Energy beyond food: foraging theory informs time spent in thermals by a large soaring bird

Current understanding of how animals search for and exploit food resources is based on microeconomic models. Although widely used to examine feeding, such constructs should inform other energy-harvesting situations where theoretical assumptions are met. In fact, some animals extract non-food forms of energy from the environment, such as birds that soar in updraughts. This study examined whether the gains in potential energy (altitude) followed efficiency-maximising predictions in the world's heaviest soaring bird, the Andean condor (Vultur gryphus). Animal-attached technology was used to record condor flight paths in three-dimensions. Tracks showed that time spent in patchy thermals was broadly consistent with a strategy to maximise the rate of potential energy gain. However, the rate of climb just prior to leaving a thermal increased with thermal strength and exit altitude. This suggests higher rates of energetic gain may not be advantageous where the resulting gain in altitude would lead to a reduction in the ability to search the ground for food. Consequently, soaring behaviour appeared to be modulated by the need to reconcile differing potential energy and food energy distributions. We suggest that foraging constructs may provide insight into the exploitation of non-food energy forms, and that non-food energy distributions may be more important in informing patterns of movement and residency over a range of scales than previously considered.     

The dilemma of foraging herbivores: dealing with food and fear

For foraging herbivores, both food quality and predation risk vary across the landscape. Animals should avoid low-quality food patches in favour of high-quality ones, and seek safe patches while avoiding risky ones. Herbivores often face the foraging dilemma, however, of choosing between high-quality food in risky places or low-quality food in safe places. Here, we explore how and why the interaction between food quality and predation risk affects foraging decisions of mammalian herbivores, focusing on browsers confronting plant toxins in a landscape of fear. We draw together themes of plant–herbivore and predator–prey interactions, and the roles of animal ecophysiology, behaviour and personality. The response of herbivores to the dual costs of food and fear depends on the interplay of physiology and behaviour. We discuss detoxification physiology in dealing with plant toxins, and stress physiology associated with perceived predation risk. We argue that behaviour is the interface enabling herbivores to stay or quit food patches in response to their physiological tolerance to these risks. We hypothesise that generalist and specialist herbivores perceive the relative costs of plant defence and predation risk differently and intra-specifically, individuals with different personalities and physiologies should do so too, creating individualised landscapes of food and fear. We explore the ecological significance and emergent impacts of these individual-based foraging outcomes on populations and communities, and offer predictions that can be clearly tested. In doing so, we provide an integrated platform advancing herbivore foraging theory with food quality and predation risk at its core.     

Finding food in the open ocean: foraging strategies in Humboldt penguins

Penguins are excellent “model” organisms allowing us to study the behaviour of marine homeotherms at sea. Penguins regularly return to their breeding colonies, enabling biologists to equip them with remote sensing devices such as physiological or behavioural data-loggers, radio- or satellite transmitters. Foraging trips at sea can last from days to weeks and after return of the birds to their breeding sites, the devices can easily be removed for analysis of on-board stored data, yielding a wealth of information. Investigation of penguin behaviour at sea becomes particularly revealing when other sources of information can be matched to the data set, such as satellite data on wind, temperature, ice cover, and chlorophyll-a concentrations.

Penguins and other marine homeotherms are true inhabitants of the high seas. Depending on the season, the marine behaviour varies: during reproduction, penguins are central-place foragers, and must return regularly to their nest to feed their chicks. During the remainder of the year, there are no constraints and the birds travel large distances at sea.

Breeding Humboldt penguins react to climatic change by varying their daily foraging range and dive duration. Similar to other representatives of the family Spheniscidae, Humboldt penguins avoid food shortages by migrating into more productive marine areas. Navigational clues such as daylength, sea surface temperature, local wind direction and olfaction might provide important aids in finding patchily distributed prey in the open ocean. DMS, a chemical compound produced by decaying algae, seems to be a further clue that indirectly points the way to feeding areas.     

Optimal foraging and beyond: how starlings cope with changes in food availability

Foraging adaptations include behavioral and physiological responses, but most optimal foraging models deal exclusively with behavioral decision variables, taking other dimensions as constraints. To overcome this limitation, we measured behavioral and physiological responses of European starlings Sturnus vulgaris to changes in food availability in a laboratory environment. The birds lived in a closed economy with a choice of two foraging modes (flying and walking) and were observed under two treatments (hard and easy) that differed in the work required to obtain food. Comparing the hard with the easy treatment, we found the following differences. In the hard treatment, daily amount of work was higher, but daily intake was lower. Even though work was greater, total daily expenditure was smaller, partly because overnight metabolism was lower. Body mass was lower, but daily oscillation in body mass did not differ. Feces' caloric density was lower, indicating greater food utilization. Energy expenditure rate expressed as multiples of basal metabolic rate (BMR) increased during the working period from 3.5 x BMR (easy) to 5.2 x BMR (hard), but over the 24-h period, it was close to 2.4 x BMR in both treatments. We also found that rate of expenditure during flight was very high in both treatments (52.3 W in easy and 45.5 W in hard), as expected for short (as opposed to cruising) flights. The relative preferences between walking and flying were incompatible with maximizing the ratio of energy gains per unit of expenditure (efficiency) but compatible with maximizing net gain per unit of time during the foraging cycle (net rate). Neither currency explained the results when nonforaging time was included. Time was not a direct constraint: the birds rested more than 90% of the time in both treatments. Understanding this complex picture requires reasoning with ecological, physiological, and cognitive arguments. We defend the role of optimality as an appropriate tool to guide this integrative perspective.     

The effect of prey density on foraging mode selection in juvenile lumpfish: balancing food intake with the metabolic cost of foraging

1. In many species, individuals will alter their foraging strategy in response to changes in prey density. However, previous work has shown that prey density has differing effects on the foraging mode decisions of ectotherms as compared with endotherms. This is likely due to differences in metabolic demand; however, the relationship between metabolism and foraging mode choice in ectotherms has not been thoroughly studied. 2. Juvenile lumpfish Cyclopterus lumpus forage using one of two modes: they can actively search for prey while swimming, or they can 'sit-and-wait' for prey while clinging to the substrate using a ventral adhesive disk. The presence of these easily distinguishable foraging modes makes juvenile lumpfish ideal for the study of foraging mode choice in ectotherms. 3. Behavioural observations conducted during laboratory experiments showed that juvenile lumpfish predominantly use the 'cling' foraging mode when prey is abundant, but resort to the more costly 'swim' mode to seek out food when prey is scarce. The metabolic cost of active foraging was also quantified for juvenile lumpfish using swim-tunnel respirometry, and a model was devised to predict the prey density at which lumpfish should switch between the swim and cling foraging modes to maximize energy intake. 4. The results of this model do not agree with previous observations of lumpfish behaviour, and thus it appears that juvenile lumpfish do not try to maximize their net energetic gain. Instead, our data suggest that juvenile lumpfish forage in a manner that reduces activity and conserves space in their limited aerobic scope. This behavioural flexibility is of great benefit to this species, as it allows young individuals to divert energy towards growth as opposed to activity. In a broader context, our results support previous speculation that ectotherms often forage in a manner that maintains a minimum prey encounter rate, but does not necessarily maximize net energy gain.     

Optimal foraging: food patch depletion by ruddy ducks

Summary I studied the foraging behavior of ruddy ducks (Oxyura jamaicensis) feeding on patchily distributed prey in a large (5-m long, 2-m wide, and up to 2-m deep) aquarium. The substrate consisted of a 4x4 array of wooden trays (1.0-m long, 0.5-m wide, and 0.1-m deep) which contained 6 cm of sand. Any tray could be removed from the aquarium and loaded with a known number of prey. One bird foraged in the aquarium at a time; thus, by removing a food tray after a trial ended and counting the remaining prey, I calculated the number of prey consumed by the bird. I designed several experiments to determine if ruddy ducks abandoned a food patch in a manner consistent with the predictions of a simple, deterministic, patch depletion model. This model is based on the premise that a predator should maximize its rate of net energy intake while foraging. To accomplish this, a predator should only remain in a food patch as long as its rate of energy intake from that patch exceeds the average rate of intake from the environment. In the majority of comparisons, the number of food items consumed by the ruddy ducks in these experiments was consistent with the predictions of the foraging model. When the birds did not forage as predicted by the model, they stayed in the patch longer and consumed more prey than predicted by the model. An examination of the relation between rate of net energy intake and time spent foraging in the food patch indicated that by staying in a patch longer than predicted, the ruddy ducks experienced only a small deviation from maximum rate of net energy intake. These results provided quantitative support for the prediction that ruddy ducks maximize their rate of net energy intake while foraging.     

The forager's dilemma: food sharing and food defense as risk-sensitive foraging options

Although many variants of the hawk-dove game predict the frequency at which group foraging animals should compete aggressively, none of them can explain why a large number of group foraging animals share food clumps without any overt aggression. One reason for this shortcoming is that hawk-dove games typically consider only a single contest, while most group foraging situations involve opponents that interact repeatedly over discovered food clumps. The present iterated hawk-dove game predicts that in situations that are analogous to a prisoner's dilemma, animals should share the resources without aggression, provided that the number of simultaneously available food clumps is sufficiently large and the number of competitors is relatively small. However, given that the expected gain of an aggressive animal is more variable than the gain expected by nonaggressive individuals, the predicted effect of the number of food items in a clump-clump richness-depends on whether only the mean or both the mean and variability associated with payoffs are considered. More precisely, the deterministic game predicts that aggression should increase with clump richness, whereas the stochastic risk-sensitive game predicts that the frequency of encounters resulting in aggression should peak at intermediate clump richnesses or decrease with increasing clump richness if animals show sensitivity to the variance or coefficient of variation, respectively.     

Diving for food: a switch of foraging strategy of dusky dolphins in Argentina

During winter, dusky dolphins (Lagenorhynchus obscurus) were observed in coordinated diving apparently in a feeding activity, contrasting with the surface feeding observed during summer. The aim of this work consisted in analyzing the diving activity as an alternative foraging strategy in Argentine dusky dolphins, based on sequential analysis. The study area was Golfo Nuevo, located in Northern Patagonia, Argentina. Random transects were surveyed by a research boat from 2001 to 2007. During behavioral sampling, group members were observed continuously and the predominant activity was recorded at 2-min intervals. Six predominant activities were identified. Each 2-min interval was classified according to the activity at the previous interval (preceding activity), the activity at the interval (following activity), and the season (cold or warm). Z scores were calculated and then used to construct sequence diagrams. An association between diving and milling behavior was observed. This could be another foraging tactics different to the surface foraging sequences and this could be related with the distribution or abundance of preys.     

The consequences of size dependent foraging for food web topology

A general question in biology is how processes at one scale, for example that of individual organisms, influence patterns at larger scales, for example communities of interacting individuals. Here we ask how changing the size‐dependence of the foraging behaviour of individuals can influence the structure of food webs. We assembled communities using a model in which species interactions are determined by allometric foraging rules of (1) handling time and (2) attack rates, and also (3) the distribution of body sizes. We systematically varied these three factors and examined their effects on three community level, food web allometries: the generality ‐ mass correlation, the vulnerability ‐ mass correlation and the trophic height ‐ mass correlation. The results demonstrate how allometries of individual foraging behaviour (handling time and attack rates) are linked across scales of organisation: different community level allometries are influenced by different individual level allometries. For example, generality allometries in the community are most affected by the individual allometric relationships of the attack rate, whereas trophic level allometries in the community are more strongly influenced by variation in individual handling time allometries. Importantly, we also find that the shape of the body size distribution from which species are drawn has a substantial influence on how these links between scales operate. This study suggests that understanding the variation of size structure among ecological networks requires knowledge about the causes of variation in individual foraging behaviour and determinants of the regional body size distribution.     

Differential time allocation of foraging workers in the subterranean termite

Background

Worker reproduction has an important influence on the social cohesion and efficiency of social insect colonies, but its role in the success of invasive ants has been neglected. We used observations of 233 captive colonies, laboratory experiments, and genetic analyses to investigate the conditions for worker reproduction in the invasive Anoplolepis gracilipes (yellow crazy ant) and its potential cost on interspecific defence. We determined the prevalence of worker production of males and whether it is triggered by queen absence; whether physogastric workers with enlarged abdomens are more likely to be reproductive, how normal workers and physogastric workers compare in their contributions to foraging and defence; and whether worker-produced males and males that could have been queen- or worker-produced differ in their size and heterozygosity.

Results

Sixty-six of our 233 captive colonies produced males, and in 25 of these, some males could only have been produced by workers. Colonies with more workers were more likely to produce males, especially for queenless colonies. The average number of days between the first appearance of eggs and adult males in our colonies was 54.1 ± 10.2 (mean ± SD, n = 20). In our laboratory experiment, queen removal triggered an increase in the proportion of physogastric workers. Physogastric workers were more likely to have yolky oocytes (37–54.9%) than normal workers (2–25.6%), which is an indicator of fertile or trophic egg production. Physogastric workers were less aggressive during interspecific aggression tests and foraged less than normal workers. The head width and wing length of worker-produced males were on average 4.0 and 4.3% greater respectively than those of males of undetermined source. Our microsatellite DNA analyses indicate that 5.5% of worker-produced males and 14.3% of males of undetermined source were heterozygous, which suggests the presence of diploid males and/or genetic mosaics in A. gracilipes.

Conclusions

Our experimental work provides crucial information on worker reproduction in A. gracilipes and its potential cost to colony defence. The ability of A. gracilipes workers to produce males in the absence of queens may also contribute to its success as an invasive species if intranidal mating can take place between virgin queens and worker-produced males.

     

Transformation of Salmonella typhimurium with plasmid DNA: differences between rough and smooth strains.

Lipopolysaccharide-defective mutants of Salmonella typhimurium were transformed by plasmid DNA with a Ca2+ treatment method. Only those mutants with an Rc or Rd2 chemotype, due to galE or rfaF mutations, respectively, gave efficiencies greater than 10(5) transformants per microgram of DNA, frequencies 8- to 630-fold higher than with smooth strains or other rough mutants.     

Interactions of multiple predators with different foraging modes in an aquatic food web

Top predators can have different foraging modes that may alter their interactions and effects on food webs. Interactions between predators may be non-additive resulting from facilitation or interference, whereas their combined effects on a shared prey may result in emergent effects that are risk enhanced or risk reduced. To test the importance of multiple predators with different foraging modes, we examined the interaction between a cruising predator (largemouth bass, Micropterus salmoides) and an ambush predator (muskellunge, Esox masquinongy) foraging on a shared prey (bluegill sunfish, Lepomis macrochirus) with strong anti-predator defense behaviors. Additive and substitution designs were used to compare individual to combined predator treatments in experimental ponds. The multiple predator interaction facilitated growth of the cruising predator in the combined predator treatments, whereas predator species had substitutable effects on the growth of the ambush predator. The combined predator treatments created an emergent effect on the prey; however, the direction was dependent on the experimental design. The additive design found a risk-reducing effect, whereas the substitution design found a risk-enhancing effect for prey fish. Indirect effects from the predators weakly extended to lower trophic levels (i.e., zooplankton community). Our results highlight the need to consider differences in foraging mode of top predators, interactions between predators, and emergent effects on prey to understand food webs.     

Breeding limits foraging time: evidence of interrupted foraging response from body mass variation in a tropical environment

Birds should store body reserves if starvation risk is anticipated; this is known as an ‘interrupted foraging response’. If foraging remains unrestricted, however, body mass should remain low to limit the predation risk that gaining and carrying body reserves entails. In temperate environments mass gain in female birds during breeding is often attributed to egg formation and mass loss after incubation to flight adaptation or the effect of reproductive workload, rather than as a result of an adaptive interrupted foraging response to the limited foraging time or unpredictable foraging conditions that breeding demands. In tropical environments, foraging conditions vary more within the breeding season than in temperate environments, and so studies in tropical environments are more suited to decouple the potentially confounded effects of increase in body reserves versus egg formation on the body mass of breeding birds. In this study, we test whether breeding results in an interrupted foraging response in a tropical savannah system using body mass data collected over a 15‐year period from female common bulbuls Pycnonotus barbatus. This species breeds both in the wet and dry season, despite fewer resources being available in the dry season. Breeding stage predicted female body mass: body mass peaked abruptly during incubation, but was not closely associated with the egg‐laying stage, and declined during brood rearing. Breeding females were heavier in the dry season than in the wet season. In the dry season, heavier birds were more likely to incubate eggs or brood chicks. These observations suggest that increased body reserves are required to buffer the consequence of limited foraging time or impoverished foraging conditions, which may be most pronounced during incubation and in the dry season, respectively. Such mass increases are consistent with an interrupted foraging response, which may apply to temperate zone birds experiencing foraging restrictions during breeding.     

Modelling locust foraging: How and why food affects group formation

Locusts are short horned grasshoppers that exhibit two behaviour types depending on their local population density. These are: solitarious, where they will actively avoid other locusts, and gregarious where they will seek them out. It is in this gregarious state that locusts can form massive and destructive flying swarms or plagues. However, these swarms are usually preceded by the aggregation of juvenile wingless locust nymphs. In this paper we attempt to understand how the distribution of food resources affect the group formation process. We do this by introducing a multi-population partial differential equation model that includes non-local locust interactions, local locust and food interactions, and gregarisation. Our results suggest that, food acts to increase the maximum density of locust groups, lowers the percentage of the population that needs to be gregarious for group formation, and decreases both the required density of locusts and time for group formation around an optimal food width. Finally, by looking at foraging efficiency within the numerical experiments we find that there exists a foraging advantage to being gregarious.     

Reef fishes foraging facilitation behavior: increasing the access to a food resource

Fishes associated in schools acquire adaptive advantages by grouping together, e.g., access to a larger variety of food resources, foraging sites, and protection against potential predators. This work presents the first record of a feeding association between the bucktooth parrotfish, Sparisoma radians and the sailor’s grunt Haemulon parra, on Tamandaré reefs, Southwestern Atlantic. Through this association, S. radians gained access to otherwise unavailable food resources to be found inside territorial damselfish domain, thus characterizing an event of foraging facilitation.