Quantifying predator dependence in the functional response of generalist predators

A long‐standing debate concerns how functional responses are best described. Theory suggests that ratio dependence is consistent with many food web patterns left unexplained by the simplest prey‐dependent models. However, for logistical reasons, ratio dependence and predator dependence more generally have seen infrequent empirical evaluation and then only so in specialist predators, which are rare in nature. Here we develop an approach to simultaneously estimate the prey‐specific attack rates and predator‐specific interference (facilitation) rates of predators interacting with arbitrary numbers of prey and predator species in the field. We apply the approach to surveys and experiments involving two intertidal whelks and their full suite of potential prey. Our study provides strong evidence for predator dependence that is poorly described by the ratio dependent model over manipulated and natural ranges of species abundances. It also indicates how, for generalist predators, even the qualitative nature of predator dependence can be prey‐specific.     

捕食者—猎物功能响应模型研究

本文通过分析在捕食的情况下猎物种群的平均绝对增长速率与捕食效应的关系以及捕食者的捕食平均绝对速率与猎物密度的关系,建立了捕食者-猎物功能响应的一般模型: 其中,A为捕食者与猎物行为常数,f(H_t)为待定函数。 在上述模型的基础上讨论了在捕食速率与猎物密度无关和有关时的功能响应行为。 通过对上面模型的分析,笔者认为功能响应模型按Holling的Ⅰ、Ⅱ、Ⅲ型响应曲线相应划分很不方便。建议按“捕食速率与猎物密度无关或有关”两个类型划分。并认为Ⅲ型模型在昆虫中也能得到较广泛的应用。     

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.     

The functional response of Toxorhynchites rutilus rutilus to changes in the population density of its prey Aedes aegypti

We present an analysis of the functional response of the predator Toxorhynchites rutilus rutilus (Coquillett) to changes in the density of the larvae of Aedes aegypti (L.) (Diptera: Culicidae). The experiment was replicated for five different ages, and at three different densities of the predator. The data were fitted to Rogers' (1972) random predator equation by non-linear least-squares in order to estimate searching efficiency and handling time for each experimental treatment. The data show that estimated searching efficiencies are highest at intermediate ages of the predator for all predator densities tested. Handling time declines exponentially with increasing predator age. There is a marked interference effect; searching efficiency decreases with increased predator density, and this is most pronounced at intermediate prey ages. Estimated handling times increase with predator density at a rate which declines with increasing predator age.     

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.     

Temperature dependence of the membrane resistance in Characeae cells

Changes in the electrical resistance of internodal cells of Nitellopsis obtusa (Desv. in Lois) J. Gr. and Lychnothamnus barbatus (Meyen) Leonh., produced by short-lasting temperature changes (3-min intervals) in the range of 4⇌48°C were measured. In the whole temperature range examined the electrical resistance of the cell membranes underwent from 5 to 9 distinct changes; the overall changes were approximately hyperbolic, while in certain narrow temperature ranges they were non-monotonic, and in others linear. Arrhenius plots of these dependencies provide data which suggest a specific, stepwise character of changes in the permeability to ions, produced by temperature alterations and probably connected with corresponding modifications of cell membrane fluidity. This seems to support the view that the cell membranes of the examined plant species may exist in different, discrete, physiological states characteristic of certain temperature ranges.     

Effect of treating eggs of cotton bollworm with Bacillus thuringiensis Berliner on functional response of Trichogramma brassicae Bezdenko

Cotton bollworm, Helicoverpa armigera (Hübner) is a cosmopolite insect pest of a wide spectrum of crops such as cotton, maize, tomato, soybean, etc. Egg parasitoids mainly Trichogramma brassicae Bezdenko and Bacillus thuringiensis Berliner (Bt) are biological control agents, that are used as components of sustainable and environmentally compatible IPM systems. Although Bt does not come in direct contact with egg parasitoids, it may persist within the host’s body and affect the quality of the host’s eggs via biochemical changes in their mother and possibly behaviour and potency of the parasitoids. In this study, the functional response of T. brassicae to different densities of H. armigera eggs was investigated in two sets of experiments at 26?±?1?°C, 65?±?5% RH, and 16: 8?h photoperiod. The first group was a control and the second one were eggs laid by hosts treated as 3rd instar larvae with LC₂₀ of Bt (determined as 9.8?×?10^5?IU/l of artificial diet based on a preliminary bioassay). A type III functional response was observed in both treatments with a direct density dependent mortality up to eight host eggs and an inverse one upward. Both handling time and searching efficiency were affected by Bt treatment as the handling time was increased by a factor of 1.5 and the searching efficiency was decreased by a factor of 0.6. The searching efficiencies were 0.0310?±?0.003 and 0.0182?±?0.005?h^?1, and handling times were 1.134?±?0.042 and 1.672?±?0.082?h in control and Bt treatment respectively.     

Dynamics of handling time and functional response by larvae of Chrysomya albiceps (Dipt., Calliphoridae) on different prey species

Abstract:  One way to understand the behavioural patterns exhibited by a predator in response to prey density is to evaluate its functional response. Such evaluation yields information about basic mechanisms of prey–predator dynamics, and is an essential component of prey–predator models. In this paper we analysed experimentally the functional response and the handling time spent by Chrysomya albiceps on different prey species and larval instars of blowflies. The type II functional response was observed when second instar larvae of Chrysomya megacephala and Chrysomya macellaria were consumed. The handling time spent by the predator was significantly different between instars and species. The implications of the functional response and handling time for the interaction dynamics of Brazilian Chrysomyinae species are discussed.     

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

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

The functional response of copepodid stages to adult of Parabroteas sarsi (copepoda,calanoida)

P. sarsi is a carnivorous calanoid commonly found in South Andes lakes. Feeding experiments were carried out in order to analyze the functional response of P. sarsi (copepodid IV to adult) on different cladoceran prey. Predation rates increased with increasing prey density up to maximum (type II) in almost cases. The highest attack coefficients were obtained when P. sarsi adults were fed with the smaller prey (C. dubia juvenile and B. longirostris). The ingestion rates of copepodid IV and CV were smaller than for the adults. The ingested biomass as a proportion of predator biomass (B_e/B_p) showed an inversal relationship with the predator length. The maximum B_e/B_p ratio, in both sex of P. sarsi, was achieved with C. dubia adult, the intermediate-sized prey.     

Know thy enemy: Behavioural response of a native mammal (Rattus lutreolus velutinus) to predators of different coexistence histories

Abstract Predation is recognized as a major selective pressure influencing population dynamics and evolutionary processes. Prey species have developed a variety of predator avoidance strategies, not least of which is olfactory recognition. However, within Australia, European settlement has brought with it a number of introduced predators, perhaps most notably the red fox (Vulpes vulpes) and domestic cat (Felis catus), which native prey species may be unable to recognize and thus avoid due to a lack of coexistence history. This study examined the response of native Tasmanian swamp rats (Rattus lutreolus velutinus) to predators of different coexistence history (native predator‐ spotted‐tail quoll (Dasyurus maculatus), domestic cats and the recently introduced red fox). We used an aggregate behavioural response of R. l. velutinus to predator integumental odour in order to assess an overall behavioural response to predation risk. Rattus lutreolus velutinus recognized the integumental odour of the native quoll (compared with control odours) but did not respond to either cat or fox scent (compared with control odur). In contrast, analyses of singular behaviours resulted in the conclusion that rats did not respond differentially to either native or introduced predators, as other studies have concluded. Therefore, measuring risk assessment behaviours at the level of overall aggregate response may be more beneficial in understanding and analysing complex behavioural patterns such as predator detection and recognition. These results suggest that fox and cat introductions (and their interactive effects) may have detrimental impacts upon small native Tasmanian mammals due to lack of recognition and thus appropriate responses.     

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.     

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.     

Role of different habitats for the functional response of Crytorrhinus lividipennis (Hemiptera: Miridae) on Nilaparvata lugens (Hemiptera: Delphacidae)

The functional response of a predator, Cyrtorrhinus lividipennis, on the brown planthopper, Nilaparvata lugens, was investigated in two different experimental habitats: a piece of tiller in a petri dish (5.5?cm in diameter) and a rice plant in a net cage (5.5?cm diameter?×?43?cm height) for 24?h at room temperature. In the petri dish experiment, 2nd–5th instar nymphs, adult male, and female C. lividipennis were introduced in separate experiments to eggs of N. lugens at densities of five, 10, 20, 30, and 40 eggs per piece of rice. In the rice plant experiment, each C. lividipennis was introduced to a cage with a rice plant containing N. lugens eggs. After 24?h, the number of dead eggs and remaining eggs were counted and data fitted to three functional response models. Among the three types of functional responses, Type II best described the predator response to host densities in N. lugens in both experimental habitats, according to the logistic regression analysis value. The results showed that C. lividipennis was a more effective predator in the rice plant experiment compared to the disc experiment. Additionally, the searching efficiency and handling time parameters were different in the two different experimental habitats. This may cause errors when applying the functional response to biological control and predator–prey models. Different habitats and other environmental conditions from the experiment and natural rice field have to be considered.     

Prey: predator ratio dependence in the functional response of a freshwater amphipod

1. First known for their shredding activity, freshwater amphipods also behave as active predators with consequences for prey population regulation and amphipod coexistence in the context of biological invasions. 2. A way to quantify predation is to determine the average consumption rate per predator, also known as its functional response (FR). 3. Although amphipods are gregarious and can display social interactions that can alter per capita consumption rates, previous studies using the FR approach to investigate amphipod predation ignored such potential mutual interference because they did not consider variations in predator density. 4. We investigated the FR of Echinogammarus berilloni feeding on dipteran larvae with joint variations in prey and predator densities. This bivariate experimental design allowed us to estimate interference and to compare the fits of the three main classes of theoretical FR models, in which the predation rate is a function of prey density alone (prey‐dependent models), of both prey and predator densities (predator‐dependent models) or of the prey‐to‐predator ratio (ratio‐dependent models). 5. The Arditi–Ginzburg ratio‐dependent FR model provided the best representation of the FR of E. berilloni, whose predation rate showed a decelerating rise to a horizontal asymptote as prey abundance increased. 6. Ratio dependence means that mutual interference between amphipods leads to prey sharing. Mutual interference is likely to vary between amphipod species, depending on their level of aggressiveness.     

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.