Understanding selection for long necks in different taxa

There has been recent discussion about the evolutionary pressures underlying the long necks of extant giraffes and extinct sauropod dinosaurs. Here we summarise these debates and place them in a wider taxonomic context. We consider the evolution of long necks across a wide range of (both living and extinct) taxa and ask whether there has been a common selective factor or whether each case has a separate explanation. We conclude that in most cases long necks can be explained in terms of foraging requirements, and that alternative explanations in terms of sexual selection, thermoregulation and predation pressure are not as well supported. Specifically, in giraffe, tortoises, and perhaps sauropods there is likely to have been selection for high browsing. It the last case there may also have been selection for reaching otherwise inaccessible aquatic plants or for increasing the energetic efficiency of low browsing. For camels, wading birds and ratites, original selection was likely for increased leg length, with correlated selection for a longer neck to allow feeding and drinking at or near substrate level. For fish‐eating long‐necked birds and plesiosaurs a small head at the end of a long neck allows fast acceleration of the mouth to allow capture of elusive prey. A swan's long neck allows access to benthic vegetation, for vultures the long neck allows reaching deep into a carcass. Geese may be an unusual case where anti‐predator vigilance is important, but so may be energetically efficient low browsing. The one group for which we feel unable to draw firm conclusions are the pterosaurs, this is in keeping with the current uncertainty about the biology of this group. Despite foraging emerging as a dominant theme in selection for long necks, for almost every taxonomic group we have identified useful empirical work that would increase understanding of the selective costs and benefits of a long neck.     

Evolution of foraging behaviour in response to chronic malnutrition in Drosophila melanogaster

Chronic exposure to food of low quality may exert conflicting selection pressures on foraging behaviour. On the one hand, more active search behaviour may allow the animal to find patches with slightly better, or more, food; on the other hand, such active foraging is energetically costly, and thus may be opposed by selection for energetic efficiency. Here, we test these alternative hypotheses in Drosophila larvae. We show that populations which experimentally evolved improved tolerance to larval chronic malnutrition have shorter foraging path length than unselected control populations. A behavioural polymorphism in foraging path length (the rover-sitter polymorphism) exists in nature and is attributed to the foraging locus (for). We show that a sitter strain (for(s2)) survives better on the poor food than the rover strain (for(R)), confirming that the sitter foraging strategy is advantageous under malnutrition. Larvae of the selected and control populations did not differ in global for expression. However, a quantitative complementation test suggests that the for locus may have contributed to the adaptation to poor food in one of the selected populations, either through a change in for allele frequencies, or by interacting epistatically with alleles at other loci. Irrespective of its genetic basis, our results provide two independent lines of evidence that sitter-like foraging behaviour is favoured under chronic larval malnutrition.     

Optic flow informs distance but not profitability for honeybees

How do flying insects monitor foraging efficiency? Honeybees (Apis mellifera) use optic flow information as an odometer to estimate distance travelled, but here we tested whether optic flow informs estimation of foraging costs also. Bees were trained to feeders in flight tunnels such that bees experienced the greatest optic flow en route to the feeder closest to the hive. Analyses of dance communication showed that, as expected, bees indicated the close feeder as being further, but they also indicated this feeder as the more profitable, and preferentially visited this feeder when given a choice. We show that honeybee estimates of foraging cost are not reliant on optic flow information. Rather, bees can assess distance and profitability independently and signal these aspects as separate elements of their dances. The optic flow signal is sensitive to the nature of the environment travelled by the bee, and is therefore not a good index of flight energetic costs, but it provides a good indication of distance travelled for purpose of navigation and communication, as long as the dancer and recruit travel similar routes. This study suggests an adaptive dual processing system in honeybees for communicating and navigating distance flown and for evaluating its energetic costs.     

Bees do not use nearest-neighbour rules for optimization of multi-location routes

Animals collecting patchily distributed resources are faced with complex multi-location routing problems. Rather than comparing all possible routes, they often find reasonably short solutions by simply moving to the nearest unvisited resources when foraging. Here, we report the travel optimization performance of bumble-bees (Bombus terrestris) foraging in a flight cage containing six artificial flowers arranged such that movements between nearest-neighbour locations would lead to a long suboptimal route. After extensive training (80 foraging bouts and at least 640 flower visits), bees reduced their flight distances and prioritized shortest possible routes, while almost never following nearest-neighbour solutions. We discuss possible strategies used during the establishment of stable multi-location routes (or traplines), and how these could allow bees and other animals to solve complex routing problems through experience, without necessarily requiring a sophisticated cognitive representation of space.     

Social diffusion of novel foraging methods in brown capuchin monkeys (Cebus apella)

It has been reported that wild capuchin monkeys exhibit several group-specific behavioural traditions. By contrast, experiments have found little evidence for the social learning assumed necessary to support such traditions. The present study used a diffusion chain paradigm to investigate whether a novel foraging task could be observationally learned by capuchins (Cebus apella) and then transmitted along a chain of individuals. We used a two-action paradigm to control for independent learning. Either of two methods (lift or slide) could be used to open the door of a foraging apparatus to retrieve food. Two chains were tested (N1=4; N2=5), each beginning with an experimenter-trained model who demonstrated to a partner its group-specific method for opening the foraging apparatus. After the demonstration, if the observer was able to open the apparatus 20 times by either method, then it became the demonstrator for a new subject, thus simulating the spread of a foraging tradition among 'generations' of group members. Each method was transmitted along these respective chains with high fidelity, echoing similar results presently available only for chimpanzees and children. These results provide the first clear evidence for faithful diffusion of alternative foraging methods in monkeys, consistent with claims for capuchin traditions in the wild.     

Raising the sauropod neck: it costs more to get less

The long necks of gigantic sauropod dinosaurs are commonly assumed to have been used for high browsing to obtain enough food. However, this analysis questions whether such a posture was reasonable from the standpoint of energetics. The energy cost of circulating the blood can be estimated accurately from two physiological axioms that relate metabolic rate, blood flow rate and arterial blood pressure: (i) metabolic rate is proportional to blood flow rate and (ii) cardiac work rate is proportional to the product of blood flow rate and blood pressure. The analysis shows that it would have required the animal to expend approximately half of its energy intake just to circulate the blood, primarily because a vertical neck would have required a high systemic arterial blood pressure. It is therefore energetically more feasible to have used a more or less horizontal neck to enable wide browsing while keeping blood pressure low.     

Thirteen-lined ground squirrel (Sciuridae: Spermophilus tridecemlineatus) antipredator vigilance decreases as vigilance cost increases

Vigilance is a commonly studied antipredator phenomenon. However, little research has been conducted on the effects of visual obstruction coupled with a manipulation of the cost of performing vigilance behaviours. We tested the hypothesis that antipredator vigilance decreases as the cost of performing antipredator vigilance increases in free-ranging thirteen-lined ground squirrels. We presented adult ground squirrels with peanut butter within six rectangular Plexiglas boxes (opaque on all sides; clear on top) ranging in length from 15.2 to 91.4 cm. Squirrels repeatedly entered and withdrew from the boxes, to scan visually the surrounding area. As box length increased and, therefore, the cost of the vigilance behaviour increased, the ground squirrels increased their mean time within the box per entry and decreased their alertness per unit of trial time. Squirrels took longer to traverse the longer boxes, but their travel time into the boxes was significantly slower than their travel time out of the boxes. We interpreted this difference in travel time to indicate a behavioural conflict that occurred only when the squirrels entered the box (food versus vigilance) and did not exist once the squirrels had begun to exit from the box. The hypothesis that a decrease in ground squirrel antipredator vigilance would benefit the squirrels by decreasing their time exposed to predators (i.e. decreased trial duration, which was determined by the squirrels' behaviour), was not supported. Copyright 1999 The Association for the Study of Animal Behaviour.     

Flexibility in the bimodal foraging strategy of a high Arctic alcid, the little auk Alle alle

A bimodal foraging strategy has previously been described for procellariiform seabird species and is thought to have evolved in response to local resource availability being too low for adult birds to meet chick requirements and simultaneously maintain their own body condition. Here, we examine the dual foraging trip pattern of an alcid, the little auk Alle alle , at five colonies with contrasting oceanographic conditions. In spite of large variation in local conditions, little auks at all colonies showed the same general pattern of alternating a single long-trip with several consecutive short-trips. However, we found that the foraging pattern was flexible and could be adjusted at three levels: (1) the length of long-trips, (2) the frequency of short-trips, and (3) the total time spent foraging. Birds facing unfavorable conditions increased the duration of long-trips and reduced the number of short-trips. These adjustments resulted in reduced provisioning rates of chicks despite the fact that birds also increased the time allocated to foraging. Travel times during foraging trips were positively correlated to the total duration of the trip suggesting that differences in trip length among colonies were partly driven by variation in the distance to foraging areas. Most birds spent substantially more time traveling during long compared to short-trips, indicating that they accessed distant foraging areas during long-trips but remained close to the colony during short-trips. However, the difference in travel times was small at the site with the most favorable conditions suggesting that bimodal foraging in the little auk may be independent of the existence of high-quality areas at distance from the breeding ground.     

Modelling the energy budget of a colonial bird of prey, the Ruppell's griffon vulture, and consequences for its breeding ecology

Colonial nesting is rare in birds of prey. In this study we develop further Pennycuick's (1979 ) model of energy balance to consider the implications of colonial nesting for the breeding ecology of Ruppell's griffon vultures. To achieve a realistic foraging range, and remain in energy balance, the birds need to do more than fill their crop once on each foraging trip. They must remain in the feeding area and digest some of this food and refill the crop to obtain sufficient energy to pay for the flight costs and have sufficient energy to satisfy their own requirements and that of the chick. Given the known distances that the birds have to travel to forage, it would be impossible for them to rear more than one chick. The low growth rate of griffon vulture chicks may be an adaptation to the low rate at which energy can be delivered by the parents. The optimal time for a bird to be away from the nest changes with the distance they have to travel. Assuming that one parent remains on the nest at all times to guard the chick, it is optimal for both parents to take turns to forage on the same day if the distance to a feeding area is under 150 km, but to switch to each parent being away for a whole day when the distance is greater than this. Soaring flight is essential for such a scavenger, because of the low energy expenditure. If a vulture relied on the more energetically demanding flapping flight its maximum foraging range would be under 40 km. Griffon vultures are known to be able to depress their basal metabolic rate, and this has major implications for their foraging range, which then becomes constrained by the flight speed rather than by the amount of food they need to obtain. Griffon vultures minimize energy expenditure on all activities, because even small increases in their energy demands have a large impact on the foraging range that the bird can use.     

Effects of increased swimming costs on foraging behavior and efficiency of captive Steller sea lions: Evidence for behavioral plasticity in the recovery phase of dives

A significant component of foraging energetics is the cost of locomotion, which for marine animals, is the cost of swimming. Increases in the cost of swimming may have significant impacts on foraging efficiency. Minimizing the cost of swimming can contribute to the optimization of foraging strategies by reducing the energetic cost of foraging. Results of several field studies suggest that an increase in the cost of locomotion may have comparable effects on foraging behavior and efficiency to a decrease in prey availability. We tested the hypothesis that an increased cost of swimming, brought on by increased hydrodynamic drag, has the same effect on dive behavior and efficiency as reduced prey availability under standard locomotion. Experiments were performed using two adult female Steller sea lions at the Alaska SeaLife Center in Seward, AK, using the same animals and general experimental design previously used to test the effects of reduced prey encounter rate on dive behavior and efficiency. Animals were fitted with a drag-inducing harness for half of the 500 simulated foraging dives in order to increase the cost of swimming. Individual dive duration and foraging time were significantly reduced in all cost-increased dives, comparable to the effects of reduced prey encounter rate. However, on a bout-by-bout basis, dive and foraging efficiency were only slightly reduced, which is likely due to an average 50% reduction in post-dive surface recovery duration during cost-increased dives. Increased heat flux across the body surface measured in a parallel study confirmed a significant increase in work during drag-increased dives. These results suggest that sea lions are able to compensate for changes in the cost of foraging and maintain their foraging efficiency by altering their dive strategy over an entire bout of dives when operating well within their aerobic scope.     

Foraging strategy quick response to temperature of Messor barbarus (Hymenoptera: Formicidae) in Mediterranean environments

Animals principally forage to try to maximize energy intake per unit of feeding time, developing different foraging strategies. Temperature effects on foraging have been observed in diverse ant species; these effects are limited to the duration of foraging or the number of foragers involved. The harvester ant Messor barbarus L. 1767 has a specialized foraging strategy that consists in the formation of worker trails. Because of the high permeability of their body integument, we presume that the length, shape, and type of foraging trails of M. barbarus must be affected by temperature conditions. From mid-June to mid-August 1999, we tested the effect on these trail characteristics in a Mediterranean forest. We found that thermal stress force ants to use a foraging pattern based on the variation of the workers trail structure. Ants exploit earlier well-known sources using long physical trails, but as temperatures increases throughout the morning, foragers reduce the length of the foraging column gradually, looking for alternative food sources in nonphysical trails. This study shows that animal forage can be highly adaptable and versatile in environments with high daily variations.     

Linking predator risk and uncertainty to adaptive forgetting: a theoretical framework and empirical test using tadpoles

Hundreds of studies have examined how prey animals assess their risk of predation. These studies work from the basic tennet that prey need to continually balance the conflicting demands of predator avoidance with activities such as foraging and reproduction. The information that animals gain regarding local predation risk is most often learned. Yet, the concept of ‘memory’ in the context of predation remains virtually unexplored. Here, our goal was (i) to determine if the memory window associated with predator recognition is fixed or flexible and, if it is flexible, (ii) to identify which factors affect the length of this window and in which ways. We performed an experiment on larval wood frogs, Rana sylvatica, to test whether the risk posed by, and the uncertainty associated with, the predator would affect the length of the tadpoles'' memory window. We found that as the risk associated with the predator increases, tadpoles retained predator-related information for longer. Moreover, if the uncertainty about predator-related information increases, then prey use this information for a shorter period. We also present a theoretical framework aiming at highlighting both intrinsic and extrinsic factors that could affect the memory window of information use by prey individuals.     

Diurnal foraging routines in a tropical bird,the rock finch Lagonosticta sanguinodorsalis: how important is predation risk?

An animal's foraging decisions are the outcome of the relative importance of the risk of starvation and predation. Fat deposition insures against periods of food shortage but it also carries a cost in terms of mass dependent predation risk due to reduced escape probability and extended exposure time. Accordingly, birds have been observed to show a unimodal foraging pattern with foraging concentrated at the end of the day under conditions of predictable food resources and high predation risk. We tested this hypothesis in a tropical granivorous finch, the rock firefinch Lagonosticta sanguinodorsalis , in an outdoor aviary experiment during which food was provided ad lib and the risk of predation was varied by providing food either adjacent to, or 5 m away from cover. Rock firefinches showed a bimodal foraging pattern regardless of the risk of predation at which they fed. The results suggest that predation is relatively unimportant in shaping their daily feeding pattern despite mass gain during the day being similar to temperate birds. Foraging patterns closely follow diurnal temperature variation and this is suggested to be the main determinant of the observed bimodal pattern.     

Experimental provisioning increases play in free-ranging meerkats

The sensitivity of play to variations in food availability has been cited as evidence of the costliness of play, since energetically stressed animals dispense with costly behaviours. However, the causality of the relationship between nutrition and play has not been adequately tested. Using weight gain as a measure of food intake, we documented the food consumption of free-ranging meerkat, Suricata suricatta, pups and found that long-term nutritional status (weight gain over a 6-week period) was positively correlated with rates of play. We confirmed the causality of this relationship by conducting long-term (4-8 weeks) provisioning experiments that raised the nutritional status of experimental pups, subadults and adults. Experimental animals more than doubled their rate of play compared with their nonprovisioned controls. Short-term variations in food consumption (daily weight gain) were not correlated with subsequent rates of play, and we used a short-term feeding experiment to document the transitory effects of hunger satiation. We established that an increase in available energy contributed to the increase in rates of play, rather than the animals simply having more time available to play as a result of being released from the constraints of foraging. We conclude that play in meerkats was energetically costly, and must be adaptive given that the cost of play to juveniles (in terms of future reproductive success) was potentially high. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Feeding and metabolic compensations in response to different foraging costs

How energetic cost of locomotion affects foraging decisions, and its metabolic consequences are poorly understood. In several groups of animals, including hermit crabs, exploratory walking enhances the efficiency of foraging by increasing the probability of finding more and better food items; however, the net gain of energy will only be enhanced if the costs of walking are lower than the benefits of enhanced food acquisition. In hermit crabs, the cost of walking increases with the mass of the shell type occupied. Thus, we expected that hermit crabs should adjust their foraging strategy to the cost of movement in different shells. We assessed the foraging, the quantity and quality of food intake, and the energetic cost of maintenance of hermit crabs paying different costs of foraging in the wild. The exploratory walking negatively correlated with shell mass, showing that hermit crabs use different foraging strategies in response to the expenditure required to move. Hermit crabs deal with high energetic costs of foraging in heavy shells by reduces their exploratory walking and overall metabolic rate, as a strategy to maximize the net energy intake. This study integrates behavioral and metabolic compensations as a response to foraging at different costs in natural conditions.     

The Origin of Winter Visitors to the British Isles 7. Fieldfare (Turdus pilaris)

Capsule Large‐scale intensification of agricultural management during the past 50 years has resulted in a reduction of invertebrate abundance and higher and denser ground vegetation. Food availability for insectivorous birds foraging on the ground has been negatively affected, but the interactions between birds and their food availability are complex and often species‐specific. Populations of Wrynecks Jynx torquilla are declining all over Europe, possibly because of reduced accessibility to their main prey, ground‐dwelling ants, due to higher and denser ground vegetation. However, it is not clear which ground vegetation structures are tolerated by foraging Wrynecks and which habitats are preferred.

Aims To identify the optimal ground vegetation structure and the main habitat types in which Wrynecks search for food.

Method We radiotracked seven Wrynecks in high‐intensity farmland in Switzerland to study foraging habitat use during the reproduction season. Several habitat variables were mapped at each foraging location and compared with locations selected randomly within individual home ranges.

Results Wrynecks preferentially foraged at places with ≥50% bare ground. Vegetation height was not important. Older fruit tree plantations and fallow land were the preferred foraging habitats.

Conclusion Conservation measures should concentrate on preserving semi‐open agricultural landscape matrices with loose ground vegetation cover to provide suitable foraging conditions. This can be achieved even in intensively managed farmland as illustrated in this study.     

Driven to distraction: detecting the hidden costs of flea parasitism through foraging behaviour in gerbils

Gerbilline rodents such as Allenby's gerbils (Gerbillus andersoni allenbyi), when parasitized by fleas such as Synosternus cleopatrae pyramidis, devote long hours of grooming to remove the ectoparasites. Yet no detrimental energetic or immunological effects of the ectoparasites have been found in adult Allenby's gerbil. Why should gerbils go to such trouble? We tested for the various ways that fleas can negatively affect gerbils by manipulating flea infestation on gerbils and the presence of a fox. We demonstrate that gerbils responded to fleas by leaving resource patches at higher giving-up densities. Furthermore, they stayed in those resource patches less time and left them at higher quitting harvest rates so long as a fox was also present. When flea-ridden, gerbils also abandoned using vigilance to manage risk and relied mainly on time allocation. Thus, having fleas imposed a foraging cost similar in nature to that arising from the risk of predation from foxes and may be even larger in magnitude. More than that, the presence of fleas acted as a magnifier of foraging costs, especially those arising from the risk of predation. The fleas reduced the gerbils' foraging aptitude and altered how they went about managing risk of predation. We hypothesize that fleas reduce the attention that gerbils otherwise have for foraging and predator detection. We suggest that this is the major cost of ectoparasitism.     

Optimal foraging in nonpatchy habitats. I. Bounded one-dimensional resource

We present a model of optimal foraging in habitats where the food has an arbitrary density distribution (continuous or not). The classical models of foraging strategies assume that the food is distributed in patches and that the animal divides its time between the two distinct behaviors of patch exploitation and interpatch travel. This assumption is hard to accept in instances where the food distribution is continuous in space, and where travel and feeding cannot be sharply distinguished. In this paper, the habitat is assumed to be one-dimensional and bounded, and the animal is assumed to have a limited foraging time available. The problem is treated mathematically in the context of the calculus of variations. The optimal solution is to divide the habitat in two subsets according to the food density. In the richer subset, the animal equalizes the density distribution; in the poorer subset, it travels as fast as possible.     

Top carnivores increase their kill rates on prey as a response to human-induced fear

The fear induced by predators on their prey is well known to cause behavioural adjustments by prey that can ripple through food webs. Little is known, however, about the analogous impacts of humans as perceived top predators on the foraging behaviour of carnivores. Here, we investigate the influence of human-induced fear on puma foraging behaviour using location and prey consumption data from 30 tagged individuals living along a gradient of human development. We observed strong behavioural responses by female pumas to human development, whereby their fidelity to kill sites and overall consumption time of prey declined with increasing housing density by 36 and 42%, respectively. Females responded to this decline in prey consumption time by increasing the number of deer they killed in high housing density areas by 36% over what they killed in areas with little residential development. The loss of food from declines in prey consumption time paired with increases in energetic costs associated with killing more prey may have consequences for puma populations, particularly with regard to reproductive success. In addition, greater carcass availability is likely to alter community dynamics by augmenting food resources for scavengers. In light of the extensive and growing impact of habitat modification, our study emphasizes that knowledge of the indirect effects of human activity on animal behaviour is a necessary component in understanding anthropogenic impacts on community dynamics and food web function.     

Noise improves collective decision-making by ants in dynamic environments

Recruitment via pheromone trails by ants is arguably one of the best-studied examples of self-organization in animal societies. Yet it is still unclear if and how trail recruitment allows a colony to adapt to changes in its foraging environment. We study foraging decisions by colonies of the ant Pheidole megacephala under dynamic conditions. Our experiments show that P. megacephala, unlike many other mass recruiting species, can make a collective decision for the better of two food sources even when the environment changes dynamically. We developed a stochastic differential equation model that explains our data qualitatively and quantitatively. Analysing this model reveals that both deterministic and stochastic effects (noise) work together to allow colonies to efficiently track changes in the environment. Our study thus suggests that a certain level of noise is not a disturbance in self-organized decision-making but rather serves an important functional role.