The role of territorial grazers in coral reef trophic dynamics from microbes to apex predators

Casey, Jordan Marie (2015) The role of territorial grazers in coral reef trophic dynamics from microbes to apex predators. PhD thesis, James Cook University.

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Territories of grazing fishes in the family Pomacentridae have been documented to cover a substantial proportion of shallow coral reefs, and these fishes can have profound effects on benthic dynamics. By cultivating palatable filamentous algae, excluding fleshy macroalgae, and aggressively defending their resources, territorial damselfishes indirectly impact coralalgal competition and play a substantial role in shaping benthic community composition, including the recruitment and post-settlement survival of scleractinian corals. Marine microbes are known to be important drivers of environmental change, and microbial community structure on coral reefs is strongly influenced by coral-algae interactions; however, the extent to which this influence is mediated by territorial grazers is unknown. Territorial damselfishes occur in distinct behavioural guilds ranging from indeterminate territorial grazers with thin algal turfs and low rates of territorial aggression to intensive territorial grazers with thick turfs and high rates of aggression. Members of the genus Stegastes are intensive territorial grazers and are known to play a major role in coral-algal dynamics. Further, most previous studies of territorial grazer effects on corals have focused on back-reef habitats although the reef crest is a highly productive environment with elevated rates of coral recruitment and settlement. Lastly, removal of marine predators via fishing is often theorized to alter community structure through trophic cascades, but empirical evidence for this phenomenon is often circumstantial on coral reefs. Given declines of predators on the Great Barrier Reef (GBR), trophic cascade theory would predict ecosystem repercussions to lower trophic levels, but it is unknown how a predator density gradient impacts the distribution of territorial damselfishes. Thus, the overall objective of this thesis was to examine the role of territorial grazers in shaping the structure and dynamics of benthic communities and the extent to which this may be mediated by higher-level trophic interactions across a gradient of fishing pressure.

To achieve this objective, I employed a variety of microbial sampling regimes and survey methods to reveal the role of territorial grazers in trophic dynamics on the GBR, Australia. To elucidate how Stegastes apicalis and S. nigricans may alter benthic microbial assemblages and coral health, I determined the benthic community composition (epilithic algal matrix (EAM) and prokaryotes) and coral disease prevalence inside and outside of damselfish territories. To determine the impact of territorial grazers on coral microbial assemblages, I established a coral transplant inside and outside of Stegastes' territories. Over the course of one year, the percent mortality of transplanted corals was monitored and coral samples were collected for microbial analysis. To assess the impact of territorial grazers on the establishment of juvenile corals, I surveyed the reef crest habitat of Lizard Island using fixed transects to assess the effects of indeterminate and intensive territorial grazers on juvenile coral abundance and taxonomic composition. In addition, the turnover of territorial pomacentrids was monitored, as well as the effects of turnover on juvenile coral assemblages. To examine trophic cascade theory and potential effects of predator removal on lower-trophic levels such as territorial damselfishes, I quantified fish and benthic assemblages across a fishing-induced predator density gradient on Australia's Great Barrier Reef. I evaluated whether the observed patterns in community structure fit the theoretical predictions of trophic cascades, and I assessed the impact of region and management zones across trophic levels.

Microbial analyses and experimental results exposed new findings on the effects of territorial grazers on marine microbial communities. 16S rDNA sequencing revealed distinct bacterial communities associated with turf algae and a two to three times greater relative abundance of phylotypes with high sequence similarity to potential coral pathogens inside Stegastes' territories. These potentially pathogenic phylotypes (totalling 30.04% of the community) were found to have high sequence similarity to those amplified from black band disease (BBD) and disease affected corals worldwide. Disease surveys further revealed a significantly higher occurrence of BBD inside S. nigricans' territories. In addition, as compared to outside damselfish territories, Stegastes were associated with a higher rate of mortality of transplanted corals. However, 16S rDNA sequencing revealed that territorial grazers do not differentially impact the microbial assemblage of corals exposed to the EAM. Regardless of Stegastes presence or absence, coral transplantation resulted in a shift in the coral-associated microbial community and an increase in coral disease associated potential pathogens. Further, transplanted corals that suffer low to high partial mortality undergo a microbial transition from a microbiome similar to that of healthy corals to that resembling the EAM.

Ecological surveys also yielded new insights into the role of small-bodied herbivorous fishes on coral reef trophic dynamics. Intensive territorial grazers were associated with a significantly lower juvenile coral abundance (34% decrease), but neither intensive nor indeterminate grazer territories impacted juvenile coral taxonomic composition. Over the course of one year, there was a high rate of territorial turnover (39.7%). Turnover from control plots to intensive damselfish territories was accompanied by a 44% decrease in juvenile corals; conversely, turnover from intensive damselfish territories to control plots coincided with a 48% increase in juvenile corals. However, although outer reef surveys indicated that protected areas enhance predator populations, we found no cascading effects from predators to lower trophic levels, such as a loss of apex predators leading to higher levels of mesopredators, which suppress mobile herbivores, followed by algal proliferation. Likewise, we found no effects of mesopredators on lower trophic levels, such as a decline of mesopredators causing higher levels of territorial grazers, resulting in lower coral and higher algae cover.

Hence, the results from this thesis reveal that territorial damselfish play a significant role in shaping coral disease dynamics and patterns of juvenile coral abundance on the reef crest, but predator density does not substantially shape the distribution of territorial grazers or other herbivorous fishes across the outer GBR. Among the microbial results, the findings demonstrate the first link among fish behaviour, reservoirs of potential coral disease pathogens and the prevalence of coral disease. Although damselfish do not seem to alter the microbial community of transplanted corals, coral transplantation significantly impacts coral microbial communities, and transplantation may increase susceptibility to coral disease. Further, damselfish substantially impact the macro-benthos: the association between damselfish territories and the abundance and spatial turnover of juvenile corals strongly implies that territorial grazers have a negative effect on juvenile coral populations. The unexpectedly high temporal turnover of damselfish territories indicates that damselfish-coralalgae linkages are highly dynamic, may be extensively influenced by local-scale effects, and have the potential to impact the structure of coral assemblages on coral reef fronts. Finally, large-scale trophic surveys indicate that top-down forces are weak on coral reefs, implying that densities of most community members, including territorial grazers, are regulated by abiotic indirect factors that vary through space. We conclude that predator-mediated trophic cascades are probably the exception rather than the rule in this ecosystem.

Item ID: 41148
Item Type: Thesis (PhD)
Keywords: algae; benthic dynamics; coral diseases; coral reef ecology; coral reef fishes; coral reefs; corals; epilithic algal matrix; Great Barrier Reef; Lizard Island; microbes; microbial ecology; predator prey interactions; Queensland; Ribbon Reefs; Swain Reefs; territorial fishes; territorial grazers; territoriality; trophic ecology
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Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 2: Casey, Jordan M., Ainsworth, Tracy D., Choat, J. Howard, and Connolly, Sean R. (2014) Farming behaviour of reef fishes increases the prevalence of coral disease associated microbes and the prevalence of black band disease. Proceedings of the Royal Society of London Series B, Biological Sciences, 281 (1788). pp. 1-8.

Date Deposited: 01 Dec 2015 05:45
FoR Codes: 06 BIOLOGICAL SCIENCES > 0602 Ecology > 060202 Community Ecology (excl Invasive Species Ecology) @ 34%
06 BIOLOGICAL SCIENCES > 0602 Ecology > 060205 Marine and Estuarine Ecology (incl Marine Ichthyology) @ 33%
06 BIOLOGICAL SCIENCES > 0605 Microbiology > 060504 Microbial Ecology @ 33%
SEO Codes: 96 ENVIRONMENT > 9608 Flora, Fauna and Biodiversity > 960808 Marine Flora, Fauna and Biodiversity @ 50%
96 ENVIRONMENT > 9613 Remnant Vegetation and Protected Conservation Areas > 961303 Protected Conservation Areas in Marine Environments @ 50%
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