycling predators: critical function analysis

It is well known that two predators with different functional responses can coexist on one prey when the system exhibits nonequilibrium dynamics. In this paper, we investigate under which conditions such coexistence is evolutionarily stable, and whether the two predators may evolve from a single ancestor via evolutionary branching. We assume that predator strategies differ in handling time, and hence in the shape of their Holling type II functional response. Longer handling times are costly in terms of lost foraging time, but allow the predator to extract more nutrients from the prey and therefore to produce more offspring per consumed prey. In the analysis, we apply a new method to accommodate arbitrary trade-off functions between handling time and offspring production. Contrary to previous results obtained assuming a particular trade-off [Kisdi, E. and Liu, S., 2006. J. Evol. Biol. 19, 49-58], we find that evolutionary branching of handling time is possible, although it does not appear to be very likely and can be excluded for a class of trade-offs. Evolutionarily stable coexistence of two predators occurs under less restrictive conditions, which are always satisfied when the trade-off function has two strongly concave parts connected by a convex piece.     

Predatory responses of selected lines of developmental variants of ladybird,Propylea dissecta (Coleoptera: Coccinellidae) in relation to increasing prey and predator densities

Individuals of the same species, population and generation frequently exhibit sub-maximal and significant genetic and phenotypic variation in their rate of development, showing slow and fast developers. Fast developers commonly have higher foraging and predation rates than slow developers. The consequence of such differences and foraging for the efficacy of biocontrol species remains under-explored. Slow and fast developers from a population of the ladybird, Propylea dissecta were separated and selected experimentally for F15 generations, and the predatory response of fourth instar larvae of control and experimentally selected slow and fast developers was then assessed at differing levels of prey (pea aphid, Acyrthosiphon pisum) and conspecific predator abundance. All individuals, whether slow or fast developers, showed a Type-II functional response, decrease in proportion of prey consumed with increasing prey biomass and an increase in proportion of prey consumed with increasing predator density. The proportion of prey consumed was highest in experimental fast developers and lowest in experimental slow developers. Attack rate was highest and handling time longest in slow developers of control/experimental groups. Mutual interference was least while area of discovery was highest in experimental fast developers. Thus, selection of fast developers for F15 generations led to higher functional responses, slower attack rates and faster prey consumption. This lower mutual interference and high searching efficiency indicates that they can be experimentally selected and used for better control of the pea aphids. This study is the first attempt to evaluate predatory responses of selected lines of an aphidophagous ladybird.