Millennial-scale change in the structure of a Caribbean reef ecosystem and the role of human and natural disturbance

Caribbean coral reefs have transformed into algal-dominated habitats over the past half-century, but the role of specific anthropogenic drivers is unresolved due to the lack of ecosystem-level data predating human disturbance. To better understand the extent and causes of long-term Caribbean reef declines, we produced a continuous 3000-yr record of the ecosystem state of three reefs in Bocas del Toro, Caribbean Panama. From fossils and sediments obtained from reef matrix cores, we tracked changes in reef accretion rates and the taxonomic and functional group composition of fish, coral, urchin, bivalve and benthic foraminifera. This dataset provided a comprehensive picture of reef community and environmental change. At all sites, reefs shifted from systems with greater relative abundance of herbivorous fish, epifaunal suspension feeding bivalves and Diadema urchins to systems with greater relative abundance of micropredator fish, infaunal bivalves and Echinometra urchins. These transitions were initiated a millennium ago at two less-degraded reefs fringing offshore islands and ~250 yr ago at a degraded patch reef near the continental coast. Ecosystem shifts were accompanied by a decline in reef accretion rates, and at the patch reef, a decline in water quality since the 18th century. Within all cores, synchronous increases in infaunal bivalves and declines in herbivorous fish regardless of water quality suggest a loss of hard substrate and increasingly hypoxic sediment conditions related to herbivore loss. While the early timing of ecosystem transitions at the fringing reefs implicates large-scale hydrological change, the more recent timing of change and loss of water quality at the patch reef implicates terrigenous runoff from land-clearing. Our whole-ecosystem reconstruction reveals that reef ecosystem deterioration appears to follow a predictable trajectory whether driven by natural or anthropogenic disturbances and that historical local human activities have quickly unraveled reefs at a scale similar to longer-term natural environmental change.     

The influence of coral reef benthic condition on associated fish assemblages

Accumulative disturbances can erode a coral reef's resilience, often leading to replacement of scleractinian corals by macroalgae or other non-coral organisms. These degraded reef systems have been mostly described based on changes in the composition of the reef benthos, and there is little understanding of how such changes are influenced by, and in turn influence, other components of the reef ecosystem. This study investigated the spatial variation in benthic communities on fringing reefs around the inner Seychelles islands. Specifically, relationships between benthic composition and the underlying substrata, as well as the associated fish assemblages were assessed. High variability in benthic composition was found among reefs, with a gradient from high coral cover (up to 58%) and high structural complexity to high macroalgae cover (up to 95%) and low structural complexity at the extremes. This gradient was associated with declining species richness of fishes, reduced diversity of fish functional groups, and lower abundance of corallivorous fishes. There were no reciprocal increases in herbivorous fish abundances, and relationships with other fish functional groups and total fish abundance were weak. Reefs grouping at the extremes of complex coral habitats or low-complexity macroalgal habitats displayed markedly different fish communities, with only two species of benthic invertebrate feeding fishes in greater abundance in the macroalgal habitat. These results have negative implications for the continuation of many coral reef ecosystem processes and services if more reefs shift to extreme degraded conditions dominated by macroalgae.     

Direct evaluation of macroalgal removal by herbivorous coral reef fishes

Few studies have examined the relative functional impacts of individual herbivorous fish species on coral reef ecosystem processes in the Indo-Pacific. This study assessed the potential grazing impact of individual species within an inshore herbivorous reef fish assemblage on the central Great Barrier Reef (GBR), by determining which fish species were able to remove particular macroalgal species. Transplanted multiple-choice algal assays and remote stationary underwater digital video cameras were used to quantify the impact of local herbivorous reef fish species on 12 species of macroalgae. Macroalgal removal by the fishes was rapid. Within 3 h of exposure to herbivorous reef fishes there was significant evidence of intense grazing. After 12 h of exposure, 10 of the 12 macroalgal species had decreased to less than 15% of their original mass. Chlorodesmis fastigiata (Chlorophyta) and Galaxaura sp. (Rhodophyta) showed significantly less susceptibility to herbivorous reef fish grazing than all other macroalgae, even after 24 h exposure. Six herbivorous and/or nominally herbivorous reef fish species were identified as the dominant grazers of macroalgae: Siganus doliatus, Siganus canaliculatus, Chlorurus microrhinos, Hipposcarus longiceps, Scarus rivulatus and Pomacanthus sexstriatus. The siganid S. doliatus fed heavily on Hypnea sp., while S. canaliculatus fed intensively on Sargassum sp. Variation in macroalgal susceptibility was not clearly correlated with morphological and/or chemical defenses that have been previously suggested as deterrents against herbivory. Nevertheless, the results stress the potential importance of individual herbivorous reef fish species in removing macroalgae from coral reefs.     

Coverage,Diversity, and Functionality of a High-Latitude Coral Community (Tatsukushi,Shikoku Island,Japan)

Background

Seawater temperature is the main factor restricting shallow-water zooxanthellate coral reefs to low latitudes. As temperatures increase, coral species and perhaps reefs may move into higher-latitude waters, increasing the chances of coral reef ecosystems surviving despite global warming. However, there is a growing need to understand the structure of these high-latitude coral communities in order to analyze their future dynamics and to detect any potential changes.

Methodology/Principal Findings

The high-latitude (32.75°N) community surveyed was located at Tatsukushi, Shikoku Island, Japan. Coral cover was 60±2% and was composed of 73 scleractinian species partitioned into 7 functional groups. Although only 6% of species belonged to the ‘plate-like’ functional group, it was the major contributor to species coverage. This was explained by the dominance of plate-like species such as Acropora hyacinthus and A. solitaryensis. Comparison with historical data suggests a relatively recent colonization/development of A. hyacinthus in this region and a potential increase in coral diversity over the last century. Low coverage of macroalgae (2% of the benthic cover) contrasted with the low abundance of herbivorous fishes, but may be reasonably explained by the high density of sea urchins (12.9±3.3 individuals m⁻²).

Conclusions/Significance

The structure and composition of this benthic community are relatively remarkable for a site where winter temperature can durably fall below the accepted limit for coral reef development. Despite limited functionalities and functional redundancy, the current benthic structure might provide a base upon which a reef could eventually develop, as characterized by opportunistic and pioneer frame-building species. In addition to increasing seawater temperatures, on-going management actions and sea urchin density might also explain the observed state of this community. A focus on such ‘marginal’ communities should be a priority, as they can provide important insights into how tropical corals might cope with environmental changes.     

Herbivorous fish assemblages and herbivory pressure on Laamu Atoll, Republic of Maldives

While herbivory is recognized as a fundamental process structuring coral reef communities, herbivore assemblages and processes are poorly described for reefs in the Indian Ocean region. We quantified herbivorous fish assemblage structure (abundance and diversity) in Laamu Atoll, Republic of Maldives, in four reef habitat types: faro reef flats, faro reef slopes, inner and outer atoll reef slopes (20 sites in total). Herbivorous fish assemblages, representing a total of 30 species, grouped strongly by habitat type, with the highest absolute abundance observed on faro reef flats and lowest abundance on inside atoll rim reef slopes. Removal of Thalassia seagrass blades by ambient herbivore assemblages was used in a bioassay to assess relative herbivory pressure among four habitat types (eight sites). Also, at one site a choice herbivory assay was performed to assess herbivore preference among four benthic plants across three depth zones. Relative herbivory, as indicated by Thalassia assays, was highest on inside atoll rim reef slopes and lowest on outside atoll rim reef slopes. Thalassia consumption did not correspond to overall herbivorous fish abundance, but corresponded more closely with parrotfish abundance. In the choice assays, herbivores showed strong preferences among plant types and consumption of most plant types was higher at mid-depth than in the shallow reef flat or deep reef knoll zones.     

Reduced Diversity and High Sponge Abundance on a Sedimented Indo-Pacific Reef System: Implications for Future Changes in Environmental Quality

Although coral reef health across the globe is declining as a result of anthropogenic impacts, relatively little is known of how environmental variability influences reef organisms other than corals and fish. Sponges are an important component of coral reef fauna that perform many important functional roles and changes in their abundance and diversity as a result of environmental change has the potential to affect overall reef ecosystem functioning. In this study, we examined patterns of sponge biodiversity and abundance across a range of environments to assess the potential key drivers of differences in benthic community structure. We found that sponge assemblages were significantly different across the study sites, but were dominated by one species Lamellodysidea herbacea (42% of all sponges patches recorded) and that the differential rate of sediment deposition was the most important variable driving differences in abundance patterns. Lamellodysidea herbacea abundance was positively associated with sedimentation rates, while total sponge abundance excluding Lamellodysidea herbacea was negatively associated with rates of sedimentation. Overall variation in sponge assemblage composition was correlated with a number of variables although each variable explained only a small amount of the overall variation. Although sponge abundance remained similar across environments, diversity was negatively affected by sedimentation, with the most sedimented sites being dominated by a single sponge species. Our study shows how some sponge species are able to tolerate high levels of sediment and that any transition of coral reefs to more sedimented states may result in a shift to a low diversity sponge dominated system, which is likely to have subsequent effects on ecosystem functioning.     

Impact of Herbivore Identity on Algal Succession and Coral Growth on a Caribbean Reef

Background

Herbivory is an important top-down force on coral reefs that regulates macroalgal abundance, mediates competitive interactions between macroalgae and corals, and provides resilience following disturbances such as hurricanes and coral bleaching. However, reductions in herbivore diversity and abundance via disease or over-fishing may harm corals directly and may indirectly increase coral susceptibility to other disturbances.

Methodology and Principal Findings

In two experiments over two years, we enclosed equivalent densities and masses of either single-species or mixed-species of herbivorous fishes in replicate, 4 m² cages at a depth of 17 m on a reef in the Florida Keys, USA to evaluate the effects of herbivore identity and species richness on colonization and development of macroalgal communities and the cascading effects of algae on coral growth. In Year 1, we used the redband parrotfish (Sparisoma aurofrenatum) and the ocean surgeonfish (Acanthurus bahianus); in Year 2, we used the redband parrotfish and the princess parrotfish (Scarus taeniopterus). On new substrates, rapid grazing by ocean surgeonfish and princess parrotfish kept communities in an early successional stage dominated by short, filamentous algae and crustose coralline algae that did not suppress coral growth. In contrast, feeding by redband parrotfish allowed an accumulation of tall filaments and later successional macroalgae that suppressed coral growth. These patterns contrast with patterns from established communities not undergoing primary succession; on established substrates redband parrotfish significantly reduced upright macroalgal cover while ocean surgeonfish and princess parrotfish allowed significant increases in late successional macroalgae.

Significance

This study further highlights the importance of biodiversity in affecting ecosystem function in that different species of herbivorous fishes had very different impacts on reef communities depending on the developmental stage of the community. The species-specific effects of herbivorous fishes suggest that a species-rich herbivore fauna can be critical in providing the resilience that reefs need for recovery from common disturbances such as coral bleaching and storm damage.     

Predicting spatially explicit coral reef fish abundance, richness and Shannon–Weaver index from habitat characteristics

The assessment of biodiversity in coral reefs requires the application of geographic information systems (GIS), remote sensing and analytical tools in order to make cost-effective spatially explicit predictions of biodiversity over large geographic areas. Here we present a spatially explicit prediction for coral reef fish diversity index, as well as habitat classification according to reef fish diversity index values in Chinchorro Bank Biosphere Reserve, one of the most important plain/atoll type reef systems in the Caribbean. We have used extensive ecological data on depth, fish and habitat characteristics to perform such prediction. Fish species assemblages and different biotic variables of benthic organisms were characterized using visual censuses and video-transects, respectively at 119 sampling stations. The information was integrated in a GIS, along with satellite imagery (LANSDAT 7 ETM+) and a digital bathymetric model. From the recorded data and a hierarchical classification procedure, we obtained nine different classes of habitats. We used a generalized regression analysis and spatial prediction methodology to create predictive maps (GIS layers) of the different reef benthic components, and a second modeling run produced predictive maps of coral reef fish diversity index. Predictive accuracy of the diversity index map presented a good correlation coefficient (r = 0.87), with maximum diversity index values en reefscapes composed of aggregation of coral colonies with seagrass beds. The implementation of our application was successful for the prediction of fish diversity hot spots and surrogate habitats.     

Coexistence of Low Coral Cover and High Fish Biomass at Farquhar Atoll,Seychelles

We report a reef ecosystem where corals may have lost their role as major reef engineering species but fish biomass and assemblage structure is comparable to unfished reefs elsewhere around the world. This scenario is based on an extensive assessment of the coral reefs of Farquhar Atoll, the most southern of the Seychelles Islands. Coral cover and overall benthic community condition at Farquhar was poor, likely due to a combination of limited habitat, localized upwelling, past coral bleaching, and cyclones. Farquhar Atoll harbors a relatively intact reef fish assemblage with very large biomass (3.2 t ha⁻¹) reflecting natural ecological processes that are not influenced by fishing or other local anthropogenic factors. The most striking feature of the reef fish assemblage is the dominance by large groupers, snappers, and jacks with large (>1 m) potato cod (Epinephelus tukula) and marbled grouper (E. polyphekadion), commonly observed at many locations. Napoleon wrasse (Cheilinus undulatus) and bumphead parrotfish (Bolbometopon muricatum) are listed as endangered and vulnerable, respectively, but were frequently encountered at Farquhar. The high abundance and large sizes of parrotfishes at Farquhar also appears to regulate macroalgal abundance and enhance the dominance of crustose corallines, which are a necessary condition for maintenance of healthy reef communities. Overall fish biomass and biomass of large predators at Farquhar are substantially higher than other areas within the Seychelles, and are some of the highest recorded in the Indian Ocean. Remote islands like Farquhar Atoll with low human populations and limited fishing pressure offer ideal opportunities for understanding whether reefs can be resilient from global threats if local threats are minimized.     

永兴岛附近海域珊瑚礁鱼类群落结构特征

为更好地保护和管理西沙永兴岛附近海域珊瑚礁鱼类,于2020—2021年对永兴岛上岸渔获物进行了调查研究,分析了鱼类群落结构组成及其变化和演替特征。结果表明:调查共发现永兴岛附近海域珊瑚礁鱼类101种,隶属于5目21科,以鲈形目鱼类最多,占总种类的84.16%,生物量超总渔获物的90%;科级水平鹦嘴鱼科鱼类最多,达21种,生物量超总渔获物的45%。28种珊瑚礁鱼类是永兴岛附近海域主要捕捞对象,占总渔获物的80%以上。永兴岛附近海域珊瑚礁鱼类呈现过度捕捞,一是主要渔获物中的中大型鱼类均重偏小;二是本海域个体体型最大的鱼类出现较多消亡;三是肉食性鱼类大量消亡;四是植食性鱼类生物量占比超过了肉食性鱼类。永兴岛附近海域珊瑚礁鱼类已经演替到以植食性鱼类为主导的生态系统;大量海胆的出现,表明了这一珊瑚礁生态系统在进一步衰退,向以海胆为主导的生态系统演变。保护西沙永兴岛附近海域珊瑚礁鱼类已经刻不容缓,需要严格地控制本海域的捕捞强度。     

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.     

Coral–algal phase shifts alter fish communities and reduce fisheries production

Anthropogenic stress has been shown to reduce coral coverage in ecosystems all over the world. A phase shift towards an algae‐dominated system may accompany coral loss. In this case, the composition of the reef‐associated fish assemblage will change and human communities relying on reef fisheries for income and food security may be negatively impacted. We present a case study based on the Raja Ampat Archipelago in Eastern Indonesia. Using a dynamic food web model, we simulate the loss of coral reefs with accompanied transition towards an algae‐dominated state and quantify the likely change in fish populations and fisheries productivity. One set of simulations represents extreme scenarios, including 100% loss of coral. In this experiment, ecosystem changes are driven by coral loss itself and a degree of habitat dependency by reef fish is assumed. An alternative simulation is presented without assumed habitat dependency, where changes to the ecosystem are driven by historical observations of reef fish communities when coral is lost. The coral–algal phase shift results in reduced biodiversity and ecosystem maturity. Relative increases in the biomass of small‐bodied fish species mean higher productivity on reefs overall, but much reduced landings of traditionally targeted species.     

Hysteresis in coral reefs under macroalgal toxicity and overfishing

Macroalgae and corals compete for the available space in coral reef ecosystems.While herbivorous reef fish play a beneficial role in decreasing the growth of macroalgae, macroalgal toxicity and overfishing of herbivores leads to proliferation of macroalgae. The abundance of macroalgae changes the community structure towards a macroalgae-dominated reef ecosystem. We investigate coral-macroalgal phase shifts by means of a continuous time model in a food chain. Conditions for local asymptotic stability of steady states are derived. It is observed that in the presence of macroalgal toxicity and overfishing, the system exhibits hysteresis through saddle-node bifurcation and transcritical bifurcation. We examine the effects of time lags in the liberation of toxins by macroalgae and the recovery of algal turf in response to grazing of herbivores on macroalgae by performing equilibrium and stability analyses of delay-differential forms of the ODE model. Computer simulations have been carried out to illustrate the different analytical results.

Electronic Supplementary Material

The online version of this article (doi:10.1007/s10867-014-9371-y) contains supplementary material, which is available to authorized users.     

The Eocene fishes of Monte Bolca: the earliest coral reef fish assemblage

The fish assemblage from the Eocene deposits of Monte Bolca, Northern Italy, are compared with those of Recent coral reefs. A family-level taxonomic definition of a Recent coral reef fish assemblage is formulated to permit direct comparisons. On this basis, the Monte Bolca fishes represent the earliest clearly defined coral reef fish assemblage. Quantitative analyses of the relative abundance of fish families revealed significant differences between the two assemblages. The Bolca assemblage has Mesozoic links (Pycnodontiformes) and non-perciform taxa are relatively abundant, particularly the Beryciformes (Holocentridae). However, Bolca represents the earliest record of a perciform-dominated benthic fish assemblage (68.4% of all non-clupeid taxa). Within the Perciformes, the abundance of the major reef fish lineages (higher squamipinnes and Labroidei) differs markedly between the two assemblages. The numerical dominance of labroid fishes on coral reefs appears to have been a relatively recent occurrence.     

Fishery-Independent Data Reveal Negative Effect of Human Population Density on Caribbean Predatory Fish Communities

Background

Understanding the current status of predatory fish communities, and the effects fishing has on them, is vitally important information for management. However, data are often insufficient at region-wide scales to assess the effects of extraction in coral reef ecosystems of developing nations.

Methodology/Principal Findings

Here, I overcome this difficulty by using a publicly accessible, fisheries-independent database to provide a broad scale, comprehensive analysis of human impacts on predatory reef fish communities across the greater Caribbean region. Specifically, this study analyzed presence and diversity of predatory reef fishes over a gradient of human population density. Across the region, as human population density increases, presence of large-bodied fishes declines, and fish communities become dominated by a few smaller-bodied species.

Conclusions/Significance

Complete disappearance of several large-bodied fishes indicates ecological and local extinctions have occurred in some densely populated areas. These findings fill a fundamentally important gap in our knowledge of the ecosystem effects of artisanal fisheries in developing nations, and provide support for multiple approaches to data collection where they are commonly unavailable.     

Structure of Caribbean coral reef communities across a large gradient of fish biomass

The collapse of Caribbean coral reefs has been attributed in part to historic overfishing, but whether fish assemblages can recover and how such recovery might affect the benthic reef community has not been tested across appropriate scales. We surveyed the biomass of reef communities across a range in fish abundance from 14 to 593 g m⁻², a gradient exceeding that of any previously reported for coral reefs. Increased fish biomass was correlated with an increased proportion of apex predators, which were abundant only inside large marine reserves. Increased herbivorous fish biomass was correlated with a decrease in fleshy algal biomass but corals have not yet recovered.     

热带珊瑚礁区海参的生境选择与生态作用

珊瑚礁生态系统是一个高生产力、高生物多样性的特殊海洋生态系统,具有为生物提供栖息地、参与生物地球化学循环、防浪护岸、指示水体污染程度等生态功能。珊瑚礁生态系统的突出特点是其生境异质性很高,各种各样的生境斑块为种类繁多、习性各异的游泳和底栖生物提供栖息场所,这些礁栖生物通过参与各项生态过程而形成各种特定的功能群,共同完成重要的生态功能。在热带珊瑚礁生态系统中,海参是大型底栖动物区系的重要一员。种类繁多的海参具有各自不同的生境选择特征,通过摄食、运动等行为活动发挥着改良底质、促进有机物矿化和营养盐再生等生态作用。近几年来,全球热带海参受人类过度捕捞和珊瑚礁退化的影响而面临资源衰退、物种多样性丧失等问题,深入认识其生态学功能、加强热带海参资源保护迫在眉睫。综述了国内外热带珊瑚礁海参的基础生态学研究进展：海参对珊瑚礁生境斑块呈现显著的偏好选择特征以及种间差异和季节变动,不同生境斑块的食物质量、底质类型和水动力条件是影响海参生境偏好的重要因素;海参通过生物扰动可以改变珊瑚礁生境沉积物的含水量、渗透性、颗粒组成、再矿化率、无机营养物质释放速率以及孔隙水的化学梯度,并增加沉积物中的溶氧浓度、促进溶解...     

Top-heavy trophic structure within benthic viral dark matter

A better understanding of system-specific viral ecology in diverse environments is needed to predict patterns of virus–host trophic structure in the Anthropocene. This study characterised viral-host trophic structure within coral reef benthic cyanobacterial mats—a globally proliferating cause and consequence of coral reef degradation. We employed deep longitudinal multi-omic sequencing to characterise the viral assemblage (ssDNA, dsDNA, and dsRNA viruses) and profile lineage-specific host–virus interactions within benthic cyanobacterial mats sampled from Bonaire, Caribbean Netherlands. We recovered 11,012 unique viral populations spanning at least 10 viral families across the orders Caudovirales, Petitvirales, and Mindivirales. Gene-sharing network analyses provided evidence for extensive genomic novelty of mat viruses from reference and environmental viral sequences. Analysis of coverage ratios of viral sequences and computationally predicted hosts spanning 15 phyla and 21 classes revealed virus–host abundance (from DNA) and activity (from RNA) ratios consistently exceeding 1:1, suggesting a top-heavy intra-mat trophic structure with respect to virus–host interactions. Overall, our article contributes a curated database of viral sequences found in Caribbean coral reef benthic cyanobacterial mats (vMAT database) and provides multiple lines of field-based evidence demonstrating that viruses are active members of mat communities, with broader implications for mat functional ecology and demography.