Decadal variability in sponge abundance and biodiversity on an Indo-Pacific coral reef

Rovellini, Alberto; Dunn, Matthew R.; Fulton, Elizabeth A.; Webster, Nicole S.; Smith, David J.; Jompa, Jamaluddin; Haris, Abdul; Berman, Jade; Bell, James J.

doi:10.3354/meps12968

Cited by 19 publications

(28 citation statements)

References 85 publications

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“…Furthermore, sponge assemblages can show strong temporal changes in abundance and biodiversity across many ecosystems. For example, censuses made over 14 years at a permanent site in Panama showed a steady decline of sponge species (53.1%) with time (Wulff, 2006 b ), while sponge abundance on an Indonesian coral reef was also found to fluctuate by as much as >60% over a 13‐year monitoring period (Rovellini et al ., 2019). Temperate and polar sponge assemblages can also show strong seasonal changes (e.g.…”

Section: Global Variation In Sponge Traitsmentioning

confidence: 99%

Interocean patterns in shallow water sponge assemblage structure and function

et al. 2020

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Sponges are a major component of benthic ecosystems across the world and fulfil a number of important functional roles. However, despite their importance, there have been few attempts to compare sponge assemblage structure and ecological functions across large spatial scales. In this review, we examine commonalities and differences between shallow water (<100 m) sponges at bioregional (15 bioregions) and macroregional (tropical, Mediterranean, temperate, and polar) scales, to provide a more comprehensive understanding of sponge ecology. Patterns of sponge abundance (based on density and area occupied) were highly variable, with an average benthic cover between ~1 and 30%. Sponges were generally found to occupy more space (percentage cover) in the Mediterranean and polar macroregions, compared to temperate and tropical macroregions, although sponge densities (sponges m–2) were highest in temperate bioregions. Mean species richness standardised by sampling area was similar across all bioregions, except for a few locations that supported very high small‐scale biodiversity concentrations. Encrusting growth forms were generally the dominant sponge morphology, with the exception of the Tropical West Atlantic, where upright forms dominated. Annelids and Arthropods were the most commonly reported macrofauna associated with sponges across bioregions. With respect to reproduction, there were no patterns in gametic development (hermaphroditism versus gonochorism), although temperate, tropical, and polar macroregions had an increasingly higher percentage of viviparous species, respectively, with viviparity being the sole gamete development mechanism reported for polar sponges to date. Seasonal reproductive timing was the most common in all bioregions, but continuous timing was more common in the Mediterranean and tropical bioregions compared to polar and temperate bioregions. We found little variation across bioregions in larval size, and the dominant larval type across the globe was parenchymella. No pattens among bioregions were found in the limited information available for standardised respiration and pumping rates. Many organisms were found to predate sponges, with the abundance of sponge predators being higher in tropical systems. While there is some evidence to support a higher overall proportion of phototrophic species in the Tropical Austalian bioregion compared to the Western Atlantic, both also have large numbers of heterotrophic species. Sponges are important spatial competitors across all bioregions, most commonly being reported to interact with anthozoans and algae. Even though the available information was limited for many bioregions, our analyses demonstrate some differences in sponge traits and functions among bioregions, and among macroregions. However, we also identified similarities in sponge assemblage structure and function at global scales, likely reflecting a combination of regional‐ and local‐scale biological and physical processes affecting sponge assemblages, along with common ancestry. Fi...

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Section: Global Variation In Sponge Traitsmentioning

confidence: 99%

Interocean patterns in shallow water sponge assemblage structure and function

et al. 2020

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“…There is a rich history of describing the biodiversity of coral reefs (Connell 1978;Huston 1985), but apart from fishes, corals, and macroalgae (Bruno et al 2009), many groups have not prominently featured in coral reef monitoring. There are exceptions to these trends, for example, including the Caribbean echinoid Diadema antillarum (Lessios 2016), the Indo-Pacific asteroid, Acanthaster planci (Moran 1986), macroalgae (McCook et al 2001;Bruno et al 2009), and in a few locations, Caribbean octocorals (Ruzicka et al 2013;Lenz et al 2015), sponges (Stevely et al 2011;Wulff 2006aWulff , 2013Wulff , 2016Rovellini et al 2019), and microbes (Glasl et al 2017). A consequence of the taxonomic restriction of most analyses of coral reefs is a limited ability to place present-day reef communities in an historic context.…”

Section: Introductionmentioning

confidence: 99%

A quarter-century of variation in sponge abundance and community structure on shallow reefs in St. John, US Virgin Islands

2020

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This study tested the hypothesis that sponge assemblages on the reefs of St. John, US Virgin Islands (18.315°N, 64.716°W), changed from 1992 to 2017. Sponges were identified to species or genus in photoquadrats and were quantified at 2-3 y intervals by density, with linear dimensions used to estimate volume as a proxy for biomass. From 1992 to July 2017, overall sponge density (pooled among taxa) increased, although trends varied among the most common species for which density increased (four species), decreased (one species), or showed no linear relationship with time (2 species). Hurricanes Irma and Maria caused a 51% decline in overall sponge density from July to November 2017, with density in November 2017 being 31% lower than in 1992. For the common sponges, densities of 6 declined by 82-100% between July and November 2017, but densities in November 2017 were 13-736% higher than in 1992 for four species, and 47-100% lower than in 1992 for 3 species. Sponge volume did not change linearly between 1992 and November 2017, but it was reduced by 54% following the hurricanes. Multivariate variation over time in benthic community structure was not strongly associated with sponge density alone, although a significant association with rainfall highlighted the potential roles of this environmental factor in directly, or indirectly, mediating changes in community structure. Overall, the mean density of sponges, as well as most of the common sponge species, trended upwards prior to the hurricanes, but these trends reversed following the storms.

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“…For example, during a 10-year study on the Great Barrier Reef, Ramsby et al (2017) reported that the percentage cover of the sponge Cliona orientalis was highly variable most likely due to the influence of fine sediment and macroalgal competition. Similarly, the studies of Carballo et al (2008) and Rovellini et al (2019) showed high temporal variability in sponge assemblages in Mexico and Indonesia, respectively, although both studies also found that the populations of some species are relatively stable or only experience gradual changes, over time. Changes in abundance and percentage cover were gradual for N. chaliniformis and S. vagabunda, although the variability in both abundance and percentage cover was species-specific.…”

Section: Temporal Changesmentioning

confidence: 85%

“…Sponge population abundance often fluctuates considerably over time (Carballo et al, 2008;Ramsby et al, 2017;Rovellini et al, 2019). For example, during a 10-year study on the Great Barrier Reef, Ramsby et al (2017) reported that the percentage cover of the sponge Cliona orientalis was highly variable most likely due to the influence of fine sediment and macroalgal competition.…”

Section: Temporal Changesmentioning

confidence: 99%

“…The temporal variability of sponges has previously been described from the Caribbean (Zea, 1994;Wulff, 2006a), Indo-Pacific (Biggerstaff et al, 2017;Rovellini et al, 2019), tropical Atlantic (Kelmo et al, 2013;de Moraes et al, 2019), Mediterranean (Koopmans & Wijffels, 2008;Di Camillo et al, 2012) and Great Barrier Reef (Ramsby et al, 2017), but there have been no studies from the Indian Ocean. From these earlier studies, multiple biotic and abiotic factors, including macroalgal competition (Ávila et al, 2015;Ramsby et al, 2017), seawater temperature (Carballo et al, 2008;Kelmo et al, 2013), salinity (Corriero et al, 2007;Longo et al, 2015) and cyanobacterial blooms (Butler et al, 1995;Stevely et al, 2010), have been reported to correlate with sponge temporal variability.…”

Section: Introductionmentioning

confidence: 99%

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Effects of elevated temperature and eutrophication on tropical lagoon sponges

Beepat¹

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Coastal lagoons are important, but fragile ecosystems, which host diverse biological assemblages. However, these ecosystems are becoming increasingly exposed to anthropogenic stressors such as ocean warming and eutrophication. Sponges are important suspension feeders and are often important components of coastal lagoon communities. However, the impacts of anthropogenic stressors on lagoon-inhabiting sponges are poorly understood. This thesis examines the effects of elevated temperature and eutrophication on the physiological responses and temporal dynamics of three lagoon-inhabiting sponges, Neopetrosia chaliniformis, Amphimedon navalis and Spheciospongia vagabunda from Mauritius (western Indian Ocean). The effects of elevated temperature on A. navalis proteome dynamics and on the bentho-pelagic interactions of S. vagabunda were also explored. In the first data chapter, I conducted a multifactorial experiment to investigate the short-term physiological responses of N. chaliniformis, A. navalis and S. vagabunda exposed to nine combinations of temperature and nitrate treatments for 14 days. Temperature treatments for this experiment were chosen based on the IPCC Representative Concentration Pathways, i.e. RCP6.0 (+2 oC) and RCP8.5 (+4 oC) projected for the year 2100. Nitrate concentrations were increased to approximately two- and three-fold the actual nitrate concentrations in the lagoons where sponges were collected. After 14 days of exposure, the photosynthetic pigment concentrations, and effective quantum yield of the two photosynthetic species (N. chaliniformis and S. vagabunda), as well as the buoyant weight of all species declined significantly. The gross photosynthetic rates and P:R ratios of N. chaliniformis and S. vagabunda also declined significantly, but the respiration rates of all species were significantly higher. The results from this chapter demonstrated that while lagoon-inhabiting sponges are susceptible to short term exposure to elevated temperatures, they are generally tolerant to elevated nitrate concentrations. For my second data chapter, I conducted a four-week thermal tolerance experiment to investigate the physiological tolerance of these three sponges to elevated temperature. I also explored the proteomic responses of A. navalis to elevated temperature. The results showed that the physiology of N. chaliniformis and A. navalis were impacted over time, where after one-week of thermal exposure, both species experienced significant loss in buoyant weight and increases in pumping and holobiont oxygen consumption rates, respectively. In contrast, the bioeroding sponge S. vagabunda experienced an increase in buoyant weight over time and after a thermal exposure of two weeks, the effective quantum yield, pumping and holobiont oxygen consumption rates of this species appeared to stabilize, indicating the possible acclimation of this species to longer thermal exposure. A. navalis proteomic analysis after four weeks revealed significant changes in the expression of 50 proteins, which were mainly involved in oxidative stress, protein transport and cytoskeletal organization. These results demonstrate that medium- or long-term thermal experiments are more indicative of possible species-specificity and acclimation potential in sponges. Moreover, this study also demonstrates that thermal stress responses are also reflected at the proteome level and that a combination of physiology and proteomics can further enhance our understanding of stress mechanisms in sponges. In my third data chapter, I aimed to assess the temporal variability in local distribution area (LDA), abundance and percentage cover of N. chaliniformis, A. navalis and S. vagabunda, respectively over a six- to eight-year period. I also aimed to explore the possible relationship between sea surface temperature (SST) and chlorophyll a (Chl a) concentration (used as a proxy for eutrophication), and temporal variability of these sponges. I found that while the LDA and percentage cover of N. chaliniformis decreased by 40.2% and 14.6%, those of S. vagabunda increased by 135.1% and 23.3%, respectively. No significant changes were observed in A. navalis LDA and percentage cover. A significant decline was seen in the abundance of N. chaliniformis and A. navalis, whereas a significant increase was noted for S. vagabunda abundance. N. chaliniformis and A. navalis abundance declines were likely due to a reduction in lagoonal coral cover, which often act as anchoring substrate for these sponges. The abundance of all species was significantly correlated with SST and Chl a concentration, but the nature of these correlations was species-specific. These results showed that lagoon-inhabiting sponges demonstrate species-specific temporal dynamics, which are mostly driven by changes in seawater temperature. For my final data chapter, I aimed to estimate the bacterial cell consumption, Chl a uptake, net dissolved organic carbon uptake and net inorganic nutrient release of S. vagabunda when exposed to elevated seawater temperature. The results from this chapter indicated that the bacterial cell consumption and S. vagabunda bentho-pelagic interactions with the water column are relatively low compared to other shallow coastal sponges for which data are available. However, under future ocean warming scenarios RCP6.0 (+2 oC) and RCP8.5 (+4 oC), S. vagabunda bacterial cell consumption, net dissolved organic carbon uptake and net inorganic nutrient release would likely increase by 115% and 142%, respectively. These results suggest that thermally tolerant lagoon-inhabiting sponges would likely have an enhanced bentho-pelagic role in future anthropogenically-impacted lagoons, although based on current abundance, S. vagabunda has limited bentho-pelagic interactions with the water column. In summary, the results presented in this thesis demonstrate that the responses of lagoon-inhabiting sponges to elevated temperature are species-specific. While some species are thermally susceptible to elevated temperature, other species such as S. vagabunda may have a potential to acclimate to at least short-term thermal stress. Consequently, thermally-tolerant species could potentially have an increasing bentho-pelagic role in coastal lagoons under future climate change scenarios. The impacts of thermal stress in sponges can also occur at the proteome level, where cellular biological functions such as redox reactions, protein transport and cytoskeletal organization are significantly disrupted. Furthermore, elevated temperature can equally contribute to the temporal variability of some lagoon-inhabiting sponge species. In contrast, this study demonstrated that lagoon-inhabiting sponges are most likely tolerant to eutrophication. Given that sponges are important components of coastal lagoons, it is critically important to assess and incorporate their potential roles to the ecological functioning of anthropogenically-impacted coastal lagoons.

show abstract

Decadal variability in sponge abundance and biodiversity on an Indo-Pacific coral reef

Cited by 19 publications

References 85 publications

Interocean patterns in shallow water sponge assemblage structure and function

Interocean patterns in shallow water sponge assemblage structure and function

A quarter-century of variation in sponge abundance and community structure on shallow reefs in St. John, US Virgin Islands

Effects of elevated temperature and eutrophication on tropical lagoon sponges

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