Extreme Heat in the Nest of a Desert Native Bee, Xylocopa californica arizonensis (Hymenoptera: Apidae)

Abstract

Native bees are increasingly under threat from anthropogenic change, including rising temperature. Deserts are home to the highest global diversity of bee species, are among Earth’s most variable and extreme climates, and are also highly sensitive to climate change. As a result, bees in deserts face unique challenges. Species in deserts tend to be adapted to extremes, but also are chronically close to the edge of their tolerances. Bees in tundra and subarctic regions, temperate zones, and the tropics are well-studied. In contrast, despite their importance and vulnerability, desert bees’ responses to climate change are not. Developing stages are minimally studied compared to adults. As a whole, we know climate is warming, especially in deserts, and that many species are declining, but we don’t actually know how individual species will fare in their habitats. Behavioral and physiological adaptations, life histories, and the microhabitat determine how insects respond to temperature, resulting in a multitude of possible context-dependent thermal responses. Temperatures approaching organisms’ critical thermal maxima (CTmax) may impact survival. In this dissertation, I test aspects of nesting that may impact bees’ thermal tolerances and the temperatures they experience, particularly in deserts, and consider how they might affect bee populations and their potential range expansions or contractions. Many studies of climate change responses focus on species that have already demonstrated population changes, or that are likely to be of high conservation concern, and with good reason. However, bees everywhere are already showing range shifts and phenological shifts driven by climate change. Evidence regarding the causes of these declines has exploded over the past decade. While most studies seeking to predict species’ responses to warming climate focus on an at-risk species, I instead selected a widespread and common bee that is likely to be more thermally tolerant than other taxa. Specifically, I asked how a common desert carpenter bee, Apidae: Xylocopa californica arizonensis (referred to throughout this document as "X. californica arizonensis"), would fare in climate change. To answer this question, I needed to know what temperatures these bees experience in the nest, their thermal tolerances, and whether projected rising temperatures would substantially reduce their thermal safety margin. I took a multi-faceted approach to exploring thermal responses of X. californica arizonensis. I incorporated physiology, abiotic and biotic interactions, and collected in situ nest temperature measurements. I first reviewed how desert bees are impacted by temperature and delved into the multi-scale factors that play into determining their responses to changing thermal regimes. I then explored various aspects of X. californica arizonensis thermal ecology. To assess its thermal tolerance during development, I used flow-through thermolimit respirometry on all larval and pupal stages. To to relate thermal tolerances of larvae and pupae temperatures to the microenvironment of the nest, I measured the internal and external temperatures of 61 Dasylirion wheeleri stalks, the preferred nesting substrate, and tested which stalk characteristics most impact nest temperature. Finally, to investigate whether nest placement affects biotic interactions, I explored an interaction between X. californica arizonensis and their woodpecker predators. D. wheeleri inflorescence stalks grow out of a dense rosette of barbed leaves, so I asked whether nesting deeper in this rosette better protects X. californica arizonensis larvae from woodpecker attacks. I recorded X. californica arizonensis nest entrance height, the locations of bird predation marks, and the height of the tallest points of D. wheeleri leaf rosettes. I found that the thermal safety margins for developing X. californica arizonensis are small, and likely to shrink with increasing extreme summer high temperatures. Early instar larvae, the least thermally tolerant life stage, died at 51.2◦C. Based on record high local air temperatures in southern Arizona (up to 46.7◦C), early instar larvae would have a thermal safety margin of only 4.5◦C. However, air temperatures may not be good representations of the temperatures developing bees experience in the nest. I measured some nest temperatures that were extremely close to bees’ tolerances. Surprisingly, I found that active X. californica arizonensis nests are warmer than inactive ones. I also found that nest placement on D. wheeleri stalks determines the temperature of the nest microenvironment. Bees could potentially modify their nest temperature by placing their nests lower or higher on stalks. However, while nesting higher on a stalk may provide some protection from thermal extremes, larvae within higher nests are also more prone to attack by predatory woodpeckers. Most of the X. californica arizonensis nests that I located were protected behind D. wheeleri leaves, rather than placed in exposed regions of the stalk, and nests that escaped predation were placed deeper within the protection of the leaves than those that were attacked. These results are consistent with the hypothesis that D. wheeleri leaves may provide X. californica arizonensis nests with protection from woodpeckers. The conflicting pressures of woodpecker predation and rising temperatures seem to constrain X. californica arizonensis nest placement options. Based on projections of increasing regional high air temperature, X. californica arizonensis early instar CTmax suggests that in less than 30 years, this critical pollinator might be close to the maximum temperature it can tolerate physiologically. Disturbingly, I did not need to apply future climate projections to nest temperatures, because I found evidence that X. californica arizonensis already faces survival challenges due to the extreme high temperatures in the nest. Despite selecting a widespread, common, heat-adapted bee that I hypothesized to be a robust species of minimal conservation concern, I still found evidence that it is facing conditions likely to surpass its tolerance in its native range. Based on these unsettling results, I conclude that X. californica arizonensis, supposedly a desert-adapted and heat tolerant bee, will face reduced nest habitat and increasing challenges to successful nesting as climate warms. The fact that such a widespread and seemingly robust species is at risk has concerning implications for conservation strategies and ecosystem risk assessment. I recommend that future studies prioritize investigating thermal profiles of species based on their network interactions and ecosystem function even if they are of lesser conservation concern. I also urge everyone to take massive immediate action towards reversing the effects of climate change.