Steven E. McMurray

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 °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.

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.

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.

Demography alters carbon flux for a dominant benthic suspension feeder, the giant barrel sponge, on Conch Reef, Florida Keys

Summary A challenge to understanding ecosystem processes is that the functional roles of species are linked with the demography of populations. In many systems, and particularly on coral reefs, the dynamics and structure of populations of many functionally important species has significantly changed over recent decades due to a variety of disturbances, and the changes in the ecological processes mediated by them are poorly understood. Benthic suspension feeders are allogenic ecosystem engineers that contribute to the flow of materials and energy in aquatic systems. There is increasing evidence that sponges dominate this functional group on Caribbean reefs. Using demographic data from 2000 to 2012 and measurements of filtration rates of particulate and dissolved organic carbon, we parameterized a stage-based matrix model of population-mediated carbon flux for the Caribbean giant barrel sponge Xestospongia muta on Conch Reef, Florida Keys, to investigate the demographic mechanisms that mediate changes in benthic-pelagic coupling. Population-mediated carbon flux increased over time with increasing sponge density and volume, with the largest individuals making the greatest contribution. Elasticity analysis revealed that the growth of sponges in all stages, the survival of sponges in the two largest stages, and the production of new recruits by the largest sponges had the greatest influence on changes in population-mediated carbon flux. We estimate the mean carbon flux over 2000-2012 for X. muta at Conch Reef was 1575 mg C d-1 m-2, a value that exceeds that of any other single-species rate. Projections indicated that population-mediated carbon flux will continue to increase under present conditions; thus, X. muta is expected to play an even larger role in the transfer of carbon from the water column to the benthos on Caribbean coral reefs. Rather than being fixed, the functional role of species within a community are often dynamic and influenced by the demography of populations. The general framework developed here, a conversion of the basic unit of measurement for population models (i.e. the individual) into quantifiable metrics of species traits or activities, may be more broadly applied by further efforts to examine interrelationships between population and ecosystem processes. This article is protected by copyright. All rights reserved.

Spawning of the basket star Astrophyton muricatum in the Bahamas

Astrophyton muricatum is a nocturnal ophiuroid (order Euryalida) found in reef and seagrass habitats in the western Atlantic and Caribbean (Hendler et al. 1995). On the night of 3 July 2010, we observed broadcast spawning of a single individual of A. muricatum perched, approximately 1 m above the substratum, on a gorgonian (Eunicea sp.) on a patch reef (17 m) off Sweetings Cay (26°33.777 †N, 77°52.890 †W), Grand Bahama Island, Bahamas. When encountered (20:15 h), the individual was in a typical feeding position with arm branches extended and was releasing a cloud of gametes that was dispersed by prevailing currents (Fig. 1a, b, c). While spawning, the individuals arms coiled toward the disk when directly illuminated (Fig. 1b), as is typical of this species (Hendler et al. 1995); arms extended after the light beam was shifted aside, and terminal tendrils ensnared epitokes of syllid polychaetes that were swimming toward the illumination (Fig. 1c). Spawning ceased 5 min after initial observations, and the individual remained in a feeding position. Four individuals of A. muricatum with extended arms were found within 20 m of the spawning individual during and immediately after this event. These individuals coiled their arms when directly illuminated, but were not observed to spawn. This event occurred during a half-moon phase and one week after the full moon; water temperature was 29.5°C. Wolfe (1978) found females of A. muricatum to have large eggs throughout the year, however, little is known about the timing of their spawning. This is the first observation of which we are aware on the spawning of Euryalida in the field (Hendler 1991).