Understanding heatwave damage through reproduction in insect systems

Recent long-term field surveys have revealed 'catastrophic' declines in insects, even in areas protected from habitat loss and pesticides. Climate change is the likely cause, but we still have 'disturbingly limited knowledge' about proximate drivers of biodiversity loss under global warming (Cahill et al 2013). This project will examine one key driver, by testing the hypothesis that exceptional thermal sensitivities within reproduction can explain why insect populations are declining. Under climate change, extreme conditions such as heatwaves are getting more frequent and severe, and such thermal variation may damage biodiversity more than average change. Male reproductive sensitivity to heat is well known in endotherms, but ectotherms have received scant attention, despite comprising most of biodiversity, and being directly affected by the thermal environment. In a recent NERC project, we identified in our Tribolium beetle model that reproduction is exceptionally sensitive to warming: heatwaves at 5-7oC above the population optimum for 5 days damage male fertility and sperm function, and a second heatwave almost completely sterilises males (Sales et al. 2018: Experimental heatwaves compromise sperm function and cause transgenerational damage in a model insect. Nature Comms). Female reproduction, by contrast, is resilient to heat, but is compromised via thermal damage to sperm in female storage. In addition to these direct impacts, we also revealed less obvious transgenerational damage to reproductive fitness and lifespan of offspring if fathers or fertilising sperm (in female storage) had experienced heatwaves.

Because a) reproduction is essential for population viability, b) heatwaves are becoming more frequent and severe, and c) most species on Earth are insects in worrying decline, we propose to measure how experimental heatwaves impact on: 1) reproduction across a suite of tropical and temperate insect species; 2) thermal vulnerabilities at different life stages and whether any damage is permanent; and 3) heatwave impacts on population resilience, viability and extinction. As proposed by recent expert reviews, we will tackle these important questions using systematic experiments across three complementary work packages:

1) MEASURE REPRODUCTIVE SENSITIVITIES IN DIFFERENT INSECT SPECIES. Building on our results from Tribolium beetles, we will investigate how heatwaves impact on sex-specific and gamete-specific reproduction across nine temperate and tropical insect model systems. We have chosen species that represent some major Orders and ecologies, and which we know from experience will breed readily within controlled lab experiments. Heatwave conditions will be simulated where temperatures exceed the average local temperature during breeding for the population by >5oC for 5 days.
2) MEASURE DIFFERENT LIFE STAGE SENSITIVITIES TO HEATWAVE CONDITIONS. Experimental work with Tribolium beetles revealed that heatwave conditions (5-7oC above the optimum for 5 days) halved the reproductive output of mature males and their sperm. New pilot data now reveal that immature males become completely sterile under the same conditions, and pupae suffer high mortality. We will therefore measure the relative vulnerabilities of embryonic, larval, pupal and adult life stages to heatwaves in beetle and moth models, and assess impacts on survival, development, reproduction and transgenerational effects in both sexes, and whether the damage is permanent.
3) MEASURE HEATWAVE IMPACTS ON INSECT POPULATION VIABILITY. Using Tribolium beetle and Plodia moth models which have proven value for the tracking of longer-term, whole-population impacts, and incorporating information about stage sensitivities from 2) as the project progresses, we will measure and model how heatwaves cause longer-term declines and extinctions in replicated populations, gaining broader insight into how extreme weather across life stages influences insect biodiversity.

Understanding how more extreme weather conditions impact on the biodiversity of insects has potentially broad public appeal and conservation relevance, especially in the context of climate change. Recent long-term field surveys have revealed 'catastrophic' declines in insects, even in areas protected from habitat loss and pesticides, but we still have 'disturbingly limited knowledge' about the proximate drivers of biodiversity loss under global warming. This project will examine one key driver by testing whether exceptional thermal sensitivities within reproduction can explain why insect populations are declining. Insects play critical roles within almost every terrestrial ecosystem, from obvious societal benefits such as pollination and decomposition, to less obvious benefits such as soil nutrient turn-over and key steps through terrestrial food webs. Insects therefore play a core role in our planet's biodiversity, and raising awareness of potentially large-scale impacts of climate change on sensitivities within insect reproduction will benefit all of us relying on Earth's life support system.

We will achieve societal impact by improving public understanding, appreciation and awareness of insect biodiversity, and vulnerability to increasing heatwaves driven by global climate change. Fostering in appreciation in the remarkable diversity of insects is critical to recognising their ecological value, and children are especially important targets for such engagement. The investigator team maintains active science communication activities, and the public will benefit from this engagement following our activities that promote impact via dissemination of our research to the public and relevant bodies through 1) spoken, written and film media, and 2) via engagement in person:

1. We will raise public, governmental, NGO and land-manager awareness of our research by publishing the results in internationally-important, peer-reviewed, widely-read, open access publications. We will produce these in tandem with active and appropriate public engagement through spoken and written media, blogs, animations, and via social media, so that maximum dissemination of the key research findings and their relevance is achieved, and the public, government bodies, NGOs and land-users are made aware of reproductive sensitivities and consequences of heatwave conditions on population abundance of insects. We will also target these activities to relevant NGOs such as Buglife and other conservation agencies.

2. At three, heavily-attended public festivals and shows that are close to Norwich (to minimise travel), we will disseminate our research findings and the wider importance of insect biodiversity to thousands of members of the public by exhibiting in person. We will attend the Latitude Festival in 2020, 2021 and 2022 and run the 'Science Tent' to promote the importance, excitement and value of biodiversity for Earth's life support system through our 'Dazzling Diversity of Nature' exhibit. At the Norwich Science Festival members of the research team will present in 2021 and 2022, and PI Gage will deliver public-facing lectures on climate change, male reproductive vulnerability and biodiversity declines, with the research team presenting an exhibition. At the Royal Norfolk Show, we will present a stand in 2021 and 2022 that delivers public-facing information on the project and wider issues to the public. The Norfolk Show attracts a large number of the regional farming community, so the exhibition will present the positive aspects of insect biodiversity through farming ecosystems, and articulate the potential for integrated insect pest management in grain storage facilities using a more detailed understanding of insect thermal responses and reproduction. At these three events, non-scientists will benefit from the impact activity by gaining wider and deeper knowledge, appreciation and awareness of the importance and fascinating biodiversity of insects.