Experimental separation of effects of consumers on sessile prey in the low zone of a rocky shore in the Bay of Panama: direct and indirect consequences of food web complexity

The effects of predation by a diverse assemblage of consumers on community structure of sessile prey was evaluated in the low rocky intertidal zone at Taboguilla Island in the Bay of Panama. Four functional groups of consumers were defined: (1) large fishes, (2) small fishes and crabs, (3) herbivorous molluscs, and (4) predaceous gastropods, (l) and (2) included fast-moving consumers and (3) and (4) included slow-moving consumers. Experimental treatments were: no consumers deleted (all groups present), most combinations of deletions of single groups (i.e., one group absent, three present), pairs of groups deleted (two absent, two present), trios of groups deleted (three absent, one present), and the entire consumer assemblage deleted (all groups absent). Changes in abundance (percent cover) of crustose algae, solitary sessile invertebrates, foliose algae, and colonial sessile invertebrates were quantified periodically in 2–4 plots of each treatment from February 1977 to January 1980 after the initiation of the experiment in January 1977.

Space on this shore is normally dominated by crustose algae; foliose algae, solitary sessile invertebrates, and colonial sessile invertebrates are all rare. After deletion of all consumers, ephemeral green algae increased from 0 to nearly 70% cover. Thereafter, a succession of spatial dominants occurred, with peak abundances as follows: the foliose coralline alga Jania spp. by July 1977, the barnacle Balanus inexpectatus by April 1978, and the rock oyster Chama echinata by January 1980. Although no longer occupying primary rock space, Jania persisted as a dominant or co-dominant turf species (with the brown alga Giffordia mitchelliae and/or the hydrozoan Abietinaria sp.) by colonizing shells of sessile animals as they became abundant instead of the rock surface.

Multivariate analysis variance (MANOVA) indicated that the effect of each group was as follows. Molluscan herbivores grazed foliose algae down to the grazer-resistant, but competitively inferior algal crusts, altered the relative abundances of the crusts, and inhibited recruitment of sessile invertebrates. Predaceous gastropods reduced the abundance of solitary sessile animals. Small fishes and crabs, and large fishes reduced the cover of solitary and colonial sessile animals and foliose algae, although they were incapable of grazing the foliose algae down to the rock surface. Many of the effects of each consumer group on prey groups or species were indirect; some effects were positive and some were negative. The variety of these indirect effects was due to both consumer-prey interactions among the consumers, and competitive or commensalistic interactions among the sessile prey. Comparison of the sum of the effects of each of the single consumer groups (i.e., the sum of the effect observed in treatments with one group absent, three present) with the total effects of all consumers (i.e., the effect observed in the treatment with all groups absent) indicates that a “keystone” consumer was not present in this community. Rather, the impacts of the consumer groups were similar but, due to dietary overlap and compensatory changes among the consumers, not readily detected in deletions of single consumer groups. The normally observed dominance of space by crustose algae is thus maintained by persistent, intense predation by a diverse assemblage of consumers on potentially dominant sessile animals and foliose algae. The large difference in structure between this and temperate intertidal communities seems due to differences in degree, not kind of ecological processes which produce the structure.     

A test of the Menge-Sutherland model of community organization in a tropical rocky intertidal food web

Summary Menge and Sutherland (1976) predicted that in physically benign habitats: (1) community structure will be most strongly affected be predation, (2) the effect of predation will increase with a decrease in trophic position in the food web, (3) trophically intermediate species will be influenced by both predation and competition, and (4) competition will occur among prey species which successfully escape consumers. These predictions were tested in a tropical rocky intertidal community on the Pacific coast of Panama. The most abundant mobile species included fishes and crabs, which occupied the top trophic level, and predaceous gastropods and herbivorous molluscs, which occupied intermediate trophic levels. The most abundant sessile organisms were encrusting algae, foliose algae, barnacles, and bivalves. Diets were broad and overlapping, and 30.3% of the consumers were omnivorous. Each consumer group had strong effects on prey occurring at lower trophic levels: (1) Fishes and crabs reduced the abundance of predaceous snails, herbivorous molluscs, foliose algae, and sessile invertebrates. (2) Predaceous gastropods reduced the abundance of herbivorous molluscs and sessile invertebrates. (3) Herbivorous molluscs reduced the abundance of foliose algae and young stages of sessile invertebrates, and altered relative abundances of the encrusting algae. The encrusting algae, although normally the dominant space occupiers, proved to be inferior competitors for space with other sessile organisms when consumers were experimentally excluded. However, the crusts escaped consumers by virtue of superior anti-herbivore defenses and competed for space despite intense grazing. Observations do not support the hypothesis that the trophically intermediate species compete. Hence, with the exception of this last observation, the predictions of the Menge and Sutherland model were supported. Although further work is needed to evaluate other predictions of the model in this community, evidence from this study joins an increasing body of knowledge supporting the model. Contradictory evidence also exists, however, indicating that aspects of the model require revision.     

Ecological Shifts in Mediterranean Coralligenous Assemblages Related to Gorgonian Forest Loss

Mediterranean gorgonian forests are threatened by several human activities and are affected by climatic anomalies that have led to mass mortality events in recent decades. The ecological role of these habitats and the possible consequence of their loss are poorly understood. Effects of gorgonians on the recruitment of epibenthic organisms were investigated by manipulating presence of gorgonians on experimental panels at 24 m depth, for Eunicella cavolinii, and at 40 m depth, for Paramuricea clavata, at two sites: Tavolara Island (Tyrrhenian Sea) and Portofino Promontory (Ligurian Sea). After 4 months, the most abundant taxa on the panels were encrusting green algae, erect red algae and crustose coralline algae at 24 m depth and encrusting brown algae and erect red algae at 40 m depth. Assemblages on the panels were significantly affected by the presence of the gorgonians, although effects varied across sites and between gorgonian species. Species diversity and evenness were lower on panels with gorgonian branches. Growth of erect algae and recruitment of serpulid polychaetes were also affected by the presence of the gorgonians, primarily at Tavolara. Crustose coralline algae and erect sponges were more abundant on E. cavolinii panels at 24 m depth, while encrusting bryozoans were more abundant on P. clavata panels at 40 m depth. Effects of gorgonians on recruited assemblages could be due to microscale modification of hydrodynamics and sediment deposition rate, or by a shading effect reducing light intensity. Gorgonians may also intercept settling propagules, compete for food with the filter-feeders and/or for space by producing allelochemicals. Presence of gorgonians mainly limits the growth of erect algae and enhances the abundance of encrusting algae and sessile invertebrates. Therefore, the gorgonian disappearances may cause a shift from assemblages characterised by crustose coralline algae to filamentous algae assemblages, decreasing complexity and resilience of coralligenous bioconstructions.     

FIELD MEASUREMENTS OF INORGANIC NITROGEN UPTAKE BY EPIFLORA COMPONENTS OF THE SEAGRASS POSIDONIA OCEANICA (MONOCOTYLEDONS,POSIDONIACEAE)1

Crustose corallines, crustose and erect brown algae, and sessile animals are major components of the epiphytic community of the Mediterranean seagrass Posidonia oceanica (L.) Delile. Production, biomass, and specific composition of this epiphyte–seagrass association are impacted by anthropogenic increase of nutrient load in this oligotrophic area. In this context, nitrogen uptake by P. oceanica and its epiflora was measured using the isotope ¹⁵N at a 10 m depth in the Revellata Bay (Corsica, Mediterranean Sea). Epiflora components showed various seasonal patterns of biomass and abundance. The epiphytic brown algae appeared at the end of spring, later than the crustose corallines, and after the nitrate peak in the bay. Because of their later development in the season, epiphytic brown algae mostly rely on ammonium for their N needs. We hypothesize that the temporal succession of epiphytic organisms plays a crucial role in the N dynamics of this community under natural conditions. The epiphytic brown algae, which have a growth rate one order of magnitude greater than that of crustose corallines, showed lower N‐uptake rates. The greater N‐uptake rates of crustose corallines probably reflect the greater N requirements (i.e., lower C/N ratios) of red algae. We determined that the epiflora incorporated ammonium and nitrate more rapidly than their host. Nevertheless, when biomass was taken into account, P. oceanica was the most important contributor to N uptake from the water column by benthic macrophytes in this seagrass bed.     

INTERSPECIFIC INTERACTIONS AND SCARCITY OF A TROPICAL LIMPET

The øcmaeid limpet Lottia stipulata occurs in the midintertidal zone of rocky Pacific shores from Colombia to ElSalvador. It is regularly present but rare (<1 m^–2)at wave-exposed to semi-protected sites in Panama. The verticaldistribution of Lottia overlaps that of a pulmonate limpet,Siphonaria gigas, the most abundant molluscan grazer in themid zone (28. m^–2). Manipulations of the density of Siphonariasuggest the pulmonate negatively affects the recruitment, growth,and abundance of Lottia. Observations of populations of limpetsin an area undergoing succession support these results –Lottia recruits quickly and reaches high levels of abundance,but cannot maintain high densities as other benthic consumerslike S. gigas settle and increase in numbers over time. Paradoxically,examination of radulae suggests that if ability to use algalcrusts (the major available food) were of primary importance,Lottia would be the superior competitor. However, competitionneed not be invoked, and results can be explained by a one-wayrelationship between these two limpets. Lottia apparently hasno effect on Siphonaria, but the larger pulmonate probably actsas an agent of disturbance by interfering with foraging by Lottiaand by bulldozing or consuming newly-settled individuals. Predationon Lottia by a predaceous gastropod, Purpura columellaris, andby the American oystercatchcr, Haematopus palliatus, is insignificantat most sites, but may be important where these consumers areabundant. The abundance of Lottia appears to be controlled primarilyby disturbance by Siphonaria and by physical factors, not bypredation or competition. ¹Present address: Department of Zoology, University of Massachusetts,Amherst, Massachusetts 01003 ²Present address: Department of Zoology, University of RhodeIsland, Kingston, Rhode Island 02881 ³Order of authorship determined by coin toss. (Received 31 July 1984;     

Effects of macrophyte growth forms on invertebrate communities in saline lakes of the Wyoming High Plains

In saline lakes, areal cover and both species and structural diversity of macrophytes often decline as salinity increases. To assess effects of the loss of certain macrophyte growth forms, we characterized benthic and epiphytic invertebrates in three growth forms (thin-stemmed emergents, erect aquatics, and low macroalgae) in oligosaline lakes (0.8–4.2 mS cm⁻¹) of the Wyoming High Plains, USA. We also measured the biomass and taxonomic composition of epiphytic and benthic invertebrates in two erect aquatics with very similar structure that are found in both oligosaline (Potamogeton pectinatus) and mesosaline (9.3–23.5 mS cm⁻¹) (Ruppia maritima) lakes. Although total biomass of epiphytic invertebrates varied among oligosaline lakes, the relative distribution of biomass among growth forms was similar. For epiphytic invertebrates, biomass per unit area of lake was lowest in emergents and equivalent in erect aquatics and low macroalgae; biomass per unit volume of macrophyte habitat was greatest in low macroalgae. For benthic invertebrates, biomass was less beneath low macroalgae than other growth forms. Taxonomic composition did not differ appreciably between growth forms for either benthic or epiphytic invertebrates, except that epiphytic gastropods were more abundant in erect aquatics. Total biomass of epiphytic and benthic invertebrates for the same growth form (erect aquatic) did not differ between oligosaline (Potamogeton pectinatus) and mesosaline (Ruppia maritima) lakes, but taxonomic composition did change. In the oligosaline to mesosaline range, direct toxic effects of salinity appeared important for some major taxa such as gastropods and amphipods. However, indirect effects of salinity, such as loss of macrophyte cover and typically higher nutrient levels at greater salinities, probably have larger impacts on total invertebrate biomass lake-wide.     

Diversity,heterogeneity and consumer pressure in a tropical rocky intertidal community

Summary Previous studies indicated that at Taboguilla Island (Gulf of Panama), persistence of many intertidal organisms depended on holes and crevices in the rock as refuges from both vertebrate (fishes) and invertebrate (crabs, gastropods, chitons) consumers. Here, we evaluate the influences of substratum heterogeneity and consumers on patterns of diversity of sessile organisms in this habitat. Local substratum topography is highly variable, ranging from smooth to irregular surfaces. Algal crusts typically dominate all low zone rock surfaces, and most other sessile spegies (invertebrates and foliose algae) occur in holes and crevices. Number (S) and diversity (H) of sessile species is lower on homogeneous surfaces than on heterogeneous surfaces. Rate of increase in S with area sampled is positively correlated with substratum heterogeneity; number of species sampled per transect at a homogeneous site would be about 10 vs 30 to 60 on a heterogeneous site. Large fishes and crabs forage intensively over both substratum types, but cannot enter holes and crevices to eat prey. Gastropods, chitons, limpets, and small crabs feed on both substrata but vary in abundance from hole to hole. Prey mortality is thus intense and constant on open surfaces, but variable in space and time in holes and crevices. When consumers are excluded from the general rock surface, algal crusts are settled upon and overgrown by foliose algae, hydrozoans, and sessile invertebrates, particularly bivalves. Both S and H first increase, as sessile species invade and become more abundant, and then decrease as the rock oyster Chama echinata begins to outcompete other species and dominate primary space. Hence, consumers normally keep local diversity low by removing most sessile prey from open surfaces.In these experiments, a consumer pressure gradient was established by removing 0, 1, 2, 3, and all of 4 distinct groups of consumers. As predicted by the intermediate disturbance hypothesis, lowest diversity occurred at lowest (total exclusion) and highest consumer pressure (normal condition). Highest diversity occurred at intermediate consumer pressure. Unexplained variation in this relationship is probably due to quantitative and qualitative differences in consumer regime, variation among plots in substratum heterogeneity, and insufficient time for competitive dominance by Chama to be fully expressed. On a small (0.25 m²) spatial scale, consumers maintain low diversity by keeping prey scarce and causing local extinctions. On larger spatial scales, they may maintain and even produce high diversity through their interaction with substratum heterogeneity and possibly low dispersal rates of sessile species.     

Spatial variation of reef fishes and the relative influence of biotic and abiotic habitat traits

Patterns of distribution of reef fishes were examined across three spatial scales and related to habitat traits along 25 km of the northern Portuguese coast. Response variables included the multivariate assemblage structure, the total number of taxa and individuals, and the abundance of single groups categorized according to their preference for the benthic, proximo-benthic or pelagic environment, feeding and reproductive behaviour. Habitat traits included topographic elements (small and large ‘drops’ like cracks and crevices) and the extent of dominant morpho-functional types of macroalgae (kelp, large foliose, small erect, turf-forming filamentous, and encrusting). All fish responses were characterized by the largest variance at the smallest scale (among transects tens m apart), followed by that among reefs (hundreds m to 1 km apart) and almost null variance among sites (some km apart). Small and large ‘drops’ of the substratum explained, respectively, considerable variation of assemblage structure and the total abundance of individuals, while the extent of bare rock influenced the richness of taxa and that of benthic fishes, fishes feeding on sessile invertebrates and fishes laying benthic eggs or having nesting behaviour. Combinations of abiotic and biotic structural attributes of reefs influenced proximo-benthic fishes, the predators of mobile animals and fishes releasing pelagic eggs. The here reported associations between patterns of distribution of reef fishes and habitat traits have implications for the design of future protection schemes suitable to guarantee the conservation of reef fish communities and of the processes responsible for their variation. Within the SLOSS (single-large vs. several-small) debate in the design of marine reserves, for example, effective protection to the studied reef fishes would be provided by a set of small reserves, rather than a single large which might be appropriate for fishes having wider home ranges.     

Re-evaluating the health of coral reef communities: baselines and evidence for human impacts across the central Pacific

Numerous studies have documented declines in the abundance of reef-building corals over the last several decades and in some but not all cases, phase shifts to dominance by macroalgae have occurred. These assessments, however, often ignore the remainder of the benthos and thus provide limited information on the present-day structure and function of coral reef communities. Here, using an unprecedentedly large dataset collected within the last 10 years across 56 islands spanning five archipelagos in the central Pacific, we examine how benthic reef communities differ in the presence and absence of human populations. Using islands as replicates, we examine whether benthic community structure is associated with human habitation within and among archipelagos and across latitude. While there was no evidence for coral to macroalgal phase shifts across our dataset we did find that the majority of reefs on inhabited islands were dominated by fleshy non-reef-building organisms (turf algae, fleshy macroalgae and non-calcifying invertebrates). By contrast, benthic communities from uninhabited islands were more variable but in general supported more calcifiers and active reef builders (stony corals and crustose coralline algae). Our results suggest that cumulative human impacts across the central Pacific may be causing a reduction in the abundance of reef builders resulting in island scale phase shifts to dominance by fleshy organisms.     

珊瑚藻类对南麂列岛潮间带底栖生物群落多样性的影响

为了解南麂列岛潮间带珊瑚藻类对于其他大型藻类和底栖动物的影响, 在南麂列岛国家级海洋自然保护区布设了4条潮间带断面, 于2012年5月至2013年2月对其生物状况进行了逐季调查, 分别分析了中低潮区大型藻类、非珊瑚藻大型藻类、底栖动物的物种多样性和均匀度, 并计算了大型底栖动物的功能多样性指数Rao's Q。主要结果如下: (1)共采集和鉴定出大型藻类52种, 其中珊瑚藻科藻类有5种; (2)珊瑚藻类在高潮区没有分布, 在中低潮区均占据优势, 占潮间带藻类生物量的68.9%。四季中低潮区大型藻类的Shannon-Wiener多样性指数范围为1.638-4.044, 非珊瑚藻大型藻类的多样性指数范围为1.495-3.809, 底栖动物为5.289-6.917; 大型藻类的Pielou均匀度指数范围为0.819-0.971, 非珊瑚藻大型藻类的均匀度指数范围为0.830-0.973, 底栖动物为0.967-0.988; (3)大型藻类物种多样性和均匀度指数的降低与珊瑚藻类优势度的增加相关, 但珊瑚藻类优势度与底栖动物物种多样性指数、均匀度指数和功能多样性指数均没有显著相关性; (4)底栖动物功能多样性与珊瑚藻类优势度均呈低潮区高于中潮区的变化规律, 但相关性分析表明两者间并无直接联系。推测珊瑚藻类通过竞争占据了其他藻类的生存空间, 从而降低了南麂列岛潮间带大型藻类的物种多样性和均匀度。底栖动物则因其自身生活特点而使得珊瑚藻类的扩张未能影响其多样性水平。     

Bioerosion of gastropod shells: with emphasis on effects of coralline algal cover and shell microstructure

Organisms boring into fifty nine species of gastropod shells on reefs around Guam were the bryozoan Penetrantia clionoides; the acrothoracian barnacles Cryptophialus coronorphorus, Cryptophialus zulloi and Lithoglyptis mitis; the foraminifer Cymbaloporella tabellaeformis, the polydorid Polydora sp. and seven species of clionid sponge. Evidence that crustose coralline algae interfere with settlement of larvae of acrothoracian barnacles, clionid sponges, and boring polychaetes came from two sources: (1) low intensity of boring in limpet shells, a potentially penetrable substrate that remains largely free of borings by virtue of becoming fully covered with coralline algae at a young age and (2) the extremely low levels of boring in the algal ridge, a massive area of carbonate almost entirely covered by a layer of living crustose corallines. There was a strong negative correlation between microstructural hardness and infestation by acrothoracian barnacles and no correlation in the case of the other borers. It is suggested that this points to a mechanical rather than a chemical method of boring by the barnacles. The periostracum, a layer of organic material reputedly a natural inhibitor of boring organisms, was bored by acrothoracican barnacles and by the bryozoan. The intensity of acrothoracican borings is shown to have no correlation with the length of the gastropod shell.     

Limited evidence for ecosystem‐level change on reefs exposed to Haliotis rubra (‘blacklip abalone’) exploitation

It is increasingly recognized that fisheries must take the broader ecosystem into account for sustainable management of marine systems, requiring an understanding of the interaction between fished species and other organisms. This study uses a correlative approach to investigate potential interactions between benthic organisms and Haliotis rubra, a dominant herbivore that is the subject of a large and valuable commercial fishery in south‐eastern Australia. Specific emphasis was placed on understanding associations between H. rubra and understorey organisms, because particular understorey algae (crustose coralline algae) provide critical habitat for H. rubra larval recruitment and juvenile ecology. Broad‐scale surveys along the 6–8 m depth contour (the depth range where H. rubra fishing activity is intense) were conducted across four regions (separated by 10⁴?10⁵ m), including at least 10 sites (separated by 10²?10³ m) within each region. Positive correlations between H. rubra and crustose coralline algae were found, while negative correlations were observed between H. rubra and sessile invertebrates and understorey algae. While significant, these associations were weak and H. rubra abundance generally only explained a small proportion of the variability in the abundance of understorey organisms (r² 0.02–0.30). H. rubra abundance also had a minor influence on community‐level understorey patterns in comparison with differences in community structure attributable to regional variation. Patterns of H. rubra abundance and benthic community structure were also examined in relation to depth at a restricted number of sites. At sites where differences in understorey groups were evident, H. rubra abundance also varied significantly, highlighting the issue of confounding when contrasting patterns of understorey abundance using a correlative approach. Further manipulative experiments are required to confirm causal relationships; however, the available correlative evidence suggests limited ecosystem effects of H. rubra depletion at the scale of individual reefs.     

Reef fish community structure in the Tropical Eastern Pacific (Panamá): living on a relatively stable rocky reef environment

We compared the community structure of reef fish over different physical complexities in 12 study zones of Bahía Honda, Gulf of Chiriquí (BH-GCH), Tropical Eastern Pacific (TEP), Panama, aiming at an analysis of the importance of the physical structure provided by corals, rocks and benthic sessile organisms. This was the first region that emerged in the Isthmus of Panama; it exhibits the oldest benthic fauna and has constant conditions in terms of temperature and salinity. Two hundred and eighty-eight visual fish censuses were conducted on 48 benthic transects from February to July 2003. One hundred and twenty-six fish species of 44 families were found. Plankton feeding pomacentrids and labrids along with haemulids that feed on mobile invertebrates were the most abundant, particularly in shallow areas. Fourteen species showed size-segregations between zones, suggesting ontogenetic migrations (smaller fishes in shallow high-complexity zones, larger-sized fishes in deeper habitats). Highly mobile and site-attached genera were abundant in most shallow, wave-exposed zones particularly on exposed rocky substrates. Planktivores were the most abundant, followed by carnivores, feeders on mobile invertebrate and piscivores. Herbivores and feeders on sessile invertebrate were lower in abundance. Species richness exceeds that of any other studied region close to the mainland in the TEP and correlates with substrate diversity, increasing size-heterogeneity of holes and structural complexity. Species diversity increases with habitat complexity and benthic diversity. It seems that water current strength, tides and waves which select for swimming, play an important role in the community organization. The study region has been proposed as a refuge-centre in the TEP, where reef fishes that evolved on coral reefs have shifted their distribution onto rocky reef habitats.     

Community Structure of Fishes and Habitat Complexity on a Tropical Rocky Shore

The relationship between the variables of reef fish community structure (fish richness, fish diversity and total number of fishes) and those of habitat complexity (total surface area, substratum diversity, topographic complexity, number of holes, percent cover of turf algae, zoanthids, millepores, massive corals, bare rock, encrusting calcareous algae, urchins, other sessile organisms and Sargassum) were examined on three different rocky shores (FA, FB and FT) at Arraial do Cabo, a tropical region located on Brazilian southeastern coast (23° S, 42° W). Fish abundance and vertical distribution were assessed by a visual census technique using strip transects. Percentage cover of benthic organisms and other substratum types were calculated by replicated transects using a chain laid down on the substratum. Topographic complexity was determined by the chain link method and number of holes were estimated by direct counts on replicated transects. More than 91 fishes belonging to 37 families were seen in all study sites during one year of visual census effort. FA and FB sites had similar fish community structure and habitat complexity characteristics, while FT showed different habitat characteristics and higher fish diversity and richness, plus total number of fishes. Vertical distribution of fishes along the rocky shores studied seemed to be predictable and was determined by factors such as feeding habits and behavior, availability of refuges and social interactions. The habitat variables that best explained the higher diversity and number of fishes observed in FT site were total surface area of rocky shores and the abundance of benthic sessile invertebrates; these conditions were typical of rocky shores more exposed to wave surge.     

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.     

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.     

Hyperspectral and Physiological Analyses of Coral-Algal Interactions

Space limitation leads to competition between benthic, sessile organisms on coral reefs. As a primary example, reef-building corals are in direct contact with each other and many different species and functional groups of algae. Here we characterize interactions between three coral genera and three algal functional groups using a combination of hyperspectral imaging and oxygen microprofiling. We also performed in situ interaction transects to quantify the relative occurrence of these interaction on coral reefs. These studies were conducted in the Southern Line Islands, home to some of the most remote and near-pristine reefs in the world. Our goal was to determine if different types of coral-coral and coral-algal interactions were characterized by unique fine-scale physiological signatures. This is the first report using hyperspectral imaging for characterization of marine benthic organisms at the micron scale and proved to be a valuable tool for discriminating among different photosynthetic organisms. Consistent patterns emerged in physiology across different types of competitive interactions. In cases where corals were in direct contact with turf or macroalgae, there was a zone of hypoxia and altered pigmentation on the coral. In contrast, interaction zones between corals and crustose coralline algae (CCA) were not hypoxic and the coral tissue was consistent across the colony. Our results suggest that at least two main characteristic coral interaction phenotypes exist: 1) hypoxia and coral tissue disruption, seen with interactions between corals and fleshy turf and/or some species of macroalgae, and 2) no hypoxia or tissue disruption, seen with interactions between corals and some species of CCA. Hyperspectral imaging in combination with oxygen profiling provided useful information on competitive interactions between benthic reef organisms, and demonstrated that some turf and fleshy macroalgae can be a constant source of stress for corals, while CCA are not.     

Microbial to reef scale interactions between the reef-building coral Montastraea annularis and benthic algae

Competition between reef-building corals and benthic algae is of key importance for reef dynamics. These interactions occur on many spatial scales, ranging from chemical to regional. Using microprobes, 16S rDNA pyrosequencing and underwater surveys, we examined the interactions between the reef-building coral Montastraea annularis and four types of benthic algae. The macroalgae Dictyota bartayresiana and Halimeda opuntia, as well as a mixed consortium of turf algae, caused hypoxia on the adjacent coral tissue. Turf algae were also associated with major shifts in the bacterial communities at the interaction zones, including more pathogens and virulence genes. In contrast to turf algae, interactions with crustose coralline algae (CCA) and M. annularis did not appear to be antagonistic at any scale. These zones were not hypoxic, the microbes were not pathogen-like and the abundance of coral-CCA interactions was positively correlated with per cent coral cover. We propose a model in which fleshy algae (i.e. some species of turf and fleshy macroalgae) alter benthic competition dynamics by stimulating bacterial respiration and promoting invasion of virulent bacteria on corals. This gives fleshy algae a competitive advantage over corals when human activities, such as overfishing and eutrophication, remove controls on algal abundance. Together, these results demonstrate the intricate connections and mechanisms that structure coral reefs.     

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.     

Effects of coral reef benthic primary producers on dissolved organic carbon and microbial activity

Benthic primary producers in marine ecosystems may significantly alter biogeochemical cycling and microbial processes in their surrounding environment. To examine these interactions, we studied dissolved organic matter release by dominant benthic taxa and subsequent microbial remineralization in the lagoonal reefs of Moorea, French Polynesia. Rates of photosynthesis, respiration, and dissolved organic carbon (DOC) release were assessed for several common benthic reef organisms from the backreef habitat. We assessed microbial community response to dissolved exudates of each benthic producer by measuring bacterioplankton growth, respiration, and DOC drawdown in two-day dark dilution culture incubations. Experiments were conducted for six benthic producers: three species of macroalgae (each representing a different algal phylum: Turbinaria ornata – Ochrophyta; Amansia rhodantha – Rhodophyta; Halimeda opuntia – Chlorophyta), a mixed assemblage of turf algae, a species of crustose coralline algae (Hydrolithon reinboldii) and a dominant hermatypic coral (Porites lobata). Our results show that all five types of algae, but not the coral, exuded significant amounts of labile DOC into their surrounding environment. In general, primary producers with the highest rates of photosynthesis released the most DOC and yielded the greatest bacterioplankton growth; turf algae produced nearly twice as much DOC per unit surface area than the other benthic producers (14.0±2.8 µmol h⁻¹ dm⁻²), stimulating rapid bacterioplankton growth (0.044±0.002 log10 cells h⁻¹) and concomitant oxygen drawdown (0.16±0.05 µmol L⁻¹ h⁻¹ dm⁻²). Our results demonstrate that benthic reef algae can release a significant fraction of their photosynthetically-fixed carbon as DOC, these release rates vary by species, and this DOC is available to and consumed by reef associated microbes. These data provide compelling evidence that benthic primary producers differentially influence reef microbial dynamics and biogeochemical parameters (i.e., DOC and oxygen availability, bacterial abundance and metabolism) in coral reef communities.