Ecological Physiology of a Coral Pathogen and the Coral Reef Environment

Laboratory studies on the ecological physiology of a coral pathogen were carried out to investigate growth potential in terms of environmental factors that may control coral diseases on reefs. The disease chosen for this study, white plague type II, is considered to be one of the major diseases of Caribbean scleractinian corals, affecting a wide range of coral hosts and causing rapid and widespread tissue loss. It is caused by a single pathogen, the bacterium Aurantimonas coralicida. A series of laboratory experiments using a pure culture of the pathogen was carried out to examine the roles of temperature, pH, and O₂ concentration on growth rate. Results revealed optimal growth between 30 and 35°C, and between pH values of 6 and 8. There was a distinctive synergistic relationship between pH and temperature. Increasing temperature from 25 to 35°C expanded the range of pH tolerance from a minimum of 6.0 down to 5.0. O₂ concentration directly affected growth rate, which increased with increasing O₂. The combined effects of increasing O₂ and increasing temperature resulted in a synergistic effect of more rapid growth. These laboratory results are discussed in terms of the coral host and the range of the environmental factors that occur on coral reefs. We conclude that changing environmental conditions in the reef environment, in particular observed increases in water temperature, may be promoting coral diseases by allowing coral pathogens to expand their ecological niches. In the case of the white plague type II pathogen, elevated temperature would allow A. coralicida to colonize the low pH environment of the coral surface mucopolysaccharide layer as an initial stage of infection. The synergistic effect between temperature and oxygen concentration appeared to be less environmentally relevant for this coral pathogen.     

Genetic and epigenetic insight into morphospecies in a reef coral

Incongruence between conventional and molecular systematics has left the delineation of many species unresolved. Reef‐building corals are no exception, with phenotypic plasticity among the most plausible explanations for alternative morphospecies. As potential molecular signatures of phenotypic plasticity, epigenetic processes may contribute to our understanding of morphospecies. We compared genetic and epigenetic variation in Caribbean branching Porites spp., testing the hypothesis that epigenetics—specifically, differential patterns of DNA methylation—play a role in alternative morphotypes of a group whose taxonomic status has been questioned. We used reduced representation genome sequencing to analyse over 1,000 single nucleotide polymorphisms and CpG sites in 27 samples of Porites spp. exhibiting a range of morphotypes from a variety of habitats in Belize. We found stronger evidence for genetic rather than epigenetic structuring, identifying three well‐defined genetic groups. One of these groups exhibited significantly thicker branches, and branch thickness was a better predictor of genetic groups than depth, habitat or symbiont type. In contrast, no clear epigenetic patterns emerged with respect to phenotypic or habitat variables. While there was a weak positive correlation between pairwise genetic and epigenetic distance, two pairs of putative clones exhibited substantial epigenetic differences, suggesting a strong environmental effect. We speculate that epigenetic patterns are a complex mosaic reflecting diverse environmental histories superimposed over a relatively small heritable component. Given the role of genetics in branching Porites spp. morphospecies we were able to detect with genomewide sequencing, use of such techniques throughout the geographic range of these corals may help settle their phylogeny.     

Pelagic Subsidies Underpin Fish Productivity on a Degraded Coral Reef

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Additive Diversity Partitioning of Fish in a Caribbean Coral Reef Undergoing Shift Transition

Shift transitions in dominance on coral reefs from hard coral cover to fleshy macroalgae are having negative effects on Caribbean coral reef communities. Data on spatiotemporal changes in biodiversity during these modifications are important for decision support for coral reef biodiversity protection. The main objective of this study is to detect the spatiotemporal patterns of coral reef fish diversity during this transition using additive diversity-partitioning analysis. We examined α, β and γ fish diversity from 2000 to 2010, during which time a shift transition occurred at Mahahual Reef, located in Quintana Roo, Mexico. Data on coral reef fish and benthic communities were obtained from 12 transects per geomorphological unit (GU) in two GUs (reef slope and terrace) over six years (2000, 2005, 2006, 2007, 2008, 2010). Spatial analysis within and between the GUs indicated that the γ-diversity was primarily related to higher β-diversity. Throughout the six study years, there were losses of α, β and γ-diversity associated spatially with the shallow (reef slope) and deeper (reef terrace) GUs and temporally with the transition in cover from mound corals to fleshy macroalgae and boulder corals. Despite a drastic reduction in the number of species over time, β-diversity continues to be the highest component of γ-diversity. The shift transition had a negative effect on α, β and γ-diversity, primarily by impacting rare species, leading a group of small and less vulnerable fish species to become common and an important group of rare species to become locally extinct. The maintenance of fish heterogeneity (β-diversity) over time may imply the abetment of vulnerability in the face of local and global changes.     

Genetic and epigenetic variations associated with adaptation to heterogeneous habitat conditions in a deciduous shrub

Environmentally induced phenotypic plasticity is thought to play an important role in the adaption of plant populations to heterogeneous habitat conditions, and yet the importance of epigenetic variation as a mechanism of adaptive plasticity in natural plant populations still merits further research. In this study, we investigated populations of Vitex negundo var. heterophylla (Chinese chastetree) from adjacent habitat types at seven sampling sites. Using several functional traits, we detected a significant differentiation between habitat types. With amplified fragment length polymorphisms (AFLP) and methylation‐sensitive AFLP (MSAP), we found relatively high levels of genetic and epigenetic diversity but very low genetic and epigenetic differences between habitats within sites. Bayesian clustering showed a remarkable habitat‐related differentiation and more genetic loci associated with the habitat type than epigenetic, suggesting that the adaptation to the habitat is genetically based. However, we did not find any significant correlation between genetic or epigenetic variation and habitat using simple and partial Mantel tests. Moreover, we found no correlation between genetic and ecologically relevant phenotypic variation and a significant correlation between epigenetic and phenotypic variation. Although we did not find any direct relationship between epigenetic variation and habitat environment, our findings suggest that epigenetic variation may complement genetic variation as a source of functional phenotypic diversity associated with adaptation to the heterogeneous habitat in natural plant populations.     

Morphological and Genetic Divergences in a Coral Reef Damselfish, Pomacentrus coelestis

Population differentiation is one of the main topics in evolutionary biology. Except the exploration of color variation, few studies focused on morphological divergences among populations of coral reef fishes. In this work, we studied morphological and genetic differentiation among populations of the damselfish, Pomacentrus coelestis, in the northwestern Pacific Ocean. The shapes of the mandible and the premaxilla were explored using geometric morphometric methods and the genetic structure was investigated using microsattelites. Various tests revealed significant shape variation among most P. coelestis populations for both skeletal units. Morphological variation of the mandible accompanies a genetic break between populations of mainland Japan and Okinawa-Taiwan. However, Mantel and Procrustes tests revealed no congruence between morphological and genetic structures. We illustrate that phenotypic plasticity and adaptive divergence are potential evolutionary mechanisms underlying shape difference among P. coelestis populations. An ecomorphological approach suggests that various diet could be related to shape variation of oral jaws.     

A complex species complex: The controversial role of ecology and biogeography in the evolutionary history of Syllis gracilis Grube, 1840 (Annelida,Syllidae)

The cryptic diversity in the polychaete Syllis gracilis Grube, 1840, in the Mediterranean Sea was examined with an integrative morpho-molecular approach. Individuals of S. gracilis were collected at eleven Mediterranean localities to provide an insight into the role of brackish environments in inducing cryptic speciation. The examination of morphological features combined with a molecular genetic analysis based on a partial sequence of the 16S rRNA gene highlighted discrepancies between morphological and molecular diversity. Morphological data allowed to identify a morphotype with short appendages occurring in coralline algae communities and another one with long appendages observed in brackish-water environments and Sabellaria reefs. Multivariate analyses showed that sampling localities were the greatest source of morphological divergence, suggesting that phenotypic plasticity may play a role in local adaptations of S. gracilis populations. Molecular data showed the occurrence of four divergent lineages not corresponding to morphological clusters. Different species delimitation tests gave conflicting results, retrieving, however, at least four separated entities. Some lineages occurred in sympatry and were equally distributed in marine and brackish-water environments, excluding a biogeographic or ecological explanation of the observed pattern and suggesting instead ancient separation between lineages and secondary contact. The co-occurrence of different lineages hindered the identification of the lineage corresponding to S. gracilis sensu stricto. The discrepancy between morphological and molecular diversity suggests that different environmental and biogeographic features may interact in a complex and unpredictable way in shaping diversity patterns. An integrative approach is needed to provide a satisfactory insight on evolutionary processes in marine invertebrates.     

Syndromes or Flexibility: Behavior during a Life History Transition of a Coral Reef Fish

The theory of behavioral syndromes focuses on quantifying variation in behavior within and among individual organisms and attempts to account for the maintenance of differences in behavior that occur in a consistent manner among individuals. Behavioral syndromes have potentially important ecological consequences (e.g. survivorship tradeoffs) and can be shaped by population dynamics through selective mortality. Here, we search for any evidence for consistency of behavior across situations in juveniles of a common damselfish, Pomacentrus amboinensis (Pomacentridae) at the transition between larval habitats in the plankton and juvenile habitats on the reef. Naïve fish leaving the pelagic phase to settle on reefs were caught by light traps and their behaviors observed using similar methods across three different situations (small aquaria, large aquaria, field setting); all of which represent low risk and well-sheltered environments. Seven behavioral traits were compared within and among individuals across situations to determine if consistent behavioral syndromes existed. No consistency was found in any single or combination of behavioral traits for individuals across all situations. We suggest that high behavioral flexibility is likely beneficial for newly-settled fish at this ontogenetic transition and it is possible that consistent behavioral syndromes are unlikely to emerge in juveniles until environmental experience is gained or certain combinations of behaviors are favored by selective mortality.     

In the foothill zone—Sabanejewia balcanica (Karaman 1922), in the lowland zone—Sabanejewia bulgarica (Drensky, 1928): Myth or reality?

The status of golden loaches (genus Sabanejewia) in the region of Central Europe and Balkans is still ambiguous. The greatest controversy is caused by species Sabanejewia balcanica and S. bulgarica. Both species are characterized by a wide spectrum of morphological variability and overlapping of distinguishing features, which then lead to difficulties in their determination. Previous phylogenetic studies aimed on the resolving of their taxonomic status did not include samples from their type localities and so led to a lack of their true distribution in this region. Therefore, the main aim of this study was to identify taxonomic status of golden loaches populations in the region of the middle Danube basin and adjacent areas on the model territory of Slovakia. For this purpose, we used novelty approach (morphological, molecular, and microhabitat) and we also included the missing samples from the type localities of both species. Based on mtDNA all the Slovakian samples reflected haplotype richness revealed on the type locality of S. bulgarica, although the genetic distances from other representatives of the genus Sabanejewia occurring are not significant. Within the morphology, we have revealed a great measure of variability in studied populations, which is largely caused by different habitat conditions and thus representing a phenotypic plasticity of these fish.     

Length-Based Assessment of Coral Reef Fish Populations in the Main and Northwestern Hawaiian Islands

The coral reef fish community of Hawaii is composed of hundreds of species, supports a multimillion dollar fishing and tourism industry, and is of great cultural importance to the local population. However, a major stock assessment of Hawaiian coral reef fish populations has not yet been conducted. Here we used the robust indicator variable “average length in the exploited phase of the population (L¯)”, estimated from size composition data from commercial fisheries trip reports and fishery-independent diver surveys, to evaluate exploitation rates for 19 Hawaiian reef fishes. By and large, the average lengths obtained from diver surveys agreed well with those from commercial data. We used the estimated exploitation rates coupled with life history parameters synthesized from the literature to parameterize a numerical population model and generate stock sustainability metrics such as spawning potential ratios (SPR). We found good agreement between predicted average lengths in an unfished population (from our population model) and those observed from diver surveys in the largely unexploited Northwestern Hawaiian Islands. Of 19 exploited reef fish species assessed in the main Hawaiian Islands, 9 had SPRs close to or below the 30% overfishing threshold. In general, longer-lived species such as surgeonfishes, the redlip parrotfish (Scarus rubroviolaceus), and the gray snapper (Aprion virescens) had the lowest SPRs, while short-lived species such as goatfishes and jacks, as well as two invasive species (Lutjanus kasmira and Cephalopholis argus), had SPRs above the 30% threshold.     

Patterns of Embryo Mortality in a Demersally Spawning Coral Reef Fish and the Role of Predatory Fishes

The biological significance of embryo mortality in demersally spawning coral reef fishes is poorly understood. Here we describe patterns of variation in embryo mortality in Pomacentrus amboinensis (Pomacentridae) at Lizard Island (Great Barrier Reef). The aim was to determine whether numbers of embryos hatched substantially differed from egg production, and if so, identify whether predatory fishes were a source of embryo mortality. Spawning success (number of eggs laid), embryo mortality (proportion of embryos that died prior to hatching) and number of embryos hatching were estimated from daily maps of clutches laid on artificial surfaces (PVC tiles) defended by nesting males. Patterns of variation in eggs laid, embryo mortality and numbers of embryos hatched were examined at three spatial scales: (1) among widely-spaced locations around the island; (2) between adjacent reef slope and patch reef habitats occupied by P. amboinensis at a single location; and (3) among different males within these two habitats. The embryo mortality was extremely high, with a mean of 25.9pm ± 6.2% (S.E.) for 4 locations examined in 1994 and a mean of 69.2pm ± 2.9% for two habitats surveyed in 1995. There were no significant differences in embryo mortality among locations or habitats in either year. This meant that spatial patterns in the number of embryos hatching reflected differences in the number of eggs laid on tiles. Embryo mortality was extremely variable on the scale of individual territories, with embryo mortality commonly ranging from 0% to 100%. Much of the mortality could be attributed to diurnal predatory fishes, especially the wrasse Thalassoma lunare. However, variation in predator densities did not explain spatial patterns in embryo mortality rates. Both solitary and group predatory behaviour was observed, with groups often causing 100% embryo mortality. The level of embryo mortality observed suggests that predation prior to hatching may have a substantial effect on the reproductive output of populations of this demersal-nesting fish.     

Characteristics of Settling Coral Reef Fish Are Related to Recruitment Timing and Success

Many marine populations exhibit high variability in the recruitment of young into the population. While environmental cycles and oceanography explain some patterns of replenishment, the role of other growth-related processes in influencing settlement and recruitment is less clear. Examination of a 65-mo. time series of recruitment of a common coral reef fish, Stegastes partitus, to the reefs of the upper Florida Keys revealed that during peak recruitment months, settlement stage larvae arriving during dark lunar phases grew faster as larvae and were larger at settlement compared to those settling during the light lunar phases. However, the strength and direction of early trait-mediated selective mortality also varied by settlement lunar phase such that the early life history traits of 2–4 week old recruit survivors that settled across the lunar cycle converged to more similar values. Similarly, within peak settlement periods, early life history traits of settling larvae and selective mortality of recruits varied by the magnitude of the settlement event: larvae settling in larger events had longer PLDs and consequently were larger at settlement than those settling in smaller pulses. Traits also varied by recruitment habitat: recruits surviving in live coral habitat (vs rubble) or areas with higher densities of adult conspecifics were those that were larger at settlement. Reef habitats, especially those with high densities of territorial conspecifics, are more challenging habitats for young fish to occupy and small settlers (due to lower larval growth and/or shorter PLDs) to these habitats have a lower chance of survival than they do in rubble habitats. Settling reef fish are not all equal and the time and location of settlement influences the likelihood that individuals will survive to contribute to the population.     

Phylogenetic and evolutionary perspectives of the Indo-Pacific grouper Plectvopomus species on the Great Barrier Reef, Australia

Molecular tools were used to investigate relationships between species of Plectropomus , an Indo-Pacific group with a potentially recent evolutionary history on the Great Barrier Reef. Plectropomus laevis appeared to be basal, with evidence of hybridization between P. leopardus/maculatus and P. maculatusllaevis .     

Plasticity of Escape Responses: Prior Predator Experience Enhances Escape Performance in a Coral Reef Fish

Teleost and amphibian prey undertake fast-start escape responses during a predatory attack in an attempt to avoid being captured. Although previously viewed as a reflex reaction controlled by the autonomic nervous system, the escape responses of individuals when repeatedly startled are highly variable in their characteristics, suggesting some behavioural mediation of the response. Previous studies have shown that fishes are able to learn from past experiences, but few studies have assessed how past experience with predators affect the fast-start response. Here we determined whether prior experience with the smell or sight of a predator (the Dottyback, Pseudochromis fuscus) affected the escape response of juveniles of the Spiny Chromis (Acanthochromis polyacanthus). Results show that individuals exposed to any of the predator cues prior to being startled exhibited a stronger escape response (i.e., reduced latency, increased escape distance, mean response speed, maximum response speed and maximum acceleration) when compared with controls. This study demonstrates the plasticity of escape responses and highlights the potential for naïve reef fish to take into account both visual and olfactory threat cues simultaneously to optimise the amplitude of their kinematic responses to perceived risk.     

The evolution of ecologically important characters in Heliconius butterflies (Lepidoptera: Nymphalidae): a cladistic review

The biology of Heliconius butterflies has provided a rich source of data to test theories of ecological genetics, coevolution and community ecology. Many putatively adaptive characters have been discussed with reference to a phylogenetic hypothesis based on a variety of morphological and life-history traits interpreted from an evolutionary taxonomic perspective. Here, alternate interpretations of characters on the traditional tree and a more recent mitochondrial DNA cladogram with a substantially different topology are compared and contrasted. It is shown that many characters ostensibly providing support for the traditional phylogenetic hypothesis are almost equally parsimoniously distributed and in some cases more parsimoniously distributed on the mtDNA tree than on the tree inferred from those characters. Discussion of alternate evolutionary scenarios based on the mDNA-based topology is presented for pupal mating, pollen feeding, foodplant coevolution, and other ecologically significant features.     

Ultraviolet Radiation Absorbance by Coral Reef Fish Mucus: photo-protection and Visual Communication

Tropical reef fishes are exposed to high levels of damaging ultraviolet radiation. Here we report the widespread distribution of both UVA- and UVB-absorbing compounds in the epithelial mucus of these fishes. Mucus from 137 reef fish species was examined by spectrophotometry and 90% were found to have strong absorbance peaks between 290 and 400nm. Most fish species (78%) had more than one peak, that suggests a broad-band ultraviolet screening function for their mucus. Thalassoma duperrey, a tropical wrasse, was able to alter the absorbance of its epithelial mucus in response to both naturally and experimentally manipulated UV regimes. Visual modeling suggests that a fish with UV vision, such as Dascyllus albisella, could detect the changes in mucus spectra of T. duperrey that occurred in these experiments.     

Extent of Mangrove Nursery Habitats Determines the Geographic Distribution of a Coral Reef Fish in a South-Pacific Archipelago

Understanding the drivers of species'' geographic distribution has fundamental implications for the management of biodiversity. For coral reef fishes, mangroves have long been recognized as important nursery habitats sustaining biodiversity in the Western Atlantic but there is still debate about their role in the Indo-Pacific. Here, we combined LA-ICP-MS otolith microchemistry, underwater visual censuses (UVC) and mangrove cartography to estimate the importance of mangroves for the Indo-Pacific coral reef fish Lutjanus fulviflamma in the archipelago of New Caledonia. Otolith elemental compositions allowed high discrimination of mangroves and reefs with 83.8% and 98.7% correct classification, respectively. Reefs were characterized by higher concentrations of Rb and Sr and mangroves by higher concentrations of Ba, Cr, Mn and Sn. All adult L. fulviflamma collected on reefs presented a mangrove signature during their juvenile stage with 85% inhabiting mangrove for their entire juvenile life (about 1 year). The analysis of 2942 UVC revealed that the species was absent from isolated islands of the New Caledonian archipelago where mangroves were absent. Furthermore, strong positive correlations existed between the abundance of L. fulviflamma and the area of mangrove (r = 0.84 for occurrence, 0.93 for density and 0.89 for biomass). These results indicate that mangrove forest is an obligatory juvenile habitat for L. fulviflamma in New Caledonia and emphasize the potential importance of mangroves for Indo-Pacific coral reef fishes.     

Rapid and repeated origin of insular gigantism and dwarfism in Australian tiger snakes

It is a well-known phenomenon that islands can support populations of gigantic or dwarf forms of mainland conspecifics, but the variety of explanatory hypotheses for this phenomenon have been difficult to disentangle. The highly venomous Australian tiger snakes (genus Notechis) represent a well-known and extreme example of insular body size variation. They are of special interest because there are multiple populations of dwarfs and giants and the age of the islands and thus the age of the tiger snake populations are known from detailed sea level studies. Most are 5000-7000 years old and all are less than 10,000 years old. Here we discriminate between two competing hypotheses with a molecular phylogeography dataset comprising approximately 4800 bp of mtDNA and demonstrate that populations of island dwarfs and giants have evolved five times independently. In each case the closest relatives of the giant or dwarf populations are mainland tiger snakes, and in four of the five cases, the closest relatives are also the most geographically proximate mainland tiger snakes. Moreover, these body size shifts have evolved extremely rapidly and this is reflected in the genetic divergence between island body size variants and mainland snakes. Within south eastern Australia, where populations of island giants, populations of island dwarfs, and mainland tiger snakes all occur, the maximum genetic divergence is only 0.38%. Dwarf tiger snakes are restricted to prey items that are much smaller than the prey items of mainland tiger snakes and giant tiger snakes are restricted to seasonally available prey items that are up three times larger than the prey items of mainland tiger snakes. We support the hypotheses that these body size shifts are due to strong selection imposed by the size of available prey items, rather than shared evolutionary history, and our results are consistent with the notion that adaptive plasticity also has played an important role in body size shifts. We suggest that plasticity displayed early on in the occupation of these new islands provided the flexibility necessary as the island's available prey items became more depauperate, but once the size range of available prey items was reduced, strong natural selection followed by genetic assimilation worked to optimize snake body size. The rate of body size divergence in haldanes is similar for dwarfs (h(g) = 0.0010) and giants (h(g) = 0.0020-0.0025) and is in line with other studies of rapid evolution. Our data provide strong evidence for rapid and repeated morphological divergence in the wild due to similar selective pressures acting in different directions.     

Non-Random Variability in Functional Composition of Coral Reef Fish Communities along an Environmental Gradient

Changes in the coral reef complex can affect predator-prey relationships, resource availability and niche utilisation in the associated fish community, which may be reflected in decreased stability of the functional traits present in a community. This is because particular traits may be favoured by a changing environment, or by habitat degradation. Furthermore, other traits can be selected against because degradation can relax the association between fishes and benthic habitat. We characterised six important ecological traits for fish species occurring at seven sites across a disturbed coral reef archipelago in Indonesia, where reefs have been exposed to eutrophication and destructive fishing practices for decades. Functional diversity was assessed using two complementary indices (FRic and RaoQ) and correlated to important environmental factors (live coral cover and rugosity, representing local reef health, and distance from shore, representing a cross-shelf environmental gradient). Indices were examined for both a change in their mean, as well as temporal (short-term; hours) and spatial (cross-shelf) variability, to assess whether fish-habitat association became relaxed along with habitat degradation. Furthermore, variability in individual traits was examined to identify the traits that are most affected by habitat change. Increases in the general reef health indicators, live coral cover and rugosity (correlated with distance from the mainland), were associated with decreases in the variability of functional diversity and with community-level changes in the abundance of several traits (notably home range size, maximum length, microalgae, detritus and small invertebrate feeding and reproductive turnover). A decrease in coral cover increased variability of RaoQ while rugosity and distance both inversely affected variability of FRic; however, averages for these indices did not reveal patterns associated with the environment. These results suggest that increased degradation of coral reefs is associated with increased variability in fish community functional composition resulting from selective impacts on specific traits, thereby affecting the functional response of these communities to increasing perturbations.