The Thermal Games Dung Beetles Play

Abstract

Dung beetles are a group of coprophagous scarabs most well known for their reliance on dung as both a source of food and as a vital component of their reproductive cycle. Intense competition between sympatric dung beetles species has spurred the evolution of a variety of complex nesting behaviours; telecoprids move dung along the soil surface; endocoprids reproduce within the dung itself; paracoprids bury dung in tunnels beneath the soil surface. The act of breaking down and relocating dung facilitates numerous biotic and abiotic processes that shape the environment and aid in maintaining ecosystem function. As a result of their ubiquity, the unique niche they inhabit, diverse range of species and life history strategies that have evolved, and strong ties to the biotic and abiotic processes in their surrounding habitat dung beetles have been the subject of research across the globe. We conducted a review of 1463 peer reviewed papers concerning dung beetles with the aim of elucidating geographical, temporal, and methodological patterns of research in order to identify gaps in the literature to better inform future research. All continents, with the exception of Antarctica, have a strong body of literature that has been shaped by the composition and structure of the local dung beetle assemblage, the ecosystems they inhabit, and the cultural and societal influences of its human inhabitants. Paracoprids were the most studied functional group overall with <i>Onthophagus</i> being the genus most frequently used in manipulative experiments, present in 10.3% (151) of the publications assessed. The species <i>Onthophagus taurus</i> is the most studied dung beetle, being one of the few species that has been the subject of genetic research, featuring in 4.5% (66) of studies. The most studied aspects of dung beetles are their ecology and behaviour, with relatively little work conducted on their genetics and physiology, although interest in these fields is increasing. Field surveys are the most frequently utilised method across the literature being used in 456 (31.2%) studies, followed by laboratory experiments (29.1%), and field experiments (13.5%). Studies of dung beetle communities across environmental gradients were also popular, particularly in South America where the focus is often on their use as a biological indicator of environmental health along disturbance gradients. Across the 1463 studies 75 types of dung were used, however the majority of studies utilised dung from livestock such as cattle (39.8%), pigs (6.6%), sheep (5.5%), and horses (4.2%). Human dung (16.9%) and carrion (9.8%) were also amongst the most frequently used types of dung, with most use occurring in South America and North America (primarily Mexico) where they have been shown to be an effective bait for a wide range of species. Studies assessing two or more types of dung are in the minority, accounting for only 22.4% of the publications assessed. Many studies failed to include important information such as the location where the study took place, a description of the habitat, the type of dung used, and whether the dung used was sourced from an animal that had been chemically treated.<br/>Dung beetles are strongly influenced by their thermal environment with sympatric species utilising thermal niche partitioning to reduce competition. Climate change models indicate that by 2070 temperature in Australia will increase by 0.4°C-4.5°C in coastal areas and 1.1°C-5.7°C further inland. Rising temperatures and increasingly variable thermal regimes will likely alter the community dynamics of Australia's dung beetle fauna, which it is reliant upon for the provision of a number of ecosystem services. The aim of this research was to determine the physiological tolerances of an Australian dung beetle community and to measure the metabolic responses of these species to thermal changes within these limits to determine whether thermal niche specialisation is driven by metabolic adaptations. Seven species of dung beetle (<i>Onthophagus australis</i>, <i>O. granulatus</i>, <i>O. binodis</i>, <i>Aphodius fimetarius</i>, <i>Euoniticellus intermedius</i>, <i>E. fulvus</i>, and <i>Sisyphus rubrus</i>), belonging to three functional groups, were retrieved from baited pitfall traps placed in grazed fragmented pasture ecosystems at Armidale and Bingara, NSW, Australia. Thermal limit respirometry was used to measure the CTmin, CTmax, V̇CO2 ml h-1, and the thermal sensitivity of their metabolic rate to changes in temperature using a dynamic temperature protocol to subject individual beetles to either increasing (25°C-60°C) or decreasing temperatures (25°C- -15°C). The telecoprid Sisyphus rubrus had the highest CTmax (53.1°C ±0.6) and a stable metabolic rate when exposed to high temperatures. The endocoprid <i>Aphodius fimetarius</i> was the most tolerant to low temperatures with a CTmin of -2.5°C ±2.0, while still having a CTmax of 43.6 ±1.3°C. Relative to the other species assessed it had a high metabolic rate across its entire thermal window, indicative of a thermal generalist. The paracoprids <i>E. fulvus</i> (CTmin: 9.1°C ±2.4; CTmax: 49.9°C ±1.4) and E. intermedius (CTmin: 8.3°C ±1.8; CTmax: 49.1°C ±1.9) have adapted to operate at higher temperatures than the onthophagine paracoprids which have thermal traits intermediary to the cold tolerant <i>A. fimetarius</i> and heat tolerant species.<br/>Given the central role of temperature in the evolution and ecology of dung beetles, and the ecosystem functions they provide, understanding the capacity of species to respond to climate change is required to understand the response of communities and implement effective management strategies. Dung beetles of the species <i>Onthophagus binodis</i> were collected from the University of New England's Kirby SMARTFARM, NSW, Australia. Beetles were placed in custom built temperature controlled chambers and soil temperature data used to program chambers with a variable temperature regime based on the natural regime experienced by the sampled population in the field. The chambers were programmed to simulate increased temperatures based on climate change warming estimates of +0°C, +2°C, +3.5°C, and +5°C. Every 10 days two beetles from each chamber were removed and dynamic thermolimit respirometry performed to measure the CTmax, V̇CO2 ml h-1, thermal sensitivity of metabolic rate, and the intercept of the regression of metabolic rate and temperature. Changes in the nesting behaviour of <i>O. binodis</i> were also assessed by recording the number of brood balls produced, brood ball burial depth, and brood ball size. Brood balls were then reared at 25°C and the experiment repeated with the second generation. <i>Onthophagus binodis</i> did not display the capacity for physiological plasticity under the simulated warming scenarios, with no significant effect of warming on CTmax (46.43°C ±1.68), V̇CO2 ml h-1 (32.28 ±8.84), thermal sensitivity (2.51 ±0.63), or the intercept of the MR-T line (-0.13±0.41). Warming regimes had no effect on brood burial depth (9.12cm ±7.02). We found evidence for a potential density dependent effect of temperature on brood ball production in the second generation: beetles from the +5°C treatment producing significantly more broods than the +0°C control. When brood ball production was low beetles from the +5°C treatment produced broods with a significantly greater volume than +0°C controls.