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Mutualistic Interactions with Phoretic Mites Poecilochirus Carabi Expand bioRxiv preprint doi: https://doi.org/10.1101/590125; this version posted March 26, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Title: 2 Mutualistic interactions with phoretic mites Poecilochirus carabi expand the 3 realised thermal niche of the burying beetle Nicrophorus vespilloides 4 5 Authors: Syuan-Jyun Sun1* and Rebecca M. Kilner1 6 Affiliations: 7 1 Department of Zoology, University of Cambridge, Downing Street, Cambridge, 8 CB2 3EJ, UK 9 10 Keywords: climate change, context dependency, phoresy, cooperation, niche theory, 11 interspecific interactions. 12 13 Corresponding author: Syuan-Jyun Sun; [email protected]; +44-1223 (3)34466 14 Statement of authorship: Both authors conceived the study, designed the 15 experiments, and wrote the draft. S.-J.S. conducted the experiments and carried out 16 data analysis. 17 18 bioRxiv preprint doi: https://doi.org/10.1101/590125; this version posted March 26, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 19 Abstract: 20 Mutualisms are so ubiquitous, and play such a key role in major biological processes, 21 that it is important to understand how they will function in a changing world. Here we 22 test whether mutualisms can help populations to persist in challenging new 23 environments, by focusing on the protective mutualism between burying beetles 24 Nicrophorus vespilloides and their phoretic mites (Poecilochirus carabi). Our 25 experiments identify the burying beetle’s fundamental thermal niche and show that it 26 is restricted by competition with blowfly larvae at higher and lower temperatures 27 (within the natural range). We further demonstrate that mites expand the burying 28 beetle’s realised thermal niche, by reducing competition with blowflies at lower and 29 higher temperatures, thereby enabling beetles to produce more offspring across a 30 wider thermal range. We conclude that mutualisms can play an important role in 31 promoting survival under novel and adverse conditions, particularly when these 32 conditions enhance the performance of a common enemy. 33 34 35 bioRxiv preprint doi: https://doi.org/10.1101/590125; this version posted March 26, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 36 Introduction: 37 Mutualisms are defined as mutually beneficial interactions between species 38 (Bronstein 2015). They are ubiquitous to all life on earth and key to structuring 39 biological processes from community dynamics to ecosystem function (Bronstein 40 2015). Nevertheless, mutualistic interactions can be unstable on an ecological 41 timescale and are prone to sliding into more antagonistic relationships (Sachs & 42 Simms 2006; Anderson & Midgley 2007; Hoek et al. 2016), depending on the wider 43 ecological or physical environments in which they are embedded (Thrall et al. 2007; 44 Jovani et al. 2017). Consequently, there is considerable interest in determining how 45 mutualisms are likely to respond to environmental degradation (Kiers et al. 2010), 46 and to rising temperatures in particular (Doremus et al. 2018). 47 Previous work has emphasized the vulnerability of mutualisms to environmental 48 change. Increased temperatures cause some mutualistic interactions to break down 49 because partner species become phenologically mismatched (Rafferty et al. 2015; 50 Renner & Zohner 2018) or because they sustain different levels of thermal tolerance 51 (Barton & Ives 2014; Fitzpatrick et al. 2014; Sagata & Gibb 2016; Doremus & Oliver 52 2017; Zhou et al. 2017). Nevertheless, other partnerships between species can 53 withstand exposure to higher temperatures (e.g. Zhou et al. 2017), and then it 54 becomes harder to predict whether the mutualism will persist or degrade. 55 The effects of rising temperatures are especially difficult to predict for protective 56 mutualisms. In this class of mutualism, one species provides a resource for its partner 57 in exchange for defence from parasites or predators (Ostlund-Nilsson et al. 2005). 58 The effect of rising temperatures on the mutualists’ natural enemies is key to 59 predicting the mutualism’s fate. For example, if the enemy species succumbs to heat 60 stress before the protective partner species, and the mutualism is rendered redundant, 61 then the protective mutualist might then become an antagonist instead (e.g. (Okabe & 62 Makino 2008)). Conversely, if the enemy species and mutualists all thrive as 63 temperatures rise then the protective mutualism might be strengthened, through a 64 greater need for the defensive service provided by the protective partner (Cheney & 65 Côté 2005). The fate of the mutualism can then be described in terms of niche theory 66 (Johnson 2015). If an enemy species thrives at higher (or lower) temperatures then a 67 species’ realised niche might become even smaller than its fundamental niche. bioRxiv preprint doi: https://doi.org/10.1101/590125; this version posted March 26, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 68 However, a protective mutualist can potentially counteract these effects and enable an 69 organism to expand its realised niche, even when the enemy species performs better at 70 higher (or lower) temperatures. Whether this ever happens, however, is largely 71 unknown. 72 Here we determine the effect of a putative protective mutualism between burying 73 beetles Nicrophorus vespilloides and their phoretic mites Poecilochirus carabi, on the 74 burying beetle’s realised thermal niche. Both species breed on the body of a small 75 dead vertebrate like a mouse or a songbird. The burying beetle serves the mite by 76 transporting it to this essential breeding resource, and by dispersing the next 77 generation of mites at the end of each reproductive bout. Whilst they are onboard the 78 beetle, the mites are benign passengers. The putative protective mutualism arises 79 during reproduction on the corpse. At this point, the mites potentially serve the 80 burying beetle by consuming eggs and larvae of rival blowflies (Calliphoridae): this is 81 how they behave when carried by congeneric burying beetles N. orbicollis and N. 82 tomentosus (Springett 1968, Sloan Wilson 1983). It is unclear whether this form of 83 protective mutualism exists between N. vespilloides and P. carabi. However, these 84 two species are known to be antagonists when blowflies are not present. At high 85 densities, mites sometimes attack beetle larvae directly (Wilson & Knollenberg 1987; 86 De Gasperin & Kilner 2015) and compete with them for carrion (Wilson & 87 Knollenberg 1987; De Gasperin et al. 2015). Therefore if blowflies disappear with 88 rising temperatures, the interactions between mites and burying beetles will become 89 more antagonistic. 90 We used a combination of field and laboratory experiments to address three 91 related questions: 1) Do P.carabi protect breeding burying beetles N. vespilloides 92 from competition with blowfly larvae? 2) Does the effectiveness of this putative 93 protective mutualism vary with temperature? 3) Specifically, does P. carabi increase 94 the realised thermal niche of the burying beetle? 95 96 Material and methods: 97 Study system 98 Burying beetles (N. vespilloides) use small vertebrate carcasses as their sole breeding 99 resource. Both males and females convert the carcass into an edible carrion nest, by 100 removing any fur or feathers, rolling it into a ball, smearing it with antimicrobial 101 exudates (Cotter & Kilner 2010), and burying it underground. During carcass bioRxiv preprint doi: https://doi.org/10.1101/590125; this version posted March 26, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 102 preparation, eggs are laid in the surrounding soil and hatch within 3-4 days. The 103 larvae feed themselves on the edible nest and also fed by both parents. Approximately 104 4-5 days after hatching, the larvae disperse away from the scant remains of the carcass 105 to pupate. Adult burying beetles carry up to 14 species of phoretic mites (Wilson & 106 Knollenberg 1987). The P. carabi species complex is the most salient and common of 107 these mite species. In natural populations, 84.4% (1156 out of 1369) of trapped adult 108 N. vespilloides carry 0-20 P. carabi mites (Sun et al. 2019). 109 A dead body is a rare “bonanza resource” (Scott 1998) generating competition 110 within and among species for the resources upon it. Blowflies (Calliphoridae) are a 111 particular competitive threat for burying beetles. They can more rapidly locate the 112 newly dead and start to lay eggs within minutes of arriving on the dead body 113 (Bornemissza 1957; Payne 1965; Matuszewski et al. 2010). Their larvae also develop 114 rapidly, quickly consuming resources on the corpse. Nevertheless, their breeding 115 success is modulated by temperature. Previous work shows that at lower temperatures 116 blowflies are less abundant on carrion, and that they develop more slowly and they 117 have lower reproductive success (Wall et al. 1992; Sun et al. 2014). 118 119 Burying beetles and phoretic mites in Madingley Wood 120 Fieldwork was carried out at Madingley Woods in Cambridgeshire UK, an ancient 121 woodland of mixed deciduous trees near the Sub-Department of Animal Behaviour, 122 University of Cambridge, (Latitude: 52.22730°; Longitude: 0.04442°).
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