Demography and impacts of habitat degradation on the giant barrel sponge Xestospongia spp. in the Indo-Pacific
Authors:   , McGrath Emily 
Published: November 2021

<p>Coral cover worldwide is in decline largely due to anthropogenic influence. In some areas reefs are transitioning into alternative states dominated by sponges, which remain largely understudied despite their abundance and functional importance. Coral reefs in the Wakatobi National Marine Park (WNMP), Indonesia are among the most diverse in the world but remain vulnerable to a multitude of stressors, including coastal development and the resultant sedimentation. Some degraded reefs are characterized by high levels of sedimentation and low coral cover in this area, but support large populations of the ecologically important giant barrel sponge Xestospongia spp. Giant barrel sponges in the genus Xestospongia may be among the largest benthic invertebrates providing habitat and fulfilling ecosystem services on reefs where coral is declining. The large size of these sponges is of particular importance as body size is mechanistically linked to pumping and nutrient cycling. This thesis examines the demographic structure and connectivity of Xestospongia spp. in four core sites within the WNMP, and attempts to elucidate the mechanisms allowing them to tolerate sedimentation. In my first data chapter I examined the influence of environmental variability on Xestospongia spp. growth and longevity over the course of two years at four sites. Specific growth rate, density, mean volume, and environmental variables were examined and compared. Four candidate growth models were fitted to the volume data each site and compared using Akaike’s Information Criterion. Best fit models were determined using a multi-model inference (MMI) approach. Models were averaged to extrapolate size-at-age, which were validated by sponge growth on an artificial structure of known age. There was no difference in model-averaged growth rates between depths or sites of varying habitat quality despite differences in density and mean volume, perhaps suggesting that Xestospongia spp. may be less reliant on their photosynthetic symbionts and feeding heterotrophically, or are able to switch between these trophic modes to maintain growth. Size-at-age estimates placed the largest measured sponges between 24 and 30 years, in contrast with published estimates of Caribbean Xestospongia muta of over 240 years for sponges of comparable size. My results highlight the accelerated growth of these massive sponges compared to estimates from the Caribbean; these differences have important implications for how these ecologically important species should be managed. In the second data chapter I used empirical data to construct an integral projection model (IPM) to explore population dynamics at two sites. My aim was to quantify the extent that the relationship between sponge size and growth, survival, and fecundity (vital rate parameters) influences population-level outcomes (growth or decline). Indicators of asymptotic population dynamics (stable size distributions and long term growth rate) and elasticities of vital rate parameters were calculated. The importance of recruitment to population growth was examined by simulating demographically open and closed systems. To assess the importance of size-dependent survival on population growth at each site, recruit and adult mortality was simulated for each system. IPM analyses suggest that in the absence of large sponges population growth would show a substantial decline but both populations are resilient to instances of poor recruitment, and that maintaining Xestospongia spp. size should be considered a principal element in management and conservation. Finally, this chapter emphasizes the importance of recruit source to population dynamics on a small scale. The results of this chapter highlight that population biomass at both sites is increasing and Xestospongia spp. are likely to remain the dominant component of these reef system in the WNMP. However, one large-scale mortality event affecting large sponges could severely impact populations with a subsequent slow recovery. My third data chapter examined the physiological effects of short-term exposure of Xestospongia spp. to suspended sediment in an effort to quantify mechanisms of local adaptation. In the Wakatobi National Marine Park, Indonesia, some degraded reefs are characterized by high levels of sedimentation and low coral cover, but support large populations of Xestospongia spp. Respiration rates increased compared to controls when sponges were exposed to environmentally relevant suspended sedimentation concentrations of 75 and 150 mg 1⁻¹. For the first time sponge mucus production was observed as a mechanism to remove settled sediment, and sediment clearance was filmed in situ over the course of 24 h. Sponges produced mucus in response to sediment addition, with a mean clearance rate of 10.82 ± 2.04% h⁻¹ (sediment size fractions 63–250 µm). Mucus production is an effective, but slow mechanism supporting barrel sponge survival in habitats experiencing high levels of sedimentation. My results suggest that there are likely to be energetic consequences for sponges living in sedimented environments, which may influence the energy available for other demographic processes and therefore have implications for barrel sponge population sustainability. My final chapter explored genetic connectivity and structuring of Xestospongia spp. at four sites using nine multilocus microsatellite markers. Genetic analyses demonstrated strong genetic structuring supporting a cryptic species complex of five genetic clusters, likely representing separate species or subspecies. Fine-scale relatedness was measured to identify potential sources of larval recruits using assignment tests, sibship analyses, and maximum-likelihood estimation of relatedness among and between study sites. Mean Maximum-likelihood estimation of relatedness estimates revealed that for three sites self-recruitment does not appear to dominate, but one site was characterized high levels of self-recruitment. In summary, Xestospongia spp. populations in the sites sampled during my study are composed of a species complex, the structure of which appears to be driven by self-recruitment and is heavily reliant upon large sponges. The study site is characterized by the highest levels of settled and suspended sediment features large and stable Xestospongia spp. populations that appear to be tolerant to varying levels of sedimentation, possibly due to the production of mucus as a sediment clearance mechanism. This tolerance comes at a cost, however, and results in elevated respiration rate which may require energy otherwise utilized for demographic processes (growth, reproduction, etc.). Growth curves suggested that sponges at sites of increased sedimentation took longer to grow to an equivalent size, although there was no difference in growth between sites; this may suggest that these sponges can shift to heterotrophic feeding in conditions less favourable to photosynthesis by its symbionts. Xestospongia spp. population dynamics appear to be heavily reliant on large individuals, and the results of my study suggest that management efforts should be targeted accordingly.</p>