How development and survival combine to determine the thermal sensitivity of insects.

Thermal performance curves (TPCs) depict variation in vital rates in response to temperature and have been an important tool to understand ecological and evolutionary constraints on the thermal sensitivity of ectotherms. TPCs allow for the calculation of indicators of thermal tolerance, such as minimum, optimum, and maximum temperatures that allow for a given metabolic function. However, these indicators are computed using only responses from surviving individuals, which can lead to underestimation of deleterious effects of thermal stress, particularly at high temperatures. Here, we advocate for an integrative framework for assessing thermal sensitivity, which combines both vital rates and survival probabilities, and focuses on the temperature interval that allows for population persistence. Using a collated data set of Lepidopteran development rate and survival measured on the same individuals, we show that development rate is generally limiting at low temperatures, while survival is limiting at high temperatures. We also uncover differences between life stages and across latitudes, with extended survival at lower temperatures in temperate regions. Our combined performance metric demonstrates similar thermal breadth in temperate and tropical individuals, an effect that only emerges from integration of both development and survival trends. We discuss the benefits of using this framework in future predictive and management contexts.

Direct and indirect effects of altered temperature regimes and phenological mismatches on insect populations.

Climate change is transforming ecosystems by altering species ranges, the composition of communities, and trophic interactions. Here, we synthesize recent reviews and subsequent developments to provide an overview of insect ecological and evolutionary responses to altered temperature regimes. We discuss both direct responses to thermal stress and indirect responses arising from phenological mismatches, altered host quality, and changes in natural enemy activity. Altered temperature regimes can increase exposure to both cold and heat stress and result in phenological and morphological mismatches with adjacent trophic levels. Host plant quality varies in a heterogenous way in response to altered temperatures with both increases and decreases observed. Density-dependent effects, spatial heterogeneity, and rapid evolutionary change provide some resilience to these threats.

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.

Herbivore seasonality responds to conflicting cues: Untangling the effects of host, temperature, and photoperiod.

Organisms from temperate ecosystems experience a cyclic alternation of favorable seasons, when they can grow and develop, and unfavorable periods, characterized by low temperatures and reduced resource availability. A common adaptation to these changing conditions is to undergo a state of metabolic arrest triggered by environmental cues (e.g. diapause) during the unfavorable periods. Altered environmental conditions resulting from global change can expose organisms to contradictory cues, potentially triggering maladaptive responses. Here, I compared the performance of an oligophagous butterfly when experiencing consistent vs contradictory environmental cues by manipulating temperature, daylength, and host plant in the laboratory. I implemented a fully factorial design with realistic temperature and photoperiodic regimes to resemble environmental conditions during mid-summer and the summer-autumn transition within the focal species' range. To assess the role of host plant at mediating the effects of abiotic factors, larvae were fed foliage of either a high or a low-quality host species. Decreasing daylength was the primary cue inducing diapause; however, feeding on a low-quality host at low temperatures also induced diapause in larvae growing under constant summer daylength. Conversely, exposure to high temperatures while feeding on a high-quality host occasionally overruled the diapause-inducing effect of decreasing daylength. Feeding on a high-quality host mitigated the lethal effects of cold, but not of hot temperatures. In addition, exposure to cold temperatures resulted in a significant reduction of pupal mass only under decreasing daylength. These results indicate that responses to environmental stressors in this multivoltine butterfly differ across the growing season according to the eco-physiological state of individuals (whether they undergo direct development or diapause). Traits related to oligophagy, such as sensitivity to multiple cues for diapause induction, as well as some of its consequences, such as the occurrence of overlapping generations, are likely to mitigate some of the detrimental effects of global change.

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.

Shelter-building behavior and natural history of two pyralid caterpillars feeding on Piper stipulaceum.

Shelter-building behavior by caterpillars provides a mechanism of defense against predators, microenvironment enhancement, and in some cases nutritional benefits. This study provides a detailed description of the life cycle and shelter-building process of caterpillars, and identifies constraints and factors influencing this adaptive behavior in Lepidomys n. sp. near proclea Druce (Pyralidae: Chrysauginae), a tropical dry forest pyralid. Five macroscopic larval instars were detected during the life cycle, and activities performed during shelter-building were categorized and timed. Caterpillar predators were identified, and 20% of all collected larvae died due to attack by parasitoid wasps. Shelter-building behavior was found to be constrained by the ontogenetic stage of caterpillars and influenced by leaf size of the host plant, Piper stipulaceum Opiz (Piperales: Piperaceae) . A similar pattern of shelter-building behavior exhibited by Tosale n. sp. near cuprealis larvae that coexisted in the same host plant is also described. Larvae of the second species were significantly less abundant than those of Lepidomys and hatched one month later in the rainy season, which could indicate some competitive interactions between these two pyralid species.