Hierarchical spatial structure of genetically variable nucleopolyhedroviruses infecting cyclic populations of western tent caterpillars

The cyclic population dynamics of western tent caterpillars, Malacosoma californicum pluviale, are associated with epizootics of a nucleopolyhedrovirus, McplNPV. Given the dynamic fluctuations in host abundance and levels of viral infection, host resistance and virus virulence might be expected to change during different phases of the cycle. As a first step in determining if McplNPV virulence and population structure change with host density, we used restriction fragment length polymorphism (RFLP) analysis to examine the genetic diversity of McplNPV infecting western tent caterpillar populations at different spatial scales. Thirteen dominant genetic variants were identified in 39 virus isolates (individual larvae) collected from field populations during one year of low host density, and another distinct variant was discovered among nine additional isolates in two subsequent years of declining host density. The distribution of these genetic variants was not random and indicated that the McplNPV population was structured at several spatial levels. A high proportion of the variation could be explained by family grouping, which suggested that isolates collected within a family were more likely to be the same than isolates compared among populations. Additionally, virus variants from within populations (sites) were more likely to be the same than isolates collected from tent caterpillar populations on different islands. This may indicate that there is limited mixing of virus among tent caterpillar families and populations when host population density is low. Thus there is potential for the virus to become locally adapted to western tent caterpillar populations in different sites. However, no dominant genotype was observed at any site. Whether and how selection acts on the genetically diverse nucleopolyhedrovirus populations as host density changes will be investigated over the next cycle of tent caterpillar populations.     

Adaptation in an insect host–plant pathogen interaction

Selection on parasites to adapt to local host populations may be direct or through other components of the system such as vectors or the food plant on which the parasite is ingested. To test for local adaptation of nucleopolyhedrovirus among island populations of western tent caterpillars, Malacosoma californicum pluviale, we compared virus isolates from three geographically distinct sites with different dominant host plants. Pathogenicity, speed of kill and virus production of each isolate were examined on the three food plants. Virus isolates from the two permanent host populations had the fastest speed of kill on the host plant from which they were isolated. This was not the case for a caterpillar population that goes extinct when populations are regionally low. Virus isolates on some plant species combined rapid speed of kill with high virus yield. Infection of hosts by mixed microparasite populations could facilitate local adaptation in response to differing food plant chemistry.     

The effect of food limitation on immunity factors and disease resistance in the western tent caterpillar

Epizootics of nucleopolyhedrovirus characterize declines of cyclic populations of western tent caterpillars, Malacosoma pluviale californicum. In field populations, infection can be apparently lacking in one generation and high in the next. This may suggest an increase in the susceptibility to infection of larvae at peak density or the triggering of a vertically transmitted virus. Here, we test the hypothesis that reduced food availability, as may occur during population outbreaks of tent caterpillars, influences the immunocompetence of larvae and increases their susceptibility to viral infection. We compared immunity factors, hemolymph phenoloxidase and hemocyte numbers, and the susceptibility to nucleopolyhedroviral infection of fifth instar larvae that were fully or partially fed as fourth instars. To determine if maternal or transgenerational influences occurred, we also determined the susceptibility of the offspring of the treated parents to viral infection. Food limitation significantly reduced larval survival, development rate, larval and pupal mass, moth fecundity and levels of hemolymph phenoloxidase, but not the numbers of hemocytes. Neither the food-reduced larvae nor their offspring were more susceptible to viral infection and were possibly even less susceptible at intermediate viral doses. Food reduction did not activate latent or covert viral infection of larvae as might be expected as a response to stress. We conclude that reducing the food intake of fourth instar larvae to an extent that had measurable and realistic impacts on their life history characteristics was not translated into increased susceptibility to viral infection.     

Population fluctuations of the western tent caterpillar in southwestern British Columbia

Cyclic populations of western tent caterpillars fluctuate with a periodicity of 6–11 years in southwestern British Columbia, Canada. Typically, larval survival is high in early stages of the population increase, begins to decline midway through the increase phase, and is low through several generations of the population decline. Fecundity is generally high in increasing and in peak populations but is also reduced during the population decline. Poor survival and low fecundity for several generations cause the lag in recovery of populations that is necessary for cyclic dynamics. The dynamics of tent caterpillar populations vary among sites, which suggests a metapopulation structure; island populations in the rainshadow of Vancouver Island have more consistent cyclic dynamics than mainland populations in British Columbia. Sudden outbreaks of populations that last a single year suggest that dispersal from source to sink populations may occur late in the phase of population increase. Wellington earlier discussed qualitative variation among tent caterpillar individuals as an aspect of population fluctuations. The variation in caterpillar activity he observed was largely statistically nonsignificant. Recent observations show that the frequency of elongate tents as described by Wellington to characterize active caterpillars varies among populations but does not change in a consistent pattern with population density. The level of infection from nucleopolyhedrovirus (NPV) was high in some populations at peak density but was not associated with all population declines. Sublethal infection can reduce the fecundity of surviving moths, and there is a weak association between viral infection and egg mass size in field populations. The impact of weather in synchronizing or desynchronizing populations is a factor to be investigated further. Received: May 25, 1999 / Accepted: March 28, 2000     

Changes in the fecundity of tent caterpillars: a correlated character of disease resistance or sublethal effect of disease?

Over the fluctuation in population density of tent caterpillars, Malacosoma californicum pluviale and M. disstria, fecundity changes from being high at peak density to low for several years during the decline. During the increase phase, fecundity rapidly returns to moderately high levels with a further increase occurring to-ward the end of the increase phase. Two hypotheses which might explain these shifts are that (1) mortality from viral disease which is common during population declines selects for resistant individuals with low fecundity as an associated characteristic, and (2) sublethal viral disease reduces fecundity of moths during population decline. In this study we observed rapid shifts in the frequencies of large and small egg masses and in the mean fecundity between different phases of the population fluctuation. Viral disease was more common in caterpillars from small egg masses of the forest tent caterpillar. These observations are consistent with the hypothesis that sublethal effects of virus reduce the fecundity of moths during the population decline, but high fecundity is quickly restored when disease is rare during the population increase.     

Spillover of tent caterpillar (Malacosoma americanum) herbivory onto willow bioenergy crops in an agricultural landscape

The circumstances and potential for insects to damage perennial bioenergy crops is not well understood in the United States. In this study, we evaluated the spillover and herbivory of eastern tent caterpillars (Malacosoma americanum) from host trees onto short rotation coppice (SRC) willow bioenergy crops (Salix sp.). Host trees were all in the Rosaceae family and included Prunus americana, Prunus virginiana and Malus sp. Willow showed greater leaf herbivory with increasing proximity to a defoliated host tree, suggesting that tent caterpillars spilled‐over to willow after denuding their host. More tent caterpillar herbivory was associated with greater mortality of willow. This study suggests that landscape context and spatial position of host trees is important to the early establishment of a willow bioenergy crop.     

Large-scale forest fragmentation increases the duration of tent caterpillar outbreak

I examined historical data (1950–1984) on the duration of outbreaks of the forest tent caterpillar (Malacosoma disstria) in northern Ontario, Canada. Outbreak duration was compared to host tree species dominance and forest structure over large areas of boreal forest partially cleared for agriculture. Abundance of the principal host tree species Populus tremuloides had no consistent effect on duration of outbreak within forest districts, and was negatively correlated with duration of outbreaks among the eight forest districts examined. The amount of forest edge per km² was the best, and most consistent, predictor of the duration of tent caterpillar outbreaks both within individual forest districts and among forest districts. Because forest tent caterpillar populations are driven largely by the impact of parasitoids and pathogens, results here suggest that large-scale increase in forest fragmentation affects the interaction between these natural enemies and forest tent caterpillar. Increased clearing and fragmentation of boreal forests, by agriculture and forestry, may be exacerbating outbreaks of this forest defoliator.     

Climate and outbreaks of the forest tent caterpillar

Some have suggested that the periodic outbreaks of the forest tent caterpillar. Malacosoma disstria are triggered by weather the temperature at the time of early larval feeding, and overwintering temperatures To assess the role of these factors, defoliation maps, compiled annually from flight surveys for the province of Ontario. were compared to similarly scaled temperature records An analysis of the year to year variation shows no relationship between the pattern of increases or declines in defoliation and either temperatures during early larval development, or overwintering temperatures Four periods of defoliation by forest tent caterpillars were observed in Ontario over 41 yr. but at individual sites extensive defoliation did not occur for each of the outbreak periods Defoliation was less severe in regions with low overwintering temperatures, but was not related to the average number of degree days m the early spring Outbreaks were most common in areas where deciduous forests were extensive, and the mean overwintering temperatures were above −40°C While these weather variables do not apparently explain the details of population dynamics of forest tent caterpillars, extreme weather conditions might synchronize populations     

Orientation and Dispersal Patterns of the Eastern Tent Caterpillar, <Emphasis Type="Italic">Malacosoma americanum</Emphasis> F. (<Emphasis Type="Italic">Lepidoptera: Lasiocampidae</Emphasis>)

Larvae of the eastern tent caterpillar, Malacosoma americanum, undergo density-dependent dispersal in response to depleted resources. Because these caterpillars have recently been implicated in abortions of pregnant mares (equine Mare Reproductive Loss Syndrome, or MRLS), there is increased interest in managing caterpillar populations, potentially through manipulation of caterpillar dispersal behavior. Consequently, we investigated dispersal patterns of food-deprived eastern tent caterpillars in artificial arenas with respect to distance, direction, and response to visual stimuli. Distance traveled is influenced by time of day, and is strongly correlated with time elapsed. Movement is non-random, and correlates closely with the position of the sun. The pattern is more pronounced with foraging third instars than with penultimate fifth instars. Visual cues appear important in caterpillar orientation, and caterpillars are responsive to vertically oriented, black objects.     

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.     

Life‐history consequences and disease resistance of western tent caterpillars in response to localised,herbivore‐induced changes in alder leaf quality

1. Plants can respond to herbivore damage with phenotypically plastic changes in quality that negatively affect herbivores and prevent subsequent attack – induced defences. 2. The present study tested whether trees respond to herbivory with localised induction, and whether life‐history traits and disease resistance of an insect herbivore are altered on induced branches of the trees. 3. The influences of localised, within‐branch, herbivore‐induced changes in red alder trees (Alnus rubra Bong.) on fitness characteristics of western tent caterpillars (Malacosoma californicum pluviale Dyar) were evaluated. In the field, randomly selected branches of trees were infested with tent caterpillar larvae and the adjacent branches were maintained as non‐infested controls. In the laboratory, larvae were fed leaves from either induced or non‐induced branches through to adult emergence. A second cohort of larvae was challenged with a viral pathogen to compare their disease susceptibility on induced versus non‐induced foliage. 4. Herbivore‐induced, localised responses of damaged branches reduced leaf quality for growth and the fecundity of female western tent caterpillars, but not that of males. Larvae fed induced leaves had a higher survival overall and a reduced mortality due to unidentified non‐viral pathogens than did their counterparts on non‐induced leaves. However, there was no influence of leaf quality on baculovirus‐induced mortality. 5. These findings suggest that localised induced changes in leaf quality could potentially influence populations of tent caterpillars in contradictory ways by reducing their growth rate and fecundity to a modest degree, while improving their survival and resistance to unidentified non‐viral pathogens to a larger extent.     

The dynamics of forest tent caterpillar outbreaks across east‐central Canada

An analysis of forest tent caterpillar Malacosoma disstria defoliation records from Ontario and Quebec over the period 1938–2002 indicates that outbreaks recur periodically and somewhat synchronously among regions of the two provinces. Cluster analysis revealed that the most strongly periodic, large‐scale, synchronized fluctuations occurred within three regions: northwestern Ontario, eastern Ontario/western Quebec and southeastern Quebec. Defoliation in the vast surrounding hinterlands tended to be infrequent and sporadic, loosely tracking defoliation in the core outbreak regions. One small cluster in northeastern Ontario stood out as anomalous, as a result of an increasing trend in the duration of periodic defoliation episodes, marked by an unprecedented double‐wave of defoliation that persisted from 1992 to 1999. This is the precise area where, in the early 2000s, trembling aspen Populus tremuloides stems were mapped as being in a state of decline of unprecedented severity and extent. Our results suggest forest tent caterpillar has the potential to cause significant impacts on forest health and, hence, carbon budgets in east‐central Canada and that the forest tent caterpillar deserves more attention as a model system of forest insect disturbance ecology.     

Social Cues and Following Behavior in the Forest Tent Caterpillar

Colonies of the social caterpillar Malacosoma disstria Hubner (Lepidoptera: Lasiocampidae) travel in groups following silk trails marked with pher-omone. This study examined first, the cues involved in following behavior and second, the responses to these cues at different larval stadia. Both second and fourth instar larvae discriminated between fresh and older trails, and travelled faster in the presence of trails. In addition to trail following, young caterpillars exhibited leader following, which might be particularly important in exploring unmarked territory. Indeed, second instar caterpillars were more likely to travel together when trails were absent. Fourth instar larvae exhibited greater independent locomotion in the absence of trails than did younger larvae. These findings help explain patterns of social behavior observed in forest tent caterpillar colonies in the field.     

Social predation by ants as a mortality source for an arboreal gregarious forest pest

Biocontrol of caterpillars by ants is highly variable, and we investigate how the strength of the trophic relationship between ants and an important outbreaking forest pest depends on phenological synchrony and on social foraging. We test the hypothesis that early spring foraging by ants, coupled with eusocial recruitment behavior, could undermine the caterpillar's strategies to achieve either enemy-free space or predator satiation.We use a series of field surveys and experiments in trembling aspen stands (Populus tremuloides) in the boreal forest of eastern Canada to assess the role of ants in early-instar mortality of the outbreaking, gregarious forest tent caterpillar (Malacosoma disstria). We also investigate individual-level mechanisms related to phenology and social behavior that underlie the effectiveness of ants as biocontrol on caterpillars. Our results show that ants climb trees early in the spring and harvest young forest tent caterpillars, suggesting that early phenology does not provide an entirely enemy-free space for caterpillars. Our findings further show that recruitment-based social foraging enables ants to deplete groups of gregarious prey, suggesting that these eusocial insects are particularly effective at generating predation pressure on gregarious herbivores since they do not satiate easily. Finally, a manipulative predator exclusion experiment confirms that ant predation is a significant mortality source for early-instar forest tent caterpillars. Taken together, these results suggest that phenology and sociality could modulate the role of ants as effective caterpillar predators and thus showcase the importance of considering natural history and behavioral traits when studying trophic interactions and their role in population dynamics.     

Effects of variable phytochemistry and budbreak phenology on defoliation of aspen during a forest tent caterpillar outbreak

1 The present study assessed the relationship between clonally variable rates of defoliation in trembling aspen (Populus tremuloides Michx.) and two potential resistance traits: defensive chemistry and leaf phenology. 2 In 2001, coincident with a major outbreak of the forest tent caterpillar (Malacosoma disstria Hubner) in the northcentral U.S.A., we monitored defoliation rates, phytochemical composition, and foliar development in 30 clones of trembling aspen. Leaf chemistry was also assessed in re‐flushed leaves and 2 years post‐outbreak. 3 Early in the season, differences in defoliation among clones were substantial but, by mid‐June, all clones were completely defoliated. Leaf nitrogen, condensed tannins, and phenolic glycosides varied among clones but did not relate to defoliation levels. Budbreak phenology differed by 3 weeks among clones and clones that broke bud early or late relative to forest tent caterpillar eclosion experienced reduced rates of defoliation. 4 Defoliation led to increased tannins and slight decreases in phenolic glycoside concentrations in damaged leaf remnants, but to moderately decreased tannins and a six‐fold increase in phenolic glycosides in reflushed leaves. This shift in chemical composition may significantly affect late season herbivores. 5 These results suggest that aspen chemical resistance mechanisms are ineffective during intense episodic eruptions of outbreak folivores such as the forest tent caterpillar. Variable budbreak phenology may lead to differential susceptibility during less intense outbreak years and, at peak forest tent caterpillar population densities, mechanisms affording tolerance are probably more important than chemical defences.     

The Spread of Infection by the Microsporidan,Nosema disstriae,in Insect Cell Lines1

Nosema disstriae, a parasite of the forest tent caterpillar, Malacosoma disstria, was cultured with cell lines UMN-MDH-1 (Malacosoma disstria), IPLB-1075 (Heliothis zea), and BTC-32 (Triatoma infestans). Infected cultured cells were used to infect the healthy cell lines. Electron micrographs of thin sections of 6-day-old cultures revealed infected cells that exocytosed vesicles containing vegetative and immature sporulating forms of the parasite. Some of these forms were believed to be responsible for intercellular transmission of the parasite. The spread of infection was augmented by culturing the cells at high densities; if the density was too low, there was little or no cross infection. Cross infection was inhibited, but not blocked completely, by high osmolality of the culture medium. The yield of spores from a confluent cell monolayer at the end of growth was generally 1–4 × 10⁷ per ml of culture medium.     

Foliar quality influences tree-herbivore-parasitoid interactions: effects of elevated CO<Subscript>2</Subscript>, O<Subscript>3</Subscript>, and plant genotype

This study examined the effects of carbon dioxide (CO₂)-, ozone (O₃)-, and genotype-mediated changes in quaking aspen (Populus tremuloides) chemistry on performance of the forest tent caterpillar (Malacosoma disstria) and its dipteran parasitoid (Compsilura concinnata) at the Aspen Free-Air CO₂ Enrichment (FACE) site. Parasitized and non-parasitized forest tent caterpillars were reared on two aspen genotypes under elevated levels of CO₂ and O₃, alone and in combination. Foliage was collected for determination of the chemical composition of leaves fed upon by forest tent caterpillars during the period of endoparasitoid larval development. Elevated CO₂ decreased nitrogen levels but had no effect on concentrations of carbon-based compounds. In contrast, elevated O₃ decreased nitrogen and phenolic glycoside levels, but increased concentrations of starch and condensed tannins. Foliar chemistry also differed between aspen genotypes. CO₂, O₃, genotype, and their interactions altered forest tent caterpillar performance, and differentially so between sexes. In general, enriched CO₂ had little effect on forest tent caterpillar performance under ambient O₃, but reduced performance (for insects on one aspen genotype) under elevated O₃. Conversely, elevated O₃ improved forest tent caterpillar performance under ambient, but not elevated, CO₂. Parasitoid larval survivorship decreased under elevated O₃, depending upon levels of CO₂ and aspen genotype. Additionally, larval performance and masses of mature female parasitoids differed between aspen genotypes. These results suggest that host-parasitoid interactions in forest systems may be altered by atmospheric conditions anticipated for the future, and that the degree of change may be influenced by plant genotype.     

Nuclear polyhedrosis virus as a biological control agent for Malacosoma americanum (Lepidoptera: Lasiocampidae)

In addition to damaging trees, the eastern tent caterpillar is implicated in early fetal loss and late‐term abortion in horses. In a field study, we evaluated the potential biological control of the caterpillar using eastern tent caterpillar nuclear polyhedrosis virus (ETNPV), a naturally occurring virus that is nearly species‐specific. Egg masses were hatched and second instar larvae were fed virus‐inoculated foliage to propagate the virus in vivo. Then, a viral pesticide was formulated at concentrations of 10⁴, 10⁶ and 10⁸ polyhedral inclusion bodies per ml. The pesticide was applied to foliage on which second, third and fourth instar caterpillars were feeding. When the majority of surviving larvae reached the sixth instar, colonies were collected and the surviving caterpillars counted. Mean numbers of surviving caterpillars per treatment were compared via 95% bootstrap confidence intervals. The data indicate second instar caterpillars were highly susceptible to the virus, but only at the highest concentration tested. Third instar caterpillars were also somewhat susceptible to high virus concentrations, while fourth instar caterpillars were fairly resistant. Our data provide the strongest evidence to date that ETNPV can be propagated, harvested and refined for formulation as a biological control agent for eastern tent caterpillar. Its use on this insect may be merited in circumstances where landowners and managers need to protect trees and horses.     

Temperature and population density: interactional effects of environmental factors on phenotypic plasticity,immune defenses,and disease resistance in an insect pest

Temperature and crowding are key environmental factors mediating the transmission and epizooty of infectious disease in ectotherm animals. The host physiology may be altered in a temperature‐dependent manner and thus affects the pathogen development and course of diseases within an individual and host population, or the transmission rates (or infectivity) of pathogens shift linearly with the host population density. To our understanding, the knowledge of interactive and synergistic effects of temperature and population density on the host–pathogen system is limited. Here, we tested the interactional effects of these environmental factors on phenotypic plasticity, immune defenses, and disease resistance in the velvetbean caterpillar Anticarsia gemmatalis. Upon egg hatching, caterpillars were reared in thermostat‐controlled chambers in a 2 × 4 factorial design: density (1 or 8 caterpillars/pot) and temperature (20, 24, 28, or 32°C). Of the immune defenses assessed, encapsulation response was directly affected by none of the environmental factors; capsule melanization increased with temperature in both lone‐ and group‐reared caterpillars, although the lone‐reared ones presented the most evident response, and hemocyte numbers decreased with temperature regardless of the population density. Temperature, but not population density, affected considerably the time from inoculation to death of velvetbean caterpillar. Thus, velvetbean caterpillars succumbed to Anticarsia gemmatalis multiple nucleopolyhedrovirus (AgMNPV) more quickly at higher temperatures than at lower temperatures. As hypothesized, temperature likely affected caterpillars' movement rates, and thus the contact between conspecifics, which in turn affected the phenotypic expression of group‐reared caterpillars. Our results suggest that environmental factors, mainly temperature, strongly affect both the course of disease in velvetbean caterpillar population and its defenses against pathogens. As a soybean pest, velvetbean caterpillar may increase its damage on soybean fields under a scenario of global warming as caterpillars may reach the developmental resistance faster, and thus decrease their susceptibility to biological control by AgMNPV.     

Macrogeographic clines in fecundity, reproductive allocation, and offspring size of the forest tent caterpillar Malacosoma disstria

1. The fecundity of the forest tent caterpillar varies considerably across its geographic range. Field data indicate that populations in the southern United States (Gulf States) produce nearly twice as many eggs as females from Canada or the Lake States, with little or no difference in the size of adult females. 2. In controlled rearing experiments, female forest tent caterpillar from the southern United States (Louisiana) had much larger clutch sizes than same sized females from northern populations in Michigan or Manitoba, Canada. Increased fecundity in Louisiana females was achieved through a significant reduction in egg size and a concomitant increase in the allocation of resources to egg production. 3. Comparison of 10 forest tent caterpillar populations spanning a 27° latitudinal gradient, validated the results of detailed comparisons among the three populations above by confirming the strong negative correlation between latitude and clutch size. 4. Neonate forest tent caterpillars from Manitoba were significantly larger than larvae from either Michigan or Louisiana. Michigan larvae were intermediate in size. It is postulated that large neonates are advantageous in thermally limiting environments. More than three times as many degree‐days are available to Louisiana neonates during the first 2 weeks after hatching. A consistently favourable climate during the vulnerable post‐hatching period may have allowed the evolution of larger clutches at the expense of neonate size in southern populations.