Branching coral as a macroalgal refuge in a marginal coral reef system

Marginal coral reef systems may provide valuable insights into the nature of ecosystem processes in systems on the trajectory towards a phase shift to an alternate ecosystem state. This study investigates the process of herbivory in a marginal coral reef system in the Keppel Islands at the southern end of the Great Barrier Reef. Branching Acropora coral and the brown macroalga Lobophora variegata occupied up to 95% of the reef crest substratum at the three surveyed reefs. Feeding rates of herbivorous fishes and removal rates of Lobophora were directly quantified within areas of branching Acropora and on planar surfaces. Feeding rates by herbivorous fishes were habitat dependent with the highest bite rates being found in planar habitats for both Lobophora and the epilithic algal matrix (EAM) by 1–2 orders of magnitude, respectively. Feeding rates on Lobophora were, however, much lower than rates on the EAM. The low rates of Lobophora removal and significantly lower rates of herbivory in branching habitats were consistent with the high biomass of this brown alga throughout the Keppel Islands and with its distribution on reef crests, where Lobophora biomass was 20 times greater in branching than in planar habitats. This lack of feeding by herbivorous fishes within branching coral habitats in the Keppel Islands contrasts with the typical role of coral and topographic complexity on herbivores on coral reefs and highlights the potential for complex interactions between algae, corals and fishes on coral reefs. On marginal systems, herbivory may modify algal distributions but may be unable to contain the proliferation of algae such as Lobophora.     

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.     

西沙群岛主要岛礁鱼类物种多样性及其群落格局

为了解珊瑚礁海域鱼类物种多样性及其群落特征,作者2003年5月在西沙群岛7座主要岛礁(北礁、华光礁、金银岛、东岛、浪花礁、玉琢礁和永兴岛)采用底层刺网进行了调查,运用聚类分析和非度量多维标度(NMDS)等多元统计分析方法,对7个岛礁鱼类的种类组成、优势种、多样性和群落格局进行了分析.调查海域共记录鱼类146种,隶属10...     

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.     

Losing 'Nemo': bleaching and collection appear to reduce inshore populations of anemonefishes

Surveys of anemonefishes (Amphiprioninae) were conducted on reefs in two regions of the Great Barrier Reef Marine Park with contrasting histories of disturbance to determine the degree to which spatial variation might be explained by bleaching or management status. Densities of anemonefishes were lower on reefs in the bleaching-impacted Keppel Islands than on reefs in Far North Queensland. No anemonefishes or anemones were found on or near bleached corals in the Keppel Islands. Furthermore, the highest densities of fishes were found on reefs closed to fishing and aquarium collecting in both the Keppel Islands and Far North Queensland, which suggests that collecting is compounding the effects of bleaching. These results emphasize the importance of understanding the interaction between bleaching events and anthropogenic disturbance upon commercially exploited species.     

Key herbivores reveal limited functional redundancy on inshore coral reefs

Marine ecosystems are facing increasing exposure to a range of stressors and declines in critical ecological functions. The likelihood of further loss of functions and resilience is dependent, in part, on the extent of functional redundancy (i.e. the capacity of one species to functionally compensate for the loss of another species) within critical functional groups. We used multiple metrics; species richness, generic richness, abundance and reserve capacity (i.e. the relative number of individuals available to fulfil the function if the numerically dominant species is lost), as indicators to assess the potential functional redundancy of four functional groups of herbivorous fishes (browsers, excavators, grazers and scrapers) in two of the worlds’ most intact coral reef ecosystems: the Great Barrier Reef (GBR) and Ningaloo Reef in Western Australia. We found marked variations in potential redundancy among habitats within each reef system and functional groups. Despite negligible fishing of herbivorous fishes, coastal habitats in both reef systems had lower functional redundancy compared to offshore locations for all herbivorous fishes collectively and the four functional groups independently. This pattern was consistent in all four indicators of redundancy. The potential vulnerability of these coastal habitats is highlighted by recent shifts from coral to macroalgal dominance on several coastal reefs of the GBR. Our approach provides a simple yet revealing evaluation of potential functional redundancy. Moreover, it highlights the spatial variation in potential vulnerability and resilience of reef systems.     

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.     

Coral reef mesopredators switch prey,shortening food chains,in response to habitat degradation

Diet specificity is likely to be the key predictor of a predator's vulnerability to changing habitat and prey conditions. Understanding the degree to which predatory coral reef fishes adjust or maintain prey choice, in response to declines in coral cover and changes in prey availability, is critical for predicting how they may respond to reef habitat degradation. Here, we use stable isotope analyses to characterize the trophic structure of predator–prey interactions on coral reefs of the Keppel Island Group on the southern Great Barrier Reef, Australia. These reefs, previously typified by exceptionally high coral cover, have recently lost much of their coral cover due to coral bleaching and frequent inundation by sediment‐laden, freshwater flood plumes associated with increased rainfall patterns. Long‐term monitoring of these reefs demonstrates that, as coral cover declined, there has been a decrease in prey biomass, and a shift in dominant prey species from pelagic plankton‐feeding damselfishes to territorial benthic algal‐feeding damselfishes, resulting in differences in the principal carbon pathways in the food web. Using isotopes, we tested whether this changing prey availability could be detected in the diet of a mesopredator (coral grouper, Plectropomus maculatus). The δ¹³C signature in grouper tissue in the Keppel Islands shifted from a more pelagic to a more benthic signal, demonstrating a change in carbon sources aligning with the change in prey availability due to habitat degradation. Grouper with a more benthic carbon signature were also feeding at a lower trophic level, indicating a shortening in food chains. Further, we found a decline in the coral grouper population accompanying a decrease in total available prey biomass. Thus, while the ability to adapt diets could ameliorate the short‐term impacts of habitat degradation on mesopredators, long‐term effects may negatively impact mesopredator populations and alter the trophic structure of coral reef food webs.     

A DESCRIPTION OF THE CORAL STRUCTURE OF TUTIA REEF (PANGANYIKA TERRITORY, EAST AFRICA), AND ITS FISH FUNA

The origin and structure of Tutia Reef, a coral reef off the Tanganyika coast, is described. It is concluded that the reef is formed in part from the cutting back flat of the older reef 14 ft above the level of the present reef, and in part from seaward growth of the reef.
Based on lines of quadrats down three sides of the reef an assessment of the cover of living coral on the reef is made, and the distribution of the dominant corals of the reef described. It is suggested that, contrary to the views of Crossland (1902, 1903), many East African coral reefs are undergoing seaward growth.
The distribution of the fishes on the reef is described, and a correlation is shown with the distribution of living coral on the reef. Many species of fishes have restricted distribution on the reef.
The feeding relationships of the fishes are discussed, and the total fish biomass divided into separate feeding categories. Tutia Reef has a low biomass of herbivorous fishes compared with the results from Eniwetok Atoll obtained by Odum & Odum (1955). This is considered to be due to the fact that Tutia Reef exhibits characteristics of an outer reef, deriving much of its energy from plankton, not those of an enclosed and almost autotrophic logoon.     

Herbivory, connectivity, and ecosystem resilience: response of a coral reef to a large-scale perturbation

Coral reefs world-wide are threatened by escalating local and global impacts, and some impacted reefs have shifted from coral dominance to a state dominated by macroalgae. Therefore, there is a growing need to understand the processes that affect the capacity of these ecosystems to return to coral dominance following disturbances, including those that prevent the establishment of persistent stands of macroalgae. Unlike many reefs in the Caribbean, over the last several decades, reefs around the Indo-Pacific island of Moorea, French Polynesia have consistently returned to coral dominance following major perturbations without shifting to a macroalgae-dominated state. Here, we present evidence of a rapid increase in populations of herbivorous fishes following the most recent perturbation, and show that grazing by these herbivores has prevented the establishment of macroalgae following near complete loss of coral on offshore reefs. Importantly, we found the positive response of herbivorous fishes to increased benthic primary productivity associated with coral loss was driven largely by parrotfishes that initially recruit to stable nursery habitat within the lagoons before moving to offshore reefs later in life. These results underscore the importance of connectivity between the lagoon and offshore reefs for preventing the establishment of macroalgae following disturbances, and indicate that protecting nearshore nursery habitat of herbivorous fishes is critical for maintaining reef resilience.     

Coral Reef Community Composition in the Context of Disturbance History on the Great Barrier Reef,Australia

Much research on coral reefs has documented differential declines in coral and associated organisms. In order to contextualise this general degradation, research on community composition is necessary in the context of varied disturbance histories and the biological processes and physical features thought to retard or promote recovery. We conducted a spatial assessment of coral reef communities across five reefs of the central Great Barrier Reef, Australia, with known disturbance histories, and assessed patterns of coral cover and community composition related to a range of other variables thought to be important for reef dynamics. Two of the reefs had not been extensively disturbed for at least 15 years prior to the surveys. Three of the reefs had been severely impacted by crown-of-thorns starfish outbreaks and coral bleaching approximately a decade before the surveys, from which only one of them was showing signs of recovery based on independent surveys. We incorporated wave exposure (sheltered and exposed) and reef zone (slope, crest and flat) into our design, providing a comprehensive assessment of the spatial patterns in community composition on these reefs. Categorising corals into life history groupings, we document major coral community differences in the unrecovered reefs, compared to the composition and covers found on the undisturbed reefs. The recovered reef, despite having similar coral cover, had a different community composition from the undisturbed reefs, which may indicate slow successional processes, or a different natural community dominance pattern due to hydrology and other oceanographic factors. The variables that best correlated with patterns in the coral community among sites included the density of juvenile corals, herbivore fish biomass, fish species richness and the cover of macroalgae. Given increasing impacts to the Great Barrier Reef, efforts to mitigate local stressors will be imperative to encouraging coral communities to persist into the future.     

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.     

Phase shifts, herbivory, and the resilience of coral reefs to climate change

Many coral reefs worldwide have undergone phase shifts to alternate, degraded assemblages because of the combined effects of over-fishing, declining water quality, and the direct and indirect impacts of climate change. Here, we experimentally manipulated the density of large herbivorous fishes to test their influence on the resilience of coral assemblages in the aftermath of regional-scale bleaching in 1998, the largest coral mortality event recorded to date. The experiment was undertaken on the Great Barrier Reef, within a no-fishing reserve where coral abundances and diversity had been sharply reduced by bleaching. In control areas, where fishes were abundant, algal abundance remained low, whereas coral cover almost doubled (to 20%) over a 3 year period, primarily because of recruitment of species that had been locally extirpated by bleaching. In contrast, exclusion of large herbivorous fishes caused a dramatic explosion of macroalgae, which suppressed the fecundity, recruitment, and survival of corals. Consequently, management of fish stocks is a key component in preventing phase shifts and managing reef resilience. Importantly, local stewardship of fishing effort is a tractable goal for conservation of reefs, and this local action can also provide some insurance against larger-scale disturbances such as mass bleaching, which are impractical to manage directly.     

The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts

Climate-driven changes in biotic interactions can profoundly alter ecological communities, particularly when they impact foundation species. In marine systems, changes in herbivory and the consequent loss of dominant habitat forming species can result in dramatic community phase shifts, such as from coral to macroalgal dominance when tropical fish herbivory decreases, and from algal forests to ‘barrens’ when temperate urchin grazing increases. Here, we propose a novel phase-shift away from macroalgal dominance caused by tropical herbivores extending their range into temperate regions. We argue that this phase shift is facilitated by poleward-flowing boundary currents that are creating ocean warming hotspots around the globe, enabling the range expansion of tropical species and increasing their grazing rates in temperate areas. Overgrazing of temperate macroalgae by tropical herbivorous fishes has already occurred in Japan and the Mediterranean. Emerging evidence suggests similar phenomena are occurring in other temperate regions, with increasing occurrence of tropical fishes on temperate reefs.     

Limited Functional Redundancy in a High Diversity System: Single Species Dominates Key Ecological Process on Coral Reefs

Herbivory is a key process structuring plant communities in both terrestrial and aquatic ecosystems, with variation in herbivory often being related to shifts between alternate states. On coral reefs, regional reductions in herbivores have underpinned shifts from coral to dominance by leathery macroalgae. These shifts appear difficult to reverse as these macroalgae are unpalatable to the majority of herbivores, and the macroalgae suppress the recruitment and growth of corals. The removal of macroalgae is, therefore, viewed as a key ecological process on coral reefs. On the Great Barrier Reef, Sargassum is a dominant macroalgal species following experimentally induced coral–macroalgal phase-shifts. We, therefore, used Sargassum assays and remote video cameras to directly quantify the species responsible for removing macroalgae across a range of coral reef habitats on Lizard Island, northern Great Barrier Reef. Despite supporting over 50 herbivorous fish species and six macroalgal browsing species, the video footage revealed that a single species, Naso unicornis, was almost solely responsible for the removal of Sargassum biomass across all habitats. Of the 42,246 bites taken from the Sargassum across all habitats, N. unicornis accounted for 89.8% (37,982) of the total bites, and 94.6% of the total mass standardized bites. This limited redundancy, both within and across local scales, underscores the need to assess the functional roles of individual species. Management and conservation strategies may need to look beyond the preservation of species diversity and focus on the maintenance of ecological processes and the protection of key species in critical functional groups.     

Broadening the taxonomic scope of coral reef palaeoecological studies using ancient DNA

Marine environments face acute pressures from human impacts, often resulting in substantial changes in community structure. On the inshore Great Barrier Reef (GBR), palaeoecological studies show the collapse of the previously dominant coral Acropora from the impacts of degraded water quality associated with European colonization. Even more dramatic impacts can result in the replacement of corals by fleshy macroalgae on modern reefs, but their past distribution is unknown because they leave no fossil record. Here, we apply DNA metabarcoding and high‐throughput sequencing of the 18S rDNA gene on palaeoenvironmental DNA (aeDNA) derived from sediment cores at two sites on Pandora Reef (GBR), to enhance palaeoecological studies by incorporating key soft‐bodied taxa, including macroalgae. We compared temporal trends in this aeDNA record with those of coral genera derived from macrofossils. Multivariate analysis of 12 eukaryotic groups from the aeDNA community showed wide variability over the past 750 years. The occurrence of brown macroalgae was negatively correlated only with the dominant coral at both sites. The occurrence of coralline and green macroalgae was positively correlated with only the dominant coral at one of the sites, where we also observed a significant association between the whole coral community and the occurrence of each of the three macroalgae groups. Our results demonstrate that reef sediments can provide a valuable archive for understanding the past distribution and occurrence of important soft‐bodied reef dwellers. Combining information from fossils and aeDNA provides an enhanced understanding of temporal changes of reefs ecosystems at decadal to millennial timescales.     

Micro-topography mediates interactions between corals,algae, and herbivorous fishes on coral reefs

Processes occurring during the early life stages of corals are important for the replenishment of coral assemblages and the resilience of coral reefs. However, the factors influencing early life stages of corals are not well understood, and the role of micro-topographic complexity for habitat associations of juvenile corals is largely unexplored. This study investigated the microhabitat distribution patterns of early life stages of corals and a potential macroalgal competitor (Turbinaria ornata) across two reef zones (reef crest and outer reef flat) on Lizard Island, Great Barrier Reef. In both reef zones, both corals and T. ornata were significantly more abundant in concealed microhabitats than in semi-concealed or open microhabitats (GLMM: P < 0.001). The prevalence of juvenile corals and T. ornata within concealed environments suggests that they might be effective refuges from grazing by herbivorous fishes. The density of juvenile corals was positively related, and density of T. ornata negatively related to the abundance of two groups of herbivorous fishes, pairing rabbitfishes, and surgeonfishes in the genus Zebrasoma (BEST ENV-BIO: r _s  = 0.72, P < 0.01), which feed in concealed microhabitats. This correlative evidence suggests that crevices may be important for early life stages of both coral and macroalgae, and that a specific suite of crevice-feeding fishes may influence benthic community dynamics in these microhabitats.     

Farming behaviour of reef fishes increases the prevalence of coral disease associated microbes and black band disease

Microbial community structure on coral reefs is strongly influenced by coral–algae interactions; however, the extent to which this influence is mediated by fishes is unknown. By excluding fleshy macroalgae, cultivating palatable filamentous algae and engaging in frequent aggression to protect resources, territorial damselfish (f. Pomacentridae), such as Stegastes, mediate macro-benthic dynamics on coral reefs and may significantly influence microbial communities. To elucidate how Stegastes apicalis and Stegastes nigricans may alter benthic microbial assemblages and coral health, we determined the benthic community composition (epilithic algal matrix and prokaryotes) and coral disease prevalence inside and outside of damselfish territories in the Great Barrier Reef, Australia. 16S rDNA sequencing revealed distinct bacterial communities associated with turf algae and a two to three times greater relative abundance of phylotypes with high sequence similarity to potential coral pathogens inside Stegastes''s territories. These potentially pathogenic phylotypes (totalling 30.04% of the community) were found to have high sequence similarity to those amplified from black band disease (BBD) and disease affected corals worldwide. Disease surveys further revealed a significantly higher occurrence of BBD inside S. nigricans''s territories. These findings demonstrate the first link between fish behaviour, reservoirs of potential coral disease pathogens and the prevalence of coral disease.     

Habitat associations of juvenile fish at Ningaloo Reef, Western Australia: the importance of coral and algae

Habitat specificity plays a pivotal role in forming community patterns in coral reef fishes, yet considerable uncertainty remains as to the extent of this selectivity, particularly among newly settled recruits. Here we quantified habitat specificity of juvenile coral reef fish at three ecological levels; algal meadows vs. coral reefs, live vs. dead coral and among different coral morphologies. In total, 6979 individuals from 11 families and 56 species were censused along Ningaloo Reef, Western Australia. Juvenile fishes exhibited divergence in habitat use and specialization among species and at all study scales. Despite the close proximity of coral reef and algal meadows (10's of metres) 25 species were unique to coral reef habitats, and seven to algal meadows. Of the seven unique to algal meadows, several species are known to occupy coral reef habitat as adults, suggesting possible ontogenetic shifts in habitat use. Selectivity between live and dead coral was found to be species-specific. In particular, juvenile scarids were found predominantly on the skeletons of dead coral whereas many damsel and butterfly fishes were closely associated with live coral habitat. Among the coral dependent species, coral morphology played a key role in juvenile distribution. Corymbose corals supported a disproportionate number of coral species and individuals relative to their availability, whereas less complex shapes (i.e. massive & encrusting) were rarely used by juvenile fish. Habitat specialisation by juvenile species of ecological and fisheries importance, for a variety of habitat types, argues strongly for the careful conservation and management of multiple habitat types within marine parks, and indicates that the current emphasis on planning conservation using representative habitat areas is warranted. Furthermore, the close association of many juvenile fish with corals susceptible to climate change related disturbances suggests that identifying and protecting reefs resilient to this should be a conservation priority.