What makes a winner? Symbiont and host dynamics determine Caribbean octocoral resilience to bleaching.

Unlike reef-building, scleractinian corals, Caribbean soft corals (octocorals) have not suffered marked declines in abundance associated with anthropogenic ocean warming. Both octocorals and reef-building scleractinians depend on a nutritional symbiosis with single-celled algae living within their tissues. In both groups, increased ocean temperatures can induce symbiont loss (bleaching) and coral death. Multiple heat waves from 2014 to 2016 resulted in widespread damage to reef ecosystems and provided an opportunity to examine the bleaching response of three Caribbean octocoral species. Symbiont densities declined during the heat waves but recovered quickly, and colony mortality was low. The dominant symbiont genotypes within a host generally did not change, and all colonies hosted symbiont species in the genus Breviolum. Their association with thermally tolerant symbionts likely contributes to the octocoral holobiont's resistance to mortality and the resilience of their symbiont populations. The resistance and resilience of Caribbean octocorals offer clues for the future of coral reefs.

Three-dimensional species distribution modelling reveals the realized spatial niche for coral recruitment on contemporary Caribbean reefs.

The three-dimensional structure of habitats is a critical component of species' niches driving coexistence in species-rich ecosystems. However, its influence on structuring and partitioning recruitment niches has not been widely addressed. We developed a new method to combine species distribution modelling and structure from motion, and characterized three-dimensional recruitment niches of two ecosystem engineers on Caribbean coral reefs, scleractinian corals and gorgonians. Fine-scale roughness was the most important predictor of suitable habitat for both taxa, and their niches largely overlapped, primarily due to scleractinians' broader niche breadth. Crevices and holes at mm scales on calcareous rock with low coral cover were more suitable for octocorals than for scleractinian recruits, suggesting that the decline in scleractinian corals is facilitating the recruitment of octocorals on contemporary Caribbean reefs. However, the relative abundances of the taxa were independent of the amount of suitable habitat on the reef, emphasizing that niche processes alone do not predict recruitment rates.

Growing up is hard to do: a demographic model of survival and growth of Caribbean octocoral recruits.

Background: Among species with size structured demography, population structure is determined by size specific survival and growth rates. This interplay is particularly important among recently settled colonial invertebrates for which survival is low and growth is the only way of escaping the high mortality that small colonies are subject to. Gorgonian corals settling on reefs can grow into colonies of millions of polyps and can be meters tall. However, all colonies start their benthic lives as single polyps, which are subject to high mortality rates. Annual survival among these species increases with size, reflecting the ability of colonies to increasingly survive partial mortality as they grow larger. Methods: Data on survival and growth of gorgonian recruits in the genera Eunicea and Pseudoplexaura at two sites on the southern coast of St John, US Virgin Islands were used to generate a stage structured model that characterizes growth of recruits from 0.3 cm until they reach 5 cm height. The model used the frequency distributions of colony growth rates to incorporate variability into the model. Results: High probabilities of zero and negative growth increase the time necessary to reach 5 cm and extends the demographic bottleneck caused by high mortality to multiple years. Only 5% of the recruits in the model survived and reached 5 cm height and, on average, recruits required 3 y to reach 5 cm height. Field measurements of recruitment rates often use colony height to differentiate recruits from older colonies, but height cannot unambiguously identify recruits due to the highly variable nature of colony growth. Our model shows how recruitment rates based on height average recruitment and survival across more than a single year, but size-based definitions of recruitment if consistently used can characterize the role of supply and early survival in the population dynamics of species.

Boundaries and hybridization in a secondary contact zone between freshwater mussel species (Family:Unionidae).

Correct species identification and delineation are crucial for effective conservation and management. However, species delineation can be problematic in the presence of morphological ambiguities due to phenotypic plasticity, convergence, and/or interspecific hybridization. Here, we investigated the degree of hybridization between two closely related freshwater mussel species [Bivalvia: Unionidae; Lampsilis siliquoidea (Barnes) and L. radiata (Gmelin)] that present intermediate forms in areas of sympatry. Unionids have a distinct form of mitochondrial DNA (mtDNA) inheritance, termed doubly uniparental inheritance (DUI) where female mtDNA (F-type) is transmitted to all progeny but male mtDNA (M-type) is mostly inherited by the males resulting in mostly homoplasmic females and heteroplasmic males. An individual was identified as hybrid when F-type and M-type mtDNA of the two different species were found in the same individual. Twelve out of 116 sequenced males were identified as hybrids indicating that these species hybridize where their geographic range overlaps in the lower Great Lakes and St. Lawrence basins. Microsatellite analyses further support the occurrence of hybridization but at a larger spatial scale than indicated by the mitochondrial analyses. We also found that strong within-species population genetic structure affects the detection of purebred individuals overestimating the number of hybrids. Given the large geographic scale and proportion of hybrids found in this study, natural hybridization and introgression need to be considered when implementing local biodiversity inventories, identifying waterbodies as source of organisms for relocation and restoration projects and when setting appropriate conservation policies.

The rise of octocoral forests on Caribbean reefs.

Coral reefs throughout the tropics have experienced large declines in the abundance of scleractinian corals over the last few decades, and some reefs are becoming functionally dominated by animal taxa other than scleractinians. This phenomenon is striking on many shallow reefs in the tropical western Atlantic, where arborescent octocorals now are numerically and functionally dominant. Octocorals are one of several taxa that have been overlooked for decades in analyses of coral reef community dynamics, and our understanding of why octocorals are favoured (whereas scleractinians are not) on some modern reefs, and how they will affect the function of future reef communities, is not commensurate with the task of scientifically responding to the coral reef crisis. We summarize the biological and ecological features predisposing octocorals for success under contemporary conditions, and focus on those features that could have generated resistance and resilience of octocoral populations to environmental change on modern reefs. There is a rich set of opportunities for rapid advancement in understanding the factors driving the success of octocorals on modern reefs, but we underscore three lines of inquiry: (1) the functional implications of strongly mixotrophic, polytrophic, and plastic nutrition, (2) the capacity to recruit at high densities and maintain rapid initial rates of vertical growth, and (3) the emergent properties associated with dense animal forests at high colony densities.

Molecular phylogeny, biogeography, and conservation status of the Texas-endemic freshwater mussel Lampsilis bracteata (Bivalvia, Unionidae).

Lampsilis bracteata (Gould), the Texas Fatmucket, is a regional endemic species in the central Texas biogeographic province which is a candidate to be listed as threatened or endangered under the Endangered Species Act of 1973. Lampsilis bracteata is morphologically similar to the common species L. hydiana (Lea). Here, we examine the molecular taxonomic identification of L. bracteata, and compare its historical range with its current geographic distribution. Tests of genetic affinities based on two mitochondrial genes typically used for DNA barcoding (cytochrome oxidase subunit 1, COI and NADH dehydrogenase subunit 1, ND1) support recognition of L. bracteata as a full species. An unexpected spin-off result was that ND1 sequences of L. satura (Lea), a threatened species in Texas, formed a highly supported cluster within putative L. cardium Rafinesque. As an endemic species, the distribution of L. bracteata has been historically restricted; however, poor land and water management practices have further reduced its distribution from eighteen to just eight streams in the Colorado River drainage and to one stream in the Guadalupe River drainage. For L. bracteata, as for many other imperiled freshwater mussel species, effective conservation measures rely on correct species identification, definition of its geographic range and assessment of its changes in the recent past.

Reference DNA barcodes and other mitochondrial markers for identifying Caribbean Octocorals.

DNA barcoding is a useful tool for documenting the diversity of metazoans. The most commonly used barcode markers, 16S and COI, are not considered suitable for species identification within some "basal" phyla of metazoans. Nevertheless metabarcoding studies of bulk mixed samples commonly use these markers and may obtain sequences for "basal" phyla. We sequenced mitochondrial DNA fragments of cytochrome oxidase c subunit I (COI), 16S ribosomal RNA (16S), NADH dehydrogenase subunits 2 (16S-ND2), 6 (ND6-ND3) and 4L (ND4L-MSH) for 27 species of Caribbean octocorals to create a reference barcode dataset and to compare the utility of COI and 16S to other markers more typically used for octocorals. The most common genera (Erythropodium, Ellisella, Briareum, Plexaurella, Muriceopsis and Pterogorgia) were effectively distinguished by small differences (5 or more substitutions or indels) in COI and 16S sequences. Gorgonia and Antillogorgia were effectively distinguished from each other by unique haplotypes, but the small genetic differences make distance approaches ineffective for these taxa. Plexaura, Pseudoplexaura and Eunicea were indistinguishable from each other but were generally effectively distinguished from other genera, further supporting the idea that these genera have undergone a rapid endemic radiation in the Caribbean.

Population structure among octocoral adults and recruits identifies scale dependent patterns of population isolation in The Bahamas.

Patterns of dispersal and connectivity of the Caribbean gorgonian Antillogorgia elisabethae in The Bahamas were assessed in both adults and recently settled recruits from 13 sites using microsatellite loci. Adult populations along the Little Bahama Bank (LBB) exhibited a clear pattern of isolation by distance (IBD) which described 86% of the variance in pairwise genetic distances. Estimates of dispersal based on the IBD model suggested dispersal distances along the LBB on the order of 100 m. Increasing the spatial scale to include sites separated by open ocean generated an apparent IBD signal but the relationship had a greater slope and explained less of the variance. This relationship with distance reflected both stepping stone based IBD and regional differentiation probably created by ocean currents and barriers to dispersal that are correlated with geographic distance. Analysis of recruits from 4 sites on the LBB from up to 6 years did not detect differences between years nor differences with adult populations. The result suggests that neither selection on recruits nor inter-annual variation in dispersal affected adult population structure. Assignment tests of recruits indicated the most likely sources of the recruits were the local or adjacent populations. Most of the patterning in population structure in the northern Bahamas can be explained by geographic distance and oceanographic connectivity. Recognition of these complex patterns is important in developing management plans for A. elisabethae and in understanding the effects of disturbance to adult populations of A. elisabethae and similar species with limited dispersal.

Recruitment and resilience of a harvested Caribbean octocoral.

Disturbance events are an important component of the ecology of coral reefs and increasingly frequent disturbances coupled with a lack of population resilience may contribute to changes in the structure of coral reef communities. The harvest of the Caribbean octocoral Antillogorgia elisabethae provides an opportunity to explore the relationship between adult abundance and recruitment and the manner in which recruitment contributes to the resilience of local populations. Recruitment of A. elisabethae was monitored in 20, 1-m(2) quadrats at 8 sites along the southern edge of the Little Bahama Bank from 2004 through 2007. A. elisabethae has been harvested in The Bahamas for over fifteen years and all of the sites had been harvested three times, including a harvest during the course of the study. Abundances of adult colonies at those sites as well as a location that had not been harvested were also determined. Recruitment was highly variable, differing between sites, transects within sites, and, depending on the site, between years. Recruitment was best correlated with adult abundance averaged across the surrounding site. Regression analyses suggest abundance on smaller scales had only small effects on recruitment. The effects of the harvesting were site specific ranging from a 38 to 67% reduction in the density of mature colonies. The sites with the most abundant A. elisabethae continued to have the highest abundances after harvesting and there was no significant difference in recruitment before and after harvesting. Population size-structure at 6 of 8 sites that have been harvested multiple times exhibited an overall depletion in small colonies suggesting long term suppression of recruitment and declining populations. Severe depression of adult abundances coupled with local recruitment can create a negative feedback and lead to the decline of local populations. Populations that are dependent on self-recruitment are not resilient to large disturbance events.

Quantifying complex shapes: elliptical fourier analysis of octocoral sclerites.

Species descriptions of most alcyonacean octocorals rely heavily on the morphology of sclerites, the calcium carbonate spicules embedded in the soft tissue. Sclerites provide taxonomic characters for species delineation but require qualitative descriptions, which introduce ambiguities in recognizing morphological features. Elliptical Fourier analysis of the outline of sclerites was used to quantify the morphology of eight species of gorgoniid octocoral in the genus Pseudopterogorgia. Sclerites from one to seven colonies of each species were compared. Scaphoids and spindles were examined separately; rods and octoradiates were excluded from the analyses because of their morphologic similarity across all species. Discriminant analysis of elliptical Fourier descriptors (EFDs) was used to determine whether the elliptical Fourier analysis could be used to identify the specimens. Sclerites were highly variable even within a single colony. Correct species assignments of individual sclerites were greater than 50% for both scaphoids and spindles. Species assignments based on averages of the EFDs for each colony approached 90%. Elliptical Fourier analysis quantifies morphological differences between species and measures colony variance in sclerite size and shape among colonies and species. Phylogenetic analysis based on EFDs did not capture monophyletic groups. The quantification of complex shapes such as sclerites provides an important tool in alpha taxonomy but may be less useful in phylogenetic analyses.

Repeated loss of coloniality and symbiosis in scleractinian corals.

The combination of coloniality and symbiosis in Scleractinia is thought to confer competitive advantage over other benthic invertebrates, and it is likely the key factor for the dominance of corals in tropical reefs. However, the extant Scleractinia are evenly split between zooxanthellate and azooxanthellate species. Most azooxanthellate species are solitary and nearly absent from reefs, but have much wider geographic and bathymetric distributions than reef corals. Molecular phylogenetic analyses have repeatedly recovered clades formed by colonial/zooxanthellate and solitary/azooxanthellate taxa, suggesting that coloniality and symbiosis were repeatedly acquired and/or lost throughout the history of the Scleractinia. Using Bayesian ancestral state reconstruction, we found that symbiosis was lost at least three times and coloniality lost at least six times, and at least two instances in which both characters were lost. All of the azooxanthellate lineages originated from ancestors that were reconstructed as symbiotic, corroborating the onshore-offshore diversification trend recorded in marine taxa. Symbiotic sister taxa of two of these descendant lineages are extant in Caribbean reefs but disappeared from the Mediterranean before the end of the Miocene, whereas extant azooxanthellate lineages have trans-Atlantic distributions. Thus, the phyletic link between reef and nonreef communities may have played an important role in the dynamics of extinction and recovery that marks the evolutionary history of scleractinians, and some reef lineages may have escaped local extinction by diversifying into offshore environments. However, this macroevolutionary mechanism offers no hope of mitigating the effects of climate change on coral reefs in the next century.

Phylogeography and morphological variation of the branching octocoral Pseudopterogorgia elisabethae.

Coral reef anthozoans exhibit extensive morphological variation across and within environmental clines making it difficult to define species boundaries. The relative contributions of genetic variation and ecophenotypic plasticity to the observed phenotypic variation are unknown in most cases. The branching octocoral Pseudopterogorgia elisabethae is widely distributed throughout the Caribbean and colonies vary in appearance within and among populations. We performed genetic and morphological analyses of P.elisabethae from multiple locations within the Bahamas, as well as a Florida Keys and a distant western Caribbean location to determine the levels of genetic and morphological variation (colony form and sclerites characteristics) across populations from different sites, and assessed whether there was congruence between the genetic and morphological variation. Based on sequences of the internal transcribed spacer region of the ribosomal DNA, four groups were found that generally correspond to the geography of the Bahamas. Morphometric analysis of branch and branchlet characteristics indicated that colonies from two of the sites differed from the rest, but there was no clear correspondence between genetic and morphological variation. In general, there were no qualitative differences in the sclerites from the different populations. However, there were some differences in the dimensions of scaphoids and rods of colonies from different sites. This study has shown that P. elisabethae displays genetic and morphologic variation among some populations of the Bahamas, Florida and San Andres, Colombia. P. elisabethae is harvested in the Bahamas and these findings should be considered in management plans and conservation efforts for the species.

High fertilization success in a surface-brooding Caribbean gorgonian.

Colonies of the Caribbean gorgonian Pseudopterogorgia elisabethae release eggs that are retained on the colony surface where they are fertilized and then develop. In December 2001, spawning on San Salvador Island, Bahamas, occurred over 6 d, with spawning by any one colony limited to 1-3 d. With the exception of the first and last days of the spawning period, fertilization success was high, often greater than 90%. Eggs collected in December 2001 had an overall fertilization success of more than 66%. At one site, the increase in fertilization after the first day of spawning correlated with male spawning, but male gonad index was a poor predictor of fertilization success. The number of male colonies close to a female was not correlated with fertilization success. Surface brooding is an efficient mechanism for "harvesting" sperm released upstream of female colonies. By maintaining their eggs at a single location, surface-brooding species can extend the period over which eggs are likely to encounter sperm. As a result, fertilization success is summed across the temporal variance in sperm availability, and the need for very high densities of sperm, with its concomitant risk of polyspermy, may be reduced.

Microsatellite variation reveals high levels of genetic variability and population structure in the gorgonian coral Pseudopterogorgia elisabethae across the Bahamas.

The primary mechanism of gene flow in marine sessile invertebrates is larval dispersal. In Pseudopterogorgia elisabethae, a commercially important Caribbean gorgonian coral, a proportion of the larvae drop to the substratum within close proximity to the maternal colony, and most matings occur between individuals in close proximity to each other. Such limited dispersal of reproductive propagules suggests that gene flow is limited in this gorgonian. In this study, we characterized the population genetic structure of P. elisabethae across the Bahamas using six microsatellite loci. P. elisabethae was collected from 18 sites across the Bahamas. Significant deviations from Hardy-Weinberg equilibrium due to deficits of heterozygotes within populations were detected for all 18 populations in at least one of the six screened loci. Levels of genetic structure among populations of P. elisabethae were high and significant. A distance analysis placed populations within three groups, one formed by populations located within Exuma Sound, a semi-isolated basin, another consisting of populations located outside the basin and a third group comprising two populations from San Salvador Island. The patterns of genetic variation found in this study are concordant with the life-history traits of the species and in part with the geography of the Bahamas. Conservation and management plans developed for P. elisabethae should considered the high degree of genetic structure observed among populations of the species, as well as the high genetic diversity found in the San Salvador and the Exuma Sound populations.

Do multi-branched colonial organisms exceed normal growth after partial mortality?

One of the advantages of modular colonial growth is the capability to recover after partial mortality. Tolerance to partial mortality is a known property of some resistant species of plants that respond to mortality with vigorous regrowth or overcompensation. It is not clear whether modular marine invertebrates such as octocorals overcompensate. This study provides evidence that following injury to colonies (by breaking apical dominance), new growth exceeds normal rates of branching, as observed in some plants, in a degree correlated to the original multi-branched network setting (e.g. the number of original branches connected to main stem), in colonies of the Caribbean gorgonian octocoral Pseudopterogorgia bipinnata. This can be explained by the network of communicating vessels and canals inside octocoral colonies, which provide the structure for effective allocation of resources to regenerating parts.

Branching and self-organization in marine modular colonial organisms: a model.

Despite the universality of branching patterns in marine modular colonial organisms, there is neither a clear explanation about the growth of their branching forms nor an understanding of how these organisms conserve their shape during development. This study develops a model of branching and colony growth using parameters and variables related to actual modular structures (e.g., branches) in Caribbean gorgonian corals (Cnidaria). Gorgonians exhibiting treelike networks branch subapically, creating hierarchical mother-daughter relationships among branches. We modeled both the intrinsic subapical branching along with an ecological-physiological limit to growth or maximum number of mother branches (k). Shape is preserved by maintaining a constant ratio (c) between the total number of branches and the mother branches. The size frequency distribution of mother branches follows a scaling power law suggesting self-organized criticality. Differences in branching among species with the same k values are determined by r (branching rate) and c. Species with r<r/2 or c>r>0). Ecological/physiological constraints limit growth without altering colony form or the interaction between r and c. The model described the branching dynamics giving the form to colonies and how colony growth declines over time without altering the branching pattern. This model provides a theoretical basis to study branching as a simple function of the number of branches independently of ordering- and bifurcation-based schemes.

Determinate growth and modularity in a gorgonian octocoral.

Growth rates of branches of colonies of the gorgonian Pseudopterogorgia elisabethae were monitored for 2 years on a reef at San Salvador Island, Bahamas. Images of 261 colonies were made at 6-month intervals and colony and branch growth analyzed. Branch growth rates differed between colonies and between the time intervals in which the measurements were made. Colonies developed a plumelike morphology through a pattern of branch origination and determinate growth in which branch growth rates were greatest at the time the branch originated and branches seldom grew beyond a length of 8 cm. A small number of branches had greater growth rates, did not stop growing, and were sites for the origination of subsequent "generations" of branches. The rate of branch origination decreased with each generation of branching, and branch growth rates were lower on larger colonies, leading to determinate colony growth. Although colonial invertebrates like P. elisabethae grow through the addition of polyps, branches behave as modules with determinate growth. Colony form and size is generated by the iterative addition of branches.

Patterns of morphological integration in marine modular organisms: supra-module organization in branching octocoral colonies.

Despite the relative simplicity of their modular growth, marine invertebrates such as arborescent gorgonian octocorals (Octocorallia: Cnidaria) generate complex colonial forms. Colony form in these taxa is a consequence of modular (polyp) replication, and if there is a tight integration among modular and supramodular traits (e.g. polyp aperture, inter-polyp spacing, branch thickness, internode and branch length), then changes at the module level may lead to changes in colony architecture. Alternatively, different groups of traits may evolve semi-independently (or conditionally independent). To examine the patterns of integration among morphological traits in Caribbean octocorals, we compared five morphological traits across 21 species, correcting for the effects of phylogenetic relationships among the taxa. Graphical modelling and phylogenetic independence contrasts among the five morphological characters indicate two groups of integrated traits based on whether they were polyp- or colony-level traits. Although all characters exhibited bivariate associations, multivariate analyses (partial correlation coefficients) showed the strongest integration among the colony-level characters (internode distance and branch length). It is a quantitative demonstration that branching characters within the octocorals studied are independent of characters of the polyps. Despite the universally recognized modularity of octocorals at the level of polyps, branching during colony development may represent an emergent level of integration and modularity.

Phylogenetic analyses among octocorals (Cnidaria): mitochondrial and nuclear DNA sequences (lsu-rRNA, 16S and ssu-rRNA, 18S) support two convergent clades of branching gorgonians.

Gorgonian octocorals lack corroborated hypotheses of phylogeny. This study reconstructs genealogical relationships among some octocoral species based on published DNA sequences from the large ribosomal subunit of the mitochondrial RNA (lsu-rRNA, 16S: 524bp and 21 species) and the small subunit of the nuclear RNA (ssu-rRNA, 18S: 1815bp and 13 spp) using information from insertions-deletions (INDELS) and the predicted secondary structure of the lsu-rRNA (16S). There were seven short (3-10bp) INDELS in the 18S with consistent phylogenetic information. The INDELS in the 16S corresponded to informative signature sequences homologous to the G13 helix found in Escherichia coli. We found two main groups of gorgonian octocorals using a maximum parsimony analysis of the two genes. One group corresponds to deep-water taxa including species from the suborders Calcaxonia and Scleraxonia characterized by an enlargement of the G13 helix. The second group has species from Alcyoniina, Holaxonia and again Scleraxonia characterized by insertions in the 18S. Gorgonian corals, branching colonies with a gorgonin-containing flexible multilayered axis (Holaxonia and Calcaxonia), do not form a monophyletic group. These corroborated results from maternally inherited (16S) and biparentally inherited (18S) genes support a hypothesis of independent evolution of branching in the two octocoral clades.