The effects of a multispecies sequential diet on the growth and survival of a tropical polyphagous caterpillar

Hylesia lineata Druce (Lepidoptera: Saturniidae) caterpillars are highly polyphagous at the individual level. I examined the effects of a multispecies sequential diet on the performance of the larvae. The experiment included three natural hosts respectively —Casearia corymbosa HBK,Thouinia paucidentata Radlk., andErythroxylum havanense Jacq — used by ovipositing females in proportion as expected by their abundance;C. corymbosa andE. havanense representing the most and least abundant hosts respectively. All possible two-host and single-host diets were tested. Larval survival to the pupal stage (as protected by a field cage) did not differ among all diets. Also, for females, regardless of the identity of the initial host, the final weight and the developmental time depended entirely on the nature of the final host. Male performance, in contrast, only differed in terms of developmental time but again the initial host did not affect the final result. It was concluded that a host switch early in the development of the caterpillars does not affect further growth on the other host plants. Caterpillars that finished their development onE. havanense reached small sizes but females devoted a larger proportion of their resources to egg biomass; as a result female fertility was similar among females regardless of their feeding history. I concluded that the caterpillar's abilities and the female compensatory flexibility may oppose selection for a strong preference hierarchy in the female ovipositing behavior.     

Seasonal insectivory by Black‐headed Trogons,a tropical dry forest frugivore

ABSTRACT Fruit‐eating birds are important seed dispersers in tropical forests, but little is known about the extent to which they rely on insects or how their diets vary seasonally. We used field observations of focal adults to quantify the diets of adult and nestling Black‐headed Trogons (Trogon melanocephalus) at nine nests in a lowland dry forest in Costa Rica. From May 2004 to August 2004, we documented 540 food deliveries to nests and 1080 food items consumed by adults. Adult and nestling trogons were largely insectivorous, feeding mainly on moth caterpillars (Lepidoptera). Fruit accounted for only 10.5% of items consumed by adults and 2.2% of items delivered to nestlings (6.1% and 0.6% of estimated dry mass, respectively). Adult and nestling diets differed significantly in both composition and prey size, with adults consuming more fruit and fewer large insects (Phasmatodea and Mantodea) than nestlings and eating more types of arthropods and fruit. Although both adults and nestlings relied heavily on moth larvae, adults preferentially consumed small caterpillars and delivered large ones to their nestlings. In addition, the proportion of large caterpillars delivered to nests remained constant throughout the nestling period, whereas the proportion of large caterpillars eaten by adults declined significantly with nestling age. Overall, arthropods delivered to nests averaged 70% heavier than those consumed by adults (estimated dry mass). Our results suggest that Black‐headed Trogons time reproduction to coincide with arthropod rather than fruit abundance, a pattern that may be more common among omnivorous forest birds than previously recognized.     

Food intake, conversion efficiency, and feeding behaviour of tobacco hornworm caterpillars given artificial diet of varying nutrient and water content

ABSTRACT Fifth stadium tobacco hornworm caterpillars, Manduca sexta (L.), given artificial diet diluted to varying extents with either cellulose or water compensated for the food's reduced nutrient content by eating more of it. This compensation was, however, in most cases not sufficient to maintain normal growth rates. When the water content of the diet was reduced, the insects ate less than the usual fresh weight of food but maintained their intake of nutrients. Nevertheless, growth rate was impaired. The insects were better able to compensate for dilution of their food with water than with cellulose. The efficiency of conversion of ingested food (ECI) was decreased when the diet was adulterated with cellulose. At moderate dilution (50% nutrient) this was due mostly to decreased approximate digestibility (AD), but at greater dilution (25% and 10% nutrient content) the efficiency of conversion of digested food (ECD) was decreased. ECI was maintained when the water content of the diet was increased to give 50% nutrient concentration, but was decreased when water content was changed more radically (200%, 25% and 10% nutrient diets). This was due mostly to increased metabolic costs (decreased ECD) in all cases. The retention time of food in the gut was progressively decreased (i.e. speed of passage was increased) as nutrients were replaced by cellulose. By contrast, dilution of the diet with water resulted in only slight changes in retention time, except at extreme dilution (10% nutrient content) when retention time was reduced. Compensation of food intake was achieved by spending more (or less) time eating. Video analysis of feeding behaviour showed that there were significant changes in the length of feeding bouts and of interfeed gaps when caterpillars fed on diets of altered composition. For diets diluted with cellulose, changes in bout length and bout frequency contributed substantially to the increased time spent feeding on the adulterated food. For diets diluted with water, however, almost all of the compensatory change in behaviour was due to increased bout length, with bout frequency affected only slightly. This suggests that volumetric feedback contributes principally to the termination of feeding bouts in caterpillars, while nutrient flow may affect both the initiation and termination of feeding.     

Glutathione transferase activity and oocyte development in copepods exposed to toxic phytoplankton

Organisms present a series of cellular mechanisms to avoid the effects of toxic compounds. Such mechanisms include the increase in activity of detoxification enzymes [e.g., 7-ethoxyresorufin-O-deethylase (EROD) and glutathione S-transferase (GST)], which could explain the low retention of ingested toxins generally observed in copepods. In addition, decreasing gross growth efficiency (GGE) of copepods with increasing concentration of toxic diets could be caused either by a high expenditure coping with toxins (e.g., increase in the activity of detoxification enzymes) or by a deterioration of reproductive tissues. To assess the effect of toxic phytoplankton on the activity of detoxification enzymes and on oocyte maturation of Acartia tonsa and Temora longicornis, feeding and egg production experiments were carried out with a variety of toxic diets and an adequate non-toxic food control (Rhodomonas spp.) all provided as single species diets. Toxic diets included the nodularin-producing cyanobacterium Nodularia spumigena, the dinoflagellates Alexandrium minutum, and A. tamarense, which contained Paralytic Shellfish Poisoning (PSP) toxins, the dinoflagellate Prorocentrum lima with Diarrhetic Shellfish Poisoning (DSP) toxins and the haptophyte Prymnesium parvum, which produces ichtyotoxins with haemolytic activity. Feeding on toxic diets was lower than on Rhodomonas spp., except for A. minutum and A. tamarense. In addition, toxic diets negatively affected reproduction in both copepod species with the production of oocytes and oocyte development impaired with A. minutum and N. spumigena. While the negative effect of N. spumigena seemed to be connected to gonad atresia likely caused by severe food limitation (starvation), the negative effect of A. minutum could have been either caused by a direct effect of saxitoxins or nutritional inadequacy on oocyte production. We could not detect EROD activity in the copepods, while the activity of GST was generally higher with the non-toxic food control and positively related to the feeding and egestion rates, suggesting relation to feeding conditions rather than to exposure to toxic diets. No relationship was found between GGE and GST activity. Our results refute the hypothesis that toxic diets, provided at ecologically relevant levels, would induce cellular mechanisms in copepods regarding GST activity. GST activity thus seems to play no role in detoxification of copepods confronted with toxic phytoplankton. Toxin detoxification and its cost for copepods still remain an open question.     

The feeding behaviour of caterpillars (Manduca sexta) on tobacco and on artificial diet

ABSTRACT. Feeding behaviour of fifth instar tobacco hornworm caterpillars, Manduca sexta (Johansen) (Lepidoptera; Sphingidae), eating tobacco or artificial diet, is quantitatively described. The insects grow at the same rate on both foods. There is no daily rhythm of feeding behaviour. For most insects, feeding on either food occurs in bouts with the lengths of interfeed gaps and of feeding bouts appearing to be distributed randomly. However, in many insects there is a strong correlation between the length of a feeding period and that of the preceding non-feeding period.
The proportion of time spent feeding on tobacco is much greater than on artificial diet. On tobacco, feeding periods are separated by shorter interfeed gaps than on the artificial diet, while the rate of bout initiation is similar on either food.
On both tobacco and artificial diet, the proportion of time spent feeding increases as the fifth stadium proceeds. This is due to both longer feeding bouts and shorter gaps. The rate of food acquisition within bouts does not change during the stadium.     

Do food protein and carbohydrate content influence the pattern of feeding and the tendency to explore of forest tent caterpillars?

This study examines whether the ratio of protein to carbohydrate affects the timing of meals and the propensity to explore of forest tent caterpillars (Malacosoma disstria). The behavior of fourth instar caterpillars was observed on three semi-defined artificial diets varying in protein (p)-carbohydrate (c) ratio. These diets were (a) p14:c28, (b) p28:c14, and (c) p35:c7. The probability of initiating feeding at first contact with the food and the duration of the first feeding event did not vary across diets, suggesting not much difference in phagostimulatory power. There was also no difference in the total time spent eating, at rest and in motion between diets. However, the timing and duration of meals varied significantly; more short meals were observed on the carbohydrate-biased diet. The duration of pauses between meals also increased with food protein content. Furthermore, caterpillars on the carbohydrate-biased diet were more likely to leave the trail leading to the known food source and to discover a second food source, suggesting that protein deprivation promotes exploration. These findings shed insight into the physiological responses to protein and carbohydrate ingestion and demonstrate how post-ingestive effects can favor consumption of foods containing protein without invoking an explicit mechanism of independent nutrient regulation, but simply by influencing the pattern of feeding and the propensity to explore.     

Plasticity in Forest Tent Caterpillar Collective Foraging Schedules

Self‐organization can generate synchronized group activity without external triggering cues, and schedules of self‐organized collective activity can vary with environmental conditions. This plasticity can improve group members’ ability to meet their requirements in different environments. In colonial caterpillars, synchronized colony foraging schedules have been postulated to depend either on avoidance of visual predators or on temperature effects on ectotherm physiology. We examine the foraging schedule of forest tent caterpillars (Malacosoma disstria) under different constant conditions to distinguish between these hypotheses. Plasticity in the foraging schedule was tested by keeping colonies under different constant regimes of light and temperature. Digital video and tracking software were used to record the colony's alternation between quiescent and active bouts. The duration and frequency of bouts was compared between treatments. The schedule of synchronized colony activity was not affected by lighting, but it accelerated at higher temperature, because of a decrease in the duration of both active and quiescent bouts. Forest tent caterpillars’ foraging schedule thus depends on the time required to accomplish the tasks of food finding (active bouts) and food processing (quiescent bouts). As caterpillars are ectotherms, locomotion and digestion rates increase at higher temperature and both tasks are accomplished faster. The forest tent caterpillar and the congeneric eastern tent caterpillar (M. americanum) both exhibit self‐organized synchronized collective foraging, but environmental modulation of foraging schedule differs between these species, according to differences in social organization and thermal ecology. Eastern tent caterpillars maintain a fixed foraging schedule under varying temperatures and use the tent to maintain high metabolic rates. In the forest tent caterpillar, flexibility of the foraging schedule in accordance with changes in metabolism lessens the constraints imposed by collective foraging. Synchronous foraging, where entire social groups travel together to and from feeding sites, is thought to have several fitness advantages including improved food finding, recruitment to profitable food sources, anti‐predator defense and group thermoregulation between foraging expeditions.     

Daily foraging schedule of field colonies of the eastern tent caterpillar Malacosoma americanum

Summary The daily foraging patterns of seven colonies of the eastern tent caterpillar, Malacosoma americanum, were monitored photoelectronically during the last three larval stadia to provide the first detailed record of the foraging behavior of a gregarious caterpillar under field conditions. Colonies were active an average of 49.3% of each day. Three bouts of foraging, centered about 0600 h, 1500 h and 2000 h (EST), occurred daily during the fourth and fifth stadia. Although ambient temperatures were less favorable for foraging and food processing than at other times of the day, the caterpillars were most active at dusk and dawn, and spent comparatively little time away from the tent during the daylight hours. In the last (sixth) stadium, the caterpillars foraged only under the cover of darkness. A lack of relationship between the rate at which the caterpillars processed food and the spacing of their feeding bouts, indicates that this species follows a schedule of feeding and growth shaped by factors other than those directly related to feeding efficiency and ambient temperature. Colony foraging patterns may reduce caterpillar mortality by minimizing contact between larvae and day-active predators and parasitiods.     

Patterns and mechanisms of growth of fifth-instar Manduca sexta caterpillars following exposure to low- or high-protein food during early instars.

For many insect herbivores, variation in protein availability is a pervasive part of the environment. I explore how variable protein availability affects growth rates of fifth-instar Manduca sexta caterpillars and how growth is related to behavior and physiology. Groups of larvae were reared on low- or high-protein artificial diets (5.9% and 17.7% casein by dry weight, respectively) and then transferred in the fifth instar to the same or opposite diet. During or after the 24-h period following transfer, I measured growth rate, consumption rate, growth efficiency, midgut proteolytic activity, and masses of midgut contents and tissues. Fifth-instar caterpillars reared in earlier instars on high-protein diet grew about 20% more rapidly over 24 h than did caterpillars reared on low-protein diet. This growth pattern appears to be caused by differences in consumption and growth efficiency: caterpillars reared on high protein consumed more food, and used it more efficiently, than did caterpillars reared on low-protein diet. Over the short term (24 h), in contrast, fifth instars that received low-protein diet grew as rapidly as caterpillars that received high-protein diet. Increased (compensatory) consumption appears to be the primary mechanism by which caterpillars consuming low-protein food maintained growth rates.     

Effect of DIMBOA on growth and digestive physiology of Sesamia nonagrioides (Lepidoptera: noctuidae) larvae

The hydroxamic acid 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) was assessed for its effect on growth and digestive physiology of larvae of the stalk corn borer Sesamia nonagrioides Lef. Nutritional indices and activities of some digestive and detoxification enzymes were determined for larvae feeding on a DIMBOA-containing diet for the first two days of the third instar (short-term feeding assays), and from neonates to third instar (long-term feeding assays). DIMBOA reduced the relative growth rate and the efficiency of conversion of ingested food without affecting the relative consumption rate in long-term feeding assays, but it had no effect in short-term assays. Moreover, elastase-like activity was significantly increased by DIMBOA in short-term feeding assays, whereas microsomal oxidase activity was increased and esterase activity was reduced in long-term feeding assays. In vitro, DIMBOA inhibited the activities of carboxypeptidases, aminopeptidase, glutathione S-transferase and esterase, but it had no effect on trypsin, chymotrypsin and elastase. The implications of the altered levels of proteases and detoxification enzyme activities on the digestive physiology of larvae feeding on DIMBOA-containing diets are discussed.     

Foraging behavior and growth of isolated larvae of a social caterpillar, Malacosoma americanum

In laboratory experiments, isolated eastern tent caterpillars, Malacosoma americanum (Fabricius) (Lepidoptera: Lasiocampidae), grew more slowly than their grouped siblings even though factors previously reported to give grouped caterpillars an advantage were eliminated from our experimental design. Analysis of time-lapse videorecordings of daily foraging bouts showed that, despite their slower growth, isolated individuals fed significantly more often than their grouped siblings. This finding is consistent with previous observations showing that the rate at which tent caterpillars assimilate food is largely independent of foraging frequency and suggests that increased metabolic costs associated with superfluous activity may cause isolated caterpillars to grow slower. More rapid growth of grouped caterpillars also appears attributable to the significantly longer periods of time solitary caterpillars spent inactive during episodes of molting. Our study shows that the distinctive temporal pattern of foraging characteristic of intact colonies of eastern tent caterpillars is a emergent property of the group.     

Influence of dietary nutritional composition on caterpillar salivary enzyme activity

Caterpillars are faced with nutritional challenges when feeding on plants. In addition to harmful secondary metabolites and protein- and water-limitations, tissues may be carbohydrate-rich which may attenuate optimal caterpillar performance. Therefore, caterpillars have multiple strategies to cope with surplus carbohydrates. In this study, we raise the possibility of a pre-ingestive mechanism to metabolically deal with excess dietary sugars. Many Noctuid caterpillars secrete the labial salivary enzyme glucose oxidase (GOX), which oxidizes glucose to hydrogen peroxide and gluconate, a nutritionally unavailable carbohydrate to the insect. Beet armyworm, Spodoptera exigua, larvae were restricted to diets varying in protein to digestible carbohydrate (P:C) ratio (42p:21c; 33p:30c; 21p:42c) and total nutrient concentration (42% and 63%). High mortality and longer developmental time were observed when caterpillars were reared on the C-biased, P-poor diet (21p:42c). As the carbohydrate content of the diet increased, caterpillars egested excess glucose and a diet-dependent difference in assimilated carbohydrates and pupal biomass was not observed, even though caterpillars restricted to the C-biased diet (21p:42c) accumulated greater pupal lipid reserves. Larval labial salivary GOX activity was also diet-dependent and gluconate, the product of GOX activity, was detected in the frass. Unexpectedly, GOX activity was strongly and positively correlated with dietary protein content.     

The effects of a phagostimulant and a deterrent on the microstructure of feeding byManduca sexta caterpillars

Caterpillars of the hawkmothManduca sexta Johan. (Lepidoptera: Sphingidae) were offered discs of agar containing one of a range of concentrations of sucrose or of quinine, and the microstructure of the resulting feeding behaviour was quantified. As sucrose concentration increased caterpillars ate more by increasing the rate of biting and the lengths of meals. Bite frequency increased, after a latency of seconds to minutes, over the entire range tested (0.005 M to 0.5 M) whereas meal length reached a maximum at 0.1 M. Larvae spent less time feeding on agar containing 1 mM quinine than on quinine-free agar. This was accomplished by a reduction in the size of meals; numbers of chewing bouts in meals were lower. No other feeding behaviours were affected. In addition there was no orderly relationship between quinine concentration and changes in feeding behaviours. These observations suggested that postingestive effects were important in decreasing feeding. This paper is dedicated to the memory of Vincent G. Dethier     

Diet factors responsible for the change of the glucose oxidase activity in labial salivary glands of Helicoverpa armigera

We investigated the change of the glucose oxidase (GOX) activity in labial salivary glands of Helicoverpa armigera larvae fed with the artificial diet or host plant tobacco and the major factors responsible for such a change. Throughout larval development, the labial salivary GOX activities in caterpillars reared on the artificial diet were remarkably higher than those fed with the plant. After fifth-instar plant-fed caterpillars were transferred to the artificial diet, their labial salivary GOX activity increased quickly, which was closely correlated with the time spent feeding on the artificial diet. The total sugar content of the artificial diet was 68 times higher than that of the tobacco leaves. We hypothesized that sugars and secondary metabolites are the possible causes of induction of GOX activity. When fifth-instar caterpillars were fed with tobacco leaves coated with glucose or sucrose, their labial salivary GOX activity was significantly higher than those fed with leaves without sugar coating. Following native PAGE, 1 single band of the labial salivary GOX was observed in all the caterpillars fed with different diets, implying that only the activity of the isoenzyme was changed in response to different diets. Furthermore, the labial salivary GOX activity was determined after caterpillars were fed with artificial diets containing chlorogenic acid, rutin, and quercetin. The results showed that all these phenolic compounds had no effect on the GOX activity. We conclude that sugar in diets was a major factor influencing the labial salivary GOX activity of the larvae. Arch. Insect Biochem. Physiol. 2008.     

Nutrient utilization by caterpillars of the generalist beet armyworm, Spodoptera exigua

Abstract.  Beet armyworm, Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae), caterpillars are destructive crop pests responsible for considerable annual economic losses. These generalist herbivores are challenged with a diversity of dietary choices that can impact their survival, development and fecundity. In the present study, dietary choices of S. exigua caterpillars, based on the protein to digestible carbohydrate (P : C) ratio of the food, and the impact of nutritionally unbalanced foods on caterpillar performance are assessed. In choice experiments, individual third-instar caterpillars are offered simultaneously a P-biased and a C-biased food until pupation. Caterpillars feed nonrandomly and select a slightly P-biased diet (22P : 20C). In no-choice experiments, second instar caterpillars are reared until pupation on diets ranging in P : C ratio from extremely P- to extremely C-biased. High mortality and delayed development are observed on the C-rich, P-poor diets, highlighting the potential deleterious effects of excess carbohydrates and the importance of protein for growth and development. Diet-dependent differences in pupal weight or pupal lipid reserves are not observed. This contrasts with closely-related Spodoptera species where pupal mass and lipid stores increase on C-rich, P-poor diets. On the extremely P-biased diet, performance is similar to that of individuals reared on the self-selected diet, suggesting that these caterpillars may efficiently be deaminating excess amino acids to generate carbon skeletons, which are shunted into lipid biosynthesis. Spodoptera exigua caterpillars exhibit flexible and efficient pre-ingestive nutrient intake regulation and post-ingestive utilization, allowing these generalist feeders to cope with the heterogeneous diets they may encounter.     

The influence of plant defensive chemicals,diet composition,and winter severity on the nutritional condition of a free‐ranging,generalist herbivore

When consuming plants, herbivores must deal with both low nutritional quality from cell wall constituents and potentially toxic plant secondary metabolites, which are often inversely related. Herbivores that consume a highly nutritious, but chemically defended plant, may consume high levels of toxins that require energy for detoxification. Alternatively, herbivores may avoid consuming high levels of toxins by consuming a diverse diet that may be lower in overall nutritional quality. In this study, we assessed the relationship among nutritional restriction, detoxification and diet diversity in a free‐ranging wild herbivore. We collected urine deposited in the snow (hereafter, snow‐urine) and feces by free‐ranging moose Alces americanus, a generalist browser, during winter. We used the ratio of urinary urea nitrogen to creatinine (UN:C), measured in snow‐urine samples, as an indicator of nutritional restriction, and the ratio of glucuronic acid to creatinine (GA:C), as an indicator of investment in detoxification. We used microhistology to determine diet composition from fecal pellets. GA:C and UN:C were positively associated, suggesting that nutritional condition tends to be worse for individuals investing more in detoxification. We found, after accounting for the influence of winter severity, diet diversity and UN:C to be negatively related, suggesting that increasingly diverse diets were associated with improved nutritional condition. Overall, the most important predictor of UN:C was winter severity and proportion of diet comprised of balsam fir Abies balsamea. Physiological indicators of nutritional restriction tended to be worse during severe winters and among individuals that had consumed more balsam fir. These results highlight complex relationships among environmental conditions, foraging decisions, and costs of detoxification that can influence nutritional condition of herbivores.     

Does a polyphagous caterpillar have the same gut microbiota when feeding on different species of food plants?

We used classical culture techniques to explore gut bacteria and changes associated with dietary change in the highly polyphagous, tropical caterpillar Automeris zugana (Saturniidae). Fifty-five third instar wild-caught sibs feeding on Annona purpurea (Annonaceae) in the Area de Conservación Guanacaste (ACG) in northwestern Costa Rica were divided into eight groups. Each of seven groups was reared to the ultimate instar on another species of food plant normally used by A. zugana. Some pupae were also analyzed for the presence of bacteria. Aerobic bacterial cultures were obtained from all 33 caterpillar guts and the eight pupae inventoried. There was no clear pattern in species composition of cultivated bacteria among the eight diets, and each caterpillar on a given food plant carried only a small fraction of the total set of species isolated from the set of caterpillars feeding on that food plant. Taken as a whole, the larvae and pupae contained 22 species of cultivable bacteria in 12 genera. Enterobacter, present in 81.8% of the samples, was the genus most frequently isolated from the caterpillars, followed by Micrococcus and Bacillus. Bacillus thuringiensis was isolated from 30.3% of the dissected caterpillars, but found in caterpillars feeding on only half of the species of food plants.     

The interplay between nutrient balancing and toxin dilution in foraging by a generalist insect herbivore

Food mixing by herbivores is thought to balance nutrient intake and possibly dilute secondary metabolites characteristic of different host plant species. Most empirical work on insect herbivores has focused on nutrient balancing in laboratory settings. In this study, we characterize food mixing behaviour of the caterpillar Grammia geneura (Strecker) (Lepidoptera: Arctiidae) in nature and use the observed patterns to design ecologically relevant experiments that reveal the relative importance of these processes in food-switching behaviour. Our design involved both choice and no-choice experiments with chemically defined diets in which primary nutrients and secondary metabolites were manipulated in tandem. We analysed two stages in the process of food-switching behaviour: leaving food and accepting new food. In nature, an individual's rate of leaving host plants was positively associated with its probability of rejecting plant species most recently eaten, but not related to its probability of accepting different host plant species. Furthermore, an individual's leaving rate was negatively related to its average feeding bout duration. This relationship resulted partly from variation in the response of individuals to nutrient imbalance and partly from shortened feeding bouts prior to switching, suggesting that a decline in feeding excitation preceded searching for food that differed from that most recently eaten. Laboratory experiments with synthetic diets indicated the importance of secondary metabolites in the decline in feeding excitation prior to switching. Preference for new food depended strongly on secondary metabolites in a manner consistent with toxin dilution. This is the first experimental evidence for the process of toxin dilution in caterpillars, and for the combined influence of nutrients and secondary metabolites on their foraging patterns in nature. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.