Nanette E. Chadwick

Bacterial associates of two Caribbean coral species reveal species-specific distribution and geographic variability.

ABSTRACT Scleractinian corals harbor microorganisms that form dynamic associations with the coral host and exhibit substantial genetic and ecological diversity. Microbial associates may provide defense against pathogens and serve as bioindicators of changing environmental conditions. Here we describe the bacterial assemblages associated with two of the most common and phylogenetically divergent reef-building corals in the Caribbean, Montastraea faveolata and Porites astreoides. Contrasting life history strategies and disease susceptibilities indicate potential differences in their microbiota and immune function that may in part drive changes in the composition of coral reef communities. The ribotype structure and diversity of coral-associated bacteria within the surface mucosal layer (SML) of healthy corals were assessed using denaturing gradient gel electrophoresis (DGGE) fingerprinting and 454 bar-coded pyrosequencing. Corals were sampled at disparate Caribbean locations representing various levels of anthropogenic impact. We demonstrate here that M. faveolata and P. astreoides harbor distinct, host-specific bacteria but that specificity varies by species and site. P. astreoides generally hosts a bacterial assemblage of low diversity that is largely dominated by one bacterial genus, Endozoicomonas, within the order Oceanospirillales. The bacterial assemblages associated with M. faveolata are significantly more diverse and exhibit higher specificity at the family level than P. astreoides assemblages. Both corals have more bacterial diversity and higher abundances of disease-related bacteria at sites closer to the mainland than at those furthest away. The most diverse bacterial taxa and highest relative abundance of disease-associated bacteria were seen for corals near St. Thomas, U.S. Virgin Islands (USVI) (2.5 km from shore), and the least diverse taxa and lowest relative abundance were seen for corals near our most pristine site in Belize (20 km from shore). We conclude that the two coral species studied harbor distinct bacterial assemblages within the SML, but the degree to which each species maintains specific microbial associations varies both within each site and across large spatial scales. The taxonomic scale (i.e., phylum versus genus) at which scientists examine coral-microbe associations, in addition to host-elicited factors and environmental fluctuations, must be considered carefully in future studies of the coral holobiont.

Competition Among Sessile Organisms on Coral Reefs

Competition among sessile organisms is a major process on coral reefs, and is becoming more important as anthropogenic disturbances cause shifts in dominance to non-reef builders such as macroalgae, soft corals, ascidians, and corallimorpharians. Long-term monitoring and field experiments have demonstrated that competition for limited space can exert major impacts on reef biodiversity and community composition across habitats and regions. Recent experiments also reveal increasingly important roles of allelopathic chemicals and the alteration of associated microbes in shaping competitive outcomes among benthic space occupiers. Competition impacts the recruitment, growth, and mortality of sessile reef organisms and alters their population dynamics. Co-settlement and aggregation of conspecific coral colonies may lead to intense intraspecific competition, including chimera formation and potential somatic and germ cell parasitism. The complexity of competitive outcomes and their alteration by a wide variety of factors, including irradiance, water motion, and nutrient levels, results in mostly circular networks of interaction, often enhancing species diversity on coral reefs. Competition is a model process for revealing impacts of human activities on coral reefs, and will become increasingly important as alternate dominants gain space at the expense of reef-building corals.

Allelochemicals produced by Caribbean macroalgae and cyanobacteria have species-specific effects on reef coral microorganisms

Coral populations have precipitously declined on Caribbean reefs while algal abundance has increased, leading to enhanced competitive damage to corals, which likely is mediated by the potent allelochemicals produced by both macroalgae and benthic cyanobacteria. Allelochemicals may affect the composition and abundance of coral-associated microorganisms that control host responses and adaptations to environmental change, including susceptibility to bacterial diseases. Here, we demonstrate that extracts of six Caribbean macroalgae and two benthic cyanobacteria have both inhibitory and stimulatory effects on bacterial taxa cultured from the surfaces of Caribbean corals, macroalgae, and corals exposed to macroalgal extracts. The growth of 54 bacterial isolates was monitored in the presence of lipophilic and hydrophilic crude extracts derived from Caribbean macroalgae and cyanobacteria using 96-well plate bioassays. All 54 bacterial cultures were identified by ribotyping. Lipophilic extracts from two species of Dictyota brown algae inhibited >50% of the reef coral bacteria assayed, and hydrophilic compounds from Dictyota menstrualis particularly inhibited Vibrio bacteria, a genus associated with several coral diseases. In contrast, both lipo- and hydrophilic extracts from 2 species of Lyngbya cyanobacteria strongly stimulated bacterial growth. The brown alga Lobophora variegata produced hydrophilic compounds with broad-spectrum antibacterial effects, which inhibited 93% of the bacterial cultures. Furthermore, bacteria cultured from different locations (corals vs. macroalgae vs. coral surfaces exposed to macroalgal extracts) responded differently to algal extracts. These results reveal that extracts from macroalgae and cyanobacteria have species-specific effects on the composition of coral-microbial assemblages, which in turn may increase coral host susceptibility to disease and result in coral mortality.

INTERSPECIFIC AGGRESSIVE BEHAVIOR OF THE CORALLIMORPHARIAN CORYNACTIS CALIFORNICA (CNIDARIA: ANTHOZOA): EFFECTS ON SYMPATRIC CORALS AND SEA ANEMONES

Corallimorpharians are sessile cnidarians that are morphologically similar to the actiniarian sea anemones and scleractinian corals. This study describes for the first time the behavioral mechanism and effects of aggression by a corallimorpharian. Polyps of the temperate clonal corallimorpharian Corynactis californica extruded their mesenteries and associated filaments onto members of certain species of sea anemones and corals. They did not exhibit this behavior intraspecifically, and members of different clones of C. californica remained expanded upon contact. In contrast, members of four species of corals and zoanthids responded to contact with C. californica by contracting their tentacles, and members of three sea anemone species bent or moved away, detached from the substrate, or attacked using their aggressive structures. When interspecific contact was prolonged, individuals of C. californica extruded filaments onto, and killed polyps of, the sea anemones Anthopleura elegantissima and Metridium senile within 3 weeks, and the corals Astrangia lajollaensis and Balanophyllia elegans within 4-10 months under laboratory conditions. The use of extruded mesenterial filaments by C. californica to attack members of other anthozoan species is similar to the aggressive behavior exhibited by many scleractinian reef corals. Field observations suggest that C. californica may use this agonistic behavior during interspecific competition for space on hard marine substrate.

Competition and locomotion in a free-living fungiid coral

Abstract Some fungiid corals asexually produce unconnected polyps that lie loose on the substratum between coral colonies. These free-living corals cannot build large three-dimensional structures and thus risk overgrowth during competition for space or light with colonial neighbors on coral reefs. This study examined the ecological importance and mechanisms of interspecific competitive damage and movement by the free-living fungiid coral Fungia scutaria (Lamarck). Over 40% of a population of F. scutaria on Hawaiian patch reefs was observed to contact other species of corals and macroalgae. F. scutaria caused unilateral damage to colonial corals in >94% of natural contacts. In contrast, macroalgae overgrew and smothered F. scutaria in all observed cases. During experimental field contacts, small polyps of F. scutaria moved away from resident coral colonies, while larger individuals remained in contact and induced tissue damage to residents. F. scutaria move over short distances by nocturnal expansion of tissues that push against adjacent surfaces. Laboratory and field experiments suggest that long-distance movement may be via passive transport by water motion. The mechanism of interspecific damage is unique among corals thus far studied; nocturnally expanded polyps deposit a thick layer of mucus 5–15 mm wide onto neighboring corals. The tissue of corals beneath this mucus layer becomes necrotic and sloughs off within 4 days. The abundant mucus secreted by F. scutaria contains numerous nematocysts, unlike that of all other Hawaiian corals examined to date. The ability of some free-living corals to actively damage or move away from encroaching corals may be important to their survival on reefs dominated by colonial species.

Abundance of giant sea anemones and patterns of association with anemonefish in the northern Red Sea

Patterns of distribution and abundance of giant sea anemones and anemonefish were compared among coral leefs along the coastline of Sinai in the northern Red Sea. The sea anemones varied widely in abundance between reef areas containing different habitat types. They were rare on steep reef slopes with abundant coral cover (=low-density anemone sites, 0.09 0.68 anemones per 1000 m 2 of reef area), but were common at a site containing patch reefs interspersed with sand (=high-density anemone site, 6.00-8.11 anemones per 1000 m 2 ). Distributions of the endemic two-band anemonefish (Amphiprion bicinctus) varied significantly between the two main host anemone species. At the high-density site, individuals of the sea anemone Heteractis crispa either did not contain anemonefish, or were occupied by single juvenile fish as shown in previous studies. At low-density sites H. crispa usually hosted clusters of juvenile anemone-fish. In contrast, individuals of the sea anemone Entacmaea quadricolor hosted either single adult fish (high-density site) or pairs of breeding adults (low-density sites), frequently in addition to some juvenile fish. Mechanisms that prevent anemonefish from reaching adult size and forming breeding pairs in H. crispa may include high fish mortality above a size threshold because this host cannot adequately protect them from predation when they become large, active emigration of fish to F. quadricolor as described in previous reports, and/or environmentally-controlled cessation of fish growth. We conclude that in the northern Red Sea, individuals of H. crispa potentially serve as nurseries for anemonefish.

Patterns of cleaning behaviour on coral reef fish by the anemoneshrimp Ancylomenes pedersoni

Little is known about the cleaning behaviour of shrimps in comparison to that of cleaner fish, and only recently have cleaner shrimps been shown to remove parasites effectively from coral reef fish. Here we describe patterns of cleaning interactions between Pederson shrimp Ancylomenes pedersoni and fish clients in St Thomas, US Virgin Islands. Clients observed here were members of at least 1 6 fish families, including three previously unreported client families. Most cleans lasted <20 seconds; surgeonfish were cleaned most frequently, but lizardfish and groupers received the longest cleans. The shrimp formed social groups of varying sizes on individuals of the host sea anemone Bartholomea annulata, which served as the centres of their cleaning stations. The number and duration of cleans per station increased with the number of resident shrimp, however most anemones hosted small groups of fewer than four individuals, while larger groups of up to nine individuals were relatively rare. Some cl i ent fish chased away other fish and competitively excluded them from anemone stations. We conclude that these shrimp clean a wide diversity of clients, vary their clean duration with fish identity, and clean more when in large groups. In addition, clients in part control these patterns of interaction by interfering with access to these stations by other clients.

Anemonefish oxygenate their anemone hosts at night

SUMMARY Many stony coral-dwelling fishes exhibit adaptations to deal with hypoxia among the branches of their hosts; however, no information exists on the respiratory ecophysiology of obligate fish associates of non-coral organisms such as sea anemones and sponges. This study investigated metabolic and behavioral interactions between two-band anemonefish (Amphiprion bicinctus) and bulb-tentacle sea anemones (Entacmaea quadricolor) at night. We measured the net dark oxygen uptake (, μmol O2 h−1) of fish–anemone pairs when partners were separate from each other, together as a unit, and together as a unit but separated by a mesh screen that prevented physical contact. We also measured the effects of water current on sea anemone and quantified the nocturnal behaviors of fish in the absence and presence of host anemones in order to discern the impacts of anemone presence on fish behavior. Net of united pairs was significantly higher than that of both separated pairs and united pairs that were separated by a mesh screen. Anemone increased with flow rate from 0.5 to 2.0 cm s−1, after which remained constant up to a water flow rate of 8.0 cm s−1. Furthermore, the percentage time and bout frequency of flow-modulating behaviors by fish increased significantly when anemones were present. We conclude that physical contact between anemonefish and sea anemones elevates the of at least one of the partners at night, and anemonefish behavior at night appears to oxygenate sea anemone hosts and to augment the metabolism of both partners.

Ammonia flux, physiological parameters, and Symbiodinium diversity in the anemonefish symbiosis on Red Sea coral reefs

Despite the ecological importance of anemonefish symbioses, little is known about how nutritional contributions from anemonefish interact with sea anemone physiology and Symbiodinium (endosymbiotic dinoflagellate) genetic identity under field conditions. On Red Sea coral reefs, we measured variation in ammonia concentrations near anemones, excretion rates of anemonefish, physiological parameters of anemones and Symbiodinium, and genetic identity of Symbiodinium within anemones. Ammonia concentrations among anemone tentacles were up to 49% above background levels, and anemonefish excreted ammonia significantly more rapidly after diurnal feeding than they did after nocturnal rest, similar to their excretion patterns under laboratory conditions. Levels of 4 physiological parameters (anemone protein content, and Symbiodinium abundance, chlorophyll a concentration, and division rate) were similar to those known for laboratory-cultured anemones, and in the field did not depend on the number of anemonefish per anemone or depth below sea surface. Symbiodinium abundance varied significantly with irradiance in the shaded reef microhabitats occupied by anemones. Most anemones at all depths harbored a novel Symbiodinium 18S rDNA variant within internal transcribed spacer region 2 (ITS2) type C1, while the rest hosted known ITS2 type C1. Association with Symbiodinium Clade C is consistent with the symbiotic pattern of these anemones on other Indo-Pacific reefs, but the C1 variant of Symbiodinium identified here has not been described previously. We conclude that in the field, anemonefish excrete ammonia at rapid rates that correlate with elevated concentrations among host anemone tentacles. Limited natural variation in anemonefish abundance may contribute to consistently high levels of physiological parameters in both anemones and Symbiodinium, in contrast to laboratory manipulations where removal of fish causes anemones to shrink and Symbiodinium to become less abundant.

Seychelles Lagoon Provides Corals with a Refuge from Bleaching

An extensive bleaching event in the summer of the year 1997-1998 affected most reefs along East Africas shores. In the aftermath of that episode, the reefs of Ile Alphonse in the Seychelles were examined and it was found that reefs along the seaward slopes of the island lost >95% of their branching coral colonies, with considerably higher survival of massive species. Ile Alphonse features a nearly circular shallow lagoon, with steep seaward slopes. Contrary to our expectations, mortality in the warmer lagoon was far lower than of coral colonies on the surrounding slopes, bathed in deeper and cooler waters. We suggest that corals in the lagoon were protected from UV radiation by leachate stemming from seagrass leaves steeped in the lagoon. Our measurements in the lagoon showed a strong attenuation of ultraviolet radiation, not observed in the waters outside the lagoon, and laboratory examination confirmed that the strong UV absorption of substances leached into seawater from decomposing leaves of the seagrass Thalassodendron (=Cymodocea) testudinaceum. Our findings demonstrate the synergism between elevated seawater temperature and UV radiation in triggering bleaching on shallow reefs.