Unpacking chimpanzee (Pan troglodytes) patch use: Do individuals respond to food patches as predicted by the marginal value theorem?

The marginal value theorem is an optimal foraging model that predicts how efficient foragers should respond to both their ecological and social environments when foraging in food patches, and it has strongly influenced hypotheses for primate behavior. Nevertheless, experimental tests of the marginal value theorem have been rare in primates and observational studies have provided conflicting support. As a step towards filling this gap, we test whether the foraging decisions of captive chimpanzees (Pan troglodytes) adhere to the assumptions and qualitative predictions of the marginal value theorem. We presented 12 adult chimpanzees with a two-patch foraging environment consisting of both low-quality (i.e., low-food density) and high-quality (i.e., high-food density) patches and examined the effect of patch quality on their search behavior, foraging duration, marginal capture rate, and its proxy measures: giving-up density and giving-up time. Chimpanzees foraged longer in high-quality patches, as predicted. In contrast to predictions, they did not depress high-quality patches as thoroughly as low-quality patches. Furthermore, since chimpanzees searched in a manner that fell between systematic and random, their intake rates did not decline at a steady rate over time, especially in high-quality patches, violating an assumption of the marginal value theorem. Our study provides evidence that chimpanzees are sensitive to their rate of energy intake and that their foraging durations correlate with patch quality, supporting many assumptions underlying primate foraging and social behavior. However, our results question whether the marginal value theorem is a constructive model of chimpanzee foraging behavior, and we suggest a Bayesian foraging framework (i.e., combining past foraging experiences with current patch sampling information) as a potential alternative. More work is needed to build an understanding of the proximate mechanisms underlying primate foraging decisions, especially in more complex socioecological environments.     

Context dependence in foraging behaviour of Achillea millefolium

Context-dependent foraging behaviour is acknowledged and well documented for a diversity of animals and conditions. The contextual determinants of plant foraging behaviour, however, are poorly understood. Plant roots encounter patchy distributions of nutrients and soil fungi. Both of these features affect root form and function, but how they interact to affect foraging behaviour is unknown. We extend the use of the marginal value theorem to make predictions about the foraging behaviour of roots, and test our predictions by manipulating soil resource distribution and inoculation by soil fungi. We measured plant movement as both distance roots travelled and time taken to grow through nutrient patches of varied quality. To do this, we grew Achillea millefolium in the centers of modified pots with a high-nutrient patch and a low-nutrient patch on either side of the plant (heterogeneous) or patch-free conditions (homogeneous). Fungal inoculation, but not resource distribution, altered the time it took roots to reach nutrient patches. When in nutrient patches, root growth decreased relative to homogeneous soils. However, this change in foraging behaviour was not contingent upon patch quality or fungal inoculation. Root system breadth was larger in homogeneous than in heterogeneous soils, until measures were influenced by pot edges. Overall, we find that root foraging behaviour is modified by resource heterogeneity but not fungal inoculation. We find support for predictions of the marginal value theorem that organisms travel faster through low-quality than through high-quality environments, with the caveat that roots respond to nutrient patches per se rather than the quality of those patches.     

The impact of patch encounter rate on patch residence time of female parasitoids increases with patch quality

Abstract.  1. For animal species that forage on patchily distributed resources, patch time allocation is of prime importance to their reproductive success. According to Charnov's marginal value theorem (MVT), the rate of patch encounter should influence negatively the patch residence time: as the rate of patch encounter decreases, the patch residence time increases. Moreover, the MVT predicts that animals should stay longer in high quality patches.
2. Using the aphid parasitoid Aphidius rhopalosiphi (Hymenoptera: Aphidiinae), the effects of these two factors (patch encounter rate and host density) were combined in order to test if the increment in patch residence time for a given decrease in patch encounter rate was larger for high quality patches than for low quality patches.
3. The results show a significant effect of the interaction between the two factors. In high host density patches, parasitoids spent more time if they experienced a low patch encounter rate, while in low host density patches, patch encounter rate had no significant effect on the patch residence time. This suggests that the response of A. rhopalosiphi females to patch encounter rate varied with host density in the patch. Moreover, the same interaction effect was observed for the number of ovipositor contacts on aphids.
4. Parasitoid females can use patch encounter rate to estimate patch density in the habitat but the effect of this estimate on their patch residence time is modulated by patch quality. Staying longer in a patch when patches are rare is more advantageous when the fitness gained by doing so is large. In low quality patches, the expected fitness gain is small and the female may gain more by leaving and taking her chance at finding another patch.     

Simulation of patch use by monkeys using operant conditioning

Food patch use by Japanese monkeys was examined using an operant conditioning procedure. Modified progressive ratio schedules, in which the probability of reinforcement decreases exponentially with the number of bar presses, were presented to 2 Japanese monkeys. Two types of schedule were used in each experimental session. One represented high quality food patches, where the probability of reinforcement was twice as high as in the other, which represented low quality food patches. The number of bar presses in each food patch was counted. Monkeys responded more frequently in high quality patches. The probability of reinforcement for the last response in each patch was the same in both types of schedule. The number of responses increased with a decrease in the occurrence of high quality patches, and with an increase in the inter-patch time interval. These results are in agreement with the predictions of Charnov’s marginal value theorem (Charnov, 1976). The pattern of patch use by monkeys observed in this study is discussed in terms of optimal foraging strategy.     

Optimal trade-offs between competing behavioural demands in the great tit

We present a dynamic optimal control model to show how territorial male great tits (Parus major L.) should combine territorial vigilance with foraging. In the model, territory owners allocate time either to feeding in patches or travelling between them. Travelling is compatible with territorial vigilance, while feeding is not. Owners are assumed to adjust their patch residence and travel times in order to minimize the costs accruing from intruders on their territories, while at the same time reducing their hunger. The relation between patch residence and travel time matches that of Charnov's (1976) marginal value theorem while hunger is high, but as hunger is reduced the dynamic model predicts shorter patch residence times for any observed travel time. We present supporting evidence from an experimental test with captive male great tits.     

Optimal patch residence time in egg parasitoids: innate versus learned estimate of patch quality

Charnovs marginal value theorem predicts that female parasitoids should exploit patches of their hosts until their instantaneous rate of fitness gain reaches a marginal value. The consequences of this are that: (1) better patches should be exploited for a longer time; (2) as travel time between patches increases, so does the patch residence time; and (3) all exploited patches should be reduced to the same level of profitability. Patch residence time was measured in an egg parasitoid Anaphes victus (Hymenoptera: Mymaridae) when patch quality and travel time, approximated here as an increased delay between emergence and patch exploitation, varied. As predicted, females stayed longer when patch quality and travel time increased. However, the marginal value of fitness gain when females left the patch increased with patch quality and decreased with travel time. A. victus females appear to base their patch quality estimate on the first patch encountered rather than on a fixed innate estimate, as was shown for another egg parasitoid Trichogramma brassicae. Such a strategy could be optimal when inter-generational variability in patch quality is high and within-generational variability is low.     

Optimal grazing of wapiti (Cervus elaphus) on grassland: Patch and feeding station departure rules

Summary We studied factors which may shape giving-up decisions of wapiti grazing grassland patches (area where a wapiti initiates and terminates a feeding sequence) and feeding stations (area within a patch that a wapiti can reach without moving its forelegs). In grassland patches, cropping rate decreased after a critical period, whereas at feeding stations cropping rate increased with cumulative bites consumed. The number of feeding stations grazed, number of bites taken and grazing time did not dictate the termination of grazing in a patch. Wapiti gave up a patch only after the cropping rate at a feeding station dropped below the seasonal expectation during trials on lush pasture in May, but gave up after the cropping rate dropped below the seasonal expectation at two consecutive feeding stations in March/April and August when foraging conditions were less favourable. This confirmed a prediction of the marginal value theorem. Wapiti did not give up a feeding station according to bites taken, grazing time or cropping rate, but they left feeding stations when their lateral neck angle reached a critical point suggesting a biokinetic explanation. Leaving feeding stations when ungrazed forage can no longer be reached and patches when intake rate drops both appeared to be rules used by wapiti grazing grasslands of the boreal mixed wood forest.     

Choosing where to feed: the influence of competition on feeding behaviour of cod, Gadus morhua L.

Groups of cod, Gadus morhua L, presented with two feeding patches with a food abundance ratio of 2:1, distributed themselves between the patches in a ratio of 2.5:1. This is slightly higher than the 2:1 ratio predicted by the ideal free distribution theory. Large differences were observed in competitive ability between individual fish. A strong correlation was found between feeding success of individuals and time spent in a feeding patch. The more successful competitors caught about 2.5 times as many food items in the rich patch as in the poor patch. The less successful competitors caught an equal amount of food in both patches. All competitors, however, spent significantly more time in the rich patch. These results suggest that hunting success is the most important factor in assessing patch quality. However, it is not the only parameter which cod use in deciding where to feed.     

Patch Time Allocation by the Parasitoid Diadegma semiclausum (Hymenoptera: Ichneumonidae). I. Effect of Interpatch Distance

We observed the foraging behavior of Diadegma semiclausum (Hymenoptera:Ichneumonidae), a larval parasitoid of the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae), in a wind tunnel to determine how interpatch distance affects patch time allocation. Individual female wasps were released onto an experimental patch infested with host larvae and were allowed freely to leave for an identically extrapatch placed upwind of the experimental patch with varying interpatch distances. The effects of interpatch distance and within-patch foraging experience on the patch-leaving tendency of the parasitoid were analyzed bymeans of the proportional hazards model. Increasing interpatch distance andunsuccessful host encounter as a result of host defense decreased the patch-leaving tendency, while successful oviposition and unsuccessful search time since last oviposition increased the patch-leaving tendency. Asa result, both patch residence time and number of ovipositions by D. semiclausum increased with increasing interpatch distance, which appears to agree with the general predictions of the marginal value theorem that a parasitoid should stay longer and parasitize more hosts with increasing interpatch distance.     

Winter foraging by muskoxen: a hierarchical approach to patch residence time and cratering behaviour

We examined the temporal and spatial patterns of feeding behaviours of muskoxen during winter in the High Arctic. Pawing motions (to uncover forages beneath snow cover) were strongly aggregated into temporal bouts. Similarly, feeding stations (areas exploitable without motion of the forelegs) were aggregated into spatial patches. Muskoxen responded to greater snow accumulation at feeding sites by increasing the rates of pawing, rates of pawing bouts, number of pawing strokes per bout, and station residence times. Patch residence times showed little relationship to snow or forage abundance because, as muskoxen increased station residence times, they decreased the number of stations per patch. Muskoxen displaced one another from feeding stations more frequently as snow thickness and group size increased. Time spent at feeding stations was positively correlated to travel costs, in accordance with the marginal value model of patch residence. The model was not supported, however, at the scale of the feeding patch. The results indicate that behavioural responses of muskoxen to foraging conditions differ across scales.     

斑块质量对大斑啄木鸟冬季觅食行为的影响

为了解大斑啄木鸟(Dendrocopos major)冬季对食物斑块的利用对策,2011年1月和2012年2～3月,在内蒙古乌拉特前旗的农田防护林中,采用目标动物取样法和全事件记录法,观察了大斑啄木鸟在食物斑块的觅食行为,利用主成分分析方法对斑块质量进行评价,通过比较不同质量斑块中大斑啄木鸟的觅食频次、停留时间、觅食成功频次及觅食成功率等指标,分析斑块质量对其觅食行为的影响。结果显示,在不同质量斑块中大斑啄木鸟的觅食频次、停留时间、觅食成功频次差异都极显著,但觅食成功率差异不显著;除停留时间外,不同性别间觅食差异不显著。大斑啄木鸟的觅食频次、停留时间、觅食成功频次与斑块质量呈显著正相关,觅食成功率与斑块质量相关性不显著。大斑啄木鸟倾向于在质量水平高的斑块觅食,表现为在这些斑块停留时间更长、往返次数更频繁;但觅食成功率不受斑块质量影响,这可能是大斑啄木鸟适应不同觅食环境的一种生存本能。     

Gibbon foraging decisions and the marginal value model

We use data from an observational field study of frugivory in two sympatric gibbons, lar (Hylobates lar) and siamang (H. syndactylus), to test assumptions and predictions of the marginal value model (MVM). A key prediction of the MVM is that marginal gain rates at the time of leaving the patch are equal across patch types. We found that this is not the case for gibbons: rates of energy intake at the end of feeding sessions were significantly different for different types of fruit, and we could not attribute this to temporal variation in fruit availability. Initial and final caloric intake rates were highly correlated. This suggests that gibbons do not adjust the time spent in patches in order to maximize the average rate of energy intake. Similar results were obtained for all other currencies considered. Gibbon foraging appears to satisfy several, but not all, assumptions of the MVM. As required by the model, fruit patches occur as discrete units, patches are encountered sequentially, travel time between patches exceeds search time between items within a patch, search for and search within patches are incompatible activities, and intake rates decline over time spent in a patch. However, the declining rates we detected may be an effect of satiation instead of patch depletion, patches probably are not encountered at random, and group members may not forage independently. Thus, our results suggest that the MVM is not an adequate model of gibbon foraging behavior, but they do not invalidate the MVM per se.     

Influence of size and density of browse patches on intake rates and foraging decisions of young moose and white-tailed deer

We examined the functional response and foraging behavior of young moose (Alces alces) and white-tailed deer (Odocoileus virginianus) relative to animal size and the size and distribution of browse patches. The animals were offered one, three, or nine stems of dormant red maple (Acer rubrum) in hand-assembled patches spaced 2.33, 7, 14, or 21 m apart along a runway. Moose took larger twig diameters and bites and had greater dry matter and digestible energy intake rates than did deer, but had lower cropping rates. Moose and deer travelled at similar velocities between patches and took similar numbers of bites per stem. We found that a model of intake rate, based on the mechanics of cropping, chewing, and encountering bites, effectively described the intake rate of moose and deer feeding in heterogeneous distributions of browses. As patch size and density declined, the animals walked faster between patches, cropped larger bites, and cropped more bites per stem, and hence, dry matter intake rates remained relatively constant. As is characteristic of many hardwood browse stems, however, potential digestible energy concentration of the red maple stems declined as the size and number of bites removed (i.e., stem diameter at point of clipping) by the animals increased. Therefore, the digestible energy content of the diet declined with decreasing patch size and density. Time spent foraging within a patch increased as patch size increased and as distance between patches increased, which qualitatively supported the marginal-value theorem. However, actual patch residence times for deer and moose exceeded those predicted by the marginal-value theorem (MVT) by approximately 250%. The difference between actual and predicted residence time may have been a result of (1) an unknown or complex gain function, (2) the artificial conditions of the experiments, or (3) assumptions of MVT that do not apply to herbivores.     

Should I stay or should I go? Patch departure decisions by herbivores at multiple scales

The question of how much time a foraging herbivore should spend in a patch of food poses a central challenge in classical foraging theory. However, there remains uncertainty about the relevance of the patch paradigm to foraging decisions by large herbivores. This paper examines evidence for successfully predicting and quantifying patch departure decisions for large mammalian herbivores foraging across several spatial and temporal scales. Departure decisions at fine scales are influenced by tradeoffs between maximizing intake rate and food quality. Classical models for departure decisions at larger spatial scales, particularly the marginal value theorem, appear inadequate. We advocate exploring alternative models for predictions of residence time at the patch scale.     

Time's crooked arrow: optimal foraging and rate-biased time perception

Time perception is critical to animal behaviours requiring anticipation of future events based on present information about the environment. Most models of animal foraging assume that animals are capable of measuring absolute time despite evidence that animals measure time with predictable biases in mean and variance. We incorporate the evidence for a rate-biased subjective time perception into a classic model of optimal foraging, the marginal value theorem. If acceleration of the clock rate is proportional to food intake rate and time is perceived similarly when in transit between patches as it is while waiting in a patch following eating, organisms are predicted to follow the predictions of the marginal value theorem exactly. However, a nonlinear relationship between clock rate and food intake rate, unequal wait and transit time perception, or any lag in the clock predicts characteristic suboptimal behaviour. We discuss how this mechanism for suboptimal behaviour compares with others in the literature and how it can be recognized in experiments. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Dispersal in a metapopulation of the bush cricket, Metrioptera bicolor (Orthoptera: Tettigoniidae)

1. I present a stochastic simulation model that describes individual movements of Metrioptera bicolor Philippi in a heterogeneous landscape, consisting of patches of suitable habitat surrounded by a matrix of unprofitable habitats. Although the model is parameterized with information about daily movement behaviour, it can generate spatially explicit predictions about inter-patch dispersal rates for much longer periods, e.g. one generation.
2. Long-term dispersal experiments were conducted to evaluate model predictions. Patch-specific emigration rates and the total distance moved by individuals could be predicted with satisfactory precision. Because of the stochastic nature of the model, it failed to predict which recipient patches emigrating individuals actually chose in a particular situation.
3. Spatially explicit simulations of the movement model were made for the whole natural distribution area of M. bicolor . The results suggest that emigration rates are negatively correlated with patch size. Local populations occurring on small patches may be more prone to extinction than those on large patches, by losing more emigrants than are compensated for by immigration.     

The detection of cryptic prey by blue jays (Cyanocitta cristata) I: the effects of travel time

The behaviour of blue jays (Cyanocitta cristata) hunting for dispersed, cryptic prey was investigated in an operant simulation in which jays were trained to search projected images for noctuid moths. Each image contained either a single moth or no moth. Each trial was structured so as to simulate travelling between patches, searching within patches, and attacking and handling each moth that was detected. In two experiments in which the travel time between patches was manipulated, increases in travel time produced increased persistence within patches. Although this qualitative effect was predicted by the marginal value theorem, quantitative analyses revealed that the blue jays were using a strategy that was more sophisticated and more efficient than the simple time-in-patch rule implied by the marginal value theorem.     

Patch exploitation strategy by an egg parasitoid in constant or variable environment

Abstract.  1. In this paper, the foraging behaviour (the proximal mechanisms involved in patch-leaving rules and the egg dispersion) of an egg parasitoid, Anaphes victus , was analysed in environments containing either patches of constant quality (i.e. predictable environment) or patches of variable quality (i.e. unpredictable environment) in order to determine the motivational mechanisms used in patch-leaving strategies.
2. Comparison of the patch exploitation strategy of A. victus between the different habitats suggested that the response of A. victus to a given patch quality strongly depended on its past experiences. Females allocated more time and more eggs in a mixed quality patch after experiencing a poor quality patch than after experiencing a good quality patch. In a poor quality patch, females superparasitised more frequently after experiencing a poor quality patch than after experiencing a good quality patch. In a good quality patch, A. victus females laid more eggs after having visited two poor quality patches than after visiting good quality patches.
3. Recent foraging experiences are used to estimate both the availability and spatial distribution of hosts in the environment and adjust foraging decisions accordingly. The observed variability in the patch-leaving rules within the same species stresses the importance of previous experience when describing behaviours of female parasitoids.     

On optimal diet in a patchy environment

Optimal foraging theory has dealt with the following questions independently: (1) On what prey types should an individual predator feed (optimal diet)? (2) How long should a predator stay in each patch if prey is patchily distributed (optimal allocation of time to patches) ? This paper explores optimal foraging in patches containing several different kinds of prey. Results obtained by simulation show that deviations from recent predictions are to be expected, particularly for long interpatch travel times and rapid depletion of profitable prey types. In these situations the tactics of feeding as either specialist or as a generalist can be inferior to a tactic which starts as a specialist and then expands the diet after some time in the patch. Furthermore, predators should not necessarily stay longer in a patch if interpatch travel time increases. Some experimental tests of these new predictions are proposed.     

Foraging Patch Selection in Winter: A Balance between Predation Risk and Thermoregulation Benefit

In winter, foraging activity is intended to optimize food search while minimizing both thermoregulation costs and predation risk. Here we quantify the relative importance of thermoregulation and predation in foraging patch selection of woodland birds wintering in a Mediterranean montane forest. Specifically, we account for thermoregulation benefits related to temperature, and predation risk associated with both illumination of the feeding patch and distance to the nearest refuge provided by vegetation. We measured the amount of time that 38 marked individual birds belonging to five small passerine species spent foraging at artificial feeders. Feeders were located in forest patches that vary in distance to protective cover and exposure to sun radiation; temperature and illumination were registered locally by data loggers. Our results support the influence of both thermoregulation benefits and predation costs on feeding patch choice. The influence of distance to refuge (negative relationship) was nearly three times higher than that of temperature (positive relationship) in determining total foraging time spent at a patch. Light intensity had a negligible and no significant effect. This pattern was generalizable among species and individuals within species, and highlights the preponderance of latent predation risk over thermoregulation benefits on foraging decisions of birds wintering in temperate Mediterranean forests.