Environmental degradation amplifies species' responses to temperature variation in a trophic interaction

Abstract

Land-use and climate change are two of the primary drivers of the current biodiversity crisis. However, we lack understanding of how single-species and multispecies associations are affected by interactions between multiple environmental stressors. We address this gap by examining how environmental degradation interacts with daily stochastic temperature variation to affect individual life history and population dynamics in a host-parasitoid trophic interaction, using the Indian meal moth, Plodia interpunctella, and its parasitoid wasp Venturia canescens. We carried out a single-generation individual life-history experiment and a multigeneration microcosm experiment during which individuals and microcosms were maintained at a mean temperature of 26°C that was either kept constant or varied stochastically, at four levels of host resource degradation, in the presence or absence of parasitoids. At the individual level, resource degradation increased juvenile development time and decreased adult body size in both species. Parasitoids were more sensitive to temperature variation than their hosts, with a shorter juvenile stage duration than in constant temperatures and a longer adult life span in moderately degraded environments. Resource degradation also altered the host's response to temperature variation, leading to a longer juvenile development time at high resource degradation. At the population level, moderate resource degradation amplified the effects of temperature variation on host and parasitoid populations compared with no or high resource degradation and parasitoid overall abundance was lower in fluctuating temperatures. Top-down regulation by the parasitoid and bottom-up regulation driven by resource degradation contributed to more than 50% of host and parasitoid population responses to temperature variation. Our results demonstrate that environmental degradation can strongly affect how species in a trophic interaction respond to short-term temperature fluctuations through direct and indirect trait-mediated effects. These effects are driven by species differences in sensitivity to environmental conditions and modulate top-down (parasitism) and bottom-up (resource) regulation. This study highlights the need to account for differences in the sensitivity of species' traits to environmental stressors to understand how interacting species will respond to simultaneous anthropogenic changes.

Keywords: climate change; environmental variation; habitat modification; host-parasitoid; life-history trajectories; phenological mismatch; population cycles; population dynamics.

Figure 1

Host and parasitoid life‐history traits were affected by temperature variation and resource degradation (% methyl cellulose). Panels show juvenile stage duration of (a) unparasitized hosts and (b) parasitoids; and (c) parasitoid adult life span. Symbols are observed means and 95% CIs. Regression lines were obtained from the best supported model for each response variable (Tables S2, S4 and S8 in Appendix S3). Numbers below error bars indicate sample size

Figure 2

Adult host and parasitoid body sizes were affected by resource degradation, but not by temperature variation. Panels show (a) host mid‐femur length and (b) parasitoid hind tibia length. Symbols are observed means and 95% CIs. The regression lines were obtained from the best supported model for each response variable (Tables S10 and S12 in Appendix S3). Numbers below error bars indicate sample size

Figure 3

Time series of the number of (a) dead adult hosts (H) and (b) parasitoids (P) according to temperature treatment, resource degradation and microcosm type. Time series were fitted with a GAMM with a negative binomial error distribution and a log link function. GAMM parameters were as follows: number of knots k = 14, theta_host = 1.91 and theta_parasitoid = 1.44. Regression lines are GAMM predictions (±SE)

Figure 4

The overall mean and variability of abundance of adult hosts (H; a, b) and parasitoids (P; c, d) were affected by temperature variation, resource degradation and microcosm type (hosts only). Data are observed mean and variability of host and parasitoid abundance. Regression lines were obtained from the best supported models for (a) and (b) (Tables S1 and S3 in Appendix S6), from the second best supported model for (c), which includes a non‐significant effect of resource degradation (ΔAIC_c = 1.47; model 6 in Table S5 in Appendix S6), and from the third best supported model for (d), which includes a significant effect of temperature variation (ΔAIC_c = 0.62; model 24 in Table S7 in Appendix S6)

Figure 5

The amplitudes of dead adult host normalized time series were affected by temperature treatments, resource degradation and microcosm types. Data are normalized amplitudes (Appendix S5). Regression lines (±SE) were obtained from the only supported model based on AIC_c