Direct benefits and indirect costs of warm temperatures for high‐elevation populations of a solitary bee

Abstract

Warm temperatures are required for insect flight. Consequently, warming could benefit many high-latitude and high-altitude insects by increasing opportunities for foraging or oviposition. However, warming can also alter species interactions, including interactions with natural enemies, making the net effect of rising temperatures on population growth rate difficult to predict. We investigated the temperature-dependence of nesting activity and lifetime reproductive output over 3 yr in subalpine populations of a pollen-specialist bee, Osmia iridis. Rates of nest provisioning increased with ambient temperatures and with availability of floral resources, as expected. However, warmer conditions did not increase lifetime reproductive output. Lifetime offspring production was best explained by rates of brood parasitism (by the wasp Sapyga), which increased with temperature. Direct observations of bee and parasite activity suggest that although activity of both species is favored by warmer temperatures, bees can be active at lower ambient temperatures, while wasps are active only at higher temperatures. Thus, direct benefits to the bees of warmer temperatures were nullified by indirect costs associated with increased parasite activity. To date, most studies of climate-change effects on pollinators have focused on changing interactions between pollinators and their floral host-plants (i.e., bottom-up processes). Our results suggest that natural enemies (i.e., top-down forces) can play a key role in pollinator population regulation and should not be overlooked in forecasts of pollinator responses to climate change.

Interannual bumble bee abundance is driven by indirect climate effects on floral resource phenology

“…Populations can be limited by top‐down instead of bottom‐up forces, and this relationship may be modified by climate (Hoekman ). For example, with warmer temperatures, the benefit of increased foraging opportunities for mason bees was negated by increases in wasp parasitism (Forrest & Chisholm ). Bumble bee populations could also be influenced by predators and intra‐ and interspecific competition, factors we were unable to capture here.…”

“…). However, warmer temperatures may also have positive effects by increasing rearing temperatures and brood production (Holland & Bourke ), or foraging activity and provisioning, as in mason bees (Forrest & Chisholm ). Climate may also have indirect effects by altering the abundance and phenology of vital floral resources (Thomson ).…”

Pollen and vegetative secondary chemistry of three pollen‐rewarding lupines

“…However, the oligolectic species that pollinate Lupinus species may experience much higher effective doses of lupine pollen alkaloids, suggesting an exciting avenue for future work. Interestingly, in sites near Gothic, Colorado, the Fabaceae specialist Osmia iridis does not collect lupine pollen, though the flowers are locally abundant in areas where they forage (Spear et al., ; Forrest and Chisholm, ). It is possible that, while low relative to other tissues, the alkaloids present in the pollen of L. argenteus are at high enough concentrations to deter these oligolectic and relatively small‐bodied bees.…”

Experimental warming in the field delays phenology and reduces body mass, fat content and survival: Implications for the persistence of a pollinator under climate change

“…It has been difficult to study the effects of climate warming on insect pollinators because relatively few long‐term datasets exist that allow researchers to link pollinator ecology to changes in climate (Bartomeus et al., ; Burkle et al., ; Kudo & Ida, ; Ogilvie et al., ). The responses of some insect pollinators to warming have been investigated under simplified laboratory conditions (Bosch & Kemp, , ; Fründ, Zieger, & Tscharntke, ; Sgolastra et al., ) and others with short‐term observational studies (Forrest & Chisholm, ; Kudo, Nishiwaki, Kasagi, & Kosuge, ). However, field experiments that manipulate temperature conditions on a meaningful aspect of the pollinator's life cycle are conspicuously lacking and can provide a more predictive understanding of the direct effects of temperature change.…”

“…These responses to climate warming may have ramifications for insect population dynamics, species interactions, ecosystem function, and the local persistence or extinction of insect species (e.g. Burkle, Marlin, & Knight, 2013;Deutsch et al, 2008;Forrest & Chisholm, 2017;Kingsolver, 1989;Sheridan & Bickford, 2011).…”