Interactions between herbivorous fish guilds and their influence on algal succession on a coastal coral reef

Herbivory is an important mechanism affecting algal succession, particularly on coral reefs where the relationship between algae and corals is largely controlled by herbivores. However, different functional groups of herbivores may have contrasting effects on succession, which may explain different trajectories of coral reef recovery after disturbance. Here, the effects of different herbivore groups (roving herbivores = foragers and territorial damselfish = farmers) were isolated by a multi-factorial experiment carried out on a coastal coral reef with high macroalgal cover, high farmer densities and relatively low forager abundance. The effects of foragers and farmers were distinguished by monitoring algal succession on settlement tiles placed inside and outside exclusion cages, with orthogonal treatments established inside and outside damselfish territories (with appropriate cage controls). Within 12 months, algal assemblages on ungrazed tiles inside exclusion cages proceeded rapidly from fine filamentous turfs, to corticated algae, to tough erect (e.g. Amphiroa spp.) and foliose (e.g. Peyssonnellidae) calcified algae. Farmers had a dramatic impact on succession, essentially arresting the development of the algal community at a point where it was dominated by palatable filamentous algae of the genus Polysiphonia. Fleshy macroalgae such as Sargassum spp. were excluded from farmer territories. In contrast, foragers did not suppress fleshy macroalgae, but rather, appeared to decelerate succession and promote a relatively diverse assemblage. In contrast to forager-dominated reefs, farmer territories did not appear to function solely as forager exclusion areas or promote algal diversity as a result of intermediate grazing pressure. The relatively strong effects of farmers observed here may represent a future scenario for coral reefs that are increasingly subject to overfishing of large grazing fishes.     

Territorial behavior of threespot damselfish (Eupomacentrus planifrons) increases reef algal biomass and productivity

Synopsis Algal growth and damselfish (Eupomacentrus planifrons) territories were studied in two reef habitats at Discovery Bay, Jamaica. Damselfish territories were contiguous in the reef flat (0 to 2.5 m), where the algal composition and biomass varied from territory to territory. In contrast, on the lower reef terrace (22 m), damselfish territories were often spatially segregated. While the algal composition of the territories was more uniform on the reef terrace, the total algal biomass was lower than in the territories on the reef flat. Damselfish are largely herbivorous, and they defend their territories against most intruding fish, including a number of herbivorous species. Areas of the reef terrace outside of damselfish territories were heavily grazed by herbivorous fishes and contained only small quantities of non-crustose algae.The reef terrace territories were characterized by a multispecific turf of algae (greens, blue-greens, and reds) covering the Acropora cervicornis framework and by the leafy, brown alga, Lobophora variegata. A rapid reduction in the biomass of brown algae and filamentous algae was noted when damselfish were permanently removed from their territories. Only calcified, encrusting algae — plants apparently somewhat undesirable as fish food sources — would be common on the terrace zone of this reef if damselfish territories were absent. Damselfish territoriality may significantly influence the dynamics of some reefs by increasing the biomass of the algal turf thereby increasing; reef productivity. Since blue-green algae, potential nitrogen fixers, occur in these algal turfs, the fish may also be indirectly affecting reef nutrition.     

Algal assemblages associated with Stegastes sp. territories on Indo-Pacific coral reefs: Characterization of diversity and controls on growth

Herbivorous fish occupy an important niche in coral reef ecosystems. Specifically, damselfish of the genus Stegastes have been shown to have a significant impact on coral community structure and algal assemblages. This study investigated the algal communities associated with Stegastes territories of the Indo-Pacific (Fiji, Solomon Islands, and Tonga), while concurrently examining the effects of nutrient enrichment and herbivore exclusion (alone and in unison) on these communities. Results evidenced differences in species composition, percent cover, and algal growth rate between Stegastes territories and non-Stegastes sites and between control sites and treatment sites. Stegastes territories consistently displayed a greater abundance of turf algae than non-Stegastes sites; the two main genera of turf algae observed at all sites were Polysiphonia and Ceramium. Although non-Stegastes sites in Fiji, the Solomon Islands, and Tonga showed a greater percent coverage of macroalgae, they contained fewer algal species compared to Stegastes territories. In Fiji, red macroalgae decreased in the herbivore exclusion treatments, while brown macroalgae increased significantly in the herbivore exclusion and nutrient treatments. The combined effect of the herbivore exclusion and nutrient treatment at this location yielded a significantly increased turf algae growth rate compared to control sites. Growth rates of turf algae in the Solomon Islands and Tonga increased significantly in caged treatments, suggesting that damselfish of the genus Stegastes can play an important role in maintaining cropped algal beds. In summation, the results demonstrated that Stegastes sustains distinct algal assemblages which may be disrupted by reduced grazing and/or eutrophication.     

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.     

Modification of benthic communities by territorial damselfish: a multi-species comparison

The effects of territorial damselfish on coral reef benthos have been well-studied for a few relatively large-bodied species with visually distinct territories. Despite a growing body of research demonstrating their abundance, and their effects on algae, corals and other grazers, there has been little research on the effects of the territorial damselfish community as a whole. This study investigated the space occupation, territory composition, and diet of ten damselfish species at three locations: Magnetic and Orpheus Islands (Great Barrier Reef), and Kimbe Bay (Papua New Guinea). Territories were measured, and the composition of benthic communities inside and outside territories was assessed both in situ and from algal collections. The stomach contents of territorial damselfishes were also quantified. Although the larger, previously well-studied species had the most visible effect on the benthic community in their territories, all the smaller species also significantly affected the algal composition, normally with an increase of palatable algae. However, the composition of algal assemblages inside the territories of different species varied considerably. Damselfish territories were highly individual, not just among species, but also among locations. Diets were diverse and indicated a greater degree of omnivory and detritivory than previously thought. At all locations, territories occupied a substantial proportion of the substratum: >25% on Magnetic Island, >50% at Orpheus Island, and ∼50% in Kimbe Bay. Within individual zones, this figure was as high as 70%. The contribution of territorial damselfishes to a range of benthic patterns and processes is considerable, and future benthic studies may need to distinguish more closely between territory and non-territory areas. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Damselfish territories as a refuge for macroalgae on coral reefs

Herbivory is widely accepted as a key process determining the benthic community structure and resilience of coral reefs. Recent studies have mostly focused on the importance of roving herbivorous fishes in ecosystem processes. Here, we examine the role of territorial damselfish in shaping patterns of macroalgal distribution based on benthic surveys and macroalgal bioassays. The territory composition and effect of resident damselfish on the removal of Sargassum bioassays were quantified for six species of damselfish on Lizard Island, a mid-shelf reef in the northern Great Barrier Reef (GBR). The functional composition of algal communities within territories varied markedly among species. The territories of four species (Dischistodus perspicillatus, Dischistodus pseudochrysopoecilus, Plectroglyphidodon lacrymatus, and Stegastes nigricans) were characterized by algal turfs, while the territories of two species (Dischistodus prosopotaenia and Hemiglyphidodon plagiometopon) were characterized by foliose and leathery brown macroalgae. Sargassum, a generally rare alga on mid-shelf reefs, was a particularly common alga within D. prosopotaenia territories on the leeward side of the island but absent within their territories on the windward side of the island. D. prosopotaenia was the only species to retain the transplanted Sargassum, with only a minimal reduction in Sargassum biomass (1.1%) being recorded within their territories at both leeward and windward sites over a 24-h period. In contrast, reductions in Sargassum biomass were high in areas adjacent to D. prosopotaenia territories (83.8%), and within and adjacent to the territories of the five remaining damselfish species (76.2–92.5%). Overall, only one of the six damselfish species provided a refuge for leathery brown macroalgae and may facilitate the development of this macroalgae on mid-shelf reefs of the GBR.     

Overgrowth and killing of corals by the brown alga Lobophora hederacea (Dictyotales,Phaeophyceae) on healthy reefs in New Caledonia: A new case of the epizoism syndrome

Coral reef degradation is often associated with regime shifts from coral‐ to macroalgal‐dominated reefs. These shifts demonstrate that under certain conditions (e.g. coral mortality, decrease in herbivory, increased nutrients supply) some macroalgae may overgrow corals. The outcome of the competition is dependent on algal aggressiveness and the coral susceptibility. In undisturbed reefs, herbivore grazing is regulating macroalgal cover, thus preventing the latter from overgrowing corals. However, some macroalgae have evolved strategies not only to outcompete corals but also to escape herbivory to some extent, allowing overgrowth of some coral species in undisturbed reefs. Epizoism represents one of those successful strategies, and has been previously documented with red algae, cyanobacteria and Lobophora variegata (Dictyotales, Phaeophyceae). Here we report a new case of epizoism leading to coral mortality, involving a recently described species of Lobophora, L. hederacea, overgrowing the coral Seriatopora caliendrum (Pocilloporidae) in undisturbed reefs in New Caledonia.     

Large-scale associations between macroalgal cover and grazer biomass on mid-depth reefs in the Caribbean

Since the 1970s, macroalgae have become considerably more abundant on many Caribbean reefs and overfishing of grazing fishes has been implicated as a contributory factor. We explored relationships between algal cover and grazers (biomass of herbivorous fishes and abundance of the sea-urchin Diadema antillarum) on mid-depth reefs (12-15 m) in 19 areas at seven locations in Jamaica, Barbados, Belize, Grand Cayman and Cuba, between April 1997 and April 1998. Diadema antillarum density was never >0.01 m^-2, while herbivorous fish biomass (acanthurids and scarids ⁸ cm total length) varied from 2-5 g m^-2 in Jamaica to 17.1 g m^-2 in Barbados, and was strongly correlated, negatively with macroalgal cover and positively with 'cropped' substratum (sum of 'bare', turf and crustose-coralline substrata) cover. However, overfishing of herbivorous fishes alone cannot explain the widespread abundance of macroalgae, as even on lightly fished reefs, macroalgal cover was mostly >20%. Herbivorous fish populations on those reefs were apparently only able to maintain approximately 40-60% of reef substratum in cropped states, but due to low space-occupation by coral and other invertebrates, 70-90% of substratum was available to algae. The abundance of macroalgae on lightly fished reefs may therefore be a symptom of low coral cover in combination with the continuing absence of Diadema antillarum.     

Geographic variation in the damselfish-red alga cultivation mutualism in the Indo-West Pacific

Background  

On coral reefs, damselfish defend their territories from invading herbivores and maintain algal turfs, from which they harvest filamentous algae. In southern Japan, intensive weeding of indigestible algae by Stegastes nigricans results in overgrowth by one filamentous alga, Polysiphonia sp. 1. Because this alga is highly susceptible to grazing and is competitively inferior to other algae, it survives only within the protective territories of this fish species, suggesting an obligate mutualism between damselfish and their cultivated alga. The wide distribution of damselfish species through the Indo-Central Pacific raises the question of whether this species-specific mutualism is maintained throughout the geographic range of the fish. To address this question, from all 18 damselfish species we conducted comprehensive surveys of algal flora within their territories throughout the Indo-West Pacific, and identified species of Polysiphonia using morphological examination and gene sequencing data.     

Effects of herbivore exclusion and nutrient enrichment on coral reef macroalgae and cyanobacteria

Although phase shifts on coral reefs from coral-dominated to algal-dominated communities have been attributed to the effects of increased nutrient availability due to eutrophication and reduced herbivore abundance due to overfishing and disease, these factors have rarely been manipulated simultaneously. In addition, few studies have considered the effects of these factors on benthic, filamentous cyanobacteria (blue-green algae) as well as macroalgae. We used a combination of herbivore-exclusion cages and nutrient enrichment to manipulate herbivore abundance and nutrient availability, and measured the impacts of these treatments on macroalgal and cyanobacterial community structure. In the absence of cages, surface cover of the cyanobacterium Tolypothrix sp. decreased, while surface cover of the cyanobacteria Oscillatoria spp. increased. Cyanobacterial cover decreased in partial cages, and Tolypothrix sp. cover decreased further in full cages. Lower cyanobacterial cover and biomass were correlated with higher macroalgal cover and biomass. Dictyota bartayresiana dominated the partial cages, while Padina tenuis and Tolypiocladia glomerulata recruited into the full cages. Palatability assays demonstrated that herbivore-exclusion shifted macroalgal species composition from relatively unpalatable to relatively palatable species. Nutrient enrichment interacted with herbivore exclusion to increase the change in cover of D. bartayresiana in the uncaged and fully caged plots, but did not affect the final biomass of D. bartayresiana among treatments. Nutrient enrichment did not significantly affect the cover or biomass of any other taxa. These results stress the critical role of herbivory in determining coral reef community structure and suggest that the relative palatabilities of dominant algae, as well as algal growth responses to nutrient enrichment, will determine the potential for phase shifts to algal-dominated communities.     

Spectral unmixing of coral reef benthos under ideal conditions

Hyperspectral remote sensing has shown promise for detailed discrimination of coral reef substratum types, but, by necessity, it samples at pixel scales larger than reef substratum patch sizes. Spectral unmixing techniques have been successful in resolving subpixel areal cover in terrestrial environments. However, the application of spectral unmixing on coral reefs is fundamentally challenging, due not only to the water column, but also to the potentially large number of spectrally similar and ecologically significant end-member (substratum) classes involved. A controlled ex-situ experiment was conducted using field-spectrometer data to assess the accuracy of spectral unmixing techniques to estimate the areal cover of small-scale (<0.25 m²) assemblages of reef substrata (e.g., changes in cover between massive corals, branching corals, bleached corals, macroalgae, and coralline red algae). Mixture compositions were obtained precisely by analysis of digital images collected by a camera calibrated to the field of view of the spectrometer. Linear unmixing techniques were applied to derive estimates of substratum proportions using the full spectral resolution data and various transformations of it, including derivatives and down sampling (merging adjacent wavelengths into broader spectral bands). Comparison of actual and estimated substratum proportions indicate that spectral unmixing may be a practical approach for estimating subpixel-scale cover of coral reef substrata. In the most accurate treatment, coefficients of determination across all mixture sets were high for most end-member classes (37 of 52 cases with r ² >0.64, i.e. r >0.8). The most successful analyses were based on derivatives of down-sampled data, implying that spectral unmixing benefits more from spectral smoothing and judicious choice of band locations than from high spectral resolution per se. Although these results show that changes in coral and algal cover can be determined by unmixing their spectra, the method is not yet an operational remote sensing tool. Primary empirical research is needed before taking the next step, which is to incorporate a water column, of variable depth, above the sea bed.     

Effects of territorial damselfish on cryptic bioeroding organisms on dead Acropora formosa

Many damselfishes exclude other grazers from their territories and “farm” filamentous algae within their territories. In this study the indirect effect of damselfish territories on faunal composition and abundance of internal bioeroders of dead Acropora formosa (Dana, 1846) was investigated in territories of two damselfish species, Stegastes nigricans (Lacepède, 1802) and Plectroglyphidodon lacrymatus (Quoy and Gaimard, 1825). S. nigricans tends to be more protective and defend their territories more aggressively than P. lacrymatus. Newly killed branches of A. formosa were placed inside and outside damselfish territories, for 1 or 2 years, at a coral reef near Zanzibar, Tanzania. As predicted, the coral branches became covered with more filamentous algae in the S. nigricans territories than in the controls, with intermediate levels in the P. lacrymatus territories. Among the internal bioeroding fauna, polychaetes were by far the most common group. In total, there were significantly more borers in the first year than the second, which was mainly due to a high abundance of sabellids. Furthermore, sabellids were significantly more abundant in control areas and in the P. lacrymatus territories compared to the S. nigricans territories. However, many other genera showed the opposite pattern, with more polychaetes in the fish territories compared to the controls. There was also a clear difference in assemblage structure between S. nigricans territories and controls. Thus, we found strong effects of whether a piece of coral was placed inside or outside a damselfish territory on the abundance of many of the bioeroding taxa. We discuss multiple reasons for these indirect effects of the territories, including that deposit feeding bioeroders may benefit from the dense algal turf found inside the territories whereas suspension feeding bioeroders may benefit from substrate with less filamentous algae found outside territories. Considering our results in the context of the large areas of coral reefs that typically are defended as territories by damselfishes, these fish are likely to have a considerable impact on the boring community of a coral reef.     

Phase shifts and the role of herbivory in the resilience of coral reefs

Cousin Island marine reserve (Seychelles) has been an effectively protected no-take marine protected area (MPA) since 1968 and was shown in 1994 to support a healthy herbivorous fish assemblage. In 1998 Cousin Island reefs suffered extensive coral mortality following a coral bleaching event, and a phase shift from coral to algal dominance ensued. By 2005 mean coral cover was <1%, structural complexity had fallen and there had been a substantial increase in macroalgal cover, up to 40% in some areas. No clear trends were apparent in the overall numerical abundance and biomass of herbivorous fishes between 1994 and 2005, although smaller individuals became relatively scarce, most likely due to the loss of reef structure. Analysis of the feeding habits of six abundant and representative herbivorous fish species around Cousin Island in 2006 demonstrated that epilithic algae were the preferred food resource of all species and that macroalgae were avoided. Given the current dominance of macroalgae and the apparent absence of macroalgal consumers, it is suggested that the increasing abundance of macroalgae is reducing the probability of the system reverting to a coral dominated state.     

40 Years of benthic community change on the Caribbean reefs of Curaçao and Bonaire: the rise of slimy cyanobacterial mats

Over the past decades numerous studies have reported declines in stony corals and, in many cases, phase shifts to fleshy macroalgae. However, long-term studies documenting changes in other benthic reef organisms are scarce. Here, we studied changes in cover of corals, algal turfs, benthic cyanobacterial mats, macroalgae, sponges and crustose coralline algae at four reef sites of the Caribbean islands of Curaçao and Bonaire over a time span of 40 yr. Permanent 9 m² quadrats at 10, 20, 30 and 40 m depth were photographed at 3- to 6-yr intervals from 1973 to 2013. The temporal and spatial dynamics in the six dominant benthic groups were assessed based on image point-analysis. Our results show consistent patterns of benthic community change with a decrease in the cover of calcifying organisms across all sites and depths from 32.6 (1973) to 9.2% (2013) for corals and from 6.4 to 1% for crustose coralline algae. Initially, coral cover was replaced by algal turfs increasing from 24.5 (1973) to 38% around the early 1990s. Fleshy macroalgae, still absent in 1973, also proliferated covering 12% of the substratum approximately 20 yr later. However, these new dominants largely declined in abundance from 2002 to 2013 (11 and 2%, respectively), marking the rise of benthic cyanobacterial mats. Cyanobacterial mats became the most dominant benthic component increasing from a mere 7.1 (2002) to 22.2% (2013). The observed increase was paralleled by a small but significant increase in sponge cover (0.5 to 2.3%). Strikingly, this pattern of degradation and phase change occurred over the reef slope down to mesophotic depths of 40 m. These findings suggest that reefs dominated by algae may be less stable than previously thought and that the next phase may be the dominance of slimy cyanobacterial mats with some sponges.     

Black reefs: iron-induced phase shifts on coral reefs

The Line Islands are calcium carbonate coral reef platforms located in iron-poor regions of the central Pacific. Natural terrestrial run-off of iron is non-existent and aerial deposition is extremely low. However, a number of ship groundings have occurred on these atolls. The reefs surrounding the shipwreck debris are characterized by high benthic cover of turf algae, macroalgae, cyanobacterial mats and corallimorphs, as well as particulate-laden, cloudy water. These sites also have very low coral and crustose coralline algal cover and are call black reefs because of the dark-colored benthic community and reduced clarity of the overlying water column. Here we use a combination of benthic surveys, chemistry, metagenomics and microcosms to investigate if and how shipwrecks initiate and maintain black reefs. Comparative surveys show that the live coral cover was reduced from 40 to 60% to <10% on black reefs on Millennium, Tabuaeran and Kingman. These three sites are relatively large (>0.75 km²). The phase shift occurs rapidly; the Kingman black reef formed within 3 years of the ship grounding. Iron concentrations in algae tissue from the Millennium black reef site were six times higher than in algae collected from reference sites. Metagenomic sequencing of the Millennium Atoll black reef-associated microbial community was enriched in iron-associated virulence genes and known pathogens. Microcosm experiments showed that corals were killed by black reef rubble through microbial activity. Together these results demonstrate that shipwrecks and their associated iron pose significant threats to coral reefs in iron-limited regions.     

Temperate macroalgae impacts tropical fish recruitment at forefronts of range expansion

Warming waters and changing ocean currents are increasing the supply of tropical fish larvae to temperature regions where they are exposed to novel habitats, namely temperate macroalgae and barren reefs. Here, we use underwater surveys on the temperate reefs of south-eastern (SE) Australia and western Japan (~33.5°N and S, respectively) to investigate how temperate macroalgal and non-macroalgal habitats influence recruitment success of a range of tropical fishes. We show that temperate macroalgae strongly affected recruitment of many tropical fish species in both regions and across three recruitment seasons in SE Australia. Densities and richness of recruiting tropical fishes, primarily planktivores and herbivores, were over seven times greater in non-macroalgal than macroalgal reef habitat. Species and trophic diversity (K-dominance) were also greater in non-macroalgal habitat. Temperate macroalgal cover was a stronger predictor of tropical fish assemblages than temperate fish assemblages, reef rugosities or wave exposure. Tropical fish richness, diversity and density were greater on barren reef than on reef dominated by turfing algae. One common species, the neon damselfish (Pomacentrus coelestis), chose non-macroalgal habitat over temperate macroalgae for settlement in an aquarium experiment. This study highlights that temperate macroalgae may partly account for spatial variation in recruitment success of many tropical fishes into higher latitudes. Hence, habitat composition of temperate reefs may need to be considered to accurately predict the geographic responses of many tropical fishes to climate change.

     

Markov chain analysis of sessile community dynamics in a degraded Philippine reef to support restoration of coral populations

Quantitative approaches are needed for assessing assisted recovery potential in degraded coral reefs. A lagoonal community (Bolinao, Philippines) that has experienced severe disturbances (overfishing, blast fishing and coral bleaching) in the past was observed for 26 months. Benthic state sequences in 4 × 4 cm patches were used to quantify monthly probabilities of transitions between reef states. Benthic cover distribution was consistent with a spatially heterogeneous Markov process, with high variability in transition probabilities within a subset of four states: crustose algae with cropped turf, the codominant sponge Callyspongia samarensis, articulated coralline algae and fleshy macroalgae (MA). Once a patch is dominated by any of these states, there is high likelihood of cycling within the set before escaping to the rarer invertebrate groups. The assemblage is unlikely to recover naturally given prevailing conditions. Patches dominated by juvenile and adult corals have mean turnover times of about 3 and 5 months, respectively, due to (partial) mortality and competition. Asymmetry was detected for coral–macroalgal competition, despite low fleshy algal cover (9.5%), that was more adverse for coral juveniles than adults. While competition between coral and the mat-forming C. samarensis was symmetrical, loss of coral cover through this path is relatively higher as a result of the higher interaction frequency. Articulated coralline algae do not appear as a constraint. Complementary strategies for assisted recovery were inferred from successional indices as well as the sensitivity of stationary coral cover to changes in transition probabilities. Results demonstrate that short-term, fine-scale observations of state variables can be used to resolve biotic constraints to inform restoration initiatives.     

The influence of multiple factors upon reef fish abundance and species richness in a tropical coral complex

The present study was conducted on Tamandaré reefs, northeast Brazil and aimed to analyse the importance of different factors (e.g. tourism activity, fishing activity, coral abundance and algal abundance) on reef fish abundance and species richness. Two distinct reef areas (A ver o mar and Caieiras) with different levels of influence were studied. A total of 8239 reef fish individuals were registered, including 59 species. Site 1 (A ver o mar) presented higher reef fish abundance and richness, with dominance of roving herbivores (29.9 %) and mobile invertebrate feeders (28.7 %). In contrast, at Site 2 (Caieiras) territorial herbivores (40.9 %) predominated, followed by mobile invertebrate feeders (24.6 %). Concerning the benthic community, at Site 1 macroalgae were recorded as the main category (49.3 %); however, Site 2 was dominated by calcareous algae (36.0 %). The most important variable explaining more than 90 % of variance on reef fish abundance and species richness was macroalgae abundance, followed by fishing activity. Phase shifts on coral reefs are evident, resulting in the replacement of coral by macroalgae and greatly influencing reef fish communities. In this context, it is important to understand the burden of the factors that affect reef fish communities and, therefore, influence the extinction vulnerability of coral reef fishes.     

A novel obligate cultivation mutualism between damselfish and Polysiphonia algae

In cultivation mutualisms, farming animals prepare fields for cultivars, enhance their growth and harvest them. For example, in terrestrial ecosystems, plant-herbivore cultivation mutualisms arose between humans and their crops only relatively recently. We discovered an obligate cultivation mutualism between a damselfish and an alga in a coral reef ecosystem. The damselfish, Stegastes nigricans, manages algal farms through territorial defence against the invading grazers and through weeding of unpalatable algae. As a result, the algal farms of S. nigricans are dominated by one species, Polysiphonia sp. We performed an exhaustive survey of algal assemblages inside and outside the territories of five damselfish species around the Ryukyu Islands, Japan, using molecular and morphological characteristics. Polysiphonia sp. 1 grew exclusively inside the farms of S. nigricans, and never elsewhere. Since only Polysiphonia sp. 1 is harvested and consumed by the damselfish as a staple food, this interdependent relationship is an obligate cultivation mutualism. This is the first record of an obligate plant-herbivore cultivation mutualism in a marine ecosystem. Our data also suggest that three other Polysiphonia species are facultatively mutual with, commensal with, or parasitic on other damselfish species.     

Detriments to post-bleaching recovery of corals

Predicting the response of coral reefs to large-scale mortality induced by climate change will depend greatly on the factors that influence recovery after bleaching events. We experimentally transplanted hard corals from a shallow reef with highly variable seawater temperature (23–36°C) to three unfished marine parks and three fished reefs with variable coral predator abundance and benthic cover. The transplanted corals were fragmented colonies collected from a reef that was relatively undisturbed by the 1997–1998 warm-water temperature anomaly, one of the most extreme thermal events of the past century, and it was assumed that they would represent corals likely to succeed in the future temperature environment. We examined the effects of four taxa, two fragment sizes, an acclimation period, benthic cover components, predators and tourists on the survival of the coral fragments. We found the lowest survival of transplants occurred in the unfished marine parks and this could be attributed to predation and not tourist damage. The density of small coral recruits approximately 6 months after the spawning season was generally moderate (~40–60/m²), and not different on fished and unfished reefs. Coral recovery between 1998 and 2002 was variable (0–25%), low (mean of 6.5%), and not different between fished and unfished reefs. There was high variability in coral mortality among the three unfished areas despite low variation in estimates of predator biomass, with the highest predation occurring in the Malindi MNP, a site with high coralline algal cover. Stepwise multiple regression analysis with 14 variables of coral predators and substratum showed that coralline algae was positively, and turf algae negatively associated with mortality of the transplants, with all other variables being statistically insignificant. This suggests that alternate food resources and predator choices are more important than predator biomass in determining coral survival. Nonetheless, large predatory fish in areas dominated by coralline algae may considerably retard recovery of eurythermal corals. This will not necessarily retard total hard coral recovery, as other more predator-tolerant taxa can recover. Based on the results, global climate change will not necessarily favor eurythermal over stenothermal coral taxa in remote or unfished reefs, where predation is a major cause of coral mortality.