Temporal resource partitioning mitigates interspecific competition and promotes coexistence among insect parasites

Abstract

A key to understanding life's great diversity is discerning how competing organisms divide limiting resources to coexist in diverse communities. While temporal resource partitioning has long been hypothesized to reduce the negative effects of interspecific competition, empirical evidence suggests that time may not often be an axis along which animal species routinely subdivide resources. Here, we present evidence to the contrary in the world's most biodiverse group of animals: insect parasites (parasitoids). Specifically, we conducted a meta-analysis of 64 studies from 41 publications to determine if temporal resource partitioning via variation in the timing of a key life-history trait, egg deposition (oviposition), mitigates interspecific competition between species pairs sharing the same insect host. When competing species were manipulated to oviposit at (or near) the same time in or on a single host in the laboratory, competition was common, and one species was typically inherently superior (i.e. survived to adulthood a greater proportion of the time). In most cases, however, the inferior competitor could gain a survivorship advantage by ovipositing earlier (or in a smaller number of cases later) into shared hosts. Moreover, this positive (or in a few cases negative) priority advantage gained by the inferior competitor increased as the interval between oviposition times became greater. The results from manipulative experiments were also correlated with patterns of life-history timing and demography in nature: the more inherently competitively inferior a species was in the laboratory, the greater the interval between oviposition times of taxa in co-occurring populations. Additionally, the larger the interval between oviposition times of competing taxa, the more abundant the inferior species was in populations where competitors were known to coexist. Overall, our findings suggest that temporal resource partitioning via variation in oviposition timing may help to facilitate species coexistence and structures diverse insect communities by altering demographic measures of species success. We argue that the lack of evidence for a more prominent role of temporal resource partitioning in promoting species coexistence may reflect taxonomic differences, with a bias towards larger-sized animals. For smaller species like parasitic insects that are specialized to attack one or a group of closely related hosts, have short adult lifespans and discrete generation times, compete directly for limited resources in small, closed arenas and have life histories constrained by host phenology, temporal resource subdivision via variation in life history may play a critical role in allowing species to coexist by alleviating the negative effects of interspecific competition.

Simulated climate change causes asymmetric responses in insect life history timing potentially disrupting a classic ecological speciation system

“…Combining eclosion data across temperature treatments showed that the three hawthorn wasp species differed in their eclosion phenologies (F = 18.75, p = 7.7 × 10 -8 , Fig. S4), as expected from previous research demonstrating temporal niche partitioning within the community (Hood et al 2015, 2021). The relative order of eclosion of the wasps from earliest to latest was Uc, Dm, and Da.…”

Spatial variation in relative abundances of two butterfly species sharing both host plant and natural enemies

“…S3). Specialist parasitoids tend to vary their use of temporal and spatial resources to facilitate coexistence (Hood et al 2021), so more natural enemies on the mainland do not necessary imply higher levels of butterfly larval mortality. The low niche overlap between the two parasitoids on the mainland can be explained by climate, habitat and/or host preferences, differences that may have originated as a result of a phenomenon of competitive exclusion.…”

A changing world: the role of phenotypic plasticity in host-parasitoid interactions facing extreme temperatures

“…It is essential to mention that despite the increase in C. vestalis competitive strength as the temperature increases, it does not necessarily imply that D. semiclausum will be displaced as environmental heterogeneity will favor coexistence of both species (Bonsall et al, 2002;Gols et al, 2005;Hood et al, 2021;Outreman et al, 2018;Poelman et al, 2014;Price, 1972). The study of the effects of ETEs on parasitoid assembly requires a high level of integration across temporal scales (e.g., seasonal), spatial scale (e.g., landscape and patch connectivity), occurrence and magnitude of extremes, and food web structure (e.g., bottom-up and top-down forces) creating multiple possible scenarios (Han et al, 2019;Rosenblatt & Schmitz, 2016;Thierry et al, 2019;Tougeron et al, 2016).…”

“…Based on the principle of mutual exclusion, two species with a perfectly overlapping ecological niche cannot coexist in the same environment, and one superior competitor dominates the interaction (Dajoz, 2006). Thus individuals and species tend to reduce their niche overlap by attacking different stages of the same host or shifting their time of activity or spatial niche (Hood et al, 2021). However, environmental filtering is expected to reduce the range of an organism's phenotype (i.e.…”

“…Parasitoid aggregation (i.e., increased parasitoid density) can lead to antagonistic encounters among different individuals leading to a decrease in per capita parasitism success (Hassell, 1971;Hassell & Varley, 1969;Mohamad et al, 2015). Interference competition in parasitoid wasps is thought to play a significant role in driving the evolution of behavioral, physiological, and morphological traits in parasitoids, as well as in structuring parasitoid communities (Bonsall et al, 2002;Hood et al, 2021;Ode et al, 2022;Price, 1972;van Alphen & Visser, 1990).…”