Sex-linked inheritance of host-plant specialization in a polyphagous butterfly

I investigated the genetic background of intraspecific variation in oviposition specificity in the generalist butterfly Polygonia c-album. Using reciprocal crosses between two populations that differ in their degree of specialization, I show that specificity is strongly sex-linked. This indicates that genes determining this difference are located primarily on the paternally inherited X-chromosome. The results suggest that intraspecific differences in specificity are caused by the same genetic mechanisms that have been shown to determine interspecific differences in host-plant ranking in other butterflies. Accordingly, the common assumption that specialization and ranking are determined by fundamentally different mechanisms was not supported.     

A rhythm underlying feeding behaviour in a highly polyphagous caterpillar

Abstract .Behavioural mechanisms of food mixing were studied in the polyphagous caterpillar Grammia geneura (Strecker) (Lepidoptera, Arctiidae) in arenas with different plant foods. Combinations of food plants, including single and multiple plant species were used. Behavioural observations on individuals of similar age were undertaken for 4 h. Foraging and feeding behaviour were monitored in detail. It was found that feeding was generally initiated during short intervals that represented the peaks of an endogenous activity rhythm. Feeding was not initiated on all peaks but at times that represented multiples of the oscillatory period. The oscillation fitted to each individual varied between 10 and 13 min. The possible significance of the oscillation is discussed.     

Sensitivity to chemically diverse phagostimulants in a single gustatory neuron of a polyphagous caterpillar

Caterpillars of the arctiid moth, Grammia geneura, are polyphagous, but species of Plantago are amongst their preferred food plants. A neuron in the medial styloconic sensillum on the galea has been shown to have a general phagostimulatory function. Experiments with binary mixtures and cross-adaptation have demonstrated that it responds to some sugars, to several amino acids, and also to catalpol. Catalpol is a plant secondary compound in Plantago and a phagostimulant for the caterpillars. The possible significance of combining sensitivity to nutrient compounds with sensitivity to a secondary compound is discussed. Accepted: 7 October 1999     

The effects of predation risk on the use of social foraging tactics

The effects of predation on the use of social foraging tactics, such as producing and scrounging, are poorly known in animals. On the one hand, recent theoretical models predict increased use of scrounging with increasing predation risk, when scroungers seeking feeding opportunities also have a higher chance of detecting predators. On the other hand, there may be no relation between tactic use and predation when antipredator vigilance is not compatible with scanning flockmates. We investigated experimentally the effects of predation risk on social foraging tactic use in tree sparrows, Passer montanus. We manipulated predation risk in the field by changing the distance between shelter and a feeder. Birds visited the feeder in smaller flocks, spent less time on it and were somewhat more vigilant far from shelter than close to it. Increased predation risk strongly affected the social foraging tactic used: birds used the scrounger tactic 30% more often far from cover than close to it. Between-flock variability in scrounging frequency was not related to the average vigilance level of the flock members, and within-flock variability in the use of scrounging was negatively related to the vigilance of birds. Our results suggest that in tree sparrows, the increased frequency of scrounging during high predation risk cannot simply be explained by an additional advantage of increasing antipredator vigilance. We propose alternative mechanisms (e.g. increased stochasticity in food supply, and that riskier places are used by individuals with lower reserves) that may explain increased scrounging when animals forage under high predation risk.     

General activity and foraging tactics in a water bug

Diplonychus indicus is a highly versatile predator that forages both actively and from ambush. However, no correlations between predatory mode changes and predatory performance have yet been evidenced. The hypotheses that time spent foraging actively was proportional to time spent locomotory active and that time spent ambushing was proportional to time spent quiescent were tested during animal development. Locomotory activity increases during development due to increases in both frequency and duration of swimming bouts. The frequency of position changes increases as well. Eggbearing males were less active than other adults. However, the proportion of active foraging did not vary significantly with developmental stage and no correlations between activity level and predatory mode were found. Changes in predatory tactics inDiplonychus indicus differ from those reported in other predators as they are not related to any of the usual biotic or abiotic factors.     

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.     

Changes in taste receptor cell sensitivity in a polyphagous caterpillar reflect carbohydrate but not protein imbalance

Caterpillars of the polyphagous arctiid, Grammia geneura, have a single cell in the medial galeal sensillum that responds to some sugars and to some amino acids. After conditioning on artificial diet containing unbalanced amounts of carbohydrate and protein, the responses of this cell alter. After protein-biased food it increases slightly, but after carbohydrate-biased food it decreases. Responses to both sucrose and amino acids change in the same direction and the changes would not provide the information necessary to redress a shortage of protein. The lateral galeal sensillum contains one cell that responds to fructose and another responding to some amino acids. The responses of each of these cells in the lateral sensillum are not consistently affected by conditioning diets. After conditioning for 20 h on a protein- or carbohydrate-biased diet, the insects started to feed without delay if offered carbohydrate-biased diet, but only after a pause if given protein-biased diet. This occurred irrespective of the conditioning diet. The duration of the first feeding bout was also longer on carbohydrate-biased diet and the longest bouts followed protein-biased conditioning.     

Genetic variation in the effect of a facultative symbiont on host-plant use by pea aphids

Ecological specialisation on different host plants occurs frequently among phytophagous insects and is normally assumed to have a genetic basis. However, insects often carry microbial symbionts, which may play a role in the evolution of specialisation. The bacterium Regiella insecticola is a facultative symbiont of pea aphids (Acyrthosiphon pisum) where it is found most frequently in aphid clones feeding on Trifolium giving rise to the hypothesis that it may improve aphid performance on this plant. A study in which R. insecticola was eliminated from a single naturally infected aphid clone supported the hypothesis, but a second involving two aphid clones did not find the same effect. We created a series of new pea aphid–R. insecticola associations by injecting different strains of bacteria into five aphid clones uninfected by symbionts. For all aphid clones, the bacteria decreased the rate at which aphids accepted Vicia faba as a food plant and reduced performance on this plant. Their effect on aphids given Trifolium pratense was more complex: R. insecticola negatively affected acceptance by all aphid clones, had no effect on the performance of four aphid clones, but increased performance of a fifth, thus demonstrating genetic variation in the effect of R. insecticola on pea aphid host use. We discuss how these results may explain the distribution and frequency of this symbiont across different aphid populations. Julia Ferrari and Claire L. Scarborough contributed equally to the work.     

Behavioural consequences of hunting by expectation: A simulation study of foraging tactics

Foraging behaviour has been simulated using a model that predicts the path taken by an animal foraging for particulate food, the path being defined by the animal's remembrance of its previous foraging success. This is represented in the model by a two-dimensional vector with its modulus encoding an exponentially smoothed average of the animal's feeding rate and its orientation encoding the average direction of travel. As food is ingested the amount ingested and its position are used to update the remembrance, and the animal turns in the adjusted direction travelling at a speed inversely proportional to the average feeding rate. Foraging paths simulated in a patchy environment are shown to have the following properties: (i) They tend to avoid crossing the boundaries of patches from the inside. (ii) They tend to avoid intersecting themselves. (iii) When they do intersect themselves they usually do so more or less at right angles. (iv) They ascend gradients of density of food.     

Mating tactics determine patterns of condition dependence in a dimorphic horned beetle

The persistence of genetic variability in performance traits such as strength is surprising given the directional selection that such traits experience, which should cause the fixation of the best genetic variants. One possible explanation is ‘genic capture’ which is usually considered as a candidate mechanism for the maintenance of high genetic variability in sexual signalling traits. This states that if a trait is ‘condition dependent’, with expression being strongly influenced by the bearer''s overall viability, then genetic variability can be maintained via mutation-selection balance. Using a species of dimorphic beetle with males that gain matings either by fighting or by ‘sneaking’, we tested the prediction of strong condition dependence for strength, walking speed and testes mass. Strength was strongly condition dependent only in those beetles that fight for access to females. Walking speed, with less of an obvious selective advantage, showed no condition dependence, and testes mass was more condition dependent in sneaks, which engage in higher levels of sperm competition. Within a species, therefore, condition dependent expression varies between morphs, and corresponds to the specific selection pressures experienced by that morph. These results support genic capture as a general explanation for the maintenance of genetic variability in traits under directional selection.     

A highly sensitive taste receptor cell for pyrrolizidine alkaloids in the lateral galeal sensillum of a polyphagous caterpillar, Estigmene acraea

Adult males of Estigmene acraea use pyrrolizidine alkaloids to produce pheromones and all stages probably use pyrrolizidine alkaloids for defense. The alkaloids are obtained from plants by the caterpillars. We demonstrate that a contact chemoreceptor neuron in the lateral galeal sensillum exhibits a dose-dependent response to seneciphylline N-oxide, a widely occurring pyrrolizidine alkaloid, down to concentrations of 10(-9) x mol l(-1), and even at 10(-12) x mol l(-1) the response is greater than to salt alone. At concentrations of 10(-6) mol x l(-1) and above the instantaneous firing rate is very high, and at 10(-4) mol x l(-1) initially exceeds 500 spikes s(-1). The firing rate declines in the 200 ms following stimulus onset but then is sustained with an instantaneous firing rate in excess of 100 spikes s(-1) for at least the next 800 ms. At lower concentrations a delay occurs before firing is initiated, and then the pattern of firing is irregular. The cell is equally sensitive to some but not all of several other pyrrolizidine alkaloids tested as free bases and their N-oxides. It also responds to ouabain, which may also serve as a defensive compound, and to asparagine and fructose but with much higher thresholds than to the pyrrolizidine alkaloids.     

Social tactics of pigs in a competitive foraging task: the 'informed forager' paradigm

Studies of the social dynamics in foraging groups have focused primarily on birds, rodents and nonhuman primates. We extended the study of animal social tactics to the domestic pig, Sus scrofa, by using an experimental analogue of natural foraging skills, the 'informed forager' paradigm. We investigated the behaviour of 16 pigs foraging in pairs in an arena in which food had been hidden in one of eight monopolizable buckets. Before each pair trial, one of the pigs, the 'informed' pig, was given privileged knowledge about the location of the food during a solitary search trial. The 'noninformed' pig was na?ve about the location of the food during pair trials, but heavier than its informed partner and thus able to displace the latter from the baited bucket. By first focusing on the informed pigs' behaviour, we show that pigs are able to remember and relocate the food site. They found the food in relocation trials, using fewer bucket investigations than expected of a random searcher. Second, by focusing on the noninformed pigs, we show that pigs are able to exploit the knowledge of others by following them to a food source. They investigated more buckets immediately after their informed partners significantly more often than expected by chance and required fewer bucket investigations to find the food in pair trials than expected from a random searcher, but not in solitary search trials. We discuss these latter findings with reference to social foraging tactics. Copyright 2000 The Association for the Study of Animal Behaviour.     

Cytokinin-mediated leaf manipulation by a leafminer caterpillar

A large number of hypotheses have been proposed to explain the adaptive significance and evolution of the endophagous-feeding mode, nutritional benefits being considered to be one of the main advantages. Leaf-mining insects should feed on most nutritional tissues and avoid tissues with high structural and/or biochemical plant defences. This selective feeding behaviour could furthermore be reinforced by manipulating the plant physiology, as suggested by the autumnal formation of 'green islands' around mining caterpillars in yellow leaves. The question we address here is how such metabolic manipulation occurs and what the nutritional consequences for the insect are. We report a large accumulation of cytokinins in the mined tissues which is responsible for the preservation of functional nutrient-rich green tissues at a time when leaves are otherwise turning yellow. The analogy with other plant manipulating organisms, in particular galling insects, is striking.     

Patterns of microhabitat and larval host-plant use by an imperiled butterfly in northern Florida

The quality of habitat for a given species is fundamental to its persistence in that habitat space. Herbivorous insects often require a specific combination of host plants, floral resources, and physical features such as shelter. Identifying these different habitat features is a focus of ecology and conservation, particularly for managing rare or imperiled taxa. We investigated the patterns of microhabitat and host plant use of the rare frosted elfin butterfly, Callophrys irus, a larval host-plant specialist found in frequently disturbed sand plains, barrens, and sandhill pine-oak forests of the eastern United States. Previous studies have been conducted on populations in the Northeastern and Midwestern US, but the southern part of its range remains unstudied. Our efforts focused on a persistent C. irus colony in northeastern Florida, resulting in a geographically referenced census of larval host-plant Lupinus perennis, along with a multiple year survey of microhabitat features relevant to both C. irus adults and immatures. Results of the larval host-plant census revealed that the highest densities of host plants were located distant to the highest densities of C. irus. Hot-spot analysis confirmed the significance of this pattern, suggesting different habitat requirements for larval host-plant L. perennis and C. irus individuals in order to achieve maximum potential densities. Our survey of C. irus immatures showed a similar pattern of microhabitat affinity that was previously recorded in the Northeast and Midwestern US, including large larval host-plants, low amounts of ground cover vegetation, and the presence of some shade. Unique to our study we found that the presence of other herbivores of L. perennis such as larvae of the crambid moth Uresiphita reversalis had a negative effect on encountering C. irus immatures. Our results suggest that management that aims to conserve these species needs to include habitat factors that favor the overlap of these species and to consider where their densities are the highest.     

Olfactory learning of plant genotypes by a polyphagous insect predator

Olfactory learning may allow insects to forage optimally by more efficiently finding and using favourable food sources. Although olfactory learning has been shown in bees, insect herbivores and parasitoids, there are fewer examples from polyphagous predators. In this study, olfactory learning by a predatory coccinellid beetle is reported for the first time. In laboratory trials, adults of the aphidophagous ladybird Coccinella septempunctata did not prefer the odour of one aphid-infested barley cultivar over another. However, after feeding on aphids for 24 h on a cultivar, they preferred the odour of that particular cultivar. The mechanism appeared to be associative learning rather than sensitisation. Although inexperienced ladybirds preferred the odour of an aphid-infested barley cultivar over uninfested plants of the same cultivar, after feeding experience on a different cultivar this preference disappeared. This may indicate the acquisition and replacement of olfactory templates. The odour blends of the different aphid-infested barley cultivars varied qualitatively and quantitatively, providing a potential basis for olfactory discrimination by the ladybird. The results show that predatory coccinellids can learn to associate the odour of aphid-infested plants with the presence of prey, and that this olfactory learning ability is sensitive enough to discriminate variability between different genotypes of the same plant.     

Geographic and parental influences on diapause by a polyphagous insect herbivore

1 Facultative diapause permits insects to initiate an additional generation when conditions are favourable, or to enter diapause when they are not. Although the principle environmental cues for diapause induction are often temperature and photoperiod, we demonstrated recently that the quality of host plant consumed by the larvae of Choristoneura rosaceana (Harris) (Lepidoptera: Tortricidae) influences the proportion of larvae that enter diapause and therefore voltinism. 2 Previous work has also suggested that non‐Mendelian parental effects influence diapause by C. rosaceana larvae, but the mechanism was not established. Here, we report further evidence for parental effects on diapause and examine whether parental diet influences diapause induction. 3 We collected larvae of C. rosaceana from six sites at three latitudes in the Province of Québec. There was an increase in the proportion of larvae entering diapause with increasing latitude. Rearing larvae under identical conditions on artificial diet for two generations significantly reduced variation in diapause among populations within a given latitude, and supported the existence of parental effects that influence offspring diapause. 4 Experiments with different host plants and high‐ vs. low‐quality artificial diets provided no evidence that the parental effects on offspring diapause were based on the quality of food consumed by parents. Diapause in C. rosaceana appears influenced by a hierarchy of cues, including temperature, photoperiod, current larval diet and parental environment.     

Retrodicting patch use by foraging swans in a heterogeneous environment using a set of functional responses

Effective conservation of important bird areas requires insight in the number of birds an area can support, and how this carrying capacity changes with habitat modifications. When food depletion is the dominant mechanism of competition, it should in principle be possible to calculate the total time foragers can spend per patch from their functional response (intake rate as a function of food density). However, in the field there are likely to be factors modulating the functional response. In this study previously published results of experiments on captive Bewick's swans were used to obtain functional responses of swans digging for tubers of Fennel pondweed on different foraging substrates: sandy and clayey sediment, and in shallow and deep water. In a field study, four 250×250 m sections belonging to different types (sandy–shallow, clayey–shallow, sandy–deep and clayey–deep) were delineated. Here tubers were sampled with sediment corers in three years, both before and after swan exploitation in autumn, and swans were observed and mapped from a hide in two of these years. Giving-up tuber biomass densities varied among sections. Substitution of these giving-up densities in the derived patch-type-specific functional responses yielded the quitting net energy intake rates in the four sections. As expected from the marginal value theorem, the quitting net energy intake rates did not vary among sections. Moreover, the observed foraging pressure (total foraging time per area) per patch type was in quantitative agreement with the integrated functional responses. These results suggest that in spatially heterogeneous environments, patch exploitation by foragers can be predicted from their functional responses after accounting for foraging substrate.     

The use of general foraging kairomones in a generalist parasitoid

Almost no comparative studies are available on the use of general and specific infochemical cues by generalist parasitoids with hosts from different families feeding on host plants also from different families. Based on literature, two hypotheses were developed and tested with host recognition cues used by the larval parasitoid Lariophagus distinguendus . This generalist parasitizes beetle species from different families developing in seeds of plant species from the Poaceae and Fabaceae. The first hypothesis predicts that for initial encounters with host species, natural enemies should innately use general cues, which are common to all hosts and their food plants. The second hypothesis predicts that natural enemies should learn specific cues from host plant and host after experience with a host species. The first hypothesis was partly confirmed. L. distinguendus innately reacted to faecal cues from several host species and chemical analyses of faeces from these hosts revealed the common occurrence of chemicals that are used for host recognition by L. distinguendus . In disagreement with the first hypothesis, parasitoids did not innately respond to cues from plant seeds. Preference experiments on the influence of experience demonstrated an increased host recognition response towards a host after experience with it. In support of the second hypothesis, L. distinguendus females learned specific cues from herbivore-damaged wheat, rice and cowpea seeds and from the faeces of the bean weevil Callosobruchus maculatus .     

Following a foraging fish-finder: diel habitat use of Blainville's beaked whales revealed by echolocation

Simultaneous high resolution sampling of predator behavior and habitat characteristics is often difficult to achieve despite its importance in understanding the foraging decisions and habitat use of predators. Here we tap into the biosonar system of Blainville''s beaked whales, Mesoplodon densirostris, using sound and orientation recording tags to uncover prey-finding cues available to echolocating predators in the deep-sea. Echolocation sounds indicate where whales search and encounter prey, as well as the altitude of whales above the sea-floor and the density of organisms around them, providing a link between foraging activity and the bio-physical environment. Tagged whales (n = 9) hunted exclusively at depth, investing most of their search time either in the lower part of the deep scattering layer (DSL) or near the sea-floor with little diel change. At least 43% (420/974) of recorded prey-capture attempts were performed within the benthic boundary layer despite a wide range of dive depths, and many dives included both meso- and bentho-pelagic foraging. Blainville''s beaked whales only initiate searching when already deep in the descent and encounter prey suitable for capture within 2 min of the start of echolocation, suggesting that these whales are accessing prey in reliable vertical strata. Moreover, these prey resources are sufficiently dense to feed the animals in what is effectively four hours of hunting per day enabling a strategy in which long dives to exploit numerous deep-prey with low nutritional value require protracted recovery periods (average 1.5 h) between dives. This apparent searching efficiency maybe aided by inhabiting steep undersea slopes with access to both the DSL and the sea-floor over small spatial scales. Aggregations of prey in these biotopes are located using biosonar-derived landmarks and represent stable and abundant resources for Blainville''s beaked whales in the otherwise food-limited deep-ocean.