Benthic-pelagic coupling on coral reefs: Feeding and growth of Caribbean sponges

Benthic-pelagic coupling and the role of bottom-up versus top-down processes are recognized as having a major impact on the community structure of intertidal and shallow subtidal marine communities. Bottom-up processes, however, are still viewed as principally affecting the outcome of top-down processes. Sponges on coral reefs are important members of the benthic community and provide a crucial coupling between water-column productivity and the benthos. Other than scleractinian corals, sponges dominate many of these habitats where water column productivity is composed of mostly autotrophic and heterotrophic picoplankton that sponges actively filter. While predation upon sponges by invertebrates, fish, and turtles occurs, the sponges Callyspongia vaginalis, Agelas conifera, and Aplysina fistularis from Florida, Belize, and the Bahamas, respectively, exhibit a consistent and significant pattern of greater biomass, rates of growth, and feeding, as does their food supply, with increasing depth. Sponges consume 65-93% of the available particulate food supply and, at all sites, sponges increase in size and growth rate as depth increases, suggesting that food supply and, therefore, bottom-up processes significantly influence the distribution and abundance of sponges in these habitats.     

Estimating three-dimensional surface areas on coral reefs

One of the main obstacles for biological assessments of coral reefs over large spatial scales is the ability to link data obtained at the laboratory scale to spatially large data sets. This is particularly the case when trying to assess the ecological function of microbial processes following dramatic large-scale events such as mass coral bleaching. To be able to infer ecological function of field corals from laboratory measurement standardised to surface area it is imperative to be able to measure the actual surface area of corals in-situ. There have been several approaches proposed to estimate the three-dimensional surface area of field corals. While these have been shown to be reliable for simple coral growth forms, large degrees of error are introduced when applying them to complex growth forms. This paper refines a technique for calculating the three-dimensional surface area based on the projected surface area, with errors associated with complex growth forms reduced to < 5%. Once developed, the simple mathematical relationship (called the surface index) can be used to estimate the three-dimensional surface area of field corals from photograph or video imagery, allowing physiological parameters of corals determined at the sub-colony scale to whole colony and spatially large data sets of coral reefs. The effectiveness of using laser scanning techniques to derive three-dimensional images of corals is also discussed.     

Aggression among sea urchins on Caribbean coral reefs

The existence and nature of intra- and interspecific aggression were examined for five species of sea urchins inhabiting Caribbean coral reefs. The studies took place in the San Blas Islands of Panama and involved the following species: Echinometra lucunter (Linnaeus), E. viridis Agassiz, Diadema antillarum Phillipi, Lytechinus williamsi Chesher, and Eucidaris tribuloides (Lamarck). An intruder was placed next to an undisturbed resident and the behaviors and responses of both individuals were followed. All pairwise combinations of resident species and intruder species were tested except for combinations involving D. antillarum as intruder.

For E. viridis and E. lucunter, agonistic interactions occurred commonly (46–79% of trials) between conspecifics and congeners. Almost all of the agonistic encounters involved pushing. Additionally, biting occurred in 8–25 % of the trials. Residents were most often the aggressors and usually succeeded in retaining their location. Intruders only succeeded in forcing residents out of their positions if the intruder was equal to or larger in size than the resident. Surveys of an undisturbed population of E. viridis during the daytime indicated that 16% of the individuals were engaged in intraspecific agonistic interactions at any one time.

D. antillarum exhibited biting behavior against both species of Echinometra in 23–24% of the trials. Biting attacks against L. williamsi and E. tribuloides occurred rarely. L. williamsi only once demonstrated pushing behavior and never was observed biting another sea urchin. E. tribuloides occasionally exhibited pushing and biting behaviors, both as residents and as intruders, and was twice observed biting Echinometra.

These studies suggest that two kinds of agonistic interactions may commonly occur among Caribbean reef-dwelling sea urchins: (1) intraspecific and interspecific aggression among Echinometra, and (2) predatory/aggressive attacks against Echinometra by D. antillarum. The former may result in greater dispersion of Echinometra relative to food and shelter resources and control the spatial distribution and concentration of Echinometra grazing pressure within an area. The attacks by D. antillarum may result in the restriction to, or higher densities of, Echinometra in crevices and rugose microhabitats that provide shelter from the larger-bodied D. antillarum.     

Spongivory on Caribbean reefs releases corals from competition with sponges

Competition for space is an important process on tropical coral reefs. Few studies have examined the role sponges play in community structure despite the fact that many sponges are competitively superior to reef-building corals in space acquisition. Surveys conducted throughout the Florida Keys indicated that Chondrilla nucula was involved in about 30% of all coral-sponge interactions; this sponge has also been observed in 40–50% of coral-sponge interactions on other Caribbean reefs. C. nucula is also the top prey item of the Hawksbill turtle, and among the preferred prey of several spongivorous fish. I examined how predation influenced sponge competitive abilities (particularly those of C. nucula), and whether this type of indirect effect had important consequences for community dynamics in the Florida Keys. Exclusion of sponge predators (primarily angelfish) resulted in increased sponge overgrowth, with a subsequent greater loss of coral cover, compared to uncaged pairwise interactions. When caged, the corals Dichocoenia stokesii and Siderastrea sideraea lost significantly greater surface area and number of polyps to the sponge C. nucula compared to uncaged interactions. For caged interactions involving the sponge Ectyoplasia ferox, there was a trend for greater loss of  S. sideraea surface area and polyps compared to uncaged interactions. Predation had a greater affect on C. nucula than on any of the other sponges examined. Predator exclusion experiments performed with naturally occurring coral-sponge interactions demonstrated a significant decrease in total coral cover compared to uncaged controls. It is proposed that indirect effects arising from spongivory (especially consumption of  C. nucula) may have large community consequences. Species diversity on Caribbean reefs may be maintained, at least in part, by spongivores. Received: 28 January 1998 / Accepted: 22 June 1998     

Anthropogenic mortality on coral reefs in Caribbean Panama predates coral disease and bleaching

Caribbean reef corals have declined precipitously since the 1980s due to regional episodes of bleaching, disease and algal overgrowth, but the extent of earlier degradation due to localised historical disturbances such as land clearing and overfishing remains unresolved. We analysed coral and molluscan fossil assemblages from reefs near Bocas del Toro, Panama to construct a timeline of ecological change from the 19th century-present. We report large changes before 1960 in coastal lagoons coincident with extensive deforestation, and after 1960 on offshore reefs. Striking changes include the demise of previously dominant staghorn coral Acropora cervicornis and oyster Dendrostrea frons that lives attached to gorgonians and staghorn corals. Reductions in bivalve size and simplification of gastropod trophic structure further implicate increasing environmental stress on reefs. Our paleoecological data strongly support the hypothesis, from extensive qualitative data, that Caribbean reef degradation predates coral bleaching and disease outbreaks linked to anthropogenic climate change.     

The effect of fishing on hysteresis in Caribbean coral reefs

Coral resilience is important for withstanding ecological disturbances as well as anthropogenic changes to the environment. However, the last several decades have demonstrated a decline in resilience that has often resulted in phase shifts to a degraded coral-depleted state with high levels of algal abundance. A major defining issue in current research is to identify when and how it is possible to reverse these phase shifts allowing for the ecosystem to escape coral depletion and maintain coral-based ecosystem services. We extend an analytic model to focus on the effects of over-harvesting of herbivorous reef fish in the Caribbean by explicitly including grazer dynamics which introduces feedbacks between habitat and grazer abundance posing constraints on management options excluded in previous studies. This allows us to develop ecosystem-based management recommendations for two distinct scenarios of coral reef recovery: The first follows significant habitat damage in response to a large disturbance and the second maintains reef structure but has suffered from events such as coral bleaching. We identify critical fishing effort levels to allow for coral recovery and demonstrate that regions exhibiting severe damage to reef structure have little resilience implying that fishing reductions should be coupled with other restoration methods. Regions that are coral-depleted but maintain reef structure allow for recovery given sufficiently small levels of fishing mortality. However, we demonstrate the difference in recovery time in response to varying levels of control efforts on fishing.     

White-band disease and the changing face of Caribbean coral reefs

In recent decades, the cover of fleshy macroalgae has increased and coral cover has decreased on most Caribbean reefs. Coral mortality precipitated this transition, and the accumulation of macroalgal biomass has been enhanced by decreased herbivory and increased nutrient input. Populations of Acropora palmata (elkhorn coral) and A. cervicornis (staghorn coral), two of the most important framework-building species, have died throughout the Caribbean, substantially reducing coral cover and providing substratum for algal growth. Hurricanes have devastated local populations of Acropora spp. over the past 20–25 years, but white-band disease, a putative bacterial syndrome specific to the genus Acropora, has been a more significant source of mortality over large areas of the Caribbean region.Paleontological data suggest that the regional Acropora kill is without precedent in the late Holocene. In Belize, A. cervicornis was the primary ecological and geological constituent of reefs in the central shelf lagoon until the mid-1980s. After constructing reef framework for thousands of years, A. cervicornis was virtually eliminated from the area over a ten-year period. Evidence from other parts of the Caribbean supports the hypothesis of continuous Holocene accumulation and recent mass mortality of Acropora spp. Prospects are poor for the rapid recovery of A. cervicornis, because its reproductive strategy emphasizes asexual fragmentation at the expense of dispersive sexual reproduction. A. palmata also relies on fragmentation, but this species has a higher rate of sexual recruitment than A. cervicornis. If the Acropora spp. do not recover, macroalgae will continue to dominate Caribbean reefs, accompanied by increased abundances of brooding corals, particularly Agaricia spp. and Porites spp. The outbreak of white-band disease has been coincident with increased human activity, and the possibility of a causal connection should be further investigated.     

Evaluation of algal regulation by herbivorous fishes on Caribbean coral reefs

The role of herbivorous fishes in maintaining low macroalgal cover was evaluated on coral reefs on several reef sites from Guadeloupe, either protected or not. Grazing by herbivorous fishes was assessed on different algal facies using fish-bite counts. Algal consumption by fish was estimated as well as algal production. Bite counts revealed that herbivorous fishes feed preferentially on algal turf and avoid brown macroalgae. The algal consumption varied between 0.4 and 2.8 g m⁻² days⁻¹ and was higher inside marine protected areas than outside. Comparison with algal production revealed that herbivorous fishes did not succeed in regulating algal growth. The insufficient number of grazers may lead to the dominance of stable assemblages of macroalgae on coral reefs, preventing the recovery of reef into previous coral-dominated ecosystems.     

Phase shifts and the stability of macroalgal communities on Caribbean coral reefs

Caribbean coral reefs are widely thought to exhibit two alternate stable states with one being dominated by coral and the other by macroalgae. However, the observation of linear empirical relationships among grazing, algal cover and coral recruitment has led the existence of alternate stable states to be questioned; are reefs simply exhibiting a continuous phase shift in response to grazing or are the alternate states robust to certain changes in grazing? Here, a model of a Caribbean forereef is used to reconcile the existence of two stable community states with common empirical observations. Coral-depauperate and coral-dominated reef states are predicted to be stable on equilibrial time scales of decades to centuries and their emergence depends on the presence or absence of a bottleneck in coral recruitment, which is determined by threshold levels of grazing intensity and other process variables. Under certain physical and biological conditions, corals can be persistently depleted even while increases in grazing reduce macroalgal cover and enhance coral recruitment; only once levels of recruitment becomes sufficient to overwhelm the population bottleneck will the coral-dominated state begin to emerge. Therefore, modest increases in grazing will not necessarily allow coral populations to recover, whereas large increases, such as those associated with recovery of the urchin Diadema antillarum, are likely to exceed threshold levels of grazing intensity and set a trajectory of coral recovery. The postulated existence of alternate stable states is consistent with field observations of linear relationships between grazing, algal cover and coral recruitment when coral cover is low and algal exclusion when coral cover is high. The term ‘macroalgal dominated’ is potentially misleading because the coral-depauperate state can be associated with various levels of macroalgal cover. The term ‘coral depauperate’ is preferable to ‘macroalgal dominated’ when describing alternate states of Caribbean reefs.     

Caribbean reefs of the Anthropocene: Variance in ecosystem metrics indicates bright spots on coral depauperate reefs

Dramatic coral loss has significantly altered many Caribbean reefs, with potentially important consequences for the ecological functions and ecosystem services provided by reef systems. Many studies examine coral loss and its causes—and often presume a universal decline of ecosystem services with coral loss—rather than evaluating the range of possible outcomes for a diversity of ecosystem functions and services at reefs varying in coral cover. We evaluate 10 key ecosystem metrics, relating to a variety of different reef ecosystem functions and services, on 328 Caribbean reefs varying in coral cover. We focus on the range and variability of these metrics rather than on mean responses. In contrast to a prevailing paradigm, we document high variability for a variety of metrics, and for many the range of outcomes is not related to coral cover. We find numerous “bright spots,” where herbivorous fish biomass, density of large fishes, fishery value, and/or fish species richness are high, despite low coral cover. Although it remains critical to protect and restore corals, understanding variability in ecosystem metrics among low‐coral reefs can facilitate the maintenance of reefs with sustained functions and services as we work to restore degraded systems. This framework can be applied to other ecosystems in the Anthropocene to better understand variance in ecosystem service outcomes and identify where and why bright spots exist.     

A clear human footprint in the coral reefs of the Caribbean

The recent degradation of coral reefs worldwide is increasingly well documented, yet the underlying causes remain debated. In this study, we used a large-scale database on the status of coral reef communities in the Caribbean and analysed it in combination with a comprehensive set of socioeconomic and environmental databases to decouple confounding factors and identify the drivers of change in coral reef communities. Our results indicated that human activities related to agricultural land use, coastal development, overfishing and climate change had created independent and overwhelming responses in fishes, corals and macroalgae. While the effective implementation of marine protected areas (MPAs) increased the biomass of fish populations, coral reef builders and macroalgae followed patterns of change independent of MPAs. However, we also found significant ecological links among all these groups of organisms suggesting that the long-term stability of coral reefs as a whole requires a holistic and regional approach to the control of human-related stressors in addition to the improvement and establishment of new MPAs.     

Flattening of Caribbean coral reefs: region-wide declines in architectural complexity

Coral reefs are rich in biodiversity, in large part because their highly complex architecture provides shelter and resources for a wide range of organisms. Recent rapid declines in hard coral cover have occurred across the Caribbean region, but the concomitant consequences for reef architecture have not been quantified on a large scale to date. We provide, to our knowledge, the first region-wide analysis of changes in reef architectural complexity, using nearly 500 surveys across 200 reefs, between 1969 and 2008. The architectural complexity of Caribbean reefs has declined nonlinearly with the near disappearance of the most complex reefs over the last 40 years. The flattening of Caribbean reefs was apparent by the early 1980s, followed by a period of stasis between 1985 and 1998 and then a resumption of the decline in complexity to the present. Rates of loss are similar on shallow (<6 m), mid-water (6–20 m) and deep (>20 m) reefs and are consistent across all five subregions. The temporal pattern of declining architecture coincides with key events in recent Caribbean ecological history: the loss of structurally complex Acropora corals, the mass mortality of the grazing urchin Diadema antillarum and the 1998 El Nino Southern Oscillation-induced worldwide coral bleaching event. The consistently low estimates of current architectural complexity suggest regional-scale degradation and homogenization of reef structure. The widespread loss of architectural complexity is likely to have serious consequences for reef biodiversity, ecosystem functioning and associated environmental services.     

Facilitation in Caribbean coral reefs: high densities of staghorn coral foster greater coral condition and reef fish composition

Recovery of the threatened staghorn coral (Acropora cervicornis) is posited to play a key role in Caribbean reef resilience. At four Caribbean locations (including one restored and three extant populations), we quantified characteristics of contemporary staghorn coral across increasing conspecific densities, and investigated a hypothesis of facilitation between staghorn coral and reef fishes. High staghorn densities in the Dry Tortugas exhibited significantly less partial mortality, higher branch growth, and supported greater fish abundances compared to lower densities within the same population. In contrast, partial mortality, branch growth, and fish community composition did not vary with staghorn density at the three other study locations where staghorn densities were lower overall. This suggests that density-dependent effects between the coral and fish community may only manifest at high staghorn densities. We then evaluated one facilitative mechanism for such density-dependence, whereby abundant fishes sheltering in dense staghorn aggregations deliver nutrients back to the coral, fueling faster coral growth, thereby creating more fish habitat. Indeed, dense staghorn aggregations within the Dry Tortugas exhibited significantly higher growth rates, tissue nitrogen, and zooxanthellae densities than sparse aggregations. Similarly, higher tissue nitrogen was induced in a macroalgae bioassay outplanted into the same dense and sparse aggregations, confirming greater bioavailability of nutrients at high staghorn densities. Our findings inform staghorn restoration efforts, suggesting that the most effective targets may be higher coral densities than previously thought. These coral-dense aggregations may reap the benefits of positive facilitation between the staghorn and fish community, favoring the growth and survivorship of this threatened species.     

Reciprocal facilitation and non‐linearity maintain habitat engineering on coral reefs

Ecosystem engineers that create habitats facilitate the coexistence of many interacting species. This biotic response to habitat engineering may result in non‐intuitive cascading interactions, potentially including feedbacks to the engineer. Such feedback mechanisms, either positive or negative, may be especially important for the maintenance of biogenic habitats and their community‐wide facilitation. Here, we describe the complex interactions and feedbacks that link marine habitat‐forming engineers, the reef‐building corals, and a group of herbivores, the parrotfishes; the latter preventing the overgrowth of macroalgae, a major competitor of corals. Using density data of eight parrotfish species on a Caribbean reef, we first describe the form of the response of parrotfish abundance to increasing topographic complexity generated by coral growth. Topographic complexity enhanced parrotfish abundance by promoting habitat suitability, but the shape (linear vs asymptotic) and strength of this response varied across species and size. Parrotfish grazing intensity, estimated from data on abundance and species‐, size‐ and life phase‐specific grazing rates also increased with topographic complexity despite an increase in the surface area over which parrotfish graze. Depending on fish species, this functional response was found to be linear or asymptotic. Using a simple analytical model we then explored the effects of topographic complexity and fishing pressure on coral‐algal competition, with particular emphasis on the implications of non‐linearities in the intensity of grazing. Simulations demonstrate that fishing and habitat degradation impair the performance of grazing, but that an asymptotic response of grazing intensity to topographic complexity increases the ecological resilience of coral reefs. Parrotfish and corals are mutually beneficial by creating a loop of positive, indirect feedbacks that maintain their own structure and function: coral growth promotes habitat suitability for parrotfish, concordantly enhancing grazing intensity, which in turn facilitates coral growth by reducing competitive exclusion by macroalgae. We conclude that the resilience of biogenic habitats is enhanced by non‐linear biotic responses to engineering and by the emergence of reciprocal facilitation linking habitat engineering and response organisms.     

Estimating the patch size of larval fishes during colonization on coral reefs

Fish larvae were sampled daily over a period of 14 days using six crest nets spaced at 200 m intervals on a coral reef on the west coast of Moorea Island, French Polynesia, to estimate the extent to which ichthyonekton arriving at one location reflected ichthyonekton arriving at neighbouring areas. Each night, the six crest nets were colonized by larval fishes from the same location.     

Diel ontogenetic shift in parasitic activity in a gnathiid isopod on Caribbean coral reefs

Ontogenetic niche shifts are characteristic of organisms with complex life cycles such as many marine invertebrates. Research has focused primarily on changes in habitat or diet. However, ontogenetic changes can also occur in the temporal pattern of foraging. Gnathiid isopods feed on fish blood throughout their larval stages and are the primary food item for cleaning organisms on coral reefs. At sites in Australia and the Caribbean, gnathiid larvae exhibit size-related differences in diel activity. However, it is unclear whether this is due to interspecific or intraspecific variation in behavior. Fish were deployed in cages near sunset on shallow reefs off St. John, U.S. Virgin Islands and allowed to be infected with larval gnathiids. Larvae collected from fish retrieved near midnight developed into adults, with most developing into females. In contrast, approximately 80% of gnathiids collected after first light developed into second or third stage larvae, and nearly all of the remaining, large, individuals developed into males. Comparison of ITS2 gene regions from individuals collected in emergence traps from the same reefs during the day versus during the night revealed no differences in this highly variable region. Thus, gnathiid larvae at this locality shift their time of activity as they develop, and larvae developing into males remain active over a longer time period than those developing into females.     

Integrating multiple species connectivity and habitat quality into conservation planning for coral reefs

Incorporating connectivity into the design of marine protected areas (MPAs) has met with conceptual, theoretical, and practical challenges, which include: 1) the need to consider connectivity for multiple species with different dispersal abilities, and 2) the role played by variable habitat quality in determining the spatial patterns of connectivity. We propose an innovative approach, combining biophysical modeling with a routinely‐used tool for marine‐reserve design (Marxan), to address both challenges by using ecologically‐informed connectivity parameters. We showed how functional demographic connectivity for four candidate reef‐associated species with varying dispersal abilities and a suite of connectivity metrics weighted by habitat quality can be used to set conservation objectives and inform MPA placement. Overall, the strength of dispersal barriers varied across modeled species and, also across species, we found a lack of spatial concordance of reefs that were high‐quality sources, self‐persistent, and stepping‐stones. Including spatially‐heterogeneous habitat quality made a considerable difference to connectivity patterns, significantly reducing the potential reproductive output from many reefs. We also found that caution is needed in combining connectivity data from modeled species into multi‐species matrices, which do not perform reliably as surrogates for all connectivity metrics of individual species. We then showed that restricting the habitat available for conservation has an inequitable impact on different connectivity objectives and species, with greatest impact on betweenness centrality and long‐distance dispersers. We used Brazilian coral reefs as a case study but our approach is applicable to both marine and terrestrial conservation planning, and offers a holistic way to design functionally‐connected reserves to tackle the complex issues relevant to planning for persistence.