Preconditioning in the reef-building coral Pocillopora damicornis and the potential for trans-generational acclimatization in coral larvae under future climate change conditions

Coral reefs are globally threatened by climate change-related ocean warming and ocean acidification (OA). To date, slow-response mechanisms such as genetic adaptation have been considered the major determinant of coral reef persistence, with little consideration of rapid-response acclimatization mechanisms. These rapid mechanisms such as parental effects that can contribute to trans-generational acclimatization (e.g. epigenetics) have, however, been identified as important contributors to offspring response in other systems. We present the first evidence of parental effects in a cross-generational exposure to temperature and OA in reef-building corals. Here, we exposed adults to high (28.9°C, 805 µatm PCO2) or ambient (26.5°C, 417 µatm PCO2) temperature and OA treatments during the larval brooding period. Exposure to high treatment negatively affected adult performance, but their larvae exhibited size differences and metabolic acclimation when subsequently re-exposed, unlike larvae from parents exposed to ambient conditions. Understanding the innate capacity corals possess to respond to current and future climatic conditions is essential to reef protection and maintenance. Our results identify that parental effects may have an important role through (1) ameliorating the effects of stress through preconditioning and adaptive plasticity, and/or (2) amplifying the negative parental response through latent effects on future life stages. Whether the consequences of parental effects and the potential for trans-generational acclimatization are beneficial or maladaptive, our work identifies a critical need to expand currently proposed climate change outcomes for corals to further assess rapid response mechanisms that include non-genetic inheritance through parental contributions and classical epigenetic mechanisms.

Use of X-radiographs to distinguish members of the Montastraea annularis reef-coral species complex

Recent work suggests the Montastraea annularis species complex consists of at least three species, which can be distinguished qualitatively in the field using features related to colony growth (e.g. overall growth form. bumpiness, growth along the colony edge). However, when whole colonies are not available and surfaces are eroded, identification becomes problematic when relying on such characteristics. Characters based on internal skeletal structures are less prone to loss due to taphonomic processes. Previous work has shown that internal corallite architectural features measured in transverse thin sections can be used to distinguish species. To determine whether internal colony-level features measured on X-radiographs can be used. eight characters related to corallite budding and accretionary growth were measured on specimens representing three modern members of the M. annularis species complex (M. annularis, M. flaveolata and M. franksi), as well as two fossil forms (columnar and organ-pipe). All eight characters showed significant differences among species. Discriminant function analysis using seven of these characters resulted in distinct species groupings In canonical scores plots and a 100% classification success for specimens from Panama. These results suggest that measurements made on X-radiographs provide a useful tool for quantitatively distinguishing members of the M. annularis complex as well as between other massive reef corals.

Shift from coral to macroalgae dominance on a volcanically acidified reef

Rising anthropogenic CO2 in the atmosphere is accompanied by an increase in oceanic CO2 and a concomitant decline in seawater pH (ref. 1). This phenomenon, known as ocean acidification (OA), has been experimentally shown to impact the biology and ecology of numerous animals and plants2, most notably those that precipitate calcium carbonate skeletons, such as reef-building corals3. Volcanically acidified water at Maug, Commonwealth of the Northern Mariana Islands (CNMI) is equivalent to near-future predictions for what coral reef ecosystems will experience worldwide due to OA. We provide the first chemical and ecological assessment of this unique site and show that acidification-related stress significantly influences the abundance and diversity of coral reef taxa, leading to the often-predicted shift from a coral to an algae-dominated state4, 5. This study provides field evidence that acidification can lead to macroalgae dominance on reefs.

Quantifying the state of populations and effects of disturbances at large spatio-temporal scales: The case of coral populations in the great barrier reef

This project was a step forward in applying statistical methods and models to provide new insights for more informed decision-making at large spatial scales. The model has been designed to address complicated effects of ecological processes that govern the state of populations and uncertainties inherent in large spatio-temporal datasets. Specifically, the thesis contributes to better understanding and management of the Great Barrier Reef.

Dimethyl sulfide and other biogenic volatile organic compound emissions from branching coral and reef seawater: Potential sources of secondary aerosol over the Great Barrier Reef

Volatile organic compounds (VOCs) in the headspace of bubble chambers containing branches of live coral in filtered reef seawater were analysed using gas chromatography with mass spectrometry (GC-MS). When the coral released mucus it was a source of dimethyl sulfide (DMS) and isoprene; however, these VOCs were not emitted to the chamber headspace from mucus-free coral. This finding, which suggests that coral is an intermittent source of DMS and isoprene, was supported by the observation of occasional large pulses of atmospheric DMS (DMSa) over Heron Island reef on the southern Great Barrier Reef (GBR), Australia, in the austral winter. The highest DMSa pulse (320 ppt) was three orders of magnitude less than the DMS mixing ratio (460 ppb) measured in the headspace of a dynamically purged bubble chamber containing a mucus-coated branch of Acropora aspera indicating that coral reefs can be strong point sources of DMSa. Static headspace GC-MS analysis of coral fragments identified mainly DMS and seven other minor reduced sulfur compounds including dimethyl disulfide, methyl mercaptan, and carbon disulfide, while coral reef seawater was an indicated source of methylene chloride, acetone, and methyl ethyl ketone. The VOCs emitted by coral and reef seawater are capable of producing new atmospheric particles < 15 nm diameter as observed at Heron Island reef. DMS and isoprene are known to play a role in low-level cloud formation, so aerosol precursors such as these could influence regional climate through a sea surface temperature regulation mechanism hypothesized to operate over the GBR.

Coral Disease and Health Workshop: Coral Histopathology II

The health and continued existence of coral reef ecosystems are threatened by an increasing array of environmental and anthropogenic impacts. Coral disease is one of the prominent causes of increased mortality among reefs globally, particularly in the Caribbean. Although over 40 different coral diseases and syndromes have been reported worldwide, only a few etiological agents have been confirmed; most pathogens remain unknown and the dynamics of disease transmission, pathogenicity and mortality are not understood. Causal relationships have been documented for only a few of the coral diseases, while new syndromes continue to emerge. Extensive field observations by coral biologists have provided substantial documentation of a plethora of new pathologies, but our understanding, however, has been limited to descriptions of gross lesions with names reflecting these observations (e.g., black band, white band, dark spot). To determine etiology, we must equip coral diseases scientists with basic biomedical knowledge and specialized training in areas such as histology, cell biology and pathology. Only through combining descriptive science with mechanistic science and employing the synthesis epizootiology provides will we be able to gain insight into causation and become equipped to handle the pending crisis. One of the critical challenges faced by coral disease researchers is to establish a framework to systematically study coral pathologies drawing from the field of diagnostic medicine and pathology and using generally accepted nomenclature. This process began in April 2004, with a workshop titled Coral Disease and Health Workshop: Developing Diagnostic Criteria co-convened by the Coral Disease and Health Consortium (CDHC), a working group organized under the auspices of the U.S. Coral Reef Task Force, and the International Registry for Coral Pathology (IRCP). The workshop was hosted by the U.S. Geological Survey, National Wildlife Health Center (NWHC) in Madison, Wisconsin and was focused on gross morphology and disease signs observed in the field. A resounding recommendation from the histopathologists participating in the workshop was the urgent need to develop diagnostic criteria that are suitable to move from gross observations to morphological diagnoses based on evaluation of microscopic anatomy. (PDF contains 92 pages)

Biology, ecology, control and management of the invasive Indo-Pacific lionfish: An updated integrated assessment

Venomous Indo-Pacific lionfish (Pterois miles and P. volitans) are now established along the Southeast U.S.A. and parts of the Caribbean and pose a serious threat to reef fish communities of these regions. Lionfish are likely to invade the Gulf of Mexico and potentially South America in the near future. Introductions of lionfish were noted since the 1980s along south Florida and by 2000 lionfish were established off the coast of North Carolina. Lionfish are now one of the more numerous predatory reef fishes at some locations off the Southeast U.S.A. and Caribbean. Lionfish are largely piscivores that feed occasionally on economically important reef fishes. The trophic impacts of lionfish could alter the structure of native reef fish communities and potentially hamper stock rebuilding efforts of the Snapper –Grouper Complex. Additional effects of the lionfish invasion are far-reaching and could increase coral reef ecosystem stress, threaten human health, and ultimately impact the marine aquarium industry. Control strategies for lionfish are needed to mitigate impacts, especially in protected areas. This integrated assessment provides a general overview of the biology and ecology of lionfish including genetics, taxonomy, reproductive biology, early life history and dispersal, venom defense and predation, and feeding ecology. In addition, alternative management actions for mitigating the negative impacts of lionfish, approaches for reducing the risk of future invasions, and directions for future research are provided.

Advantages of using crest nets to sample presettlement larvae of reef fishes in the Caribbean Sea

Identifying the spatial and temporal patterns of larval fish supply and settlement is a key step in understanding the connectivity of meta-populations (Sale et al., 2005). Because of the potentially dispersive nature of the pelagic larval phase of most reef fishes, tracking cohorts from hatching to settlement is extremely difficult (but see Jones et al., 1999). However, for many studies it is sufficient to sample larvae immediately before settlement. Many coral reef fish species use mangrove and seagrass beds as nursery habitats (Nagelkerken et al., 2001; Mumby et al., 2004) and larvae of these species must pass over the reef crest in order to arrive at their preferred settlement habitats. The ability to sample this new cohort of larval fishes provides opportunities for researchers to explore the intricacies of the transition from larva to juvenile (Searcy and Sponaugle, 2001). Quantifying the potential settlers also provides valuable information about the spatial and temporal supply of presettlement larvae (Victor, 1986). Therefore a number of larval sampling methods were developed, one of which is the use of crest nets (Dufour and Galzin, 1993).

Benthic habitats of Fish Bay, Coral Bay and the St. Thomas East End Reserve

NOAA’s National Centers for Coastal Ocean Science Biogeography Branch has mapped and characterized large portions of the coral reef ecosystems inside the U.S. coastal and territorial waters, including the U.S. Caribbean. The complementary protocols used in these efforts have enabled scientists and managers to quantitatively and qualitatively compare marine ecosystems in tropical U.S. waters. The Biogeography Branch used similar protocols to generate new benthic habitat maps for Fish Bay, Coral Bay and the St. Thomas East End Reserve (STEER). While this mapping effort marks the third time that some of these shallow-water habitats (≤40 m) have been mapped, it is the first time that nearly 100% of the seafloor has been characterized in each of these areas. It is also the first time that high resolution imagery describing seafloor depth has been collected in each of these areas. Consequently, these datasets provide new information describing the distribution of coral reef ecosystems and serve as a spatial baseline for monitoring change in the Fish Bay, Coral Bay and the STEER. Benthic habitat maps were developed for approximately 64.3 square kilometers of seafloor in and around Fish Bay, Coral Bay and the STEER. Twenty seven percent (17.5 square kilometers) of these habitat maps describe the seafloor inside the boundaries of the STEER, the Virgin Islands National Park and the Virgin Islands Coral Reef National Monument. The remaining 73% (46.8 square kilometers) describe the seafloor outside of these MPA boundaries. These habitat maps were developed using a combination of semi-automated and manual classification methods. Habitats were interpreted from aerial photographs and LiDAR (Light Detection and Ranging) imagery. In total, 155 distinct combinations of habitat classes describing the geology and biology of the seafloor were identified from the source imagery.

Benthic habitats of Buck Island Reef National Monument

NOAA’s Center for Coastal Monitoring and Assessment’s Biogeography Branch has mapped and characterized large portions of the coral reef ecosystems inside the U.S. coastal and territorial waters, including the U.S. Caribbean. The complementary protocols used in these efforts have enabled scientists and managers to quantitatively compare different marine ecosystems in tropical U.S. waters. The Biogeography Branch used these same general protocols to generate three seamless habitat maps of the Bank/Shelf (i.e., from 0 ≤50 meters) and the Bank/Shelf Escarpment (i.e., from 50 ≤1,000 meters and from 1,000 ≤ 1,830 meters) inside Buck Island Reef National Monument (BIRNM). While this mapping effort marks the fourth time that the shallow-water habitats of BIRNM have been mapped, it is the first time habitats deeper than 30 meters (m) have been characterized. Consequently, this habitat map provides information on the distribution of mesophotic and deep-water coral reef ecosystems and serves as a spatial baseline for monitoring change in the Monument. A benthic habitat map was developed for approximately 74.3 square kilometers or 98% of the BIRNM using a combination of semi-automated and manual classification methods. The remaining 2% was not mapped due to lack of imagery in the western part of the Monument at depths ranging from 1,000 to 1,400 meters. Habitats were interpreted from orthophotographs, LiDAR (Light Detection and Ranging) imagery and four different types of MBES (Multibeam Echosounder) imagery. Three minimum mapping units (MMUs) (100, 1,000 and 5,000 square meters) were used because of the wide range of depths present in the Monument. The majority of the area that was characterized was deeper than 30 m on the Bank/Shelf Escarpment. This escarpment area was dominated by uncolonized sand which transitioned to mud as depth increased. Bedrock was exposed in some areas of the escarpment, where steep slopes prevented sediment deposition. Mesophotic corals were seen in the underwater video, but were too sparsely distributed to be reliably mapped from the source imagery. Habitats on the Bank/Shelf were much more variable than those seen on the Bank/Shelf Escarpment. The majority of this shelf area was comprised of coral reef and hardbottom habitat dominated by various forms of turf, fleshy, coralline or filamentous algae. Even though algae was the dominant biological cover type, nearly a quarter (24.3%) of the Monument’s Bank/Shelf benthos hosted a cover of 10%-<50% live coral. In total, 198 unique combinations of habitat classes describing the geography, geology and biology of the sea-floor were identified from the three types of imagery listed above. No thematic accuracy assessment was conducted for areas deeper than about 50 meters, most of which was located in the Bank/Shelf Escarpment. The thematic accuracy of classes in waters shallower than approximately 50 meters ranged from 81.4% to 94.4%. These thematic accuracies are similar to those reported for other NOAA benthic habitat mapping efforts in St. John (>80%), the Main Eight Hawaiian Islands (>84.0%) and the Republic of Palau (>80.0%). These digital maps products can be used with confidence by scientists and resource managers for a multitude of different applications, including structuring monitoring programs, supporting management decisions, and establishing and managing marine conservation areas. The final deliverables for this project, including the benthic habitat maps, source imagery and in situ field data, are available to the public on a NOAA Biogeography Branch website (http://ccma.nos.noaa.gov/ecosystems/coralreef/stcroix.aspx) and through an interactive, web-based map application (http://ccma.nos.noaa.gov/explorer/biomapper/biomapper.html?id=BUIS). This report documents the process and methods used to create the shallow to deep-water benthic habitat maps for BIRNM. Chapter 1 provides a short introduction to BIRNM, including its history, marine life and ongoing research activities. Chapter 2 describes the benthic habitat classification scheme used to partition the different habitats into ecologically relevant groups. Chapter 3 explains the steps required to create a benthic habitat map using a combination of semi-automated and visual classification techniques. Chapter 4 details the steps used in the accuracy assessment and reports on the thematic accuracy of the final shallow-water map. Chapter 5 summarizes the type and abundance of each habitat class found inside BIRNM, how these habitats compare to past habitat maps and outlines how these new habitat maps may be used to inform future management activities.

Coral health and disease in the Pacific: vision for action

Shallow coral reefs in the IndoPacific contain the highest diversity of marine organisms in the world, with approximately 1500 described species of fish, over 500 species of scleractinian corals, and an estimated 1-10 million organisms yet to be characterized (Reaka-Kudla et al. 1994). These centers of marine biodiversity are facing significant, multiple threats to reef community and habitat structure and function, resulting in local to wide-scale regional damage. Wilkinson (2004) characterized the major pressures as including (1) global climate change, (2) diseases, plagues and invasive species, (3) direct human pressures, (4) poor governance and lack of political will, and (5) international action or inaction. Signs that the natural plasticity of reef ecosystems has been exceeded in many areas from the effects of environmental (e.g., global climate change) and anthropogenic (e.g., land use, pollution) stressors is evidenced by the loss of 20% of the world’s coral reefs (Wilkinson 2004). Predictions are that another 24% (Wilkinson 2006) are under imminent risk of collapse and an additional 26% are under a longer term threat from reduced fitness, disease outbreaks, and increased mortality. These predictions indicate that the current list of approximately 30-40 fatal diseases impacting corals will expand as will the frequency and extent of “coral bleaching” (Waddell 2005; Wilkinson 2004). Disease and corallivore outbreaks, in combination with multiple, concomitant human disturbances are compromising corals and coral reef communities to the point where their ability to rebound from natural disturbances is being lost.

Biogeographic characterization of fish communities and associated benthic habitats within the Flower Garden Banks National Marine Sanctuary: sampling design and implementation of scuba surveys on the coral caps

The Flower Garden Banks National Marine Sanctuary (FGBNMS) is located in the northwestern Gulf of Mexico approximately 180 km south of Galveston, Texas. The sanctuary’s distance from shore combined with its depth (the coral caps reach to within approximately 17 m of the surface) result in limited exposure of this coral reef ecosystem to natural and human-induced impacts compared to other coral reefs of the western Atlantic. In spite of this, the sanctuary still confronts serious impacts including hurricanes events, recent outbreaks of coral disease, an increase in the frequency of coral bleaching and the massive Diadema antillarum die-off during the mid-1980s. Anthropogenic impacts include large vessel anchoring, commercial and recreational fishing, recreational scuba diving, and oil and gas related activities. The FGBNMS was designated in 1992 to help protect against some of these impacts. Basic monitoring and research efforts have been conducted on the banks since the 1970s. Early on, these efforts focused primarily on describing the benthic communities (corals, sponges) and providing qualitative characterizations of the fish community. Subsequently, more quantitative work has been conducted; however, it has been limited in spatial scope. To complement these efforts, the current study addresses the following two goals put forth by sanctuary management: 1) to develop a sampling design for monitoring benthic fish communities across the coral caps; and 2) to obtain a spatial and quantitative characterization of those communities and their associated habitats.

The biology and ecology of the invasive Indo-Pacific lionfish

The Indo-Pacific lionfishes, Pterois miles and P. volitans, are now established along the Southeast U.S. and Caribbean and are expected to expand into the Gulf of Mexico and Central and South America. Prior to this invasion little was known regarding the biology and ecology of these lionfishes. I provide a synopsis of chronology, taxonomy, local abundance, reproduction, early life history and dispersal, venomology, feeding ecology, parasitology, potential impacts, and possible control and management strategies for the lionfish invasion. This information was collected by review of the literature and by direct field and experimental study. I confirm the existence of an unusual supraocular tentacle phenotype and suggest that the high prevalence of this phenotype in the Atlantic is not the result of selection, but likely ontogenetic change. To describe the trophic impacts of lionfish, I report a comprehensive assessment of diet that describes lionfish as a generalist piscivore that preys on over 40 species of teleost comprising more than 20 families. Next, I use the histology of gonads to describe both oogenesis and reproductive dynamics of lionfish. Lionfish mature relatively early and reproduce several times per month throughout the entire calendar year off North Carolina and the Bahamas. To investigate predation, an important component of natural mortality, I assessed the vulnerability of juvenile lionfish to predation by native serranids. Juvenile lionfish are not readily consumed by serranids, even after extreme periods of starvation. Last, I used a stage-based, matrix population model to estimate the scale of control that would be needed to reduce an invading population of lionfish. Together, this research provides the first comprehensive assessment on lionfish biology and ecology and explains a number of life history and ecological interactions that have facilitated the unprecedented and rapid establishment of this invasive finfish. Future research is needed to understand the scale of impacts that lionfish could cause, especially in coral reef ecosystems, which are already heavily stressed. This research further demonstrates the need for lionfish control strategies and more rigorous prevention and early detection and rapid response programs for marine non-native introductions.

PCR-based assay for detection of four coral pathogens

Several microorganisms have been identified as pathogenic agents responsible for various outbreaks of coral disease. Little has been learned about the exclusivity of a pathogen to given disease signs. Most pathogens have only been implicated within a subset of corals, leaving gaps in our knowledge of the host range and geographic extent of a given pathogen. PCR-based assays provide a rapid and inexpensive route for detection of pathogens. Pathogen-specific 16S rDNA primer sets were designed to target four identified coral pathogens: Aurantimonas coralicida, Serratia marcescens, Vibrio shilonii, and Vibrio coralliilyticus. Assays detected the presence of targets at concentrations of less than one cell per microliter. The assay was applied to 142 coral samples from the Florida Keys, Puerto Rico, and U.S. Virgin Islands as an in situ specificity test. Assays displayed a high-level of specificity, seemingly limited only by the resolution of the 16S rDNA.

Age and size composition, growth rate, reproductive biology, and habitats of the West Australian dhufish (Glaucosoma hebraicum) and their relevance to the management of this species

Samples of the commercially and recreationally important West Australian dhufish (Glaucosoma hebraicum) were obtained from the lower west coast of Australia by a variety of methods. Fish <300 mm TL were caught over flat, hard substrata and low-lying limestone reefs, whereas larger fish were caught over larger limestone and coral reef formations. Maximum total lengths, weights, and ages were 981 mm, 15.3 kg, and 39 years, respectively, for females and 1120 mm, 23.2 kg, and 41 years, respectively, for males. The von Bertalanffy growth curves for females and males were significantly different. The values for L∞, k, and t0 in the von Bertalanffy growth equations were 929 mm, 0.111/year, and –0.141 years, respectively, for females, and 1025 mm, 0.111/year, and –0.052 years, respectively, for males. Preliminary estimates of total mortality indicated that G. hebraicum is now subjected to a level of fishing pressure that must be of concern to fishery managers. Glaucosoma hebraicum, which spawns between November and April and predominantly between December and March, breeds at a wide range of depths and is a multiple spawner. The L50’s for females and males at first maturity, i.e. 301 and 320 mm, respectively, were attained by about the end of the third year of life and are well below the minimum legal length (MLL) of 500 mm. Because females and males did not reach the MLL until the end of their seventh and sixth years of life, respectively, they would have had, on average, the opportunity of spawning during four and three spawning seasons, respectively, before they reached the MLL. However, because G. hebraicum caught in water depths >40 m typically die upon release, a MLL is of limited use for conserving this species. Alternative approaches, such as restricting fishing activity in highly fished areas, reducing daily bag limits for recreational fishermen, introducing quotas or revising specific details of certain commercial hand-line licences (or doing both) are more likely to provide effective conservation measures.