Emma Despland

From Disorder to Order in Marching Locusts

Recent models from theoretical physics have predicted that mass-migrating animal groups may share group-level properties, irrespective of the type of animals in the group. One key prediction is that as the density of animals in the group increases, a rapid transition occurs from disordered movement of individuals within the group to highly aligned collective motion. Understanding such a transition is crucial to the control of mobile swarming insect pests such as the desert locust. We confirmed the prediction of a rapid transition from disordered to ordered movement and identified a critical density for the onset of coordinated marching in locust nymphs. We also demonstrated a dynamic instability in motion at densities typical of locusts in the field, in which groups can switch direction without external perturbation, potentially facilitating the rapid transfer of directional information.

Gregarious behavior in desert locusts is evoked by touching their back legs

Desert locusts in the solitarious phase were repeatedly touched on various body regions to identify the site of mechanosensory input that elicits the transition to gregarious phase behavior. The phase state of individual insects was measured after a 4-h period of localized mechanical stimulation, by using a behavioral assay based on multiple logistic regression analysis. A significant switch from solitarious to gregarious behavior occurred when the outer face of a hind femur had been stimulated, but mechanical stimulation of 10 other body regions did not result in significant behavioral change. We conclude that a primary cause of the switch in behavior that seeds the formation of locust swarms is individuals regularly touching others on the hind legs within populations that have become concentrated by the environment.

Mechanosensory-induced behavioural gregarization in the desert locust Schistocerca gregaria

SUMMARY Desert locusts show an extreme form of phenotypic plasticity, changing between a cryptic solitarious phase and a swarming gregarious phase that differ in many aspects of behaviour, physiology and appearance. Solitarious locusts show rapid behavioural phase change in response to tactile stimulation directed to the hind femora. Repeatedly touching as little as one quarter of the anterior (outer) surface area of a hind femur produced full behavioural gregarization within 4 h. Solitarious locusts have approximately 30% more mechanosensory trichoid sensilla on the hind femora than do gregarious locusts but have similar or fewer numbers of sensilla elsewhere on the legs. Tactile stimulation of a hind femur in solitarious locusts that had been restrained so that they could not move their legs failed to induce any behavioural gregarization. Patterned electrical stimulation of metathoracic nerve 5, which innervates the hind leg, however, produced full gregarization in restrained locusts. Our data show for the first time that the gregarizing signal combines both exteroceptive and proprioceptive components, which travel in both nerves 5B1 and 5B2, and provides us with a powerful experimental method with which to elicit and study neuronal plasticity in this system. Acetic acid odour, a strong chemosensory stimulus that activates the same local processing pathways as exteroceptive stimuli, failed to elicit behavioural gregarization, suggesting an early segregation in the central nervous system of the mechanosensory signals that leads to gregarization.

CLIMATE INFLUENCES ON GROWTH AND REPRODUCTION OF PINUS BANKSIANA (PINACEAE) AT THE LIMIT OF THE SPECIES DISTRIBUTION IN EASTERN NORTH AMERICA

The presence of conflicts in the allocation of resources among the different functions of an organism is a fundamental postulate of modern ecology. It is assumed that reproduction occurs at a cost because it monopolizes resources that could be used for other functions (e.g., growth). These conflicts may be particularly evident under stressful conditions, such as under low water or nutrient availability, or under severe climatic conditions. There we may expect to find strong negative relationships between an organisms growth and reproduction. We studied a population of Pinus banksiana (Pinaceae) at the northern limit of the species distribution, in subarctic Québec (Canada) where Pinus banksiana occupies nutrient-poor, sandy terraces along the Great Whale river. Serotinous cones of Pinus banksiana produced between 1969 and 1992 were sampled to estimate interannual variations in several variables representing reproduction, and to relate these to climate and tree growth. Climate appears to influence each developmental stage involved in the production of viable seeds, from the time of cone initiation to that of seed maturation. In general, reproductive variables are positively related to high temperatures during the three growing seasons required for seed production; growth is also positively correlated to summer temperatures. Consequently, investment in maturing seeds is positively associated with growth. Thus, both reproduction and growth covary with climate: during relatively warm and long growing seasons, resource allocation to both functions increases. Under these conditions, no trade-off is apparent.

Food choices of solitarious and gregarious locusts reflect cryptic and aposematic antipredator strategies

Desert locusts, Schistocerca gregaria, switch between the cryptic solitarious phase and the swarming aposematic gregarious phase with increased population density. We tested whether solitarious- and gregarious-phase locusts respond differently to hyoscyamine, a plant alkaloid that protects against predators. Solitarious-phase locusts were deterred by the taste of this compound and discriminated against it in long-term choice tests. Gregarious-phase locusts readily accepted the alkaloid and fed equally from a choice of foods that did or did not contain hyoscyamine. Solitarious insects that had begun the transition to the gregarious phase (i.e. that had been crowded) accepted and even seemed to prefer food containing the alkaloid. We did not detect any physiological costs associated with consuming hyoscyamine. Solitarious-phase locusts avoid predator detection through crypsis and would not benefit greatly from consuming toxic plants. Gregarious-phase locusts follow a foraging strategy found in other aposematic grasshoppers: they switch frequently between food plants with little regard to allelochemical content, and could acquire antipredator defence by feeding on a variety of toxic plants. Solitarious locusts in transition to the gregarious phase might benefit more from chemical defence than isolated individuals because predator avoidance learning is enhanced when distasteful prey are aggregated. Phase differences in locust feeding behaviour form part of integrated cryptic and aposematic antipredator strategies that also include differences in coloration and aggregation.

Effects of synchronization with host plant phenology occur early in the larval development of a spring folivore

Early spring feeding Lepidoptera depend on synchronization of larval emergence with host plant phenology for optimal growth and development. Physical and chemical characteristics of foliage change over the course of the growing season, and a delay in larval emergence therefore results in larvae foraging on lower quality food. We examine the effect of synchronization of larval emergence with leaf phenology on the entire larval stage of the forest tent caterpillar, Malaco- soma disstria Hubner, 1820 (Lepidoptera: Lasiocampidae). Caterpillars were reared from egg hatch to pupation on trem- bling aspen, Populus tremuloides Michx; 10 days separated egg hatch in the early and late treatments. Late-hatching caterpillars experienced reduced growth in the early instars, but growth in the later instars did not differ between treat- ments. Reduced growth early in development resulted in both prolongation of the larval stage through the occurrence of ad- ditional instars, and lower pupal mass. Aspen foliage quality changes rapidly during leaf expansion, and the late-hatching caterpillars likely missed the narrow window of opportunity for young larvae to feed on high-quality developing foli-

Small-scale vegetation patterns in the parental environment influence the phase state of hatchlings of the desert locust

Desert locusts (Schistocerca gregaria Forskål (Orthoptera: Acrididae)) change phase in response to population density. Solitarious insects avoid one another; when crowded, they shift to the gregarious phase and aggregate. Laboratory experiments and individual‐based modelling have shown that small‐scale resource distribution can affect locust phase state via an influence on crowding. Laboratory work has also shown that parental phase state is transmitted to offspring via maternal inheritance. These effects had not been investigated in the field previously. We maintained small populations of adult desert locusts in semi‐field enclosures with different distribution patterns of a single plant species (Hyoscyamus muticus L. (Solanaceae)). The offspring of locusts exposed to more clumped patterns of vegetation exhibited more gregarious behaviour when tested in a behavioural phase assay than did progeny from parents left in enclosures with more scattered vegetation. These effects on nymphal behaviour appeared to be mediated by influences of resource distribution on adult phase state. Phase state in small semi‐field populations was influenced by small‐scale vegetation distribution. Phase differences engendered by environmental structure were maintained in time and transmitted to progeny.

How well do specialist feeders regulate nutrient intake? Evidence from a gregarious tree-feeding caterpillar

SUMMARY Nutritional regulation is a powerful mechanism used by generalist feeders to obtain the balance of nutrients they require from nutritionally diverse, perhaps unbalanced, foods. We examined nutritional regulation in a species with a narrow individual diet breadth: the forest tent caterpillar, Malacosoma disstria. Fourth instar caterpillars were provided with artificial foods consisting of different ratios of protein to digestible carbohydrate in no-choice, choice and compensatory feeding experiments. In the no-choice test, caterpillars were confined to a single food source of varying protein/carbohydrate ratio for the duration of the fourth larval stadium. Caterpillars performed best on equal-ratio and slightly protein-biased diets. Significant reductions in performance were only observed on extremely protein- or carbohydrate-biased diets. Daily consumption of the three acceptable intermediate diets was consistent with volumetric regulation, but the timing of the moult to the next instar appeared linked instead to protein intake. In the choice test, caterpillars were provided with two complementary foods, one biased toward protein and the other toward carbohydrate, for the duration of the stadium. The caterpillars fed randomly from the two food sources presented to them, except for the extremely protein-biased diet (P:C ratio of 35:7), which they avoided. The compensatory feeding experiment tested whether forest tent caterpillars deprived of either protein or digestible carbohydrate would select a food containing the deficient nutrient. Insects were conditioned on either protein-only, carbohydrate-only, protein-and-carbohydrate or no-nutrient foods, then offered a choice between protein-only and carbohydrate-only foods. Unlike previously studied generalist feeders, our caterpillars did not compensate for protein deficiency and showed only very weak evidence of compensation for carbohydrate deficiency. Forest tent caterpillars are colonial trail-laying forest folivores that are generally confined to a single host plant and hence do not experience much diversity in food nutrient ratios. We show that forest tent caterpillars do not independently regulate protein and carbohydrate intake. These findings are consistent with predictions that nutritional regulation abilities should be less important in animals with narrower diet breadths.

Pros and cons of group living in the forest tent caterpillar : separating the roles of silk and of grouping

Group living can incur both benefits and costs, mediated by different mechanisms. In many gregarious caterpillars, collective use of a network of silk trails is thought to improve foraging. Grouping, i.e., close contact with conspecifics, has been postulated to have both positive (thermoregulation and predator defense) and negative (competition and pathogen transmission) effects. The present experiment distinguishes between silk produced by group members and grouping per se in their effects on growth and development of both early and late larval stadia of the forest tent caterpillar [Malacosoma disstria Hübner (Lepidoptera: Lasiocampidae)] in a laboratory context. For both developmental stadia tested, pre‐established silk trails decreased latency to food finding and hence increased food consumption and growth rate. For younger larvae, pre‐established silk also decreased investment in silk production. Grouping young caterpillars accelerated development at the expense of growth, possibly as a mechanism to avoid intraspecific competition in later larval stadia. In older caterpillars, grouping decreased meal duration, suggesting that competition can indeed occur towards the end of larval development, even in the presence of surplus food. This led to a decrease in growth without any effect on instar duration. The benefits of exogenous silk thus decreased during larval development, whereas the costs associated with crowding increased. Ontogenetic shifts in grouping are common in many taxa: the present study is among the first to provide empirical evidence for an adaptive explanation of observed ontogenetic changes in aggregative behavior.

Larval nutrition affects life history traits in a capital breeding moth.

SUMMARY Fitness depends not only on resource uptake but also on the allocation of these resources to various life history functions. This study explores the life-history consequences of larval diet in terms not only of larval performance but also of adult body composition and reproductive traits in the forest tent caterpillar (Malacosoma disstria Hübner). Caterpillars were reared on their preferred tree host, trembling aspen (Populus tremuloides), or on one of three artificial foods: high protein:low carbohydrate, equal protein-to-carbohydrate ratio or low protein:high carbohydrate. Survivorship, larval development rate and adult body size were lowest on the carbohydrate-biased diet and similar on the protein-biased and equal-ratio diets. Fecundity increased with body size but did not otherwise differ between diets. Moths reared on the carbohydrate-biased diet allocated a lower proportion of their mass to the ovaries and more to somatic growth whereas those on equal-ratio and protein-biased diets allocated more to reproductive tissue and less to somatic tissue. These differences in allocation to reproduction arose from differences in the size of eggs, an index of offspring quality. No differences were found in lipid and protein content of female ovaries, accessory glands or somatic tissue, or of the whole body of male moths. The findings show that physiological processes regulate the composition of the different components of the adult body. Diet effects occur as differences in overall body size and in relative allocation to these components. Although lepidopterans can, to a large extent, compensate post-ingestively for nutritionally deficient diets, investment in reproduction vs somatic growth depends on the nutrients available.