Caterpillars Cooperate to Overcome Plant Glandular Trichome Defenses

One common advantage proposed for group-living in animals is social facilitation of feeding, by which food acquisition by an individual is made easier by feeding neighbors. The present paper provides an explanation of social facilitation of feeding in a gregarious leaf-chewing insect, demonstrating how caterpillars cooperate to overwhelm plant trichome defenses and pierce a hole in the leaf on which they feed collectively. Specifically, it tests the hypotheses that Mechanitis menapis caterpillars feed collectively, that the glandular trichomes of Solanum acerifolium are effective defenses against this specialist herbivore, and that feeding by early-instar M. menapis is socially facilitated in the presence of glandular trichomes. A field survey showed that Mechanitis menapis on trichome–bearing plants feed collectively on the abaxial surface of leaves during the first larval instars. In a lab experiment comparing feeding on control and ethanol-washed leaves, caterpillars on the glandular-trichome-free washed sides of leaves initiated feeding sooner and had higher survival rates, suggesting that glandular trichomes are effective defenses. Behavioral observations showed that feeding is socially facilitated in response to glandular trichomes: caterpillars on the washed sides of leaves were more likely to begin feeding alone and initiated more separate feeding sites, suggesting that caterpillars are less able to initiate feeding independently in the presence of glandular trichomes. These results demonstrate a novel mechanism of cooperation among folivores, showing how they can benefit from grouping to tackle food sources that would be unavailable to isolated individuals. This study thus demonstrates that social facilitation of feeding extends to insect folivores, a hyper-diverse and abundant feeding guild

Plasticity of collective behavior in a nomadic early spring folivore

Collective behavior in the forest tent caterpillar (Malacosoma disstria) meets the thermal constraints of being an early spring folivore, but introduces other constraints in food choice. These are minimized by state-dependent, inter-individual, and ontogenetic variations in responses to social cues. Forest tent caterpillars use pheromone trails and tactile communication among colony members to stay together during foraging. At the group level, these rules lead to cohesive synchronized collective nomadic foraging, in which the colony travels en masse between feeding and resting sites. This paper proposes that synchronized collective locomotion prevents individuals from becoming separated from the colony and hence permits them to reap the advantages of group-living, notably collective basking to increase their body temperature above ambient and collective defense against natural enemies. However, this cohesive behavior also implies conservative foraging, and colonies can become trapped on poor food sources. High fidelity to pheromone trails leads to strong amplification of an initial choice, such that colonies seldom abandon the first food source contacted, even if a better one is nearby. The risk of this trapping is modulated both by consistent inter-individual variations in exploratory behavior and by inner state. Colonies consisting of active-phenotype or protein-deprived individuals that explore more-off trails exhibit greater collective flexibility in foraging. An ontogenetic shift toward more independent movement occurs as caterpillars grow. This leads to colony break-up as the season advances. Selection pressures facing older caterpillars favor solitary living more than in the earlier instars. Caterpillars respond to this predictably changing environment by altering their behavioral rules as they grow

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 organism's 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

Effects of polymorphic melanism and larval diet on life history traits of Malacosoma disstria moths

In this study we investigated the presence and possible genetic basis of polymorphic melanism in the forest tent caterpillar (Malacosoma disstria) moth. Adult moths were classified into pattern-based phenotypes and wing darkness was measured to quantify the degree of melanization. We found that two distinct phenotypes, melanic and simple, are present in these moths. Although the full melanic phenotype is sex-limited to males, it is partially expressed in females. We also provide support for the theory that the melanic allele is autosomal and dominant. The effects of larval diet quality on the survival, development and wing melanization of each phenotype were studied by rearing larvae on the foliage of either a primary or secondary host. Diet quality did not differentially affect the two phenotypes; however, melanic males were found to be smaller than simple males regardless of larval diet. Such inherent developmental differences between the two phenotypes could have important consequences for the frequencies of the two morphs

Larval nutrition affects life history traits in a capital breeding moth

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 vssomatic growth depends on the nutrients available

Group leadership depends on energetic state in a nomadic collective foraging caterpillar

Group living is a common strategy among animals and has arisen independently in over 300 species of Lepidoptera. Yet, activity synchrony between individuals is necessary to derive the benefits that ensue from an aggregated lifestyle. Which individuals decide which activities to perform and when to perform them is, therefore, a fundamental question. In some species of social caterpillars and sawflies, the role of a potential behavioral polyethism between individuals has been suggested, whereby certain individuals are consistently more likely to initiate and lead a foraging event. However, in these cases, evidence in support of division of labor is lacking. This study was undertaken to determine if certain individuals of Malacosoma disstria are more likely to be consistent group leaders or if transient leaders could be predicted by the differences in energetic states between individuals. The results of this study indicate that unfed caterpillars initiate foraging bouts and are more likely to lead locomotion. There was no size or sex-based bias in those individuals that acted as temporary leaders. Consistent behavioral differences between individuals, if they exist, are therefore not necessary to explain task allocation and synchronization during foraging in this species

SERG Final report: Ecosystemic impacts of forest tent caterpillar outbreaks

The forest tent caterpillar (Malacosoma disstria) is a significant defoliator of hardwoods throughout Canada. Historically, infestations usually collapsed after one or two years of defoliation, but longer and more severe outbreaks have been observed in recent years, leading to mortality of both sugar maple and trembling aspen, and making the forest tent caterpillar another pest whose impacts are increasing under a changing climate. This project examines how forest tent caterpillar outbreaks influence soil ecosystems, in both temperate deciduous and mixed boreal forests. We will assess inputs to soil ecosystems associated with forest tent caterpillar outbreaks and determine impacts on soil arthropod communities and tree regeneration. We also examine the different sources of mortality of the forest tent caterpillar colonies during and after the outbreak. It will thus provide empirical data to assess effects of forest tent caterpillar outbreaks on forest ecosystems and successional processes as well as population dynamics throughout the outbreaking cycle. Results suggest that defoliation favours the growth of non-host saplings. They also suggest that sources of mortality change during the different parts of the outbreak. Results will also contribute to the development of novel silvicultural approaches taking into account the effects of forest tent caterpillar outbreaks on forest regeneration and the need to keep process promoting regulation of forest tent caterpillar populations. La livrée des forêts (Malacosoma disstria) est un défoliateur important des forêts feuillues du Canada. Dans le passé, les épidémies s’effondraient généralement après une ou deux années de défoliation sans causer de dommages significatifs à la forêt, mais l’observation récente d’épidémies plus longues et plus sévères, suivies de mortalité des tiges de peuplier faux-tremble et d’érable à sucre, suggèrent que les impacts de la livrée des forêts, comme de plusieurs autres insectes ravageurs, augmentent en raison des changements climatiques. Ce projet examine les effets d’une épidémie de livrée des forêts sur l’écosystème du sol dans deux écosystèmes forestiers: la forêt feuillue et la forêt boréale mixte. Nous examinerons les apports en nutriments au sol associés aux épidémies de livrée et évaluerons les effets sur la communauté d’arthropodes du sol et sur la régénération des arbres. Nous avons aussi examiné les sources de mortalité des colonies de livrée des forêts durant et après l’épidémie. Les résultats fourniront des données empiriques pour évaluer les impacts des épidémies de livrée sur les écosystèmes forestiers et les processus de succession écologiques ainsi que les dynamiques de populations à travers les cycles épidémiques. Les résultats suggèrent que la défoliation peut bénéficier la croissance des jeunes arbres non-hôtes. Ils suggèrent aussi que les sources de mortalité diffèrent lors des différentes parties du cycles épidémiques. Les résultats contribueront aussi au développement d’approches sylvicoles qui prennent en considération le rôle de la livrée dans la régénération des forêts

Spruce budworm feeding and oviposition are stimulated by monoterpenes in white spruce epicuticular waxes

Monoterpenes, source of the distinctive odor of conifers, are generally considered plant defensive compounds. However, they are also known to act as long‐range insect attractants, as they are volatile and permeate forest airspaces. Moreover, they are lipid soluble and can be absorbed into plant epicuticular waxes. We test their role in short‐range host plant choice by both adult females and larvae of a folivorous forest pest (Choristoneura fumiferana). We conducted laboratory assays testing the responses of Eastern spruce budworm to an artificial monoterpene mix (α‐pinene, β‐pinene, limonene, myrcene) and to white spruce (Picea glauca) epicuticular waxes in closed arenas. Ovipositing females preferred filter paper discs treated with P. glauca waxes to controls, and preferred the waxes + monoterpenes treatment to waxes alone. However, females showed no preference between the monoterpene‐treated disc and the control when presented without waxes. Feeding larvae prefered wax discs to control discs. They also consumed discs treated with realistic monoterpene concentrations and wax preferentially over wax‐only discs, but showed no preference between extremely high monoterpene concentrations and wax‐only controls. In an insect‐free assay, P. glauca epicuticular wax decreased monoterpene volatilization. These results suggest that P. glauca waxes and realistic concentrations of monoterpenes are stimulatory to both egg‐laying females and feeding larvae, and that their effects are synergistic

Defensive responses by a social caterpillar are tailored to different predators and change with larval instar and group size

Gregariousness in animals is widely accepted as a behavioral adaptation for protection from predation. However, predation risk and the effectiveness of a prey’s defense can be a function of several other factors, including predator species and prey size or age. The objective of this study was to determine if the gregarious habit of Malacosoma disstria caterpillars is advantageous against invertebrate natural enemies, and whether it is through dilution or cooperative defenses. We also examined the effects of larval growth and group size on the rate and success of attacks. Caterpillars of M. disstria responded with predator-specific behaviors, which led to increased survival. Evasive behaviors were used against stinkbugs, while thrashing by fourth instar caterpillars and holding on to the silk mat by second instar caterpillars was most efficient against spider attacks. Collective head flicking and biting by groups of both second and fourth instar caterpillars were observed when attacked by parasitoids. Increased larval size decreased the average number of attacks by spiders but increased the number of attacks by both stinkbugs and parasitoids. However, increased body size decreased the success rate of attacks by all three natural enemies and increased handling time for both predators. Larger group sizes did not influence the number of attacks from predators but increased the number of attacks and the number of successful attacks from parasitoids. In all cases, individual risk was lower in larger groups. Caterpillars showed collective defenses against parasitoids but not against the walking predators. These results show that caterpillars use different tactics against different natural enemies. Overall, these tactics are both more diverse and more effective in fourth instar than in second instar caterpillars, confirming that growth reduces predation risk. We also show that grouping benefits caterpillars through dilution of risk, and, in the case of parasitoids, through group defenses. The decreased tendency to aggregate in the last larval instar may therefore be linked to decreasing predation risk

Ontogenetic shift from aposematism and gregariousness to crypsis in a Romaleid grasshopper - dataset

Traits of chemically-defended animals can change as an individual grows and matures, and both theoretical and empirical evidence favour a direction of change from crypsis to aposematism. This study examines the suite of traits involved in an unusual opposite shift from aposematism to crypsis in a neotropical toxic-plant-feeding Romaleid grasshopper, Chromacris psittacus (Gerstaecker, 1873). Field surveys, behavioural observations and a rearing experiment compare host plant choice, aggregation, locomotion and thermoregulation between life history stages. Results showed that both nymphs and adults fed exclusively on a narrow range of Solanaceae plants, suggesting that the shift in defensive syndrome is not due to a change in chemical defense. Instead, nymphal aposematism appears linked to aggregation in response to plant-based selection pressures. Slow nymphal development suggests a cost to feeding on toxic plant compounds, and grouping could mitigate this cost. Grouping also increases conspicuousness, and hence can favour warning colourating in chemically-defended insects. The role of diet breadth in aposematism is poorly understood, and these results suggest how constraints imposed by feeding on toxic plants can generate bottom-up selection pressures shaping the adaptive suites of traits of chemically-defended animals