Ecology and evolution of the African ant acacia, Vachellia drepanolobium, and its multiple symbionts
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Childers, Richard A
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CitationChilders, Richard A. 2021. Ecology and evolution of the African ant acacia, Vachellia drepanolobium, and its multiple symbionts. Doctoral dissertation, Harvard University Graduate School of Arts and Sciences.
AbstractAnt-plants provide food rewards and housing for resident ant colonies, and in exchange, the workers protect their host plant from herbivores and pathogens. The specific outcomes of these symbioses are highly context-dependent, affected by changes in specific biotic or abiotic factors, and the impacts of these factors are often studied separately, precluding a determination of their relative importance in structuring these symbioses. In this dissertation, I conduct a broad examination of how ant and plant partners perceive, respond to, and are ultimately shaped by a range of biotic and abiotic factors, utilizing a particularly well-studied myrmecophytic system, the African Whistling-Thorn Acacia, Vachellia drepanolobium, and its associated ants, Crematogaster sjostedti, C. mimosae, C. nigriceps, and Tetraponera penzigi. All chapters of this thesis were carried out collaboratively, and within the thesis itself, attribution of effort is discussed explicitly for each chapter.
First, I analyzed the distribution, mortality, and symbiotic associations of Vachellia drepanolobium with its ants and microbial communities in response to various factors, such as soil nutrients or local conspecific tree density. I measured soil nutrients and patterns of ant occupancy and tree mortality at two timepoints across a long-term monitoring plot in Kenya, and found that environmental variation, driven by the concentration of sodium and cations in the soil, is linked to differences in the mortality of V. drepanolobium and its patterns of association with the different resident ant species. I then used multiplexed amplicon sequencing and traditional culturing to characterize the bacterial and fungal communities of focal trees from this plot. I found that these communities are dominated by endophytic fungi and that environmental variation, driven by concentration of cations, sodium, and phosphorus, as well as local tree density, is associated with considerable differences in bacterial and fungal alpha diversity. Collectively, these results indicate that within-site variation in specific environmental factors, such as sodium and cation concentration, and local conspecific tree density, is associated with large differences in key plant traits and likely fitness.
Second, I conducted two growth experiments with V. drepanolobium under controlled greenhouse conditions, to determine its responsiveness to environmental volatiles. In the first experiment I exposed V. drepanolobium seedlings to different ant colony headspace volatile treatments. Volatiles of its symbiotic ants induced more branching than those of an unassociated ant species or controls. Furthermore, trees exposed to the volatiles of T. penzigi, which routinely destroys the extrafloral nectaries of its hosts, produced significantly fewer extrafloral nectaries. I next tested whether this fire-adapted plant species could respond to fire-associated cues such as smoke. After exposing cohorts of V. drepanolobium of different ages to smoke volatiles, I found that larger, two-year old trees responded to these volatiles by increasing allocation of carbon and nitrogen to their roots and away from their leaves. Young seedlings showed the opposite pattern, and intermediate-aged seedlings did not respond, suggesting that either plant ontogeny and/or the relative strength of nutrient sources and sinks affects either the sensitivity or magnitude of this response to smoke.
Finally, I examined the impact on growth and development that the ant and plant partners have on each other, employing a field study measuring tree architecture, queen location and ant biomass distribution, followed by a greenhouse experiment where field collected ant colonies could inhabit trees under controlled conditions. The field results show that the different ant species inhabit trees with distinctive morphologies, and that differences in tree morphology result in differences in the distribution of ant biomass. Furthermore, domatia appear to be thermally buffered with respect to the ambient environment, providing a potential means of exerting control on the rate of growth and development of their ectothermic ant partners. In the greenhouse, ant behaviors result in direct changes to host morphology that recapitulate those we observed in the field, but also result in several indirect ant effects upon morphology that suggest a plant response to ant partner identity. Collectively, these patterns are likely the result of differences in the costs and benefits provided by the different ants to their hosts, and are indicative of the tug-of-war that ensues when ant and plant partners are each attempting to maximize their respective fitness interests within the context of the symbiosis.
Citable link to this pagehttps://nrs.harvard.edu/URN-3:HUL.INSTREPOS:37368410
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