Diversity and abundance of photosynthetic sponges in temperate Western Australia.
ABSTRACT: BACKGROUND: Photosynthetic sponges are important components of reef ecosystems around the world, but are poorly understood. It is often assumed that temperate regions have low diversity and abundance of photosynthetic sponges, but to date no studies have investigated this question. The aim of this study was to compare the percentages of photosynthetic sponges in temperate Western Australia (WA) with previously published data on tropical regions, and to determine the abundance and diversity of these associations in a range of temperate environments. RESULTS: We sampled sponges on 5 m belt transects to determine the percentage of photosynthetic sponges and identified at least one representative of each group of symbionts using 16S rDNA sequencing together with microscopy techniques. Our results demonstrate that photosynthetic sponges are abundant in temperate WA, with an average of 63% of sponge individuals hosting high levels of photosynthetic symbionts and 11% with low to medium levels. These percentages of photosynthetic sponges are comparable to those found on tropical reefs and may have important implications for ecosystem function on temperate reefs in other areas of the world. A diverse range of symbionts sometimes occurred within a small geographic area, including the three "big" cyanobacterial clades, Oscillatoria spongeliae, "Candidatus Synechococcus spongiarum" and Synechocystis species, and it appears that these clades all occur in a wide range of sponges. Additionally, spongin-permeating red algae occurred in at least 7 sponge species. This study provides the first investigation of the molecular phylogeny of rhodophyte symbionts in sponges. CONCLUSION: Photosynthetic sponges are abundant and diverse in temperate WA, with comparable percentages of photosynthetic to non-photosynthetic sponges to tropical zones. It appears that there are three common generalist clades of cyanobacterial symbionts of sponges which occur in a wide range of sponges in a wide range of environmental conditions.
Project description:In 2015/16, a marine heatwave associated with a record El Niño led to the third global mass bleaching event documented to date. This event impacted coral reefs around the world, including in Western Australia (WA), although WA reefs had largely escaped bleaching during previous strong El Niño years. Coral health surveys were conducted during the austral summer of 2016 in four bioregions along the WA coast (~17 degrees of latitude), ranging from tropical to temperate locations. Here we report the first El Niño-related regional-scale mass bleaching event in WA. The heatwave primarily affected the macrotidal Kimberley region in northwest WA (~16°S), where 4.5-9.3 degree heating weeks (DHW) resulted in 56.6-80.6% bleaching, demonstrating that even heat-tolerant corals from naturally extreme, thermally variable reef environments are threatened by heatwaves. Some heat stress (2.4 DHW) and bleaching (<30%) also occurred at Rottnest Island (32°01'S), whereas coral communities at Ningaloo Reef (23°9'S) and Bremer Bay (34°25'S) were not impacted. The only other major mass bleaching in WA occurred during a strong La Niña event in 2010/11 and primarily affected reefs along the central-to-southern coast. This suggests that WA reefs are now at risk of severe bleaching during both El Niño and La Niña years.
Project description:Hosting symbionts provides many eukaryotes with access to the products of microbial metabolism that are crucial for host performance. On tropical coral reefs, many (High Microbial Abundance [HMA]) but not all (Low Microbial Abundance [LMA]) marine sponges host abundant symbiont communities. Although recent research has revealed substantial variation in these sponge-microbe associations (termed holobionts), little is known about the ecological implications of this diversity. We investigated the expansion of diverse sponge species across isotopic niche space by calculating niche size (as standard ellipse area [SEA c ]) and assessing the relative placement of common sponge species in bivariate (? (13)C and ? (15)N) plots. Sponges for this study were collected from the relatively isolated reefs within the Miskito Cays of Honduras. These reefs support diverse communities of HMA and LMA species that together span a gradient of photosymbiont abundance, as revealed by chlorophyll a analysis. HMA sponges occupied unique niche space compared to LMA species, but the placement of some HMA sponges was driven by photosymbiont abundance. In addition, photosymbiont abundance explained a significant portion of the variation in isotope values, suggesting that access to autotrophic metabolism provided by photosymbionts is an important predictor in the location of species within isotopic space. Host identity accounted for over 70% of the variation in isotope values within the Miskito Cays and there was substantial variation in the placement of individual species within isotopic niche space, suggesting that holobiont metabolic diversity may allow taxonomically diverse sponge species to utilize unique sources of nutrients within a reef system. This study provides initial evidence that microbial symbionts allow sponges to expand into novel physiochemical niche space. This expansion may reduce competitive interactions within coral reefs and promote diversification of these communities.
Project description:The giant barrel sponges Xestospongia muta and Xestospongia testudinaria are ubiquitous in tropical reefs of the Atlantic and Pacific Oceans, respectively. They are key species in their respective environments and are hosts to diverse assemblages of bacteria. These two closely related sponges from different oceans provide a unique opportunity to examine the evolution of sponge-associated bacterial communities. Mitochondrial cytochrome oxidase subunit I gene sequences from X. muta and X. testudinaria showed little divergence between the two species. A detailed analysis of the bacterial communities associated with these sponges, comprising over 900 full-length 16S rRNA gene sequences, revealed remarkable similarity in the bacterial communities of the two species. Both sponge-associated communities include sequences found only in the two Xestospongia species, as well as sequences found also in other sponge species and are dominated by three bacterial groups, Chloroflexi, Acidobacteria, and Actinobacteria. While these groups consistently dominate the bacterial communities revealed by 16S rRNA gene-based analysis of sponge-associated bacteria, the depth of sequencing undertaken in this study revealed clades of bacteria specifically associated with each of the two Xestospongia species, and also with the genus Xestospongia, that have not been found associated with other sponge species or other ecosystems. This study, comparing the bacterial communities associated with closely related but geographically distant sponge hosts, gives new insight into the intimate relationships between marine sponges and some of their bacterial symbionts.
Project description:Sponge-associated microbial communities include members from the three domains of life. In the case of bacteria, they are diverse, host specific and different from the surrounding seawater. However, little is known about the diversity and specificity of Eukarya and Archaea living in association with marine sponges. This knowledge gap is even greater regarding sponges from regions other than temperate and tropical environments. In Antarctica, marine sponges are abundant and important members of the benthos, structuring the Antarctic marine ecosystem. In this study, we used high throughput ribosomal gene sequencing to investigate the three-domain diversity and community composition from eight different Antarctic sponges. Taxonomic identification reveals that they belong to families Acarnidae, Chalinidae, Hymedesmiidae, Hymeniacidonidae, Leucettidae, Microcionidae, and Myxillidae. Our study indicates that there are different diversity and similarity patterns between bacterial/archaeal and eukaryote microbial symbionts from these Antarctic marine sponges, indicating inherent differences in how organisms from different domains establish symbiotic relationships. In general, when considering diversity indices and number of phyla detected, sponge-associated communities are more diverse than the planktonic communities. We conclude that three-domain microbial communities from Antarctic sponges are different from surrounding planktonic communities, expanding previous observations for Bacteria and including the Antarctic environment. Furthermore, we reveal differences in the composition of the sponge associated bacterial assemblages between Antarctic and tropical-temperate environments and the presence of a highly complex microbial eukaryote community, suggesting a particular signature for Antarctic sponges, different to that reported from other ecosystems.
Project description:The impact of temperature on photo-symbiotic relationships has been highly studied in the tropical reef-forming corals but overlooked in less charismatic groups such as solar-powered sacoglossan sea slugs. These organisms display one of the most puzzling symbiotic features observed in the animal kingdom, i.e., their mollusk-plastid association, which enables them to retain photosynthetic active chloroplasts (i.e., kleptoplasts) retrieved from their algae feed sources. Here we analyze the impact of thermal stress (+4°C) and high pCO2 conditions (?pH = 0.4) in survival, photophysiology (i.e., bleaching, photosynthetic efficiency, and metabolism) and stress defense mechanisms (i.e., heat shock and antioxidant response) of solar-powered sacoglossan sea slugs, from tropical (Elysia crispata) and temperate (E. viridis) environments. High temperature was the main factor affecting the survival of both species, while pH only affected the survival of the temperate model. The photobiology of E. viridis remained stable under the combined scenario, while photoinhibition was observed for E. crispata under high temperature and high pCO2. In fact, bleaching was observed within all tropical specimens exposed to warming (but not in the temperate ones), which constitutes the first report where the incidence of bleaching in tropical animals hosting photosynthetic symbionts, other than corals, occurs. Yet, the expulsion of kleptoplasts by the tropical sea slug, allied with metabolic depression, constituted a physiological response that did not imply signs of vulnerability (i.e., mortality) in the host itself. Although the temperate species revealed greater heat shock and antioxidant enzyme response to environmental stress, we argue that the tropical (stenotherm) sea slug species may display a greater scope for acclimatization than the temperate (eurytherm) sea slug. E. crispata may exhibit increased capacity for phenotypic plasticity by increasing fitness in a much narrower thermal niche (minimizing maintenance costs), which ultimately may allow to face severe environmental conditions more effectively than its temperate generalist counterpart (E. viridis).
Project description:Ocean warming is driving species poleward, causing a 'tropicalization' of temperate ecosystems around the world. Increasing abundances of tropical herbivores on temperate reefs could accelerate declines in habitat-forming seaweeds with devastating consequences for these important marine ecosystems. Here we document an expansion of rabbitfish (Siganus fuscescens), a tropical herbivore, on temperate reefs in Western Australia following a marine heatwave and demonstrate their impact on local kelp forests (Ecklonia radiata). Before the heatwave there were no rabbitfish and low rates of kelp herbivory but after the heatwave rabbitfish were common at most reefs and consumption of kelp was high. Herbivory increased 30-fold and kelp abundance decreased by 70% at reefs where rabbitfish had established. In contrast, where rabbitfish were absent, kelp abundance and herbivory did not change. Video-analysis confirmed that rabbitfish were the main consumers of kelp, followed by silver drummers (Kyphosus sydneyanus), a temperate herbivore. These results represent a likely indirect effect of the heatwave beyond its acute impacts, and they provide evidence that range-shifting tropical herbivores can contribute to declines in habitat-forming seaweeds within a few years of their establishment.
Project description:The tropicalization of temperate marine ecosystems can lead to increased herbivory rates, reducing the standing stock of seaweeds and potentially causing increases in detritus production. However, long-term studies analysing these processes associated with the persistence of tropical herbivores in temperate reefs are lacking. We assessed the seasonal variation in abundances, macrophyte consumption, feeding modes and defecation rates of the range-extending tropical rabbitfish Siganus fuscescens and the temperate silver drummer Kyphosus sydneyanus and herring cale Olisthops cyanomelas on tropicalized reefs of Western Australia. Rabbitfish overwintered in temperate reefs, consumed more kelp and other macrophytes in all feeding modes, and defecated more during both summer and winter than the temperate herbivores. Herbivory and defecation increased with rabbitfish abundance, but this was dependent on temperature, with higher rates attained by big schools during summer and lower rates in winter. Still, rabbitfish surpassed temperate herbivores, leading to a fivefold acceleration in the transformation of macrophyte standing stock to detritus, a function usually attributed to sea urchins in kelp forests. Our results suggest that further warming and tropicalization will not only increase primary consumption and affect the habitat structure of temperate reefs but also increase detritus production, with the potential to modify energy pathways.
Project description:Climate-driven changes in biotic interactions can profoundly alter ecological communities, particularly when they impact foundation species. In marine systems, changes in herbivory and the consequent loss of dominant habitat forming species can result in dramatic community phase shifts, such as from coral to macroalgal dominance when tropical fish herbivory decreases, and from algal forests to 'barrens' when temperate urchin grazing increases. Here, we propose a novel phase-shift away from macroalgal dominance caused by tropical herbivores extending their range into temperate regions. We argue that this phase shift is facilitated by poleward-flowing boundary currents that are creating ocean warming hotspots around the globe, enabling the range expansion of tropical species and increasing their grazing rates in temperate areas. Overgrazing of temperate macroalgae by tropical herbivorous fishes has already occurred in Japan and the Mediterranean. Emerging evidence suggests similar phenomena are occurring in other temperate regions, with increasing occurrence of tropical fishes on temperate reefs.
Project description:Coral reefs are experiencing increasing anthropogenic impacts that result in substantial declines of reef-building corals and a change of community structure towards other benthic invertebrates or macroalgae. Reefs around Zanzibar are exposed to untreated sewage and runoff from the main city Stonetown. At many of these sites, sponge cover has increased over the last years. Sponges are one of the top spatial competitors on reefs worldwide. Their success is, in part, dependent on their strong chemical defenses against predators, microbial attacks and other sessile benthic competitors. This is the first study that investigates the bioactive properties of sponge species in the Western Indian Ocean region. Crude extracts of the ten most dominant sponge species were assessed for their chemical defenses against 35 bacterial strains (nine known as marine pathogens) using disc diffusion assays and general cytotoxic activities were assessed with brine shrimp lethality assays. The three chemically most active sponge species were additionally tested for their allelopathic properties against the scleractinian coral competitor Porites sp.. The antimicrobial assays revealed that all tested sponge extracts had strong antimicrobial properties and that the majority (80%) of the tested sponges were equally defended against pathogenic and environmental bacterial strains. Additionally, seven out of ten sponge species exhibited cytotoxic activities in the brine shrimp assay. Moreover, we could also show that the three most bioactive sponge species were able to decrease the photosynthetic performance of the coral symbionts and thus were likely to impair the coral physiology.
Project description:Background:Geographical patterns of species diversity are one of the key topics in biogeography and ecology. The effects of biogeographical affinities on the elevational patterns of species diversity have attracted much attention recently, but the factors driving elevational patterns of the percentages of plants with tropical and temperate biogeographical affinities have not been adequately explored. Methods:We first used univariate least squares regressions to evaluate the effects of each predictor on the elevational patterns of the percentages of plant genera with tropical and temperate affinities in Nepal. Then, the lowest corrected Akaike information criterion value was used to find the best-fit models for all possible combinations of the aforementioned predictors. We also conducted partial regression analysis to investigate the relative influences of each predictor in the best-fit model of the percentages of plant genera with tropical and temperate affinities. Results:With the increase of elevation, the percentage of plant genera with tropical affinity significantly decreased, while that of plant genera with temperate affinity increased. The strongest predictor of the percentages of plant genera with tropical affinity in the examined area was the minimum temperature of the coldest month. For the elevational patterns of the percentages of plant genera with temperate affinity, the strongest predictor was the maximum temperature of the warmest month. Compared with mid-domain effects (MDE), climatic factors explained much more of the elevational variation of the percentages of plant genera with tropical and temperate affinities. Discussion:The elevational patterns of the percentages of plant genera with tropical affinities and the factors driving them supported the revision of the freezing-tolerance hypothesis. That is, freezing may filter out plant genera with tropical affinity, resulting in the decrease of their percentages, with winter coldness playing a predominant role. Winter coldness may not only exert filtering effects on plant genera with tropical affinity, but may also regulate the interactions between plant genera with tropical and temperate affinities. The elevational patterns of tropical and temperate plant diversities, and those of their percentages, might be controlled by different factors or mechanisms. Freezing-tolerance and the interactions between plant genera with tropical and temperate affinities regulated by climatic factors played stronger roles than MDE in shaping the elevational patterns of the percentages of plant genera with tropical and temperate affinities in Nepal.