Laboratory and field studies on diet choice in three-spined sticklebacks, Gasterosteus aculeatus L., in relation to profitability and visual features of prey

Diet choice by three-spined sticklebacks was investigated under both laboratory and field conditions. In the laboratory, sticklebacks did not always choose the more profitable of two prey items; instead, they apparently selected prey according to a set of proximate decision rules based on visual cues provided by the prey. Studies of the diet of sticklebacks in the field suggest that they may use the same set of proximate decision rules to select their food and that in these more complex conditions this may lead them to feed preferentially on the more profitable types of prey. In general, sticklebacks selected zooplanktonic rather than benthic prey (which is less profitable), but the importance of benthos in the diet increased as the density of zooplankton decreased.     

Parasites grow larger in faster growing fish hosts

Parasites depend on host-derived energy for growth and development, and so are potentially affected by the host's ability to acquire nutrients under competitive foraging scenarios. Although parasites might be expected to grow faster in hosts that are better at acquiring nutrients from natural ecosystems, it is also possible that the most competitive hosts are better at countering infections, if they have an improved immune response or are able to limit the availability of nutrients to parasites. I first quantified the ability of uninfected three-spined sticklebacks Gasterosteus aculeatus to compete in groups for sequentially-presented food items, and then exposed either the best or worst competitors to infective stages of the cestode Schistocephalus solidus. Fish were subsequently raised in their original groups, under competitive feeding regimes, for 96 days, after which fish and parasite growth was determined. Unexpectedly, pre-exposure host competitive ability had no effect on susceptibility to infection, or on post-infection growth rate. Furthermore, despite a 120-fold variation in parasite mass at the end of the study, pre-infection competitive ability was not related to parasite growth. The closest predictor of parasite mass was body size-corrected host growth rate, indicating that the fastest growing fish developed the largest parasites. Faster growing hosts therefore apparently provide ideal environments for growing parasites. This finding has important implications for ecology and aquaculture.     

Constraints on prey size selection by the three-spined stickleback: energy requirements and the capacity and fullness of the gut

An experiment was designed to study how gut fullness and encounter with 5-mm Asellus aquaticus influenced acceptance or rejection of less profitable 8-mm Asellus . 45-mm sticklebacks were found to always accept 5-mm prey whereas 8-mm prey were accepted with an initial probability of about 0.9. This probability decreased as the gut filled. Fish of differing sizes and sex had similar daily energy intakes per unit body size, however the acceptance of 8-mm prey was related to fish size. Whenever a fish orientated to a prey it was followed by pursuit and manipulation independently of prey size. The decision to accept or reject prey occurred after one manipulation, a criterion that was more variable for the larger prey. For one feeding session per day the total energy intake was almost constant despite the changing combination of prey sizes eaten. The fish ate prey with long handling times if the energetic contents of the stomach had not reached 450 J. Calculations were made of how many of each millimetre prey size group would satisfy the 450 J demand and how long the estimated number would take to handle. This showed that the best option is to consume 5-mm prey if given the choice.     

Foraging on patchily distributed prey by a cichlid fish (Teleostei,Cichlidae): A test of the ideal free distribution theory

Cichlid fish (Aequidens curviceps) distributed themselves and allocated their foraging time between two drift food patches in close approximation to the patch profitability ratio, as predicted by the ideal free distribution theory. The fish thereby achieved similar average feeding rates in the two patches, in two of three patch profitability ratio experiments. However, one major assumption of the ideal free model was violated, since individual fish differed in their competitive abilities for limited food resources, which resulted in unequal payoffs among individuals within each patch. Individual variation in feeding rates, and thus in competitive ability, was not related to despotism, but perhaps rather to individual differences in perceptual ability and in the ability to learn which patch was currently the more profitable. The strategy used by the fish to assess patch profitability included sampling available patches. However, individual fish switched (sampled) patches with varying frequency. Sampling had an associated cost, since high-frequency switchers had lower feeding rates on average than low-frequency switchers. Differences in foraging strategy among the fish therefore contributed to the observed in-equality in individual payoffs within patches.     

On Predator Selection against Abnormalities of Movement A Test of an Hypothesis1

If debilitated prey items can be caught more efficiently than healthy ones, there is a selective advantage for predators to detect any weakness in their prey. This study investigates whether three-spined sticklebacks (Gastcrosteus aculeatus L.) accustomed to feeding on one or the other of two types of waterfleas differing in their swimming pattern capture the unfamiliar type when given a choice. Such sequential oddity selection might serve as a mechanism for the detection of sick prey.     

Competitive resource sharing: An experimental test of a learning rule for ESSs

Six sticklebacks (Gasterosteus aculeatus) distributed themselves between two simulated drift food patches in the ratio of patch profitabilities (Milinski 1979). The present study investigated the rule with which each fish decides to stay in one or the other patch, and whether the fish have more difficulties in reaching a decision when the prey is supplied irregularly as is the case under natural conditions. With frame by frame analysis of filmed experiments the hunting success and sampling effort of each individual fish could be determined continuously. The results support the hypothesis that the fish used the relative payoff sum (RPS) learning rule (Harley 1981; Regelmann 1984). There was a close correlation between all decisions of individual fish during a trial, whether to stay or leave a patch, and decisions predicted by the RPS learning rule using the actual experience of the fish. Differences in competitive ability between the fish influenced the dynamics of the distribution in the predicted way, the more successful competitors deciding earlier where to stay than the less successful ones. This had the effect that the good competitors as well as the poor ones were distributed between the patches in the ratio of patch profitabilities. It is also compatible with the RPS learning rule that the fish reached their decision as quickly whether they were supplied with prey regularly or irregularly.     

Uniform persistence for sigmoidal diet selection with keystone prey species

In this paper we discuss uniform persistence (UP) criteria of two prey- one predator systems, where we consider that the predator's diet selection is a sigmoidal function of the most profitable prey type in place of a step function of conventional diet choice theory. We also derive UP results of the system with direct interspecific competition between the prey. The role of the most profitable prey item as a keystone species, the magnitude of its carrying capacity, the ability to withstand predation of both prey species, and the ratios of their profitability values (to predators) are important to whether or not adaptive foraging may promote UP. In general, foraging decision rules play no role in UP if the alternative prey item is the keystone species. The result is also not affected by the effect of direct competitive coexistence or dominance relationship of the prey. In some cases, dominance of one of the prey species provides the most advantageous situation for ensuring UP. Received: 1 February 1999 / Revised version: 20 September 1999 / Published online: 4 July 2000     

Sticklebacks from Greenland

Greenland freshwater sticklebacks Gasterosteus aculeatus were low-plated. Length distribution of 1 + and 2+ fish peaked at 33 and 46 mm, in early July. Pre-reproductive fish including 1 + fish were infected with Schistocephalus solidus . The diet consisted of chironomid larvae and pupae. Infected individuals ate smaller prey than non-infected ones, on one occasion where competition for food was likely to occur. Infected fish had lower stomach fullness, and the parasite compressed the stomach in heavily infected fish. The other fish species was charr, and the stickleback seemed to occupy a wide range of habitats.     

The influence of prey size and abundance, and individual phenotype on prey choice by the three-spined stickleback, Gasterosteus aculeatm L.

Prey selection behaviour of three-spined sticklebacks, Gasterosteus aculeatus L., was studied in two experiments. Where possible, the experimental apparatus satisfied the assumptions of the simplest optimal diet model (the basic prey model); prey were presented sequentially, the fish could not search for and handle prey at the same time, and net energy gain, handling time and encounter rate were fixed. Experiment 1 presented fish with a range of Asellus sizes so that pursuit ( p ) and handling ( h ) time could be related to prey size. Published energy values of Asellus together with pursuit and handling times were used to calculate E /( p+h ) for Asellus measuring 3,4,5,6,7 and 9 mm. Pursuit times did not differ with prey size but handling times did. E /( p+h ) was very variable particularly at the larger prey sizes. Experiment 2 presented fish with two sequences of prey differing in the encounter rate with the most profitable prey sizes. Fish did not select the diet predicted by the basic prey model tending to always ignore the largest prey even when net energy gain would have been maximized by including them in the diet. Further analysis showed that the probability of a prey size being taken was a function of prey size, fish stomach fullness and encounter rate. It is concluded that the basic prey model is too simple to capture the behaviour of the fish. One of its main faults is that the changing state of the fish through the feeding bout is ignored.     

Preference for Cannibalism and Ontogenetic Constraints in Competitive Ability of Piscivorous Top Predators

Occurrence of cannibalism and inferior competitive ability of predators compared to their prey have been suggested to promote coexistence in size-structured intraguild predation (IGP) systems. The intrinsic size-structure of fish provides the necessary prerequisites to test whether the above mechanisms are general features of species interactions in fish communities where IGP is common. We first experimentally tested whether Arctic char (Salvelinus alpinus) were more efficient as a cannibal than as an interspecific predator on the prey fish ninespine stickleback (Pungitius pungitius) and whether ninespine stickleback were a more efficient competitor on the shared zooplankton prey than its predator, Arctic char. Secondly, we performed a literature survey to evaluate if piscivores in general are more efficient as cannibals than as interspecific predators and whether piscivores are inferior competitors on shared resources compared to their prey fish species. Both controlled pool experiments and outdoor pond experiments showed that char imposed a higher mortality on YOY char than on ninespine sticklebacks, suggesting that piscivorous char is a more efficient cannibal than interspecific predator. Estimates of size dependent attack rates on zooplankton further showed a consistently higher attack rate of ninespine sticklebacks compared to similar sized char on zooplankton, suggesting that ninespine stickleback is a more efficient competitor than char on zooplankton resources. The literature survey showed that piscivorous top consumers generally selected conspecifics over interspecific prey, and that prey species are competitively superior compared to juvenile piscivorous species in the zooplankton niche. We suggest that the observed selectivity for cannibal prey over interspecific prey and the competitive advantage of prey species over juvenile piscivores are common features in fish communities and that the observed selectivity for cannibalism over interspecific prey has the potential to mediate coexistence in size structured intraguild predation systems.     

High activity and Levy searches: jellyfish can search the water column like fish

Over-fishing may lead to a decrease in fish abundance and a proliferation of jellyfish. Active movements and prey search might be thought to provide a competitive advantage for fish, but here we use data-loggers to show that the frequently occurring coastal jellyfish (Rhizostoma octopus) does not simply passively drift to encounter prey. Jellyfish (327 days of data from 25 jellyfish with depth collected every 1 min) showed very dynamic vertical movements, with their integrated vertical movement averaging 619.2 m d(-1), more than 60 times the water depth where they were tagged. The majority of movement patterns were best approximated by exponential models describing normal random walks. However, jellyfish also showed switching behaviour from exponential patterns to patterns best fitted by a truncated Lévy distribution with exponents (mean μ=1.96, range 1.2-2.9) close to the theoretical optimum for searching for sparse prey (μopt≈2.0). Complex movements in these 'simple' animals may help jellyfish to compete effectively with fish for plankton prey, which may enhance their ability to increase in dominance in perturbed ocean systems.     

Host defence mediates interspecific competition in ectoparasites

1. Interspecific competition influences which, how many and where species coexist in biological communities. Interactions between species in different trophic levels can mediate interspecific competition; e.g. predators are known to reduce competition between prey species by suppressing their population sizes. A parallel phenomenon may take place in host-parasite systems, with host defence mediating competition between parasite species. 2. We experimentally investigated the impact of host defence (preening) on competitive interactions between two species of feather-feeding lice: 'wing' lice Columbicola columbae and 'body' lice Campanulotes compar. Both species are host-specific parasites that co-occur on rock pigeons Columba livia. 3. We show that wing lice and body lice compete and that host defence mediates the magnitude of this competitive interaction. 4. Competition is asymmetrical; wing louse populations are negatively impacted by body lice, but not vice versa. This competitive asymmetry is consistent with the fact that body lice predominate in microhabitats on the host's body that offer the most food and the most space. 5. Our results indicate that host-defence-mediated competition can influence the structure of parasite communities and may play a part in the evolution of parasite diversity.     

Experience affects performance of ten-spined sticklebacks foraging on zooplankton

To study the effects of short-term experience on prey size-selection ten-spined sticklebacks (Pungitius pungitius) were fed 7–13 days with five differing diets of novel prey, Daphnia magna. The diets consisted either of a mixture of two prey size classes (1.7 and 2.2 mm) or of single-sized (1.7 and 2.2 mm) prey. Before and after the diets, the sticklebacks' prey size selection was tested with a 1:1 ratio of 1.7 and 2.2 mm D. magna. Sticklebacks made more attempts to capture large than small prey, but their foraging success was better for small than for large prey. Sticklebacks fed with a diet of both prey sizes chose significantly more large prey on the 13th day than on the 7th day or at the beginning of the experiment. Handling times for both Daphnia size classes decreased slightly with increasing foraging experience. Inexperienced sticklebacks made more unsuccessful strikes on large prey than did experienced fish. Foraging success on large prey improved somewhat with increasing experience in all but one diet group. The results indicate that experience affected ten-spined sticklebacks' prey selection.     

Producing and scrounging can have stabilizing effects at multiple levels of organization

This study shows, for the first time, that the evolution of a simple behavior, scrounging, at the individual level can have effects on populations, food chains, and community structure. In particular, the addition of scrounging in consumer populations can allow multiple consumers to coexist while exploiting a single prey. Also, scrounging in the top predator of a tritrophic food chain can stabilize interactions between the top predator, its prey, and its prey's prey. This occurs because the payoffs to scrounging for food in a population are negative frequency dependent, allowing scroungers to invade a population and to coexist with producers at a frequency which is density‐dependent. The presence of scroungers, who do not search for resources but simply use those found by others (producers) reduces the total amount of resource acquired by the group. As scrounging increases with group size, this leads to less resource acquired per individual as the group grows. Ultimately, this limits the size of the group, its impact on its prey, and its ability to outcompete other species. These effects can promote stability and thus increase species diversity. I will further suggest that prey may alter their spatial distribution such that scrounging will be profitable among their predators thus reducing predation rate on the prey.     

Experience of natural prey and feeding efficiency in three-spined sticklebacks (Gasterosteus aculeatus L.)

The possibility that efficiency of feeding on different prey in three-spined sticklebacks ( Gasterosteus aculeatus L.) increases by experience of such items was investigated experimentally by comparing sticklebacks reared with only non-moving prey (frozen brine shrimps) with sticklebacks caught in the wild from localities where a wide range of prey species was available. Fish without experience of natural food scored less well than those from the wild on various components of foraging and so had reduced feeding efficiency. However, feeding efficiency in naive fish improved after just a few days of experience with natural prey. Such experience-induced changes in foraging efficiency will alter the profitability of prey items for individual fish.     

Foraging tactics of a terrestrial salamander: Sustained yield in territories

Territorial red-backed salamanders (Plethodon cinereus) were given a high density of two prey types differing in size and caloric profitability. They chose a diet that approximated optimal foraging when they foraged in areas previously marked with advertisement pheromones. However, when foraging in previously unmarked or conspecific-marked areas they did not forage optimally, in a short time frame. In the latter two situations they evinced a lower rate of net energy due to their failure to specialize on the more profitable prey type and their longer intercapture intervals while time was devoted either to marking behaviour or submissive posturing. The salamanders appeared to opt for a strategy of sacrificing initial caloric yield until they had established marked territories and then switching to a higher sustained caloric yield. The data show that experimental handling of a predator per se can alter its foraging behaviour. Also a predator just initiating a territory may forage quite differently from one that has already established ownership, making the time frame during which observations are made important to understanding the predator's foraging strategy.     

Horseshoe bats make adaptive prey-selection decisions, informed by echo cues

Foragers base their prey-selection decisions on the information acquired by the sensory systems. In bats that use echolocation to find prey in darkness, it is not clear whether the specialized diet, as sometimes found by faecal analysis, is a result of active decision-making or rather of biased sensory information. Here, we tested whether greater horseshoe bats decide economically when to attack a particular prey item and when not. This species is known to recognize different insects based on their wing-beat pattern imprinted in the echoes. We built a simulation of the natural foraging process in the laboratory, where the bats scanned for prey from a perch and, upon reaching the decision to attack, intercepted the prey in flight. To fully control echo information available to the bats and assure its unambiguity, we implemented computer-controlled propellers that produced echoes resembling those from natural insects of differing profitability. The bats monitored prey arrivals to sample the supply of prey categories in the environment and to inform foraging decisions. The bats adjusted selectivity for the more profitable prey to its inter-arrival intervals as predicted by foraging theory (an economic strategy known to benefit fitness). Moreover, unlike in previously studied vertebrates, foraging performance of horseshoe bats was not limited by costly rejections of the profitable prey. This calls for further research into the evolutionary selection pressures that sharpened the species's decision-making capacity.     

Predator-prey shell games: large-scale movement and its implications for decision-making by prey

Many classical models of food patch use under predation risk assume that predators impose patch-specific predation risks independent of prey behavior. These models predict that prey should leave a chosen patch only if and when the food depletes below some critical level. In nature, however, prey individuals may regularly move among food patches, even in the apparent absence of food depletion. We suggest that such prey movement is part of a predator-prey "shell game", in which predators attempt to learn prey location, and the prey attempt to be unpredictable in space. We investigate this shell game using an individual-based model that allows predators to update information about prey location, and permits prey to move with some random component among patches, but with reduced energy intake. Our results show the best prey strategy depends on what the predator does. A non-learning (randomly moving) predator favors non-moving prey – moving prey suffer higher starvation and predation. However, a learning predator favors prey movement. In general, the best prey strategy involves movement biased toward, but not completely committed to, the richer food patch. The strategy of prey movement remains beneficial even in combination with other anti-predator defenses, such as prey vigilance.     

Optimal foraging on the roof of the world: Himalayan langurs and the classical prey model

Optimal foraging theory has only been sporadically applied to nonhuman primates. The classical prey model, modified for patch choice, predicts a sliding “profitability threshold” for dropping patch types from the diet, preference for profitable foods, dietary niche breadth reduction as encounter rates increase, and that exploitation of a patch type is unrelated to its own abundance. We present results from a 1‐year study testing these predictions with Himalayan langurs (Semnopithecus entellus) at Langtang National Park, Nepal. Behavioral data included continuous recording of feeding bouts and between‐patch travel times. Encounter rates were estimated for 55 food types, which were analyzed for crude protein, lipid, free simple sugar, and fibers. Patch types were entered into the prey model algorithm for eight seasonal time periods and differing age‐sex classes and nutritional currencies. Although the model consistently underestimated diet breadth, the majority of nonpredicted patch types represented rare foods. Profitability was positively related to annual/seasonal dietary contribution by organic matter estimates, whereas time estimates provided weaker relationships. Patch types utilized did not decrease with increasing encounter rates involving profitable foods, although low‐ranking foods available year‐round were taken predominantly when high‐ranking foods were scarce. High‐ranking foods were taken in close relation to encounter rates, while low‐ranking foods were not. The utilization of an energetic currency generally resulted in closest conformation to model predictions, and it performed best when assumptions were most closely approximated. These results suggest that even simple models from foraging theory can provide a useful framework for the study of primate feeding behavior. Am J Phys Anthropol, 2010. © 2009 Wiley‐Liss, Inc.     

Parasitized Salamanders are Inferior Competitors for Territories and Food Resources

Parasites have been shown to impair the behaviour of their hosts, compromising the host's ability to exploit and compete for resources. We conducted two experiments to determine whether infestation with an ectoparasitic mite (Hannemania eltoni) was associated with changes in aggressive and foraging behaviour in the Ozark zigzag salamander, Plethodon angusticlavius. In a first experiment, male salamanders with high parasite loads were less aggressive overall than males with low parasite loads during territorial disputes. In addition, males with high parasite loads were more aggressive toward opponents with high parasite loads (symmetric contests) than toward opponents with low parasite loads (asymmetric contests). In contrast, males with low parasite loads did not adjust their level of aggression according to the parasite load of the opponent. In a second experiment, foraging behaviour of females was tested in response to ‘familiar’ (Drosophila) prey and ‘novel’ (termite) prey. Latency to first capture was significantly longer for parasitized than non‐parasitized females when tested with ‘familiar’ prey, but not for ‘novel’ prey. Our results suggest that parasite‐mediated effects may have profound influences on individual fitness in nature.