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.     

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.     

Learning in the nectar foraging behaviour of Helicoverpa armigera

Abstract .1. Learning may enable insects to obtain nectar from flowers more efficiently. Learning in nectar foraging has been shown primarily in studies of bees and butterflies. Here, learning is demonstrated in the nectar foraging behaviour of a noctuid moth, Helicoverpa armigera .
2. The present studies show that: (1) previous experience with a flowering host species increases the probability of that species being selected for nectar foraging, and (2) previous experience of a particular flower type (food source at bottom or top of the corolla tube) increases the likelihood of the food source being found when that flower type is being searched.
3. The implications of these findings for understanding the pattern of oviposition observed in wild populations of this important pest species are discussed.     

Phenotypic plasticity and selection in Drosophila life-history evolution. I. Nutrition and the cost of reproduction

Earlier experiments have shown that the evolution of postponed senescent populations can be achieved by selection on either demographic or stress resistance characters. Both types of selection have produced results in which survival characters (stress resistance and longevity) have apparently traded-off against early-life fecundity. Here we present the results of a series of experiments in which an environmental variable — the level of live yeast inoculate applied to the substrate — produces a qualitatively similar phenotypic response: longevity and starvation resistance are enhanced by lower yeast levels, at the expense of fecundity. For the starvation resistance versus fecundity experiments we show a negative and linear relationship between the norms of reaction for each character across a gradient of yeast levels. This phenotypic trade-off is stable across the 20 populations and 4 selection treatments reported on here, and its general agreement with earlier selection results suggests that the evolutionary response and the phenotypically plastic response may share a common physiological basis. However, an important discrepancy in the lifetime fecundity data between the selection response and the dietary manipulations preclude strict analogy. The results broadly conform to a simple “Y-model” of allocation, in which a limited resource is divided between survival and reproduction; here the characters are starvation resistance and longevity versus fecundity.     

Evolution of increased adult longevity in Drosophila melanogaster populations selected for adaptation to larval crowding

In holometabolous animals such as Drosophila melanogaster, larval crowding can affect a wide range of larval and adult traits. Adults emerging from high larval density cultures have smaller body size and increased mean life span compared to flies emerging from low larval density cultures. Therefore, adaptation to larval crowding could potentially affect adult longevity as a correlated response. We addressed this issue by studying a set of large, outbred populations of D. melanogaster, experimentally evolved for adaptation to larval crowding for 83 generations. We assayed longevity of adult flies from both selected (MCUs) and control populations (MBs) after growing them at different larval densities. We found that MCUs have evolved increased mean longevity compared to MBs at all larval densities. The interaction between selection regime and larval density was not significant, indicating that the density dependence of mean longevity had not evolved in the MCU populations. The increase in longevity in MCUs can be partially attributed to their lower rates of ageing. It is also noteworthy that reaction norm of dry body weight, a trait probably under direct selection in our populations, has indeed evolved in MCU populations. To the best of our knowledge, this is the first report of the evolution of adult longevity as a correlated response of adaptation to larval crowding.     

Inheritance of optimal foraging behaviour in Columbian ground squirrels

Summary I examined the potential inheritance of the ability of Columbian ground squirrels (Spermophilus columbianus) to select an optimal diet. I calculated the diet that would maximize daily energy intake for each of 21 adult females and their litters, using a linear programming optimization model for each individual. The absolute value of the difference between an individual's predicted optimal diet and observed diet (deviation from an optimal diet) was used as a measure of an individual's foraging ability. The foraging ability of individuals was consistent over time and in different foraging environments, so I considered foraging ability to be a potentially heritable trait.Inheritance was determined from correlations of mother and offspring foraging ability. I experimentally removed some mothers just as they weaned their offspring so that offspring could not be influenced by their mother while learning to forage, while leaving the other mothers to raise their litters normally. In both cases, offspring strongly resembled their mother in foraging ability. However, offspring with mothers absent exhibited significantly larger deviations from their optimal diet. Offspring with mothers absent appeared to imitate their mother's diet during lactation, and this tendency partially explained their greater deviation. Consequently, offspring appear to inherit the ability to forage optimally from their mother, perhaps through observational learning or imitation. There may also be a genetic basis to foraging ability, but uncontrolled maternal effects in the experiment prevent a proper test for it.     

Feeding ecology and foraging behaviour of impala Aepyceros melampus in Lake Mburo National Park, Uganda

Intersexual and seasonal variation in foraging behaviour of impala (Aepyceros melampus), was studied in the Lake Mburo National Park, Uganda. There was a moderate seasonal difference in foraging efficiency (as measured by ‘acceptable food abundance’), with a minimum in dry season and a maximum in Rainy season. The variation between sexes was more distinct with a pronounced minimum in time spent browsing of males in early wet season. By distinguishing between feeding time spent grazing and feeding time spent browsing the seasonal variation was confirmed. The proportion of foraging time spent feeding (expressed as ‘food ingestion rate’) showed an inverse pattern with a maximum in the late dry season (75.5%), decreasing values throughout the Rainy season and a minimum in early dry season (57.8%). Differences between sexes were explained in terms of reproductive demands and seasonal balance in terms of moderate climate throughout the year. Impala foraging patterns in the bimodal tropics (two Rainy seasons) is discussed and compared with unimodal tropics. The findings are matched against current ideas on optimal foraging.     

延迟投饵对史氏鲟仔鱼摄食、存活及生长的影响

为了解史氏鲟仔鱼阶段的开口摄食习性,为史氏鲟的人工育苗提供基础资料,研究了延迟投饵对史氏鲟仔鱼摄食、存活及生长的影响。结果表明:仔鱼6日龄开口,7日龄史氏鲟仔鱼初次摄食,10日龄卵黄基本吸收完毕,16~17日龄,不能建立外源性营养的仔鱼进入饥饿的不可逆点(PNR)期,故其PNR是16日龄;史氏鲟仔鱼存活率随延迟投饵天数的增加而降低,6日龄后,延迟投饵时间在7d内,仔鱼存活率可达60%以上,延迟投饵时间在8~10d内,仔鱼的成活率下降至40%左右,延迟投饵时间为11d,存活率下降至10%,延迟投饵时间为12d及以后,存活率为0;史氏鲟仔鱼全长和体质量在延迟投饵4d内均增加;延迟投饵超过4d则均下降。延迟投喂时间在8d以内,仔鱼全长和体质量与对照组无显著性差异;延迟投喂超过9d,全长和体质量低于对照组;史氏鲟仔鱼适宜投饵的时间是孵出后9~10d。     

Sensory and skeletal development and growth in relation to the duration of the embryonic and larval stages in damselfishes (Pomacentridae)

Several trends were found in comparisons of rates of growth and development of larvae of four coral-reef damselfishes ( Chromis atripectoralis, Pomacentrus amboinensis, Premnas biaculeatus, Acanthochromis polyacanthus ), which were reared under constant temperature conditions in the laboratory, and which varied in their early life stage durations (respectively, egg stage durations were 2, 4, 7, 16; larval stage durations were 25, 23, 14, 0). Parameters measured included standard length, muscle area, eye diameter, and selected stages of retinal development, olfactory development, and skeletal ossification. Rates of ossification and olfactory development were inversely related to growth rate (in length and muscle area) among most species. Rates of eye growth and retinal development were also negatively correlated among all species. These results are consistent with the concept of a trade-off between growth and development. We observed a positive relationship between egg stage duration and developmental rate, and a negative correlation between larval stage duration and developmental rate. Acanthochromis developed slower than predicted by the general trends, although retinal development was very rapid. Specific retinal stages correlated with settlement, regardless of ontogenetic rates. Olfactory development was especially rapid in the anemonefish Premnas biaculeatus , which imprints to olfactory cues as an embryo. Skeletal ossification was rapid in species with pelagic larvae, and much slower in the benthic brooder. Literature-derived data on size and age at hatching and settlement from > 40 species of tropical pomacentrids were transformed into growth and developmental rates; correlations of these literature-derived parameters were mostly consistent with our controlled four-species comparison.  © 2003 The Linnean Society of London, The Biological Journal of the Linnean Society , 2003, 80 , 187−206.     

Study on foraging mechanism of leeches with different feeding habits based on chemoreception and foraging behavior

The leeches Whitmania pigra and Hirudo nipponia live in similar environments but have different feeding habits. At present, there are few studies of the foraging mechanism of leeches with different feeding habits. In this study, we first used maze tests to show that these two species of leeches could locate and distinguish their prey through chemosensory activity without mechanical stimulation. However, the two leech species have different foraging behaviors: Individuals of W. pigra move slowly and repeatedly adjust direction through probing and crawling to detect the location of prey (snails), whereas individuals of H. nipponia move quickly, and after determining the location of food (porcine blood), they quickly swim or crawl to the vicinity of their prey. Scanning electron microscopy (SEM) revealed that there are two types of sensory cilia and pore structures related to mucus secretion in the heads of both leeches. There are two differently sized types of chemoreceptors on the dorsal lip in W. pigra, which may have different functions during foraging, whereas in H. nipponia there is only one type of chemoreceptor, which is small. We detected the chemical components in the natural food of these two leech species by UHPLC–MS. There were 934 metabolites in the body fluid of snails and 751 metabolites in porcine serum; five metabolites unique to the body fluid of snails and to porcine serum were screened as candidate feeding attractants. Of these metabolites, betaine and arginine effectively attracted individuals of W. pigra and H. nipponia, respectively. In summary, leeches with different feeding habits use chemoreceptors to sense external chemical signals when foraging, and there are significant differences between species in foraging behavior, chemoreceptors, and attractants.     

The influence of developmental environment on the evolution of olfactory foraging behaviour in procellariiform seabirds

The evolutionary origins of foraging behaviour by procellariiform seabirds (petrels, albatrosses and shearwaters) are poorly understood. Moreover, proximate factors affecting foraging ecology, such as the influence of environment on the development of sensory systems, have yet to be addressed. Here, we apply comparative methods based on current procellariiform phylogenies to identify associations between sensory modalities and the developmental environment that may underlie the evolution of complex foraging behaviour. We postulate that, for burrow-nesting species, smell is likely to dominate the sensory world of the developing chick. Alternatively, for ground-nesting species, chicks receive exposure to a range of visual, auditory and olfactory cues. We employ maximum likelihood to test models of correlated trait evolution between nesting habit and olfactory foraging style and to reconstruct the ancestral states of these characters when coded as binary states. Our results suggest that nesting behaviour has evolved in conjunction with foraging style. Based on this analysis, we propose that nesting on the surface was a life-history innovation that opened up a new developmental environment with profound effects on the foraging ecology of procellariiform seabirds.     

Consequences of adaptation to larval crowding on sexual and fecundity selection in Drosophila melanogaster

Sexual selection is a major force influencing the evolution of sexually reproducing species. Environmental factors such as larval density can manipulate adult condition and influence the direction and strength of sexual selection. While most studies on the influence of larval crowding on sexual selection are either correlational or single-generation manipulations, it is unclear how evolution under chronic larval crowding affects sexual selection. To answer this, we measured the strength of sexual selection on male and female Drosophila melanogaster that had evolved under chronic larval crowding for over 250 generations in the laboratory, along with their controls which had never experienced crowding, in a common garden high-density environment. We measured selection coefficients on male mating success and sex-specific reproductive success, as separate estimates allowed dissection of sex-specific effects. We show that experimental evolution under chronic larval crowding decreases the strength of sexual and fecundity selection in males but not in females, relative to populations experiencing crowding for the first time. The effect of larval crowding in reducing reproductive success is almost twice in females than in males. Our study highlights the importance of studying how evolution in a novel, stressful environment can shape adult fitness in organisms.     

Effects of life phase and schooling patterns on the foraging behaviour of coral‐reef fishes from the genus Haemulon

During this study (December 2009 to December 2010), underwater visual surveys using the focal animal method were performed in the coastal reefs of Tamandaré, north‐eastern Brazil. The aim was to analyse the effects of the life phase (juvenile and adult) and schooling patterns (school and solitary) on the feeding behaviour (foraging rates and substratum preferences) of four species of the genus Haemulon (Haemulon aurolineatum, Haemulon parra, Haemulon plumieri and Haemulon squamipinna). PERMANOVA analysis (P < 0·05) indicated that ontogenetic changes and schooling patterns directly influence foraging behaviour. Schooling individuals had low foraging rates (mean ± s.d . = 2·3 ± 2·1 bites 10 min^?1) and mobility, usually remaining near the bottom; however, solitary fishes had high foraging rates (mean ± s.d . = 12·5 ± 4·6 bites 10 min^?1). Juveniles preferred feeding in the water column (75% of the total number of bites), whereas adults foraged mainly in sand (80%) and bare rock (20%). All four Haemulon species displayed similar patterns of feeding behaviour as well as preferences for foraging sites and display competition for food resources. In contrast, little is known about their habitat use and foraging behaviour over the diel cycle, particularly the newly settled and early juvenile stages.     

Kin recognition and co‐operative foraging in Drosophila melanogaster larvae

A long‐standing goal for biologists and social scientists is to understand the factors that lead to the evolution and maintenance of co‐operative behaviour between conspecifics. To that end, the fruit fly, Drosophila melanogaster, is becoming an increasingly popular model species to study sociality; however, most of the research to date has focused on adult behaviours. In this study, we set out to examine group‐feeding behaviour by larvae and to determine whether the degree of relatedness between individuals mediates the expression co‐operation. In a series of assays, we manipulated the average degree of relatedness in groups of third‐instar larvae that were faced with resource scarcity, and measured the size, frequency and composition of feeding clusters, as well as the fitness benefits associated with co‐operation. Our results suggest that larval D. melanogaster are capable of kin recognition (something that has not been previously described in this species), as clusters were more numerous, larger and involved more larvae, when more closely related kin were present in the social environment. These findings are discussed in the context of the correlated fitness‐associated benefits of co‐operation, the potential mechanisms by which individuals may recognize kin, and how that kinship may play an important role in facilitating the manifestation of this co‐operative behaviour.     

Sexual selection shapes development and maturation rates in Drosophila

Explanations for the evolution of delayed maturity usually invoke trade‐offs mediated by growth, but processes of reproductive maturation continue long after growth has ceased. Here, we tested whether sexual selection shapes the rate of posteclosion maturation in the fruit fly Drosophila melanogaster. We found that populations maintained for more than 100 generations under a short generation time and polygamous mating system evolved faster posteclosion maturation and faster egg‐to‐adult development of males, when compared to populations kept under short generations and randomized monogamy that eliminated sexual selection. An independent assay demonstrated that more mature males have higher fitness under polygamy, but this advantage disappears under monogamy. In contrast, for females greater maturity was equally advantageous under polygamy and monogamy. Furthermore, monogamous populations evolved faster development and maturation of females relative to polygamous populations, with no detectable trade‐offs with adult size or egg‐to‐adult survival. These results suggest that a major aspect of male maturation involves developing traits that increase success in sexual competition, whereas female maturation is not limited by investment in traits involved in mate choice or defense against male antagonism. Moreover, rates of juvenile development and adult maturation can readily evolve in opposite directions in the two sexes, possibly implicating polymorphisms with sexually antagonistic pleiotropy.     

Effects of insecticides on the foraging behaviour and survival of Cotesia vestalis,a larval parasitoid of the diamondback moth,Plutella xylostella

The effects of the insecticides etofenprox, malathion, diazinon, methomyl, alanycarb, clothianidin and emamectin benzoate on the foraging behaviour and survival of Cotesia vestalis (Hymenoptera: Braconidae), a larval parasitoid of the diamondback moth Plutella xylostella (Lepidoptera: Plutellidae) were investigated in the laboratory. The period required for C. vestalis females to reach P. xylostella‐infested Komatsuna (Brassica rapa) plants treated with etofenprox, methomyl or malathion was significantly longer than that to infested plants treated with emamectin benzoate or clothianidin; and the period to reach alanycarb or diazinon‐treated plants was intermediate between them. The period to reach emamectin benzoate‐ or clothianidin‐treated plants was not significantly different from that to distilled water‐sprayed plants, suggesting that etofenprox, methomyl and malathion have strong inhibitory effects on the flight response, whereas the inhibitory effects of alanycarb and diazinon are relatively weak. By contrast, emamectin benzoate and clothianidin showed no inhibitory effect. The time of residency on the clothianidin‐treated plants was significantly longer than that on other insecticide‐treated plants (etofenprox, methomyl, alanycarb, malathion or diazinon), with the time of residency on emamectin benzoate‐treated plants being intermediate between them. These results suggest that etofenprox, methomyl, alanycarb, malathion, and diazinon have a strong inhibitory effect on host‐searching behaviour, while emamectin benzoate and clothianidin have a relatively weak effect. Furthermore, the mortality of wasps after foraging on the clothianidin‐treated plants was significantly higher than after foraging on other insecticide‐treated plants (etofenprox, methomyl or malathion), with subsequent mortality on alanycarb‐, diazinon‐ and emamectin benzoate‐treated plants being intermediate between them. Our results suggest that subsequent mortality increases with decreased inhibitory effect on the foraging behaviour of C. vestalis.     

The effects of perceived competition and parasitism on the foraging behaviour of the upland bully (Eleotridae)

Prey choice by fish is subject to many constraints, some of which may interact to determine the relative preference of fish for prey with different profitabilities. The constraining effects of parasitism and perceived competition on foraging behaviour were examined in the upland bully, Gobiomorphus breviceps . In the laboratory, bullies faced with a choice of prey items of two different sizes chose the larger prey significantly more often than the smaller ones. The presence of a conspecific fish near the source of large prey significantly reduced the bullies'preference for larger prey. Neither the size of the test fish, nor the number of digenean metacercarial cysts they harboured, had any influence on their relative preference for larger prey, or on how that preference was dampened by the presence of a competitor. The threat of competition appears to be a more important constraint on prey choice in upland bullies than parasitism.     

Multi-scale effects of resource patchiness on foraging behaviour and habitat use by longnose dace, Rhinichthys cataractae

1. We examined the response of a predatory benthic fish, the longnose dace ( Rhinichthys cataractae ), to patchiness in the distribution of benthic macroinvertebrates on cobbles at three hierarchical spatial scales during summer and autumn 1996, and spring 1997 in a southern Appalachian stream. 2. At the primary scale (four to five individual cobbles separated by <1 m), the intensity of foraging was not correlated with the biomass of benthic macroinvertebrates/cobble, regardless of season. 3. At the secondary scale (i.e. foraging patches <5 m in diameter) we found that benthic macroinvertebrates were patchily distributed in summer, but not in autumn or spring. Concomitantly, in summer, longnose dace foraged on cobbles with a significantly higher biomass of benthic macronvertebrates than nearby, randomly selected cobbles with similar physical conditions (i.e. longnose dace tended to avoid low-prey foraging patches). In contrast, when benthic macroinvertebrates were distributed homogeneously (spring and autumn), dace did not select patches with a significantly higher biomass of benthic macroinvertebrates than that available on randomly selected cobbles. 4. At the tertiary scale (i.e. stream reaches 11–19 m long), the biomass of benthic macroinvertebrates (per cobble per reach) was patchily distributed (i.e. differed significantly among reaches) in all seasons. Among reaches with physical characteristics preferred by longnose dace, (i.e. erosional reaches dominated by cobble/boulder substratum and high current velocity), we detected a significant, positive correlation between the biomass of benthic macroinvertebrates/cobble and longnose dace density in all seasons. 5. Our results demonstrated that both spatial and temporal patchiness in resource availability influenced significantly the use of both foraging patches and stream reaches by longnose dace.     

Density-dependent prey behaviours and mutable predator foraging modes induce Allee effects and over-prediction of prey mortality rates

1. Predator–prey models are often used to represent consumptive interactions between species but, typically, are derived using simple experimental systems with little plasticity in prey or predator behaviours. However, many prey and predators exhibit a broad suite of behaviours. Here, we experimentally tested the effect of density-dependent prey and predator behaviours on per capita relative mortality rates using Florida bass (Micropterus floridanus) consuming juvenile Bluegill (Lepomis macrochirus).
2. Experimental ponds were stocked with a factorial design of low, medium, and high prey and predator densities. Prey mortality, prey–predator behaviours, and predator stomach contents were recorded over or after 7 days. We assumed the mortality dynamics followed foraging arena theory. This pathologically flexible predator–prey model separates prey into invulnerable and vulnerable pools where predators can consume prey in the latter. As this approach can represent classic Lotka–Volterra and ratio-dependent dynamics, we fit a foraging arena predator–prey model to the number of surviving prey.
3. We found that prey exhibited density-dependent prey behaviours, hiding at low densities, shoaling at medium densities, and using a provided refuge at high densities. Predators exhibited ratio-dependent behaviours, using an ambush foraging mode when one predator was present, hiding in the shadows at low prey–high predator densities, and shoaling at medium and high prey–high predator densities. The foraging arena model predicted the mortality rates well until the high prey–high predator treatment where group vigilance prey behaviours occurred and predators probably interfered with one another resulting in the model predicting higher mortality than observed.
4. This is concerning given the ubiquity of predator–prey models in ecology and natural resource management. Furthermore, as Allee effects engender instability in population regulation, it could lead to inaccurate predictions of conservation status, population rebuilding or harvest rates.