Transitions from coral- to sponge-dominated reef states: An example from within the Coral Triangle

Abstract

Coral abundance on tropical reefs is declining on a global scale. Increases in sediment deposition have been shown to induce coral mortality at many locations worldwide, with this primarily attributed to sediment impairing coral symbiont photosynthesis. However, at multiple locations where sediment induced coral declines have occurred there have been increases in sponge abundance, with many of these sponge species containing photosymbionts. Within the Wakatobi Marine Biosphere Reserve (WMBR) UNESCO, Indonesia, at a reef system with increased levels of sedimentation (Sampela), a coral to sponge regime shift has been observed over the last decade. This reef is now sponge-dominated with a very high abundance of the phototrophic sponge, Lamellodysidea herbacea.

In my first chapter I used genetic tools to confirm a previous anatomical species identification for L. herbacea in the WMBR and also to ascertain whether the three morphotypes in this region represent a species complex. A phylogenetic analysis of L. herbacea ITS2 sequences from different morphotypes from the WMBR was performed. The phylogenetic analysis confirmed the taxonomic identity of L. herbacea for all samples and provided further evidence to support that one of the morphotypes of L. herbacea (blue-ridged) could represent a distinct species with this ascertained from samples collected from the Sampela reef. Furthermore results in this chapter have highlighted the possibility that this regime shift has had an effect on the distribution of molecularly and potentially biochemically distinct green smooth L. herbacea clades. However further phylogenetic analyses and biochemical analyses of the L. herbacea holobiont would be required to confirm this hypothesis.

In my second chapter I aimed to define whether the observed regime shift at Sampela is still transitioning, stable or reversing, to determine how changes in L. herbacea percentage cover and abundance could be occurring at this reef system and to assess L. herbacea abundance on a broader regional scale in the WMBR. The abundance and percentage cover of L. herbacea, and also measures of growth and recruitment rates, were monitored over 3 years at Sampela. In addition, individual assessments of L. herbacea percentage cover and abundance were made at multiple other sites in the wider WMBR region along with measurements of settled sediment. L. herbacea appear to still be increasing in abundance and percent cover at the Sampela reef system in conjunction with a high but stable sedimentation rate. At the Sampela reef system L. herbacea growth rates were found to be high and recruitment rates were low. L. herbacea populations are small and stable at less sedimented sites with higher coral cover in the WMBR. The increasing percentage cover of L. herbacea at Sampela with a stable sedimentation rate in conjunction with the current high level of L. herbacea benthic cover indicates that maintaining the current sedimentation rate, or even significantly reducing it, may be insufficient to reverse this regime shift.

In my third chapter I defined the photoacclimatory ability of cyanobacterial photosymbionts (Oscillatoria spongeliae) of L. herbacea in response to different levels of light availability. PAM fluorometry measurements were performed at the in situ environmental extremes of high-light and low-light availability, during extreme shading experiments and during transplant experiments from the high-light to the low-light environment. Photosymbionts of L. herbacea were photoacclimated to both environmental extremes of light availability and these photosymbionts appear to be important for L. herbacea survival, as significant tissue loss of L. herbacea was observed with extreme shading. I have also reported a rapid photoacclimatory ability of L. herbacea which was recorded during transplants from clear to turbid environments with this result potentially contributing to the explanation of how L. herbacea is proliferating at Sampela where other phototrophic benthic invertebrates are declining.

In my final experimental chapter I determined the settled sediment clearance mechanism, sediment clearance rate and impacts of settled sediment on the metabolic rate for L. herbacea exposed to different levels of settled sediment. Experimental additions of sediment both in situ and in a laboratory were used to define sediment clearance mechanisms and rates, as well as in aquarium based experiments measuring the short and long term effects of settled sediment on L. herbacea’s respiration rate. L. herbacea could clear high levels of settled sediment by utilising mucus production. The sponges also decreased their respiration rate immediately after sediment exposure, presumably as a result of a reduction in pumping as a protective mechanism, but then increased their respiration rate with sustained sediment exposure to cope with the associated metabolic demands of mucus production. Furthermore the results indicate that there could be a threshold level of sedimentation for L. herbacea that if surpassed initiates mucus production as a sediment clearance mechanism.

The results presented in this thesis indicate that this observed coral- to sponge-dominated regime shift is likely still in transition. Also some mechanisms by which the L. herbacea holobiont can tolerate high sediment concentrations have been defined which contribute to the explanation of how L. herbacea can survive at Sampela and subsequently capitalise on available benthic space from declines in other species. This regime shift provides an example of how anthropogenic impacts can majorly influence coral reef ecosystems and through discussion of the results presented in this thesis and knowledge of current local reef management practices in the WMBR, this regime shift is unlikely to be reversed in the near future.