Research by marine biologists from Wageningen University has shown that feeding on zooplankton by scleractinian corals has been greatly underestimated.
|Caribbean barrel sponges|
|Written by Steven McMurray, M.Sc. and Joseph Pawlik, Ph.D.|
Sponges are an important part of the coral reef ecosystem, and of exceptional beauty. Steven McMurray and Joseph Pawlik discuss Caribbean barrel sponges and the importance of protecting them.
Coral reefs, often described as the ‘rainforests of the sea’ because of their high productivity and species diversity, are probably best known for the vast array of coral and fish species that inhabit them. However, there is a lesser-known but equally important group that inhabits coral reef communities – sponges. In fact, in the Caribbean, the diversity and abundance of coral reef sponges exceeds that of reef-building corals. Our understanding of the ecology of sponges on coral reefs has been hindered by the spectacular variability in color and morphology among sponges, which can make species assignments difficult. But recent efforts by sponge taxonomists, including pictorial keys (e.g., www.spongeguide.org) have made sponge identification easier, and promoted an increasing awareness of the importance of sponges on coral reefs.
Figure 1: Sponges are an abundant and diverse component of coral reefs, especially in the Caribbean (photograph: Steven McMurray).
Functional roles of sponges
Sponges support several key ecological processes on coral reefs. They filter large volumes of seawater and thereby influence the coupling of water-column and benthic processes. Sponge filtration can enhance water clarity and may indirectly affect coral and algal populations that are dependent on light availability. Sponges also serve as habitat to numerous reef organisms, are often the dominant competitors within the benthic community, and may harbor a diverse assemblage of bacteria that can take part in nitrification and carbon fixation (Diaz and Rützler 2001).
Figure 2: Sponges (Phylum Porifera: pore-bearing) filter large volumes of seawater. Scientists are able to measure sponge filtering rates with the use of a fluorescent dye called fluorescein. Injected into the water next to the side of the sponge, the dye is quickly drawn in through thousands of tiny pores (ostia) that cover the outer surface and then expelled through the large exhalent opening (osculum). Scientists film the fluorescein-dyed excurrent seawater and calculate flow rates with video analysis software (photograph: Steven McMurray).
The giant barrel sponge Xestospongia muta
Xestospongia muta is a conspicuous and abundant member of coral reef communities at depths greater than 10 m throughout the Caribbean, with populations of this species occupying greater than 9% of the available substrate on some reefs. Populations of this sponge provide essential habitat for numerous fish and invertebrate species, and the biomass and seawater-filtering capacity of this species exceeds that of any other benthic invertebrate. Individuals are often very large, with heights and diameters in excess of 1 meter. Despite its importance, only recently have scientists been able to address many of the fundamental questions surrounding the life history and ecology of the giant barrel sponge.
Figure 3: The giant barrel sponge Xestospongia muta. Barrel sponges can reach sizes several meters in height and diameter (photograph: Dr. Joseph Pawlik).
Demographic studies focus on the growth, age, population dynamics and population structure of organisms and require repeated and sustained observations over time – a resource-intensive effort that has limited the number of these kind of studies for coral reef species. Long-term monitoring programs have provided scientists with key insights into the dynamics of changing coral populations. Recently, researchers at the University of North Carolina Wilmington have began reporting on the demography of the giant barrel sponge, X. muta after 10 years of monitoring this important species on Florida coral reefs.
"In the Caribbean, the diversity and abundance of coral reef sponges exceeds that of reef-building corals."
Beginning in 1997, researchers established a total of 12 permanent 16 m-diameter circular plots on two reefs and at three depths along the reef tract within the Florida Keys National Marine Sanctuary. Given the amount of work involved and the bottom-time limitations of SCUBA diving at 10-30 m depth, scientists undertook a series of 2-week long ‘missions’ in the Aquarius underwater laboratory operated by the National Oceanic and Atmospheric Administration (NOAA) to establish the deepest transects. Within each plot, each sponge was mapped and given a unique stainless steel tag attached with a plastic cable-tie to a masonry nail driven into the limestone substratum next to the base of the sponge. Once established, twice-yearly monitoring surveys were conducted at all transects using SCUBA diving from surface vessels using compressed air or nitrox.
During each survey, new sponges (recruits) were identified and tagged and each sponge was assessed for condition, bleaching, disease, and mortality. Additionally, each sponge was photographed with a digital camera from above and in profile. A slate displaying the unique tag number of each sponge and a scale marker was also photographed in each digital image. Since 1997, over 650 sponges have been monitored and a library of over 8500 digital images has been amassed.
Figure 4: On reefs throughout the Caribbean, Xestospongia muta is a common member of the community (photograph: Dr. Joseph Pawlik).
In recent decades, coral reef ecosystems have suffered degradation due to the influences of climate change, overfishing, eutrophication, and diseases. Sponges have not been immune to these threats, and evidence suggests that anthropogenic and natural disturbances are affecting sponge populations.
Diseases affecting coral reef sponges have been observed more frequently over the last decade, and monitoring efforts have documented a particularly disturbing disease-like phenomenon affecting barrel sponges termed “sponge orange band” (SOB) (Cowart et al. 2006). SOB appears as a bright orange band that progresses through the sponge, resulting in the complete loss of color, tissue disintegration and sponge mortality – a process termed ‘fatal bleaching’. After symptoms of SOB appear, most sponges die within 6 weeks. SOB generally affects only a small fraction (<1%) of the overall sponge population in a given year, however large outbreaks have been observed. Interestingly, large sponges have been observed to be primarily affected. Because water filtration increases with sponge size, large sponges may have a greater chance of contacting potential pathogens in the water column compared to small sponges. Alternatively, the rapid mortality of affected sponges may bias observations in favor of larger sponges. If diseases of sponges similar to SOB are becoming more prevalent, profound changes in the age structure of long-lived coral reef sponges such as X. muta are predicted. Scientists are currently investigating SOB to better understand its causes.
Figure 5: Sponge orange band (SOB). Sponges with SOB develop a distinct orange band along a zone of healthy and dead tissue. As SOB spreads across the sponge, fatal bleaching results in the complete loss of color, tissue disintegration and sponge mortality. Fatally bleached sponges are vigorously consumed by coral reef fishes (photograph: Steven McMurray).
In addition, barrel sponges are particularly vulnerable to damage and mortality from severe storms, vessel groundings, and the cutting movements of anchors, chain, rope, monofilament line, netting, and other marine debris. After storm events, detached sponges are commonly found, still alive and intact, between reef spurs on sand or rubble where they slowly erode under the action of oscillating currents. Until recently, however, suitable methods for sponge reattachment did not exist and large sponges were generally excluded from restoration efforts.
Figure 6: Diver holding a giant barrel sponge that was detached from the substratum by marine debris dragged during a storm event (photograph: Steven McMurray).
Unlike some small, fast-growing reef sponges, barrel sponges, which may exceed 100 years of age (see below), are unable to reattach to the substratum when dislodged. However, a recently developed technique for the reattachment of large sponges offers coral reef managers a novel conservation tool for restoration efforts (McMurray and Pawlik 2009). The technique was originally designed to keep barrel sponges stationary for manipulative experiments; however, it was discovered that some sponges had reattached to the substratum after only 6 months. Sponges were detached from the substratum using long knives and transplanted to both a shallow and deep site. At each site, sponges were skewered with two stainless steel threaded rods that were then attached to sponge holders composed of concrete, plastic mesh, and slotted plastic pipes and secured to the substratum. The transplanted sponges were monitored for up to 3 years to see if they had re-attached to the ocean floor. Despite an unusually rigorous test period that included four hurricanes, the reattachment technique proved successful. Ninety percent of deep and thirty-five percent of shallow transplants survived, with nearly eighty percent reattaching to the substratum. After reattachment, the apparatus was removed and small wounds left from removal of the rods quickly healed. The reattachment technique may be generally adapted for other large sponge species in coral reef restoration efforts.
Figure 7: Side and top images of a transplanted giant barrel sponge secured to the substrate with a novel reattachment technique. After reattachment, sponge holders are removed from the sponge (photographs: Steven McMurray).
Many coral reef species, including hard corals, sea whips, and sea anemones, host symbiotic algae ( zooxanthellae) in their tissues. In many cases, the golden-brown symbionts are responsible for the coloration of the host animal. When stressed, the symbiosis can break down, and the host loses coloration as the algae are expelled – a process termed ‘bleaching’. Bleaching is best known to affect reef-building corals and has attracted significant attention since reports of large-scale bleaching events first appeared in the 1980’s. Bleaching is not limited to corals, however, and can potentially affect all reef species that harbor photosynthetic symbionts (Glynn 1996). Because of its widespread occurrence across several taxa of reef organisms, it has been suggested that the phenomenon be termed ‘coral reef bleaching’ (Williams and Bunkley-Williams 1990). While intensively studied for reef-building corals, bleaching is poorly understood for other ecologically important reef species.
"Evidence suggests that anthropogenic and natural disturbances are affecting sponge populations."
The characteristic reddish-brown coloration of X. muta is due to cyanobacterial symbionts that live within the peripheral tissues of the sponge. While the majority of sponges that harbor symbionts appear to be unaffected during coral reef bleaching events, giant barrel sponges have commonly been reported to bleach. Long-term monitoring has revealed that barrel sponges undergo cycles of bleaching and recovery of pigmentation. Bleaching can be moderate, affecting only localized areas of the sponge, or it can be severe, but rarely results in sponge mortality. This form of “cyclic” bleaching is distinct from the bleaching observed from diseases, such as SOB.
Scientists have found that sponges with symbiotic cyanobacteria appear to fall into one of two general groups– one group includes sponges that rely on their symbionts for much of their nutrition (known as a mutualism, as both the sponge and symbiont benefit from the relationship), and another group includes sponges that do not receive any benefit from their symbionts (known as a commensalism, as the sponge receives no benefit from the relationship while the symbiont does benefit) (Erwin and Thacker 2008). To determine if bleaching is a stressful condition for barrel sponges, researchers used molecular genetic techniques to monitor the production of heat shock proteins (HSPs) – proteins common to all animals, that are produced under stressful conditions – in the tissues of bleached and unbleached barrel sponges. Bleached sponges did not produce HSPs. Therefore, unlike corals, bleaching of barrel sponges is not a sign of stress, but rather a response by cyanobacterial symbionts that has no negative effect on their host sponge (López- Legentil et al. 2008).
Several stressors can cause reef-building corals to bleach, but high water temperatures are the primary agent of widespread bleaching events (Glynn 1996). The occurrence of barrel sponge bleaching during coral bleaching events suggested a similar cause. To investigate this, researchers deployed underwater temperature recorders near permanent sponge monitoring transects and statistically evaluated the relationship between seawater temperature and sponge bleaching over five years.
Bleaching of giant barrel sponges was found to be greater in the fall compared to the spring, and greater at deep compared to shallow sites. A correlation between anomalous seawater temperatures and bleaching of barrel sponges was only found at the deepest site, contrary to the expectations, but further work is needed to determine whether temperature variations cause bleaching of barrel sponges. It may be that, as in the coral-zooxanthellae symbiosis, different strains of cyanobacteria harbored by sponges have different tolerances to environmental stressors such as high water temperatures. Moreover, available evidence suggests that cyanobacterial abundance in the tissue of barrel sponges is dependent on light intensity, which may explain why bleaching is greater at depth.
Figure 8: Bleaching of X. muta. Unlike disease-related bleaching (SOB), this form of “cyclic” bleaching does not appear to harm the sponge, and the normal color generally reappears after a few months (photograph: Dr. Susanna López-Legentil).
The structure of Caribbean coral reef communities has been altered by both human-made and natural stressors. For example, many reefs have experienced dramatic reductions in coral cover since the 1980s and some reefs have experienced increases in the cover of macro algae. Little is known, however, about the demographics of sponges on coral reefs, despite their abundance and the important functions they perform.
By tracking the total number, mortality, and addition of new recruits to the population of barrel sponges in plots on reefs off the Florida Keys, researchers have been able to study the population dynamics of this important coral reef sponge (McMurray et al. 2009). In contrast to the dramatic decline of coral populations on Florida reefs, the number of barrel sponges have increased significantly since 2000 – by almost 50%! Further, population models indicate that populations will continue to increase. Large pulses of new recruits and high sponge survival were found to fuel the population increases. It may be that the decline of reef-building corals has provided more space on the reef for sponges to colonize.
Barrel sponge population increases may have both positive and negative implications for the Florida coral reef community. More sponges may provide increased reef complexity and habitat for fishes and invertebrates. In addition, increased sponge filtration may increase water clarity, benefitting coral populations that are dependent on light availability. But barrel sponges may also release high concentrations of dissolved inorganic nitrogen that could ‘fertilize’ the reef and promote the growth of macro algae, which compete with corals for space. It has been theorized that the structure of some natural communities can be altered from one stable state to another, with a different set of dominant species, over a relatively short period of time. On coral reefs, this sort of ‘phase shift’ could result from a decrease in reef-building corals and an increase in fast-growing species such as macro algae, zoanthids and sponges. While reef-building corals have declined dramatically throughout the Florida Keys, it remains to be seen whether a phase shift is occurring that includes stable population increases of slower-growing, longer-lived species such as X. muta.
While barrel sponge populations are currently increasing on Florida’s reefs, it is not clear that this will continue. Demographic analyses revealed that changes in the mortality rates of the largest sponges have the greatest potential to negatively affect sponge populations. This is disturbing because large sponges appear to be particularly vulnerable to SOB. The largest sponges account for the greatest proportion of overall population biomass and space occupation on the reef. Large sponges also constitute the greatest source of reproductive potential for new sponges to colonize the reef. Therefore, it may be necessary to enact conservation measures for large barrel sponges (McMurray and Pawlik 2009).
Figure 9: The giant barrel sponge is an important component of coral reef communities, even in areas where corals are not abundant. (photograph: Steven McMurray).
Redwood of the reef
The way in which most kinds of animals grow has been well understood for a long time, but sponges have remained a notable exception. While Xestospongia muta had earned the nickname “redwood of the reef” because of its large size, the presumed great age of this species was only the subject of conjecture. Studies of sponge growth rates have been particularly challenging because sponges have highly variable shapes and sizes and lack structures that accrete regularly so as to indicate age (e.g. tree rings).
"The largest barrel sponges on Caribbean reefs are over 2000 years old."
As part of the demographic study of X. muta, a time-series of digital images of hundreds of sponges was collected throughout the monitoring period. By comparing the sizes of sponges in digital images over time, growth rates were obtained. Field measurements were used to validate the accuracy of the technique. Sponge size data was then fit to sophisticated growth models that allowed estimates of sponge age from size measurements (McMurray et al. 2008).
Results of the growth studies have been surprising. Barrel sponges exhibit variable growth rates, retain the ability to grow throughout their life (a phenomenon known as indeterminate growth), and some sponges decrease in size over short time intervals. As sponges grew larger, growth rate decreased, and sponges changed from cone- to barrel-shaped.
Most remarkable was the age estimates obtained for the largest sponges. Oil drum-sized sponges were found to be 100-200 years old, while photograph estimates of the very largest barrel sponges on Caribbean reefs make them over 2000 years old! These findings place barrel sponges among the longest-lived animals on earth and on par with the oldest known specimens of the redwood tree, Sequoia sempervirens. Considering their large size and great age, “redwood of the reef” is an apt designation for X. muta.
Cowart, J.D., Henkel, T.P., McMurray, S.E. and Pawlik, J.R. 2006. Sponge orange band (SOB): a pathogenic-like condition of the giant barrel sponge, Xestospongia muta. Coral Reefs 25: 513.
Diaz, M.C. and Rutzler, K. 2001. Sponges: an essential component of Caribbean coral reefs. Bulletin of Marine Science 69: 535-546.
Erwin, P.M. and Thacker, R.W. 2008. Cryptic diversity of the symbiotic cyanobacterium Synechococcus spongaiarum among sponge hosts. Molecular Ecology 17: 2937- 2947.
López-Legentil, S., Song, B.K., McMurray, S.E. and Pawlik, J.R. 2008. Bleaching and stress in coral reef ecosystems: hsp70 expression by the giant barrel sponge Xestospongia muta. Molecular Ecology 17: 1840-1849.
McMurray, S.E. Blum, J.E. and Pawlik, J.R. 2008. Redwood of the reef: growth and age of the giant barrel sponge Xestospongia muta in the Florida Keys. Marine Biology 155: 159-171.
McMurray, S.E., Henkel, T.P. and Pawlik, J.R. 2009. Demographics of increasing populations of the giant barrel sponge Xestospongia muta in the Florida Keys. Ecology in press.
McMurray, S.E. and Pawlik, J.R. 2009. A novel technique for the reattachment of large coral reef sponges. Restoration Ecology 17: 192-195.
Williams, E.H. and Bunkely-Williams, L. 1988. Bleaching of coral reef animals in 1987- 1988: an updated summary. In: Ogden, J. and Wicklund, R. (eds) Mass bleaching of coral reefs in the Caribbean: a research strategy. National Undersea Research Program, Research Report 88-2, 51pp.