Periodical cicadas disrupt trophic dynamics through community-level shifts in avian foraging.

Once every 13 or 17 years within eastern North American deciduous forests, billions of periodical cicadas concurrently emerge from the soil and briefly satiate a diverse array of naive consumers, offering a rare opportunity to assess the cascading impacts of an ecosystem-wide resource pulse on a complex food web. We quantified the effects of the 2021 Brood X emergence and report that more than 80 bird species opportunistically switched their foraging to include cicadas, releasing herbivorous insects from predation and essentially doubling both caterpillar densities and accumulated herbivory levels on host oak trees. These short-lived but massive emergence events help us to understand how resource pulses can rewire interaction webs and disrupt energy flows in ecosystems, with potentially long-lasting effects.

Host Plant and Thermal Stress Induce Supernumerary Instars in Caterpillars.

Environmental stressors may induce variation in the number of larval instars of holometabolous insects. Host plant quality and ambient temperature can both induce this life history shift in the silver-spotted skipper, Epargyreus clarus (Cramer 1775) (Lepidoptera: Hesperiidae). To better understand this phenomenon, we raised larvae on high-quality (kudzu) or low-quality (wisteria) host plants in growth chambers under three temperature regimes (20, 26, and 32°C) that were either constant or diurnally fluctuating (T ± 5°C), and recorded survival and incidence of supernumerary instars. Larvae feeding on the low-quality host and/or experiencing thermal stress were more likely to show supernumerary development (SD). A subset of treatments yielded a mix of SD and TD (typical development) individuals, allowing for comparisons between phenotypes. Under the most stressful treatment (20 ± 5°C, wisteria), development time was 9 days longer in SD than in TD individuals; by contrast, at typical summer temperatures (26 ± 5°C), also on wisteria, total development time did not differ between these two phenotypes. Head capsules of both second and third instars were smaller in SD individuals. A retrospective logistic regression analysis indicated that third-instar head capsule size could be used to predict expression of the SD phenotype. By the ultimate instar, however, there were no detectable differences in head capsule size, and SD and TD individuals did not differ in pupal mass, strongly suggesting that the SD phenotype functions as a compensatory mechanism allowing E. clarus larvae to achieve the same size at metamorphosis (a strong fitness correlate) as TD larvae.

Latitudinal variation in responses of a forest herbivore and its egg parasitoids to experimental warming.

Disrupted biotic interactions are a predicted consequence of anthropogenic climate change when interactants differ in the magnitude or direction of phenological responses. Here, we examined the responses to artificial warming of northern, southern and central populations of the eastern tent caterpillar and its hymenopteran egg parasitoids. We subjected egg masses from each region to the typical conditions they experience in their source locality or to a warmer temperature regime, to quantify the effects of simulated warming on their relative phenology, survival and neonate starvation endurance. In addition, we characterized spring heat accumulation and cloud cover at each collection site using 30 years of hourly weather station data. As predicted, degree-day accumulation rates decreased with latitude; however, the mid-latitude site experienced what we predict to be the harshest spring conditions for tent caterpillars: slow heat accumulation combined with thick cloud cover. Remarkably, caterpillars from this site exhibited the largest phenological plasticity, hatching a month earlier under warmer than under typical conditions and doubling caterpillar survival. Survival of caterpillars from all regions was enhanced at warmer temperatures, whereas parasitoid survival was unaffected. The starvation endurance of hatchlings increased under warmer conditions in the central and southern populations only. We show that phenological responses to warming differed between hosts and parasitoids, resulting in a 5-day reduction in the relative phenology of wasps and caterpillars in the northern population. Our findings caution that responses to global warming are likely to be population or region specific and cannot be readily generalized, particularly for wide-ranging organisms.

Warming affects hatching time and early season survival of eastern tent caterpillars.

Climate change is disrupting species interactions by altering the timing of phenological events such as budburst for plants and hatching for insects. We combined field observations with laboratory manipulations to investigate the consequences of climate warming on the phenology and performance of the eastern tent caterpillar (Malacosoma americanum). We evaluated the effects of warmer winter and spring regimes on caterpillar hatching patterns and starvation endurance, traits likely to be under selection in populations experiencing phenological asynchrony, using individuals from two different populations (Washington, DC, and Roswell, GA). We also quantified the proximate and extended fitness effects of early food deprivation and recorded spring phenology of local caterpillars and their host plants. In addition, we conducted laboratory assays to determine if caterpillars are using plant chemical cues to fine-tune their hatching times. Warmer winter temperatures induced earlier hatching and caterpillars from GA survived starvation for periods that were 30% longer than caterpillars from DC. Warmer spring regimes reduced the starvation endurance of caterpillars overwintering in the wild but not in the laboratory. Early starvation dramatically reduced hatchling survival; however, surviving caterpillars did not show detrimental effects on pupal mass or development time. In the field, hatching preceded budburst in both 2013 and 2014 and the period of optimal foliage quality was 2 weeks shorter in 2013. Hatching time was unaffected by exposure to plant volatiles. Overall, we found that warmer temperatures can trigger late-season asynchrony by accelerating plant phenology and caterpillars from different populations exhibit differential abilities to cope with environmental unreliability.

Enemy-free space for parasitoids.

Natural enemies often cause significant levels of mortality for their prey and thus can be important agents of natural selection. It follows, then, that selection should favor traits that enable organisms to escape from their natural enemies into "enemy-free space" (EFS). Natural selection for EFS was originally proposed as a general force in structuring ecological communities, but more recently has become conceptually narrow and is typically only invoked when studying the evolutionary ecology of host plant use by specialized insect herbivores. By confining the application of EFS to specialist herbivores, its potential value to community and evolutionary ecology has been marginalized. As a first step toward exploring the potential explanatory power of EFS in structuring ecological niches of higher trophic-level organisms, we consider host use by parasitoids. Here, we present three distinct mechanisms from our studies of caterpillar host-parasitoid interactions suggesting that parasitoids may be under selection to exploit traits of their hosts and the plants on which those hosts feed to garner EFS for their developing offspring. The neglect of EFS as a top-down selective force on host use by parasitoids may be a serious limitation to basic and applied ecology, given the great diversity of parasitoids and their significance in controlling herbivore populations in both natural and managed ecosystems. Parasitoids and other mesopredators represent excellent candidates for further developments of EFS theory and testing of its broader importance.

Intraplant movement of generalist slug caterpillars (Limacodidae: Lepidoptera): effects of host plant and light environment.

Insect herbivores frequently move about on their host plants to obtain food, avoid enemies and competitors, and cope with changing environmental conditions. Although numerous plant traits influence the movement of specialist herbivores, few studies have examined movement responses of generalist herbivores to the variable ecological conditions associated with feeding and living on an array of host plants. We tested whether the movement patterns of two generalist caterpillars (Euclea delphinii Boisduval and Acharia stimulea Clemens, Limacodidae) differed on six different host tree species over 10 d. Because these tree species vary in the range of light environments in which they commonly grow, we also compared the movement responses of E. delphinii caterpillars to two contrasting light environments, sun and shade. For both caterpillar species, multiple measures of movement varied significantly among host tree species. In early censuses, movement rates and distances were highest on red oak and black cherry and lowest on white oak. Site fidelity was greatest on white oak and lowest on black cherry. Movement of both caterpillar species varied inversely with mean predator density on five of the six host trees. Other ecological predictors (e.g., leaf size and the density of other herbivores) were unrelated to movement. Light environment altered behavior such that caterpillars in the shade moved and fed more often, and moved greater distances, than caterpillars in the sun. Although the mechanism(s) promoting or inhibiting movement under these different conditions requires further study, the consequences of increased movement for caterpillar development and mortality from natural enemies are discussed.

Facilitative effects of group feeding on performance of the saddleback caterpillar (Lepidoptera: Limacodidae).

Gregarious feeding by insect herbivores is a widely observed, yet poorly understood, behavioral adaptation. Previous research has tested the importance of group feeding for predator deterrence, noting the ubiquity of aposematism among group-feeding insects, but few studies have examined the role of feeding facilitation for aggregates of insect herbivores. We tested the hypothesis that group feeding has facilitative effects on performance of the saddleback caterpillar, Acharia stimulea Clemens, a generalist herbivore of deciduous trees. In an understory forest setting, we reared caterpillars alone or in groups on two different host plants, white oak (Quercus alba L.) and American beech (Fagus grandifolia Ehrlich), and recorded multiple measures of insect performance during regular field censuses. As predicted, A. stimulea caterpillars feeding in groups on white oak had increased relative growth rates compared with caterpillars feeding alone, and the magnitude of this facilitative effect varied among censuses, conferring benefits both early and late in development. By contrast, no facilitative effects of group feeding were detected on beech, suggesting that the benefits of facilitative feeding may be host specific. On both hosts, caterpillar development time was slightly faster for group-feeding cohorts compared with their solitary counterparts. Because early instar caterpillars are particularly vulnerable to predation and parasitism, even modest increases in growth rates and reductions in development time may decrease exposure time to enemies during these vulnerable stages. On both hosts, group feeding also reduced the trade-off between individual development time and cocoon mass, suggesting that feeding efficiency is improved in group feeders relative to solitary caterpillars.

Direct and indirect effects of light environment generate ecological trade-offs in herbivore performance and parasitism.

A variety of ecological factors influence host use by parasitoids, including both abiotic and biotic factors. Light environment is one important abiotic parameter that differs among habitats and influences a suite of plant nutritional and resistance traits that in turn affect herbivore performance. However, the extent to which these bottom-up effects "cascade up" to affect higher trophic levels and the relative importance of direct and indirect effects of sunlight on tritrophic interactions are unclear. The objective of this study was to test how light environment (light gap vs. shaded forest understory) and leaf type (sun vs. shade leaves) affect the performance and incidence of parasitism of two species of moth larvae, Euclea delphinii and Acharia stimulea (Limacodidae). We manipulated the leaf phenotype of potted white oak saplings by growing them in either full sun or full shade throughout leaf expansion to produce sun and shade leaves, respectively. These saplings were then placed in light gap and adjacent shaded understory habitats in the forest in a full-factorial design, and stocked with sentinel larvae that were exposed to parasitism ("exposed" experiments). We reared additional larvae in sleeve cages (protected from parasitism) to isolate light environment and leaf phenotype treatment effects on larval performance in the absence of enemies ("bagged" experiments). In the exposed experiments, light environment strongly affected the likelihood of parasitism, while leaf phenotype did not. Euclea delphinii larvae were up to 6.6 times more likely to be parasitized in light gaps than in shaded understory habitats. This pattern was consistent for both tachinid fly and wasp parasitoids across two separate experiments. However, the larval performance of both species in the bagged experiments was maximized in the shade-habitat/sun-leaf treatment, a habitat/leaf-type combination that occurs infrequently in nature. Taken together, our results suggest that the direct effects of light environment on the incidence of parasitism supersede any indirect effects resulting from altered leaf quality and reveal inherent ecological trade-offs for herbivores confronted with choosing between sunny (high leaf quality, harsh environment, high parasitism) and shaded (reduced leaf quality less harsh environment, reduced parasitism) habitats.

Hemocyte density increases with developmental stage in an immune-challenged forest caterpillar.

The cellular arm of the insect immune response is mediated by the activity of hemocytes. While hemocytes have been well-characterized morphologically and functionally in model insects, few studies have characterized the hemocytes of non-model insects. Further, the role of ontogeny in mediating immune response is not well understood in non-model invertebrate systems. The goals of the current study were to (1) determine the effects of caterpillar size (and age) on hemocyte density in naïve caterpillars and caterpillars challenged with non-pathogenic bacteria, and (2) characterize the hemocyte activity and diversity of cell types present in two forest caterpillars: Euclea delphinii and Lithacodes fasciola (Limacodidae). We found that although early and late instar (small and large size, respectively) naïve caterpillars had similar constitutive hemocyte densities in both species, late instar Lithacodes caterpillars injected with non-pathogenic E. coli produced more than a twofold greater density of hemocytes than those in early instars. We also found that both caterpillar species contained plasmatocytes, granulocytes and oenocytoids, all of which are found in other lepidopteran species, but lacked spherulocytes. Granulocytes and plasmatocytes were found to be strongly phagocytic in both species, but granulocytes exhibited a higher phagocytic activity than plasmatocytes. Our results strongly suggest that for at least one measure of immunological response, the production of hemocytes in response to infection, response magnitudes can increase over ontogeny. While the underlying raison d' être for this improvement remains unclear, these findings may be useful in explaining natural patterns of stage-dependent parasitism and pathogen infection.

Phenological variation in the composition of a temperate forest leaf tie community.

Arthropod communities in an array of temperate ecosystems follow similar phenological patterns of distinct compositional turnovers during the course of a season. The arthropod community inhabiting leaf ties is no exception. Many caterpillars build leaf ties, shelters between overlapping leaves attached together with silk, which are colonized secondarily by a variety of arthropods. We created experimental leaf ties by clipping overlapping leaves together with metal clips. We censused the arthropod community within experimental ties on two host plants, American beech (Fagus grandifolia Ehrhart), and white oak (Quercus alba L.), weekly for 10 wk during the summer of 2009. Diversity measures for leaf-tying caterpillars and the entire arthropod community within ties varied little between tree species and sampling periods, but caterpillar and arthropod density per tie was significantly higher on white oak than beech and abundance increased on both tree species as the season progressed. The composition (i.e., species presence and abundance) of the leaf-tying caterpillar community and the arthropod community as a whole differed between host-tree species and sampling periods. Although the arthropod communities on American beech and white oak differed, they showed similar patterns of compositional turnover, with distinct communities in early and late summer and a transitional community midsummer.

A simple protocol for extracting hemocytes from wild caterpillars.

Insect hemocytes (equivalent to mammalian white blood cells) play an important role in several physiological processes throughout an insect's life cycle. In larval stages of insects belonging to the orders of Lepidoptera (moths and butterflies) and Diptera (true flies), hemocytes are formed from the lymph gland (a specialized hematopoietic organ) or embryonic cells and can be carried through to the adult stage. Embryonic hemocytes are involved in cell migration during development and chemotaxis regulation during inflammation. They also take part in cell apoptosis and are essential for embryogenesis. Hemocytes mediate the cellular arm of the insect innate immune response that includes several functions, such as cell spreading, cell aggregation, formation of nodules, phagocytosis and encapsulation of foreign invaders. They are also responsible for orchestrating specific insect humoral defenses during infection, such as the production of antimicrobial peptides and other effector molecules. Hemocyte morphology and function have mainly been studied in genetic or physiological insect models, including the fruit fly, Drosophila melanogaster, the mosquitoes Aedes aegypti and Anopheles gambiae and the tobacco hornworm, Manduca sexta. However, little information currently exists about the diversity, classification, morphology and function of hemocytes in non-model insect species, especially those collected from the wild. Here we describe a simple and efficient protocol for extracting hemocytes from wild caterpillars. We use penultimate instar Lithacodes fasciola (yellow-shouldered slug moth) (Figure 1) and Euclea delphinii (spiny oak slug) caterpillars (Lepidoptera: Limacodidae) and show that sufficient volumes of hemolymph (insect blood) can be isolated and hemocyte numbers counted from individual larvae. This method can be used to efficiently study hemocyte types in these species as well as in other related lepidopteran caterpillars harvested from the field, or it can be readily combined with immunological assays designed to investigate hemocyte function following infection with microbial or parasitic organisms.

Winter predation of diapausing cocoons of slug caterpillars (Lepidoptera: Limacodidae).

Predators exert strong top-down pressure on herbivorous insects, but research on how predators affect herbivore fitness often focuses on the more active juvenile and adult life stages while ignoring the pupal or cocoon life stage. Few studies have investigated predation of lepidopteran pupae or cocoons and even fewer have investigated species that are not forest pests. Here we present a study on overwinter survival for two moth species in the family Limacodidae, a group of polyphagous species found in deciduous forests. We placed cocoons of the saddleback caterpillar, Acharia stimulea (Clemens), and the spiny oak-slug caterpillar, Euclea delphinii (Boisduval), in the field under saplings of six different tree species and monitored predation and survival. This is the first study to examine predation rate among different host plants within a site. We found that cocoon predation was fairly high and differed significantly between limacodid species (29% for A. stimulea vs. 22% for E. delphinii). Predation rate did not differ among the six host plant species that we tested and also did not vary annually. Through phenotypic selection analyses, we found that cocoon mass affected both the likelihood of predation and overwinter survival; larger cocoons were less likely to be depredated and more likely to successfully emerge the following year. Overall our results indicate that cocoon predation is an important source of mortality for these two limacodid species and that there may be positive selection for greater cocoon mass for both limacodid species.

Impact of plant architecture versus leaf quality on attack by leaf-tying caterpillars on five oak species.

Because shelter-building herbivorous insect species often consider structural features of their host plants in selecting construction sites, their probability of attack is likely to be a function of some combination of plant architectural traits and leaf quality factors. We tested the hypothesis that plant architecture, in the form of the number of touching leaves, influences interspecific variation in attack by leaf-tying caterpillars in five species of sympatric Missouri oaks (Quercus). We compared colonization on control branches, in which both architecture and leaf quality were potentially important, with colonization on experimental branches for which we controlled for the effects of architecture by creating equal numbers of artificial ties. Colonization of artificial ties was highly correlated with natural colonization on neighboring control branches, suggesting that leaf quality factors and not architecture influenced interspecific variation in attack by leaf-tying caterpillars. Of the leaf quality factors measured (water, protein-binding capacity, nitrogen, specific leaf area, pubescence, and toughness), nitrogen was the most explanatory. With the exception of white oak, natural leaf tie colonization was positively correlated with nitrogen availability (ratio of nitrogen to protein-binding capacity), and negatively correlated with protein-binding capacity of leaf extracts. Both host plant species and subgenus oak influenced the community composition of leaf-tying caterpillars and the non-tying symbionts colonizing the ties. Host plant differences in leaf nitrogen content were positively correlated with pupal weight of one of two caterpillar species reared on all five host plant species. Thus, interspecific differences in nitrogen, nitrogen availability, and protein-binding capacity of leaf extracts are the best predictors at this time of interspecific differences in attack by leaf-tying caterpillars, in turn affecting their success on individual host plants in the laboratory.

Impacts of alternative timber harvest practices on leaf-chewing herbivores of oak.

Studies of the effects of logging on Lepidoptera rarely address landscape-level effects or effects on larval, leaf-feeding stages. We examined the impacts of uneven-aged and even-aged logging on the abundance, richness, and community structure of leaf-chewing insects of white (Quercus alba L.) and black (Q. velutina L.) oak trees remaining in unharvested areas by sampling 3 years before and 7 years after harvest. After harvest, white oaks in uneven-aged sites had 32% fewer species of leaf-chewing insects than control sites. This reduction in species richness may have resulted from changes in microclimate (reducing plant quality and/or changing leaf phenology) that affected a much larger total area of each site than did even-aged cuts. For black oak after harvest, species richness in uneven- and even-aged sites increased relative to levels before harvest. Harvesting did not alter total insect density or community structure in the unlogged habitat for either oak species with one exception: insect density on black oak increased in the oldest forest block. Community structure of herbivores of black and white oaks in clearcut gaps differed from that of oaks in intact areas of even-aged sites. Furthermore, both richness and total insect density of black oaks were reduced in clearcut gaps. We suggest that low-level harvests alter herbivore species richness at the landscape level. Treatment effects were subtle because we sampled untreated areas of logged landscapes, only one harvest had occurred, and large temporal and spatial variation in abundance and richness existed. Although the effects of logging were greater in uneven-aged sites, the effects of even-aged management are likely to increase as harvesting continues.

The effects of leaf quality on herbivore performance and attack from natural enemies.

A diverse array of sublethal plant secondary compounds are commonly found in the foliage of temperate deciduous trees. These traits are thought to defend a plant in two principal ways, either directly by reducing insect oviposition, feeding, or biomass gain, or indirectly, through digestive inhibition. Such inhibition is hypothesized to slow the rate of herbivore development, thereby increasing their susceptibility to natural enemies (the slow-growth-high-mortality hypothesis). To clarify the defensive role of these compounds, field experiments were conducted to examine the relationships among oak leaf quality, herbivore family, and three herbivore performance measures: survivorship, development time, and pupal mass, for a bivoltine leaf-tying caterpillar, Psilocorsis quercicella (Lepidoptera: Oecophoridae). Two experiments, one for each generation of the insect, were conducted to examine the effects of intraspecific variation in leaf chemistry of its host, white oak trees (Quercus alba). In each experiment, full-sib neonate larvae were placed in experimental leaf ties on high- versus low-quality trees and allowed to feed for 2 weeks under field conditions. To determine the effect of the third trophic level, a portion of each family in each leaf-quality treatment was bagged to prevent attack from natural enemies. This treatment also allowed us to test a prediction of the slow-growth-high-mortality hypothesis, i.e., that development time, as measured for full sibs in the bagged treatment, should be positively correlated with mortality of their full sibs exposed to natural enemies. Low leaf quality significantly reduced survivorship of the caterpillars in the first generation but not the second. The third trophic level decreased survivorship in both generations. Larval development time was not affected by leaf quality in either generation, but varied significantly among insect families in both generations. In turn, larvae from slower-developing families did not suffer increased predation and parasitism, as predicted by the slow-growth-high mortality hypothesis. In contrast to development time, pupal mass showed a greater response to intraspecific variation in leaf quality, although the effect was only significant in generation 1. Concentrations of both total phenolics and hydrolyzable tannins in Q. alba foliage appear to be important negative predictors of pupal mass in P. quercicella. In marked contrast to development time, no main family effect was found for pupal mass in either experiment; however, significant family×environment interactions were found for the effects of the bagging treatment (generation 1) and the leaf-quality treatment (generation 2). Overall, the first trophic level had a greater influence on pupal mass (a fecundity correlate), while larval development time was determined more by the insect's family (genotype+maternal environment). The third trophic level was a consistently strong source of mortality in both experiments, but as a whole did not respond to familial differences in development time. Thus, from the perspective of P. quercicella, plant quality appears to serve as a defense more through its direct effect on herbivore survivorship and fecundity than through an indirect effect on predation via changes in development time.