Changes in inundation drive carbon dioxide and methane fluxes in a temperate wetland.

Wetlands cycle carbon by being net sinks for carbon dioxide (CO2) and net sources of methane (CH4). Daily and seasonal temporal patterns, dissolved oxygen (DO) availability, inundation status (flooded or dry/partially flooded), water depth, and vegetation can affect the magnitude of carbon uptake or emissions, but the extent and interactive effects of these variables on carbon gas fluxes are poorly understood. We characterized the linkages between carbon fluxes and these environmental and temporal drivers at the Old Woman Creek National Estuarine Research Reserve (OWC), OH. We measured diurnal gas flux patterns in an upstream side channel (called the cove) using chamber measurements at six sites (three vegetated and three non-vegetated). We sampled hourly from 7 AM to 7 PM and monthly from July to October 2022. DO concentrations and water levels were measured monthly. Water inundation status had the most influential effect on carbon fluxes with flooded conditions supporting higher CH4 fluxes (0.39 µmol CH4 m-2 s-1; -1.23 µmol CO2 m-2 s-1) and drier conditions supporting higher CO2 fluxes (0.03 µmol CH4 m-2 s-1; 0.86 µmol CO2 m-2 s-1). When flooded, the wetland was a net CO2 sink; however, it became a source for both CH4 and CO2 when water levels were low. We compared chamber-based gas fluxes from the cove in flooded (July) and dry (August) months to fluxes measured with an eddy covariance tower whose footprint covers flooded portions of the wetland. The diurnal pattern of carbon fluxes at the tower did not vary with changing water levels but remained a CO2 sink and a CH4 source even when the cove where we performed the chamber measurements dried out. These results emphasize the role of inundation status on wetland carbon cycling and highlight the importance of fluctuating hydrologic patterns, especially hydrologic drawdowns, under changing climatic conditions.

The Emerging Ecological and Biogeochemical Importance of Sponges on Coral Reefs.

With the decline of reef-building corals on tropical reefs, sponges have emerged as an important component of changing coral reef ecosystems. Seemingly simple, sponges are highly diverse taxonomically, morphologically, and in terms of their relationships with symbiotic microbes, and they are one of nature's richest sources of novel secondary metabolites. Unlike most other benthic organisms, sponges have the capacity to disrupt boundary flow as they pump large volumes of seawater into the water column. This seawater is chemically transformed as it passes through the sponge body as a consequence of sponge feeding, excretion, and the activities of microbial symbionts, with important effects on carbon and nutrient cycling and on the organisms in the water column and on the adjacent reef. In this review, we critically evaluate developments in the recently dynamic research area of sponge ecology on tropical reefs and provide a perspective for future studies.

Growth estimates of Caribbean reef sponges on a shipwreck using 3D photogrammetry.

The growth rates and ages of many benthic marine organisms are poorly understood, complicating our understanding of ecosystem change. This is particularly true for sponges, which are morphologically diverse and lack indicators of annual growth. In this study, we used emerging technologies to measure volume, surface area, and approximate age of 16 sponge species on the Tibbetts shipwreck off Cayman Brac, Caribbean Sea. Photogrammetry was used to determine the volume of individual sponges on the wreck surface, and a time series of YouTube videos was amassed in order to approximate the greatest possible age of the sponges as 8.74 y. Applying the volume measurements to an existing growth equation for the Caribbean sponge Aiolochroia crassa yielded age estimates of 5.2-10.4 y for the largest individuals of the 16 species. Specific growth rates were then calculated for 7 species from the Tibbetts and 8 species from a second shipwreck (Spiegel Grove, Key Largo, FL). Subsequent growth forecasts from these 15 species corroborate a resource trade-off between growth and the production of chemical defenses. Shipwrecks and other anthropogenic structures can be an important source of demographic information for benthic organisms, provided that certain assumptions about their provenance and history can be met.

Testing the relationship between microbiome composition and flux of carbon and nutrients in Caribbean coral reef sponges.

BACKGROUND: Sponges are important suspension-feeding members of reef communities, with the collective capacity to overturn the entire water column on shallow Caribbean reefs every day. The sponge-loop hypothesis suggests that sponges take up dissolved organic carbon (DOC) and, via assimilation and shedding of cells, return carbon to the reef ecosystem as particulate organic carbon (POC). Sponges host complex microbial communities within their tissues that may play a role in carbon and nutrient cycling within the sponge holobiont. To investigate this relationship, we paired microbial community characterization (16S rRNA analysis, Illumina Mi-Seq platform) with carbon (DOC, POC) and nutrient (PO4, NOx, NH4) flux data (specific filtration rate) for 10 common Caribbean sponge species at two distant sites (Florida Keys vs. Belize, ~ 1203 km apart). RESULTS: Distance-based linear modeling revealed weak relationships overall between symbiont structure and carbon and nutrient flux, suggesting that the observed differences in POC, DOC, PO4, and NOx flux among sponges are not caused by variations in the composition of symbiont communities. In contrast, significant correlations between symbiont structure and NH4 flux occurred consistently across the dataset. Further, several individual symbiont taxa (OTUs) exhibited relative abundances that correlated with NH4 flux, including one OTU affiliated with the ammonia-oxidizing genus Cenarchaeum. CONCLUSIONS: Combined, these results indicate that microbiome structure is uncoupled from sponge carbon cycling and does not explain variation in DOC uptake among Caribbean coral reef sponges. Accordingly, differential DOC assimilation by sponge cells or stable microbiome components may ultimately drive carbon flux in the sponge holobiont.

A review of bottom-up vs. top-down control of sponges on Caribbean fore-reefs: what's old, what's new, and future directions.

Interest in the ecology of sponges on coral reefs has grown in recent years with mounting evidence that sponges are becoming dominant members of reef communities, particularly in the Caribbean. New estimates of water column processing by sponge pumping activities combined with discoveries related to carbon and nutrient cycling have led to novel hypotheses about the role of sponges in reef ecosystem function. Among these developments, a debate has emerged about the relative effects of bottom-up (food availability) and top-down (predation) control on the community of sponges on Caribbean fore-reefs. In this review, we evaluate the impact of the latest findings on the debate, as well as provide new insights based on older citations. Recent studies that employed different research methods have demonstrated that dissolved organic carbon (DOC) and detritus are the principal sources of food for a growing list of sponge species, challenging the idea that the relative availability of living picoplankton is the sole proxy for sponge growth or abundance. New reports have confirmed earlier findings that reef macroalgae release labile DOC available for sponge nutrition. Evidence for top-down control of sponge community structure by fish predation is further supported by gut content studies and historical population estimates of hawksbill turtles, which likely had a much greater impact on relative sponge abundances on Caribbean reefs of the past. Implicit to investigations designed to address the bottom-up vs. top-down debate are appropriate studies of Caribbean fore-reef environments, where benthic communities are relatively homogeneous and terrestrial influences and abiotic effects are minimized. One recent study designed to test both aspects of the debate did so using experiments conducted entirely in shallow lagoonal habitats dominated by mangroves and seagrass beds. The top-down results from this study are reinterpreted as supporting past research demonstrating predator preferences for sponge species that are abundant in these lagoonal habitats, but grazed away in fore-reef habitats. We conclude that sponge communities on Caribbean fore-reefs of the past and present are largely structured by predation, and offer new directions for research, such as determining the environmental conditions under which sponges may be food-limited (e.g., deep sea, lagoonal habitats) and monitoring changes in sponge community structure as populations of hawksbill turtles rebound.

Indirect effects of overfishing on Caribbean reefs: sponges overgrow reef-building corals.

Consumer-mediated indirect effects at the community level are difficult to demonstrate empirically. Here, we show an explicit indirect effect of overfishing on competition between sponges and reef-building corals from surveys of 69 sites across the Caribbean. Leveraging the large-scale, long-term removal of sponge predators, we selected overfished sites where intensive methods, primarily fish-trapping, have been employed for decades or more, and compared them to sites in remote or marine protected areas (MPAs) with variable levels of enforcement. Sponge-eating fishes (angelfishes and parrotfishes) were counted at each site, and the benthos surveyed, with coral colonies scored for interaction with sponges. Overfished sites had >3 fold more overgrowth of corals by sponges, and mean coral contact with sponges was 25.6%, compared with 12.0% at less-fished sites. Greater contact with corals by sponges at overfished sites was mostly by sponge species palatable to sponge predators. Palatable species have faster rates of growth or reproduction than defended sponge species, which instead make metabolically expensive chemical defenses. These results validate the top-down conceptual model of sponge community ecology for Caribbean reefs, as well as provide an unambiguous justification for MPAs to protect threatened reef-building corals. An unanticipated outcome of the benthic survey component of this study was that overfished sites had lower mean macroalgal cover (23.1% vs. 38.1% for less-fished sites), a result that is contrary to prevailing assumptions about seaweed control by herbivorous fishes. Because we did not quantify herbivores for this study, we interpret this result with caution, but suggest that additional large-scale studies comparing intensively overfished and MPA sites are warranted to examine the relative impacts of herbivorous fishes and urchins on Caribbean reefs.

Sizing ocean giants: patterns of intraspecific size variation in marine megafauna.

What are the greatest sizes that the largest marine megafauna obtain? This is a simple question with a difficult and complex answer. Many of the largest-sized species occur in the world's oceans. For many of these, rarity, remoteness, and quite simply the logistics of measuring these giants has made obtaining accurate size measurements difficult. Inaccurate reports of maximum sizes run rampant through the scientific literature and popular media. Moreover, how intraspecific variation in the body sizes of these animals relates to sex, population structure, the environment, and interactions with humans remains underappreciated. Here, we review and analyze body size for 25 ocean giants ranging across the animal kingdom. For each taxon we document body size for the largest known marine species of several clades. We also analyze intraspecific variation and identify the largest known individuals for each species. Where data allows, we analyze spatial and temporal intraspecific size variation. We also provide allometric scaling equations between different size measurements as resources to other researchers. In some cases, the lack of data prevents us from fully examining these topics and instead we specifically highlight these deficiencies and the barriers that exist for data collection. Overall, we found considerable variability in intraspecific size distributions from strongly left- to strongly right-skewed. We provide several allometric equations that allow for estimation of total lengths and weights from more easily obtained measurements. In several cases, we also quantify considerable geographic variation and decreases in size likely attributed to humans.

Sponge communities on Caribbean coral reefs are structured by factors that are top-down, not bottom-up.

Caribbean coral reefs have been transformed in the past few decades with the demise of reef-building corals, and sponges are now the dominant habitat-forming organisms on most reefs. Competing hypotheses propose that sponge communities are controlled primarily by predatory fishes (top-down) or by the availability of picoplankton to suspension-feeding sponges (bottom-up). We tested these hypotheses on Conch Reef, off Key Largo, Florida, by placing sponges inside and outside predator-excluding cages at sites with less and more planktonic food availability (15 m vs. 30 m depth). There was no evidence of a bottom-up effect on the growth of any of 5 sponge species, and 2 of 5 species grew more when caged at the shallow site with lower food abundance. There was, however, a strong effect of predation by fishes on sponge species that lacked chemical defenses. Sponges with chemical defenses grew slower than undefended species, demonstrating a resource trade-off between growth and the production of secondary metabolites. Surveys of the benthic community on Conch Reef similarly did not support a bottom-up effect, with higher sponge cover at the shallower depth. We conclude that the structure of sponge communities on Caribbean coral reefs is primarily top-down, and predict that removal of sponge predators by overfishing will shift communities toward faster-growing, undefended species that better compete for space with threatened reef-building corals.

Demographics of increasing populations of the giant barrel sponge Xestospongia muta in the Florida Keys.

The structure of Caribbean coral reef communities has been altered by numerous anthropogenic and natural stressors. Demographic studies of key functional groups have furthered efforts to describe and understand these changes. Little is known, however, about the demographics of sponges on coral reefs, despite their abundance and the important functions they perform (e.g., increased habitat complexity, water filtration). We have monitored permanent plots on reefs off Key Largo, Florida, USA, to study the demography of a particularly important species, the giant barrel sponge, Xestospongia muta. From 2000 to 2006, population densities of X. muta significantly increased at sites on Conch Reef by a mean of 46% (range = 16-108%) and on Pickles Reef by a mean of 33%. In 2006, densities of X. muta on Conch Reef ranged from 0.134 to 0.277 sponges/m2, and mean sponge volume was 1488 cm3/m2, with the largest size class of sponges constituting 75% of the total volume. Increased population density resulted from a significant increase in the number of sponges in the smallest size class. Recruit survival did not significantly change through time; however, a significant interaction between season and year on recruitment suggests that large recruitment pulses are driving population increases. Mean yearly recruitment rates ranged from 0.011 to 0.025 recruits x m(-2) x yr(-1), with pulses as high as 0.036 recruits/m2. To explore the demographic processes behind the population increase and determine future population growth of X. muta under present reef conditions, a stage-based matrix modeling approach was used. Variable recruitment pulses and mortality events were hypothesized to be large determinants of the demographic patterns observed for X. muta. Elasticity and life table response analysis revealed that survival of individuals in the largest size class has the greatest effect on population growth. Projections indicate that populations of X. muta will continue to increase under present conditions; however population growth may be negatively affected by continued mortality of the largest individuals from a recently described pathogenic syndrome.

Bleaching and stress in coral reef ecosystems: hsp70 expression by the giant barrel sponge Xestospongia muta.

Sponges are a prominent component of coral reef ecosystems. Like reef-building corals, some sponges have been reported to bleach and die. The giant barrel sponge Xestospongia muta is one of the largest and most important components of Caribbean coral reef communities. Tissues of X. muta contain cyanobacterial symbionts of the Synechococcus group. Two types of bleaching have been described: cyclic bleaching, from which sponges recover, and fatal bleaching, which usually results in sponge death. We quantified hsp70 gene expression as an indicator of stress in X. muta undergoing cyclic and fatal bleaching and in response to thermal and salinity variability in both field and laboratory settings. Chlorophyll a content of sponge tissue was estimated to determine whether hsp70 expression was related to cyanobacterial abundance. We found that fatally bleached sponge tissue presented significantly higher hsp70 gene expression, but cyclically bleached tissue did not, yet both cyclic and fatally bleached tissues had lower chlorophyll a concentrations than nonbleached tissue. These results corroborate field observations suggesting that cyclic bleaching is a temporary, nonstressful state, while fatal bleaching causes significant levels of stress, leading to mortality. Our results support the hypothesis that Synechococcus symbionts are commensals that provide no clear advantage to their sponge host. In laboratory experiments, sponge pieces incubated at 30 degrees C exhibited significantly higher hsp70 expression than control pieces after 1.5 h, with sponge mortality after less than 15 h. In contrast, sponges at different salinities were not significantly stressed after the same period of time. Stress associated with increasing seawater temperatures may result in declining sponge populations in coral reef ecosystems.