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

Abstract

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.

Wide Diurnal Temperature Amplitude and High Population Density Can Positively Affect the Life History of Sitobion avenae (Hemiptera: Aphididae)

“…Thus, early-instar nymph growth and survival were inhibited by increasing population density. This finding is essentially consistent with that in the literature: insect population density significantly affects their development ( Woodhead and Paulson 1983 , Hooper et al 2003 , Ma et al 2010 ) and life history traits such as survival ( Kong et al 2013 , Silva et al 2016 ). This phenomenon may be attributed to intensified food competition, reduced living space, and increased quantities of excreta when population density is too high, which reduces habitat quality and causes increased development duration and reduced individual survival ( Stiling 1988 ).…”

“…These findings are in contrast to those of prior studies on the effects of temperature amplitude and population density on insects. Wide temperature amplitude has been shown to inhibit development ( Xing et al 2014 , Verheyen et al 2019 ) and reduce survival ( Xing et al 2019 ), longevity ( Cao et al 2018 ), and fecundity ( Carrington et al 2013 , Stoks et al 2017 ); high population density has produced similar results ( Hooper et al 2003 , Gao et al 2012 , Kong et al 2013 , Silva et al 2016 ). However, we found that with increasing population density, differences in nymph development and survival between the constant temperature and wide temperature amplitude treatments gradually decreased.…”

Lower bioenergetic costs but similar immune responsiveness under a heat wave in urban compared to rural damselflies

“…Exposure to very high temperatures often causes a decrease in immune responses, typically attributed to a reduced energy storage (e.g., Fischer et al., 2014; Janssens, Dinh Van, & Stoks, 2014; Prokkola, Roff, Kärkkäinen, Krams, & Rantala, 2013; Seppälä & Jokela, 2011). Yet, this response is not general, and also increased immune responsiveness under heat stress has been observed (Dittmar et al., 2014; Silva & Elliot, 2016; Wojda & Jakubowicz, 2007). In line with the latter studies, and despite the reduced available net energy, the encapsulation response was stronger under the heat wave.…”

Immune Defenses of a Beneficial Pest: The Mealworm Beetle, Tenebrio molitor

“…Several recent studies have investigated the effects of temperature on life history traits of insects and conclusions vary depending on the model studied ( Prokkola et al., 2013 ; Kaunisto et al., 2015 ; Silva and Elliot, 2016 ; Yin et al., 2016 ; Laughton et al., 2017 ). For example, when reared in a higher set of temperatures, the Indian meal moth, Plodia punctella , presents more hemocytes ( Laughton et al., 2017 ).…”

“…For example, when reared in a higher set of temperatures, the Indian meal moth, Plodia punctella , presents more hemocytes ( Laughton et al., 2017 ). Conversely, the velvet bean caterpillar, Anticarsia gemmatalis , presents fewer hemocytes when developing at a higher temperature ( Silva and Elliot, 2016 ). As organisms evolve and build trade-offs between their life history traits influenced by their environment, it is expected that mechanisms underlying resistance or tolerance to stress correlate differently to the impacted life history traits.…”