Symbiodinium Photosynthesis in Caribbean Octocorals

Symbioses with the dinoflagellate Symbiodinium form the foundation of tropical coral reef communities. Symbiodinium photosynthesis fuels the growth of an array of marine invertebrates, including cnidarians such as scleractinian corals and octocorals (e.g., gorgonian and soft corals). Studies examining the symbioses between Caribbean gorgonian corals and Symbiodinium are sparse, even though gorgonian corals blanket the landscape of Caribbean coral reefs. The objective of this study was to compare photosynthetic characteristics of Symbiodinium in four common Caribbean gorgonian species: Pterogorgia anceps, Eunicea tourneforti, Pseudoplexaura porosa, and Pseudoplexaura wagenaari. Symbiodinium associated with these four species exhibited differences in Symbiodinium density, chlorophyll a per cell, light absorption by chlorophyll a, and rates of photosynthetic oxygen production. The two Pseudoplexaura species had higher Symbiodinium densities and chlorophyll a per Symbiodinium cell but lower chlorophyll a specific absorption compared to P. anceps and E. tourneforti. Consequently, P. porosa and P. wagenaari had the highest average photosynthetic rates per cm² but the lowest average photosynthetic rates per Symbiodinium cell or chlorophyll a. With the exception of Symbiodinium from E. tourneforti, isolated Symbiodinium did not photosynthesize at the same rate as Symbiodinium in hospite. Differences in Symbiodinium photosynthetic performance could not be attributed to Symbiodinium type. All P. anceps (n = 9) and P. wagenaari (n = 6) colonies, in addition to one E. tourneforti and three P. porosa colonies, associated with Symbiodinium type B1. The B1 Symbiodinium from these four gorgonian species did not cluster with lineages of B1 Symbiodinium from scleractinian corals. The remaining eight E. tourneforti colonies harbored Symbiodinium type B1L, while six P. porosa colonies harbored type B1i. Understanding the symbioses between gorgonian corals and Symbiodinium will aid in deciphering why gorgonian corals dominate many Caribbean reefs.     

Phenotypic plasticity or speciation? A case from a clonal marine organism

Background  

Clonal marine organisms exhibit high levels of morphological variation. Morphological differences may be a response to environmental factors but also they can be attributed to accumulated genetic differences due to disruption of gene flow among populations. In this study, we examined the extensive morphological variation (of 14 characters) in natural populations observed in the gorgonian Eunicea flexuosa, a widely distributed Caribbean octocoral. Eco-phenotypic and genetic effects were evaluated by reciprocal transplants of colonies inhabiting opposite ends of the depth gradient and analysis of population genetics of mitochondrial and nuclear genes, respectively.     

An inducible release of reactive oxygen radicals in four species of gorgonian corals

The capability for physical injury or heat stress to elicit the production of reactive oxygen species was examined in four species of gorgonian corals. The sea plumes Pseudopterogorgia elisabethae, Pseudopterogorgia americana, the sea rod Eunicea fusca and the azooxanthellate red branching gorgonian Lophogorgia chilensis were physically injured using sonic sound cavitations and heat shocked by incubation in 33°C sea water. The pharmacological probe, diphenylene iodonium chloride (DPI), an inhibitor of NAD(P)H oxidase and peroxidases was used to identify an enzymatic surrogate of the oxidative burst. Both injury and heat stress were capable of inducing the release of reactive oxygen species (ROS) in all gorgonians tested, yet the kinetics and amplitude of ROS release varied among genera. In both the treatments, P. americana demonstrated the largest oxidative burst among the other corals tested.     

Phenotypic plasticity and morphological integration in a marine modular invertebrate

Background  

Colonial invertebrates such as corals exhibit nested levels of modularity, imposing a challenge to the depiction of their morphological evolution. Comparisons among diverse Caribbean gorgonian corals suggest decoupling of evolution at the polyp vs. branch/internode levels. Thus, evolutionary change in polyp form or size (the colonial module sensu stricto) does not imply a change in colony form (constructed of modular branches and other emergent features). This study examined the patterns of morphological integration at the intraspecific level. Pseudopterogorgia bipinnata (Verrill) (Octocorallia: Gorgoniidae) is a Caribbean shallow water gorgonian that can colonize most reef habitats (shallow/exposed vs. deep/protected; 1–45 m) and shows great morphological variation.     

Patterns of chemical defense among Caribbean gorgonian corals: a preliminary survey

Ship-board assays employing the common Caribbean wrasse Thalassoma bifasdatum (Bloch) were undertaken to determine the palatability of food pellets coated with freshly-extracted, lipid-soluble metabolites of 37 types of Caribbean gorgonian corals representing at least 19 species from 11 genera. Extracts of 19 types (51%) were highly unpalatable (zero or one of five pellets eaten), four types (11%) were moderately unpalatable (two or three of five pellets eaten) and 14 (38%) were palatable (four or five of five pellets eaten) to fish in feeding assays. Gorgonians of the genera Pterogorgia (three types) and Eunicea (nine types) were consistently highly unpalatable, those of the genus Plexaurella (four types) were palatable and those of the genus Plexaura were most frequently palatable (six of eight types). Further assays of serial dilutions of extracts from seven representative, unpalatable types revealed that extracts inhibited fish feeding at pellet concentrations near or below the concentrations that metabolites occur in the gorgonian soft tissue. Extracts of Erythropodium caribaeorum (Duchassaing and Michelotti) and Pseudopterogorgia rigida (Bielschowsky) deterred fish feeding at pellet concentrations less than an order of magnitude lower than those found in the soft tissues of the corresponding gorgonians. Thin layer chromatographic analyses of extracts revealed the presence of lipid-soluble, secondary metabolites in a majority of the highly unpalatable extracts, although secondary metabolites were also present in a smaller percentage of palatable extracts. These data support the hypothesis that the soft tissues of many gorgonian corals contain lipid-soluble feeding deterrents which act as a defense against predation.     

Cryptic diversity hides host and habitat specialization in a gorgonian‐algal symbiosis

Shallow water anthozoans, the major builders of modern coral reefs, enhance their metabolic and calcification rates with algal symbionts. Controversy exists over whether these anthozoan–algae associations are flexible over the lifetimes of individual hosts, promoting acclimative plasticity, or are closely linked, such that hosts and symbionts co‐evolve across generations. Given the diversity of algal symbionts and the morphological plasticity of many host species, cryptic variation within either partner could potentially confound studies of anthozoan‐algal associations. Here, we used ribosomal, organelle and nuclear sequences, along with microsatellite variation, to study the relationship between lineages of a common Caribbean gorgonian and its algal symbionts. The gorgonian Eunicea flexuosa is a broadcast spawner, composed of two recently diverged, genetically distinct lineages largely segregated by depth. We sampled colonies of the two lineages across depth gradients at three Caribbean locations. We find that each host lineage is associated with a unique Symbiodinium B1/184 phylotype. This relationship between host and symbiont is maintained when host colonies are reciprocally transplanted, although cases of within phylotype switching were also observed. Even when the phylotypes of both partners are present at intermediate depths, the specificity between host and symbiont lineages remained absolute. Unrecognized cryptic diversity may mask host‐symbiont specificity and change the inference of evolutionary processes in mutualistic associations. Symbiotic specificity thus likely contributes to the ecological divergence of the two partners, generating species diversity within coral reefs.     

The genetic identity of dinoflagellate symbionts in Caribbean octocorals

Many cnidarians (e.g., corals, octocorals, sea anemones) maintain a symbiosis with dinoflagellates (zooxanthellae). Zooxanthellae are grouped into clades, with studies focusing on scleractinian corals. We characterized zooxanthellae in 35 species of Caribbean octocorals. Most Caribbean octocoral species (88.6%) hosted clade B zooxanthellae, 8.6% hosted clade C, and one species (2.9%) hosted clades B and C. Erythropodium caribaeorum harbored clade C and a unique RFLP pattern, which, when sequenced, fell within clade C. Five octocoral species displayed no zooxanthella cladal variation with depth. Nine of the ten octocoral species sampled throughout the Caribbean exhibited no regional zooxanthella cladal differences. The exception, Briareum asbestinum, had some colonies from the Dry Tortugas exhibiting the E. caribaeorum RFLP pattern while elsewhere hosting clade B. In the Caribbean, octocorals show more symbiont specificity at the cladal level than scleractinian corals. Both octocorals and scleractinian corals, however, exhibited taxonomic affinity between zooxanthella clade and host suborder.Communicated by R.C. Carpenter     

Species boundaries within the<Emphasis Type="Italic"> Acropora humilis</Emphasis> species group (Cnidaria; Scleractinia): a morphological and molecular interpretation of evolution

Species boundaries remain unresolved in many scleractinian corals. In this study, we examine evolutionary boundaries of species in the Acropora humilis species group. Five morphologically discrete units are recognized using principal components and hierarchical cluster analyses of quantitative and qualitative characters, respectively. Maximum parsimony and likelihood analyses of partial 28S rDNA sequences suggest that these morphological units diverged to form two evolutionarily distinct lineages, with A. humilis and A. gemmifera in one lineage and A. digitifera and two morphological types of A. monticulosa in the other. Low levels of sequence divergence but distinct morphologies of A. humilis and A. gemmifera within the former lineage suggest recent divergence or ongoing hybridization between these species. Substantially higher levels of divergence within and between A. digitifera and A. monticulosa suggest a more ancient divergence between these species, with sequence types being shared through occasional introgression without disrupting morphological boundaries. These results suggest that morphology has evolved more rapidly than the 28S rDNA marker, and demonstrate the utility of using morphological and molecular characters as complementary tools for interpreting species boundaries in corals.     

Inter- and intraspecific variation in gorgonian colony morphology: quantifying branching patterns in arborescent animals

Geomorphological methods for quantifying branching networks are used to describe inter- and intra-specific differences in branching patterns among two species of arborescent Caribbean gorgonian, Plexaura homomalla, P. flexuosa, and a third, undescribed plexaurid from the San Blas Islands, Panama. There were significant differences among species for first, second and third order branch lengths, and for tributary to source ratios for first and second order branches. Extrapolations from the branching parameters successfully predicted differences in the branch structure of naturally generated colony fragments. Within P. homomalla, significant differences with depth in the lengths and tributary to source ratios of first, second, and third order branches provide a measure of the greater bushiness of shallow water colonies. These measures can be used to quantify morphological differences in both ecological and systematic analyses. Data on the branching characters of these three gorgonian species demonstrate that gross colony form can be studied as a quantifiable component of phenotype and that gorgonians display both species level and ecophenotypic variation in colony form.     

New Species of Closely Related Endosymbiotic Dinoflagellates in the Greater Caribbean have Niches Corresponding to Host Coral Phylogeny

Symbiotic dinoflagellates in the genus Breviolum (formerly Symbiodinium Clade B) dominate coral communities in shallow waters across the Greater Caribbean. While some formally described species exist, mounting genetic, and ecological evidence indicate that numerous more comprise this genus, many of which are closely related. To test this, colonies of common reef‐building corals were sampled across a large geographical range. Phylogenetic and population genetic markers then used to examine evolutionary divergence and delineate boundaries of genetic recombination. Three new candidate species were distinguished by fixed differences in nucleotide sequences from nuclear and chloroplast DNA. Population connectivity was evident within each lineage over thousands of kilometers, however, substantial genetic structure persisted between lineages co‐occurring within sampling locations, signifying reproductive isolation. While geographically widespread with overlapping distributions, each species is ecologically distinct, exhibiting specific mutualisms with phylogenetically distinct coral hosts. Moreover, significant differences in mean cell sizes provide some morphological evidence substantiating formal species distinctions. In providing evidence that satisfies the biological, phylogenetic, ecological, and morphological species concepts, we classify and formally name Breviolum faviinorum n. sp., primarily associated with Caribbean corals belonging to the Caribbean subfamily Faviinae; B. meandrinium n. sp., associated with corals belonging to the family Meandrinidae; and B. dendrogyrum n. sp., a symbiont harbored exclusively by the threatened coral Dendrogyra cylindrus. These findings support the primary importance of niche diversification (i.e. host habitat) in the speciation of symbiotic dinoflagellates.     

Speciation‐by‐depth on coral reefs: Sympatric divergence with gene flow or cryptic transient isolation?

The distributions of many sister species in the sea overlap geographically but are partitioned along depth gradients. The genetic changes leading to depth segregation may evolve in geographic isolation as a prerequisite to coexistence or may emerge during primary divergence leading to new species. These alternatives can now be distinguished via the power endowed by the thousands of scorable loci provided by second‐generation sequence data. Here, we revisit the case of two depth‐segregated, genetically isolated ecotypes of the nominal Caribbean candelabrum coral Eunicea flexuosa. Previous analyses based on a handful of markers could not distinguish between models of genetic exchange after a period of isolation (consistent with secondary contact) and divergence with gene flow (consistent with primary divergence). Analyses of the history of isolation, genetic exchange and population size based on 15,640 new SNP markers derived from RNAseq data best support models where divergence began 800K BP and include epochs of divergence with gene flow, but with an intermediate period of transient isolation. Results also supported the previous conclusion that recent exchange between the ecotypes occurs asymmetrically from the Shallow lineage to the Deep. Parallel analyses of data from two other corals with depth‐segregated populations (Agaricia fragilis and Pocillopora damicornis) suggest divergence leading to depth‐segregated populations may begin with a period of symmetric exchange, but that an epoch of population isolation precedes more complete isolation marked by asymmetric introgression. Thus, while divergence‐with‐gene flow may account for much of the differentiation that separates closely related, depth‐segregated species, it remains to be seen whether any critical steps in the speciation process only occur when populations are isolated.     

Postembryonal morphological variation of <Emphasis Type="Italic">Daphnia galeata</Emphasis> in water bodies of different types

Despite many ecological studies the population morphological variability within the freshwater crustacean genus Daphnia is poorly investigated, especially during postembryonic development. Unusual phenotypic plasticity of some Daphnia species results in tremendous difficulties in morphological species delineation. The ontogenetic morphological variation of this species was studied, revealing the general trends in body shape variation in different populations. The morphotypes of size and age groups of D. galeata turned out to be more variable at the mouth of the Kargat River (Lake Chany basin) than in Lake Todzha (Bol’ shoi Yenisei River basin); however, the growth of characters such as the helmet and tail spine was described by an allometric function and their absolute sizes decreased with age in Daphnia from both water basins. It is shown that the first mature size-and-age group of D. galeata is most suitable for investigating population morphological variation.     

Cultivable bacteria associated with Caribbean octocorals are active against coral pathogens but exhibit variable bioactivity when grown under different temperature conditions

Caribbean scleractinian corals have been declining in recent decades while octocorals appear to be thriving. Although microbial communities associated with scleractinians have been extensively studied, less is known about octocoral-associated communities. To investigate whether octocoral-associated microorganisms can provide resistance against coral pathogens, bacteria from the mucus and external surfaces of three common Caribbean octocoral species (Gorgonia ventalina, Eunicea flexuosa, and Antillogorgia americana) were isolated. Isolates were tested for bioactivity against six scleractinian coral pathogens at three temperatures to capture potential differences under varying conditions. Production of bioactive metabolites was evaluated using disk diffusion assays while growth competition assays determined whether the pathogen and isolate could establish simultaneously. Over half of the isolates, members of the phyla Actinobacteria, Firmicutes and Proteobacteria, produced compounds that inhibited the growth of one or more pathogens with some variation in bioactivity noted across temperatures. When inoculated simultaneously, most isolates were able to grow in presence of the pathogens while temperature did not have a significant impact. Collectively, these results demonstrate that octocorals support a diverse group of culturable bacteria capable of competing against coral pathogens. The putative protective roles of these bacteria provide insight into why Caribbean octocorals may be less susceptible to diseases and might explain their increasing prevalence on degraded reefs.

     

Coral in Alaska: distribution,abundance, and species associations

To help identify fishery management actions that minimize the adverse impacts of fishing activities on corals in Alaska, the distribution and abundance of corals were analyzed based on trawl survey data collected during 1975–1998. We also examined the species of commercially managed fish that are associated with coral. Soft corals, primarily Gersemia sp. (=Eunephthya sp.), were the most frequently encountered corals in the Bering Sea. In the Aleutian Islands gorgonian corals, primarily in the genera Callogorgia, Primnoa, Paragorgia, Thouarella, and Arthrogorgia were the most common corals. In the Gulf of Alaska, gorgonian corals, primarily in the genera Callogorgia and Primnoa, and cup corals, primarily `Scleractinia unidentified', occurred most frequently. The Aleutian Islands area appears to have the highest abundance and diversity of corals. Some fish groups are associated with particular types of coral. Rockfish (Sebastes spp. and Sebastolobus alascanus) and Atka mackerel (Pleurogrammus monopterygius) were the most common fish captured with gorgonian, cup, and hydrocorals, whereas flatfish and gadids were the most common fish captured with soft corals.     

Gold coral (<Emphasis Type="Italic">Savalia savaglia</Emphasis>) and gorgonian forests enhance benthic biodiversity and ecosystem functioning in the mesophotic zone

The twilight or mesophotic zone is amongst the less explored marine regions. In coastal areas, investigations and manipulative experiments on benthic biodiversity and ecosystem functioning at depths up to >50 m have been recently made possible by the progress of SCUBA techniques. In this study, we tested the effects of the presence of a gorgonian forest characterised by a large and dense population of the gold coral Savalia savaglia (Bertoloni 1819) on the benthic biodiversity (nematode species richness, and meiofauna community structure and richness of taxa), trophic guilds state (molluscs) and ecosystem functioning in the surrounding sediments. The S. savaglia colonies create elevated and complex tertiary structures. Our results indicate that the presence of these colonies was associated with a significantly increased deposition of bioavailable substrates and enhanced biodiversity, when compared with soft bottoms at the same depth but without gold corals. The higher biodiversity and altered trophic conditions resulted in higher rates of ecosystem functioning (e.g., higher benthic biomasses). These results suggest that S. savaglia should be particularly protected not only for its specific rarity, endemism and vulnerability but also because it has a prominent role in sustaining high levels of biodiversity and ecosystem functioning in the surrounding benthos of the twilight zone.     

Patterns of morphological diversification of mainland Anolis lizards from northwestern South America

Anolis lizards are one of the most diverse vertebrate genera and are the classic example of adaptive radiation and convergent evolution. Anoles exhibit great morphological diversity produced by the ecological opportunity to exploit several arboreal niches. Anole radiation in the Caribbean islands is well studied, but the mainland radiation is less understood. We used a large morphological data set and a molecular phylogeny to describe the morphological diversification of anoles from northwestern South America, a region with the highest anole diversity on a mainland. We describe morphological diversity as summarized by ten morphotypes, defined mainly by body size, limb proportions, and subdigital lamellae. We show that some morphotypes are limited to forested lowlands and others to Andean highlands; by contrast, Anolis assemblages from tropical rainforests are comprised of the same four morphotypes. We demonstrate that morphological diversification followed a pattern of adaptive radiation across a landscape of adaptive peaks. Our results are consistent with the most recent hypothesis of convergence stated for Caribbean radiation, and demonstrate convergence between mainland morphotypes and Caribbean ecomorphs, which suggests that common processes are driving both radiations. © 2016 The Linnean Society of London     

Symbiont footprints highlight the diversity of scleractinian‐associated Zanclea hydrozoans (Cnidaria,Hydrozoa)

Hydrozoans of the genus Zanclea have been acknowledged only recently as a fundamental component of the highly diverse fauna associated with reef‐building scleractinian corals. Although widely distributed in coral reefs and demonstrated to be important in protecting corals from predation and diseases, the biodiversity of these hydrozoans remains enigmatic due to the paucity of available morphological characters, incomplete morphological characterisations and the possible existence of cryptic species. Recently, molecular techniques have revealed the existence of multiple hidden genetic lineages not yet supported by diagnostic morphological characters. In this work, we further explore the morpho‐diversity of three genetic lineages, namely Zanclea associated with the coral genera Goniastrea (clade I), Porites (clade II) and Pavona (clade VI). Aside from providing a complete classical characterisation of the polyp and medusa stage of each clade, we searched for new potential taxonomic indicators either on symbiotic hydroids or on host corals. On the hydroids, statistical analyses on almost 7,000 nematocyst capsules revealed a significant difference in terms of nematocyst size among the three Zanclea clades investigated. On each host coral genus, we identified peculiar skeletal modifications related to the presence of Zanclea symbionts. Lastly, we discussed the potential diagnostic value of these footprints in the characterisation of Zanclea–scleractinian associations.     

Phenotypic variability in the Caribbean Orange Icing sponge Mycale laevis (Demospongiae: Poecilosclerida)

Sponge species may present several morphotypes, but sponges that are morphologically similar can be separate species. We investigated morphological variation in Mycale laevis, a common Caribbean reef sponge. Four morphotypes of M. laevis have been observed (1) orange, semi-cryptic, (2) orange, massive, (3) white, semi-cryptic, and (4) white, massive. Samples of M. laevis were collected from Key Largo, Florida, the Bahamas Islands, and Bocas del Toro, Panama. Fragments of the 18S and 28S rRNA ribosomal genes were sequenced and subjected to phylogentic analyses together with sequences obtained for 11 other Mycale species and additional sequences retrieved from GenBank. Phylogenetic analyses confirmed that the genus Mycale is monophyletic within the Order Poecilosclerida, although the subgenus Aegogropila is polyphyletic and the subgenus Mycale is paraphyletic. All 4 morphotypes formed a monophyletic group within Mycale, and no genetic differences were observed among them. Spicule lengths did not differ among the 4 morphotypes, but the dominant megasclere in samples collected from Florida and the Bahamas was the strongyle, while those from Panama had subtylostyles. Our data suggest that the 4 morphotypes constitute a single species, but further studies would be necessary to determine whether skeletal variability is due to phentotypic or genotypic plasticity.