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On the ecological transitions between parasitism and mutualism


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Abstract

Species interactions are pivotal to biodiversity structure and ecosystem functioning. Nevertheless, interactions between species are ecologically variable within the same pair of interacting species, lying on a mutualism-parasitism continuum. Identifying the underlying mechanisms and context dependency of such ecological dynamics is essential to understand the responses of interacting species to rapidly changing environments. In this thesis, I investigate the ecological factors that cause transitions between parasitism and mutualism, using the burying beetles (Nicrophorus vespilloides) and their phoretic mites (the species complex Poecilochirus carabi) as a model symbiosis. I begin by showing that P. carabi is the most abundant mite species associating with burying beetles, and that it coexists with the mite Macrocheles nataliae. I show that each species attaches to a distinct part of the beetle’s body, so facilitating their co-existence. Furthermore, I show that distinct behavioural and biomechanical adaptations enable each mite species to occupy their preferred locations. This finding reveals that niche partitioning can occur within macroscopic symbiotic communities even when they coexist upon the same host animal. Next, I investigate whether P. carabi mites and N. vespilloides are ever (by-product) mutualists. I assess whether mites assist beetles when competing with conspecifics for ownership of the carcass. Using infrared thermography, I find that beetles with mites attain a higher body temperature, and that this makes them more likely to win contests against conspecifics. However, mites confer this thermal benefit only upon smaller beetles, who generate more heat than larger beetles when carrying mites, which is then trapped by the layer of mites on the beetle’s body. For larger beetles, mites are parasitic. They maintain a high body temperature and win contests for a carcass singlehandedly, and then produce fewer larvae when breeding alongside mites. Burying beetles also commonly face fierce competition from blowflies for the resources upon a carcass. Combining field manipulations and laboratory experiments, I find that mites are in a protective mutualism with beetles because they eliminate blowflies from the carcass, and so promote burying beetle reproductive success. I also find that the extent of this mutualism is dependent upon temperature. At lower temperatures, and when blowflies are absent, mites reduce beetle reproductive success. They are most effective at promoting beetle reproductive success at higher temperatures, at which blowflies pose more of a competitive threat. Finally, I investigate whether the number of burying beetle species present in a woodland can tip the relationship between mites and their N. vespilloides hosts from mutualism to parasitism. I discover that neighbouring woodlands (Waresley and Gamlingay Woods in Cambridgeshire, UK) harbour two and four species of burying beetle, respectively. Furthermore, each species of burying beetle is associated with a different race of P. carabi mite. I show that mite races can be locally adapted to their host beetle species. However, I also find that mite races mix, so that one burying beetle species can be host to multiple P. carabi mite races, and that this happens more frequently when there are more burying beetle species present in one woodland. Burying beetles are then more likely to be in an antagonistic relationship with the mites they carry: local adaptation experiments reveal that N. vespilloides in Gamlingay Wood is in a more antagonistic relationship with P. carabi mites than N. vespilloides from Waresley Wood. Thus temperature, the density of mites and the density of rivals for the carrion breeding resource independently influence whether the relationship between N. vespilloides and P. carabi is more likely to be mutualistic or antagonistic.

Description

Date

2019-04-16

Advisors

Kilner, Rebecca

Keywords

behavioural ecology, niche theory, interspecific interactions, local adaptation, burying beetles, phoretic mites, mutualism, parasitism

Qualification

Doctor of Philosophy (PhD)

Awarding Institution

University of Cambridge
Sponsorship
Taiwan Cambridge Scholarship (The Cambridge Commonwealth, European & International Trust)

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