2017 CCRE Annual Report

Smithsonian Institution

2017 CCRE Annual Report Caribbean Coral Reef Ecosystems • National Museum of Natural History

CCRE Fiscal Year 2017

With 92 scientific visitors contributing to over 1200 research days at the station, 2017 was one Carrie Bow Cay’s busiest years on record. Additionally, research divers conducted over 1400 dives and spent over 1,000 hours underwater, making the island one of the Smithsonian scientific diving program’s busiest sites.

The island continues to be a venue for a diverse spectrum of research into biodiversity, ecology, and conservation. This year marks 20 years of continuous environmental monitoring (see page 27) and 24 years of CARICOMP research (see page 25) at the station. These efforts have generated some of the longest and most important datasets in the region. The research taking place at Carrie Bow Cay is more critical now than ever as coastal marine environments undergo rapid changes. The station is proud to host Smithsonian researchers and their colleagues from all over the world.

Table of Contents 4 Carrie Bow Cay Field Station 5 Research Highlights 29 Research Briefs 35 Scientific Publications 38 Visitors and Station Managers 40 Acknowledgements

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Carrie Bow Cay Field Station

Carrie Bow Cay Field Station has operated on the Belize barrier reef since 1972. The station is open to scientific visitors year-round and offers unparalleled access to coral reef environments, seagrass meadows, and mangrove forests.

This small, highly functional field laboratory boasts a flow-through seawater system, wet and dry laboratory space, full SCUBA facilities, small boats, and living quarters for up to six scientists at a time.

For more information, visit: www.ccre.si.edu

Does climate change affect coral’s ability to choose a home?

Jennifer Sneed, Audrey Looby, Justin Campbell, and Valerie Paul

Corals can reproduce asexually or sexually. When they reproduce sexually, the developing coral goes through a larval stage. During this stage the coral can swim in the water column and is able to choose an appropriate place to attach to the reef. Often times, corals will attach to rocks and rubble covered in encrusting algae called crustose coralline algae (CCA). Some corals prefer certain species of CCA over others. The elkhorn coral (Acorpora palmata) consistently chooses the CCA Hydrolithon boergesenii over Paragoniolithon solubile under normal conditions. Researchers from the Smithsonian Marine Station investigated whether changes in seawater pH and temperature expected to occur in the near future impact the decisions corals make when given the choice between these two CCA species. They collected pieces of CCA from the back reef near Carrie Bow Cay and conditioned them in buckets that contained seawater at current ambient conditions (pH = 8.1, temperature = 29°C) or conditions expected to occur by the year 2100 (pH 7.9, temperature = 31°C) for seven days. While the CCA conditioned, researchers collected gametes from elkhorn (A. palmata) and staghorn (A. cervicornis) corals in the field, facilitated fertilization in the lab, and reared the developing larvae for five days until the larvae were competent to settle. They were then added to chambers containing one piece of H. boergesenii and one piece of P. solubile under current or future seawater conditions and given 48 hours to choose a surface. Elkhorn larvae chose H. boergesenii more often than P. solubile under current ambient condition and did not change their preferences under future pH and temperature levels. Staghorn larvae had no preferences for one CCA over the other under any conditions tested. Although future climate change conditions will likely be harmful to corals in a variety ways, this research suggests that it will not impact the preferences that corals have for some CCA over others. However, the CCA were only conditioned for a short period of time (seven days) and longer exposure might result in different outcomes.

Several small, free-swimming coral larvae are transferred in a small pipette for settlement experiments at Carrie Bow Cay.

Caribbean Coral Reef Ecosystems | 6

Sponge biodiversity in Belize

Deborah Gochfeld, Michael Lesser, and Marc Slattery With the decline of corals, sponges are becoming increasingly common on Caribbean reefs. As part of a broader study to evaluate the ecological importance of sponges on reefs throughout the Caribbean, the biodiversity of sponges on several reefs near Carrie Bow Cay on the Belize Barrier Reef was studied. Surveys of sponge abundance, biomass and species diversity were performed and small samples were collected to identify rare or possible new species, and to characterize the functional role of sponges and the bacterial communities that they host. On 3 reefs surveyed at the same depth at Carrie Bow Cay, a total of 80 species were identified, as compared with 45 species at the same depth contour in Curaรงao. Species assemblages differed dramatically between Curaรงao and Belize. Within Belize, there were differences among species assemblages across fore-reef sites at the same depth contour, but there were even greater differences in sponge assemblages between the fore-reef and shallower patch reef sites. In addition to sponge diversity, fish predation on sponges and fish diversity were quantified. Genetic analysis of the sponges and their bacterial communities will aim to identify genes involved in the production of chemical defenses that may protect them from predators, and in nutrient cycling on reefs. Data obtained from this research in Belize will be compared with similar data obtained on reefs in Curaรงao, the Cayman Islands, and the Florida Keys, to identify variability in the structure of sponge communities across the Caribbean basin, environmental drivers of sponge community structure, and how different sponge communities may be contributing to the ecology of reefs in those regions.

7 | Caribbean Coral Reef Ecosystems

Diver measuring sponges to assess sponge biomass.

Are marine crab and shrimp populations of coastal Belize uniquely diverse?

Darryl L. Felder, Rafael Lemaitre, and Jennifer M. Felder

Ongoing studies of diverse marine microhabitats near Carrie Bow Cay and Twin Cays are producing a remarkable account of crab and shrimp species, some being familiar members of a widespread Caribbean fauna, but others apparently unique to the region. Most of these are small animals of less than 5-10 mm in size and can be easily overlooked. However, careful study has shown that their color in life is generally very distinctive. This provides a valuable tool for their identification and is being extensively documented by photography. As part of this project, nine new species have already been described and named, while an additional seven newly discovered species are presently in description. Among previously known Caribbean forms, a number have rarely been seen since their original discovery, sometimes many decades ago. Beyond this, molecular genetic studies indicate that a number of decapods in Belize, while identifiable as Caribbean species, are genetically diverged populations and may reflect unique regional biological adaptations. Among habitats richest in decapod diversity are eroded coralline rubble, sponges, seagrasses, and calcareous algae. The complexity of crab and shrimp communities in these substrates remains very poorly understood, though a growing number of symbiotic associations are becoming evident, and clearly contribute to measured diversity. Non-native invasive species have also been detected, though there fortunately appears to be no evidence that their populations are thus far rapidly expanding. A full understanding of the biodiversity and resilience of crab and shrimp communities requires an exhaustive account of the regional fauna and an advancement of identification tools. Once that is achieved, careful monitoring and informed habitat management can follow. Only then can communities in Belize be quantitatively compared to those in other areas of the Caribbean. This project has contributed substantially to production of a coming color-illustrated reference book, intended for use in identification of regional crabs, lobsters, hermit crabs and their relatives. To date, such a comprehensive resource has not been available.

The banded clinging crab, Mitrhaculus cinctimanus, collected from the waters around Carrie Bow Cay.

Caribbean Coral Reef Ecosystems | 10

What factors control distribution and abundance of sponges living in coral reef, seagrass meadow, and mangrove habitats?

Janie Wulff and KlaÓĽs Rutlzer

Extreme mortality of entire sponge faunas, overgrowth of corals by a handful of aggressive sponge species, the undocumented idea that sponges are becoming more abundant, and apparent cross-ocean invasions of sponge species raise urgent questions about what processes might control these players of key functional role on coral reefs and which species are actually increasing or declining. The relative importance of abiotic factors and ecological interactions in enhancing or curtailing the distribution and abundance of over 100 species of Caribbean sponges is being studied in three distinct but linked habitats: coral reefs, seagrass meadows, and mangroves. From reciprocal transplant experiments of sponges typical of each of these habitats to each of the other habitats, it is clear that coral reef sponges are controlled by relatively low abundance of their food (i.e., bacteria-sized plankton) in the water column over coral reefs. Reef sponges are prevented from living in seagrass meadows by the large seagrass-dwelling starfish Oreaster reticulatis, and prevented from living on mangrove roots by being out-competed by faster-growing species typical of mangrove prop roots (Wulff 2017). Coral reef sponges can grow much faster in the food-rich water surrounding mangroves, but sponge species typical of mangroves are eaten when transplanted to reefs or seagrass meadows. Repeated annual censuses of corals and sponges on a Blue Ground Range reef for the past 11 years have revealed an alarming pattern: recovery of sponges after dramatic losses to the summer 2011 phytoplankton bloom is not progressing in a way that will restore ecosystem services to the degree that had been provided by sponges before the mass mortality. These combined results raise serious concerns about the negative effects on coral reefs of increased water column nutrients that can spur growth of bacteria-sized plankton and phytoplankton.

Two individuals of the coral reef sponge, Mycale laevis, that are of the same genotype and were the same initial size, after 5 years of growth on a mangrove prop root vs. coral reef. Growth on the mangrove root (left) is over an order of magnitude greater in the same time period.

11| Caribbean Coral Reef Ecosystems

A wide variety of sponges are found on reefs, mangroves, and seagrass habitats.

Coral reproduction and climate change

Nicole Fogarty, Megan Bock, Kelly Habicht, Leah Harper, Morgan Hightshoe, Alicia Vollmer Anthropogenic increases in carbon dioxide emissions have altered global oceanic chemical properties by increasing temperature and decreasing pH [ocean acidification (OA)]. These two pressures of climate change pose as major threats to mature corals. However, only a handful of studies have examined the effects of thermal stress and OA on the early, potentially most vulnerable, life stages of corals. This project examines the ability of four Atlantic corals to withstand these environmental stressors throughout three complete early life history stages: fertilization, survivorship and settlement.

In August and September of 2017, researchers from Nova Southeastern University utilized a neighboring reef of the Carrie Bow Cay field station to examine the spawning event of Orbicella faveolata and the only known hybrid system of the Atlantic. Acropora cervicornis and Acropora palmata form Acropora prolifera, a hybrid that is thriving in areas of both parental species. These four hermatypic broadcast spawning corals reproduce by synchronously releasing gamete bundles of sperm and eggs into the water column. Bundles were collected via nets and brought back to the lab for immediate separation before fertilization. Crosses of each coral taxa were formed by combining sperm and eggs. All crosses were separately subjected to ambient water conditions based on measurements of the surrounding reefs as well as environmental stress conditions of high temperature and OA projected by 2100.

This project investigated larval survivability and settlement onto a tile substrate by rearing larvae in each treatment condition directly following fertilization. The quantity of surviving and settled larvae were counted daily for a period of six days. Thermal stress and OA both separately reduced settlement and survivorship of each of these four important reef building corals. Settlement and survivorship was mitigated in the combined thermal stress and OA treatments for all four coral taxa. Coral reef recovery is critically dependent upon the success of larval recruitment. Understanding how corals cope with future environmental conditions is the first step in protecting these fragile ecosystems.

Elkhorn coral (Acropora palmata) spawning. These corals simultaneously release gametes once per year.

Caribbean Coral Reef Ecosystems | 14

Does biodiversity enhance the ecosystem stability?

Simon Brandl and Jordan Casey

This project used small, bottom-dwelling (cryptobenthic) reef fishes to assess the effect of disturbance on ecological communities and whether biodiversity can mediate this effect. Specifically, the project used communities on marine dock pilings to test their response to scraping off the sessile community from Panama all the way up to the icy waters of Maine. Dock pilings are used as a standardized habitat that permits excellent replication and tractability across a wide geographic range. Cryptobenthic fishes, which are characterized by small size (<150mm), crypsis, and tight associations with the benthic community, represent the experimental community and provide a diverse and responsive assemblage of vertebrates that permits holistic sampling.

The first round of sampling in 2016 established a strong latitudinal gradient in diversity, with the highest diversity of fishes occurring in Panama, Belize and Florida, while communities were less diverse in North Carolina, Massachusetts and Maine. When re-sampling the pilings in 2017, we examined the recovery of the fish communities compared to the previous year. Surprisingly, it appears that communities at the extreme ends of the sampling distributions (Panama, Belize, Massachusetts and Maine) were more affected by the disturbance than the two sub-tropical locations, but this remains to be formally tested. These results, if confirmed statistically, suggest that resilience to disturbance may be greatest in sub-tropical, highly productive environments compared to tropical and temperate ecosystems.

The implications of the present project are important from various angles. First, by examining the response of communities to a severe disturbance, the results will shed light on the capacity of marine coastal systems to cope with the widespread loss of marine habitat. Second, by uncovering the role of biodiversity in a systemâ&#x20AC;&#x2122;s response to disturbance, the project takes on one of the most heavily debated ecological paradigms.

Finally, by exploring the potential of marine dock pilings and their cryptobenthic fish communities to serve as experimental communities over a large spatial scale, the current research program may prime a new wave of experimental marine ecology, performed on dock pilings across the globe.

15 | Caribbean Coral Reef Ecosystems

Cryptobenthic fishes found near Carrie Bow Cay: (top to bottom) Yellowprow goby, warteye sandgazer, and roughhead blenny.

Hydrographic surveying of bioluminescent ostracod habitats

Colin Belby, Gretchen Gerrish, and Karl Radke High levels of genetic divergence have been observed between bioluminescent ostracod populations in Belizeâ&#x20AC;&#x2122;s South Water Caye Marine Reserve, and it is hypothesized that ostracod gene flow is limited over short distances by spatially variable currents, depths, and substrates (coral, sand, seagrass). A hydrographic survey was conducted north of the Carrie Bow Cay Field Station to assess the extent to which these physical properties influence ostracod movement. The potential for using relatively inexpensive side-scan sonar units for marine habitat mapping was also evaluated. High-accuracy mapping of ocean depths was accomplished with a survey-grade echosounder. A low cost fishfinder was mounted adjacent to the echosounder to also log depths and to capture side-scan sonar images of the seafloor. An acoustic Doppler current profiler measured ocean currents in the study area. During a span of 5 days ,over 160 kilometers were traversed within the 6 square kilometer study area by following transects spaced 50 meters apart from each other, providing geospatial data at a resolution exceeding what was previously available. A comparison of the echosounder and fishfinder data indicates the fishfinder is sufficiently accurate for mapping depths, with the added benefit that it is easy to use and provides sonar images of the seafloor that can be processed with inexpensive software. A comparison of the georeferenced side-scan images to satellite imagery also demonstrates that substrate types can be distinguished on the sonar images. These geospatial data are currently being incorporated into a geographic information system to model how the physical environment affects ostracod dispersal.

In addition to mapping habitats, bioluminescent ostracods were collected at patch reefs near South Water Cay and Carrie Bow Cay. These specimens are currently being used to prepare a taxonomic description of a new genus and species. An undergraduate student assisted with mapping and he presented the fishfinder results at a conference. This was the studentâ&#x20AC;&#x2122;s first time conducting research abroad and the opportunity provided him a rich cultural experience and helped develop new skills relevant to his Geography degree. The project has also fostered new collaborations with researchers mapping resources in the Belize Barrier Reef System.

Colin Belby setting up hydrographic surveying equipment at Carrie Bow Cay Field Station with student researcher, Karl Radke.

Caribbean Coral Reef Ecosystems | 18

Phenotypic plasticity and epigenetics in reef corals Jay Dimond

As human influence on the planet expands, many organisms must acclimatize and adapt to rapid environmental change. Phenotypic plasticity facilitates the fastest response to this change, and will likely be critical to the persistence of many species. Epigenetic processes, which contribute to gene regulation without affecting underlying DNA sequences, are increasingly recognized as molecular mechanisms that underlie phenotypic plasticity. The most researched and best understood epigenetic process is DNA methylation, which most commonly involves the addition of a methyl group to a cytosine in a CpG dinucleotide pair. DNA methylation has been shown to mediate environmental effects on gene expression and phenotype in a wide range of taxa.

Reef-building corals are known to display a significant degree of phenotypic plasticity. As long-lived, sessile organisms, corals are thought to be particularly reliant on phenotypic plasticity to cope with environmental heterogeneity, because they must be able to withstand whatever nature imposes on them over long periods of time. Reef corals worldwide are experiencing severe declines due to a variety of anthropogenic stressors, including climate change, ocean acidification, and degrading water quality. This has raised doubt concerning the ability of corals to survive coming decades. Yet there are also signs that, at least in some cases, corals possess sufficient resiliency to overcome their numerous challenges. Recent studies on gene expression variation, for example, support the view that phenotypic plasticity in corals is robust and may provide resilience in the face of ocean warming. Low levels of DNA methylation are correlated with transcriptional plasticity in corals and other invertebrates (Dimond and Roberts 2016), suggesting that DNA methylation may play a role in their response to environmental change.

This year, researchers from Western Washington University returned to Carrie Bow to collect Porites astreoides colonies transplanted to a common garden the previous year. They were able to recover nearly all of them. With these specimens they will evaluate changes in DNA methylation in response to changes in a coralâ&#x20AC;&#x2122;s environment. Further work will address the degree to which gene expression is related to DNA methylation patterns in these same specimens.

Dimond, J.L, and S. Roberts. 2016. Germline DNA methylation in reef corals: patterns and potential roles in response to environmental change. Molecular Ecology, 25(8): 1895-1904.

Microscopic view of the mustard hill coral, Porites asteroides.

19 | Caribbean Coral Reef Ecosystems

Mesophotic reefs

Josh Voss, Michael Studivan, Danielle Dodge, Alycia Shatters, and Ryan Eckert

In March 2017, a team from Florida Atlantic University’s Harbor Branch Oceanographic Institute returned to Smithsonian’s Carrie Boy Cay Field Station to continue and expand their coral ecology and connectivity research. Dr. Joshua Voss and graduate students Michael Studivan, Danielle Dodge, Alycia Shatters, and Ryan Eckert collected almost 200 coral samples along the Mesoamerican Barrier Reef System near Carrie Bow Cay and Glover’s Atoll. The team’s research is focused on addressing two central questions: 1) How well are shallow and mesophotic reefs connected across the Gulf of Mexico and Caribbean? and 2) How do shallow and mesophotic conspecific corals differ with respect to morphology, symbionts, and physiology? For 2017’s field sampling, the team collected coral samples from 4 discrete depth zones at each site to improve resolution of vertical connectivity and to test for hypothesized shifts in the abundance and composition of the corals’ endosymbiotic algae.

Back at FAU Harbor Branch, as part of his master’s thesis research, Eckert will be genotyping colonies through microsatellite analyses and assessing the endosymbiotic algal assemblages with next-generation sequencing.

The results will provide important information about the connectivity and population structure of the coral Montastraea cavernosa among sites and depths within Belize, as well as the role Belize may play in providing coral larvae for reefs downstream in Cuba, Florida, and the Gulf of Mexico. The overarching goals of this study, funded by NOAA’s Cooperative Institute for Ocean Exploration, Research, and Technology, are to explore and characterize vulnerable coral reefs and to provide data and recommendations that enhance management strategies for coral reefs through the Tropical Western Atlantic.

Between the team’s multiple dives to 40m, Studivan and Voss also completed several flights with a DJI Inspire 4K aerial camera to generate a high resolution georeferenced map of Carrie Bow Cay, Curlew Cay, and the visually stunning reefs nearby. Thanks to favorable winds and outstanding support from the Smithsonian staff and volunteer station managers, the team surpassed their goals for the trip and can’t wait to return for more field work in 2018.

FAU Harbor Branch graduate student Danielle Dodge samples a Montastraea cavernosa coral colony.

Caribbean Coral Reef Ecosystems | 22

Citizen Science GIS: Open Reef Nick Altizer

Open Reef is a research initiative through Citizen Science GIS, a 2017 Esri Special Achievement in GIS Award winner, at University of Central Florida that changes the way science and society see and explore vulnerable island environments in Belize through drone mapping, open data, storytelling, and citizen science. Through the use of low-cost, easily accessible drone technology we create high-resolution, opensource imagery of the Belize islands. Features such as island boundaries, structures, docks, and seawalls are then analyzed to understand developmental changes and vulnerabilities on each island. All the while we are interacting with and involving local communities to learn more about the changes that are occurring and to share their stories.

Open Reef took off on its inaugural journey in October 2016. Since then the initiative has mapped 150 islands across three trips and 22 fieldwork days. We have mapped a wide variety of islands, ranging from 13 acres to 1100 acres. Some of these islands include small ones like Foremanâ&#x20AC;&#x2122;s Caye, where old tires are used for sea-level rise adaptation in the form of seawalls. Other islands, such as Caye Caulker, are booming tourist locations with year-round development. When examining publicly available satellite imagery in coastal and island communities in Belize we find the resolution usually exceeds 1m and very rarely approaches 50cm. With our drone mapping capabilities we are able to collect imagery as low as 3.21cm up to 7.49cm.

There is a great need in places like Belize for such high-resolution drone imagery to replace the often outdated and poor resolution satellite imagery found in developing countries.

Open Reef also fosters positive education outcomes by connecting educators from different disciplines to develop K-12 lesson plans aligned with Next Generation Science Standards, focusing on climate adaptation, geography, technology, ecology, and more. In the process we inspire the next generation of community focused scientists through hands-on learning applications in mapping and drone experiences. Our open data platform allows for shared partnership opportunities, improved data quality, and community engagement and input.

To find out more please visit www.citizensciencegis.org/openreef or contact Dr. Timothy Hawthorne at timothy.hawthorne@ucf.edu.

Citizen Science GIS researchers use drone mapping technology to create high-resolution open-source imagery of Belizeâ&#x20AC;&#x2122;s numerous offshore cays.

23 | Caribbean Coral Reef Ecosystems

Trends in water temperature and visibility across the Caribbean Karen Koltes and John Tschirky

Coastal ecosystems and the livelihoods they support are threatened by stressors acting at global and local scales. Long-term, in situ datasets documenting temporal changes in the physical environment of coastal areas, where most economically valuable ecosystems are located, are rare. A first of its kind in the wider Caribbean, the international Caribbean Coastal Marine Productivity program (CARICOMP) was established almost 30 years ago to fill this gap. Its goals were to study processes at the land-sea interface and understand productivity, structure and function of the three main coastal habitats (mangroves, seagrass meadows, and coral reefs) across the region.

CARICOMP was initiated at Carrie Bow Cay in 1993 and represents one of the longest continuous monitoring programs in the western Caribbean. As part of the CARICOMP monitoring Secchi disk deployed at seagrass site. protocols, participating field stations make weekly measurements of water visibility (using a Secchi disk) and surface temperature (0.5m depth). At Carrie Bow Cay, these measurements are made twice weekly in the seagrass beds adjacent to Twin Cays (1.2m depth) and in the ocean east of the drop-off.

In 2017, investigators in the CARICOMP network used the CARICOMP data to look for long-term local and regional-scale trends. Analyses focused on temperature and water clarity (visibility), two proxies of global and local chronic stressors in marine environments. There were two aims: 1) quantify significant changes in these environmental variables over time; and 2) understand if these stressors are influencing the entire basin in a homogeneous way and if not, what factors (i.e. water movement, rainfall, and human influence) could explain differences among sites. To be included in the analyses, sites needed at least 3 years or 30 months of records.

Sixty percent of the CARICOMP stations, including Carrie Bow Cay, met these criteria (48 sites in 18 countries/territories) for a total of 28 reef, seagrass, and mangrove sites in the temperature data analyses and 24 reef and seagrass sites in the visibility analyses. In addition, four variables were also examined for correlation with local trends in water visibility: (1) average wave exposure; (2) average current speed; (3) changes in human population density; and (4) rainfall patterns.

Results showed large spatial variability in temperature and visibility trends across the CARICOMP network (Fig 1). Of the 28 sites, 18% (1 mangrove, 2 seagrass meadows, and 2 coral reef sites), all in the southern Caribbean, showed a significant increasing trend in temperature while one site (Bonaire reef) showed a significant 25 | Caribbean Coral Reef Ecosystems

decrease (Fig. 1A). On the other hand, of the 24 reef and seagrass sites analyzed for visibility trends, 42% (4 seagrass meadows and 6 reefs) showed a significant decreasing trend in visibility (including Carrie Bow Cay), and 2 sites (Jamaica seagrass and Bermuda reef) showed a positive trend (Fig 1B).

Neither warming nor decreases in visibility were observed to be more common in any one of the three habitats monitored (Chi-squared tests, p > 0.05).

Long-term decreases in visibility were more likely to occur at stations with slow water motion, characterized either by low exposure or low current speed. Conversely, long-term increases in visibility were more likely at stations with high wave exposure and current speed, although these variables had a very small effect on long-term increases in visibility. Decreases in visibility were more likely to occur in areas that were getting wetter, and increases were more likely in areas that were getting drier. Decreases in visibility, like those observed at Carrie Bow Cay, were more likely to occur in areas where human population (and associated coastal development) has increased the most.

That visibility decreased at almost half of the stations indicates that local-scale chronic stressors are widespread. On the other hand, only 18% of the stations showed increases in water temperature that would be expected from global warming, partially reflecting the limits in detecting trends due to inherent natural variability of temperature data. The lack of signal in the CARICOMP time series were attributed to two related issues: the larger variability of in situ temperature data and the need for longer time series to detect significant trends.

Decreases in visibility were associated with increased human density. However, physical factors such as water flow (flushing) can help to dampen the effects of increasing human influence in coastal areas.

Figire 1- Changes in temperature and visibility throughout the CARICOMP network. Map of 166 CARICOMP stations showing significant increases, decreases, or non-significant trends for temperature (A) and visibility (B). Labels in Upper case indicate the CARICOMP network field sites while lower case labels indicate habitats (seagrass meadow, coral reef, mangrove forest within those sites.

Carrie Bow Cay Environmental Monitoring: 2 decades of operation Tom Opishinski

On August 12, 1997 a radio signal was transmitted from Carrie Bow Cay at 3:45 pm CST to a receiving station in Dangriga. The signal carried a packet of environmental data that, after reaching the station in Dangriga, was forwarded to Dr. Klaus Rützler in Washington, D.C. using a dial-up Internet connection. Dr. Rützler recognized the importance of water quality and weather measurements on the Mesoamerican barrier reef and had long sought to establish a continuous monitoring system at the CCRE laboratory on Carrie Bow Cay. The data packet was the first of millions of samples acquired over the past two decades but, more significantly, it represented the first milestone for CCRE’s environmental monitoring program.

Dr. Valerie Paul, who shares Dr. Rützler’s recognition for the importance of monitoring on the reef, assumed management of the CCRE program in 2010 and has continued to provide support for the monitoring program. Under the guidance of Dr. Paul along with CCRE management and donations from the Smithsonian’s MarineGEO program, a series of upgrades and additions to the monitoring program and supporting infrastructure have improved system performance and permitted more parameters to be measured at a higher sampling rate. These improvements as well as a more expansive real-time data distribution network has Carrie Bow’s new GLOSS sea level monitoring platform measures sea level every minute. enhanced use of the data by scientists, environmental managers, the Belizean government and the public. As the program begins its third decade, the modernization of hardware and upgrades to data delivery systems insures the continuation of measurements for the Mesoamerican barrier reef. Additionally, it augments historical records acquired at Carrie Bow Cay because the length of the record is sufficient to begin analysis of long-term trends and variations.

One major addition to the monitoring system at Carrie Bow was the construction of a new offshore instrumentation platform north of Carrie Bow Cay in May of 2015 (see photo above). In order to make millimeter-accuracy measurements of sea level, the platform is designed to be absolutely stable and is built on three 12-inch cement pilings driven ~ 15 meters below the seabed. To insure the stability is maintained, 27 | Caribbean Coral Reef Ecosystems

a geodetic control network of two survey benchmarks was installed on Carrie Bow Cay and another on the platform deck. Extensive surveys were conducted to determine the positions of the level sensors relative to the benchmarks, which allows the data to be referenced to the true mean sea level. Measurements of water level are acquired every minute and transmitted every 5 minutes to provide real-time tide information and to also monitor and provide early warnings for tsunamis. The data is incorporated by UNESCO’s Intergovernmental Oceanographic Commission’s Sea Level Monitoring facility in Belgium (http://www.ioc-sealevelmonitoring.org) and the station is part of the Caribe-EWS, or early warning system for tsunami prediction that operates under NOAA’s Pacific Tsunami Warning Center (http://www.ioc-tsunami.org). The data is also available in the updated data portal at http://nmnhmp.riocean.com.

The environmental monitoring system at Carrie Bow is a critical resource because it is the only continuously-operated system monitoring both oceanographic and meteorological conditions on the Mesoamerican barrier reef. The addition of high-accuracy sea level sensors and new abiotic/nutrient sensors expands the utility of the system and further solidifies its value as a critical tool for scientific insight of the reef ’s health. To strengthen the visibility and value of the data, the portal includes automated feeds that transfer and integrate data with third party organizations (e.g., NOAA (multiple sub-agencies), British Oceanographic Data Commission, Weather Underground, etc.).

No one could have guessed in 1997 the significance of a single data packet transferred from a remote island in Central America to Washington D.C. Today the system manages tens of thousands of packets daily that traverse the globe to the benefit of many. The system has reached many milestones in the past twenty years and has contributed valuable information to numerous scientific studies and publications. It is well positioned to continue serving present demands of the scientific community and the public and numerous opportunities exist to expand capabilities for both present and future requirements. Analysis of historical data captured at Carrie Bow Cay will help us gain a better understanding of the health of the reef and better understand observed changes to the ecosystem as it responds to future conditions.

Metereological sensor tower at Carrie Bow Cay.

Understanding habitat movement in peppermint shrimp Molly Ashur and Danielle Dixson Chemical cues can be viewed as a â&#x20AC;&#x153;languageâ&#x20AC;? used by marine organisms to determine an appropriate behavioral response.

Many marine organisms rely solely on chemical cues to determine if they should mate with, escape from, eat, or fight with their neighbor. Therefore, a better understanding of this language provides insight in reef restoration and may lead to more effective conservation activities. Research activities conducted this year at Carrie Bow Cay have concentrated on understanding the chemical A peppermint shrimp ready for deployment in field experiment near CBC. cues used by organisms in habitat selection with a focus on understanding the concentrations, specific chemicals, and the influence chemical cues have on the behavior of marine organisms. Using both laboratory and field-based studies, a better understanding on the use of chemical cues has been identified for various reef creatures.

The peppermint shrimp, Lysmata pederseni, is a small cleaner shrimp that dwells in tube sponges and can be found throughout the Caribbean. Molly Ashur, a graduate student at the University of Delaware, set out to uncover how the shrimp chooses its tube sponge home by conducting both laboratory and field experiments.

She used different bioassays in the lab, including a two-chamber choice flume and choice experiment, which allowed her to test habitat preference cues (chemical vs. morphological) in isolation, while in situ patch reef experiments were conducted to test for preference among potential tube sponge habitats.

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How do different herbivores shape algal communities?

Lindsay Spiers and Tom Frazer In the Caribbean region, overfishing of herbivorous fish and a mass die-off of the sea urchin Diadema antillarum have contributed to increased macroalgal abundance which, in turn, has contributed to a general decline in coral reef health. The return of D. antillarum to some Caribbean sites has been connected to decreases in macroalgal abundance and increases to coral recruitment. Concurrently, many countries (including Belize) have enacted marine protected areas and bans on fishing to protect herbivorous fish and, in some areas, there has been a marked recovery of fish and subsequent decline in macroalgae. The recovery of these two types of herbivores has led to questions about the role of these different herbivores on coral reefs. To examine how herbivorous fish and D. antillarum affect the growth and structure of macroalgae communities a 4-month caging experiment was conducted on a shallow patch reef near Carrie Bow Cay. Treatments used were full herbivore exclusion, cages that excluded sea urchins but allowed fish access, partial cage controls and nocage controls. The substrate in all treatments was scrubbed clean of macroalgae at the beginning of the experiment and then macroalgae were allowed to settle and grow. As expected, at the end of the experiment the abundance of macroalgae was greatest in cages that excluded herbivores and these cages also supported an algal assemblage distinctly different from other treatment types, i.e. cages that allowed grazers access. The different treatments that allowed different types of herbivoresâ&#x20AC;&#x2122; access did not result in different abundances of macroalgae but did result in differences in what macroalgae were present. These findings suggest that at abundances and biomasses found on these reefs, herbivorous fish exert sufficient grazing pressure to maintain macroalgae in a low abundance state. However, fish and sea urchins together result in a different algal community than fish alone, and this algal community is comparable to the algal community in the surrounding reef, indicating that Diadema antillarum may be a driving force in determining community structure on these reefs.

An herbivore exclusion cage deployed near CBC.

Coral microbiomes

Matthew Hoch, Craig Nelson, Linda Wegley Kelly, Craig Carlson, Mark McNab, Hostin May, Katelin Catching, B. Tran T. Nguyen, and Emmett Worsham.

Coral reefs support tremendous biodiversity and essential ecological services, yet multiple human impacts over recent decades are resulting in declining coral health, increased benthic fleshy macroalgal dominance, and biodiversity loss. The mechanisms of coral decline and macroalgal replacement are hypothesized to involve feedback interactions among macroalgae, dissolved organic matter (DOM), and microbes. Thermal stress may have a synergistic effect on the microbial response to macroalgal exudates (DOM release by algae) and accelerate coral decline.

This project focused on defining responses of microbial communities (microbiomes) to benthic macroalgal exudates and temThe rose coral (Manicina areolata) among seagrass. perature, specifically hypoxia and pathogen growth leading to coral decline. The target coral species used in thermal stress and algal exudate experiments were a common coral of seagrass meadows, Manicina areolata (rose coral) and the cosmopolitan reef coral, Porites astreoides (mustard hill coral). Effects of temperature on the microbiome composition was studied for both coral species; whereas, the added or synergistic impact of exposure to temperature and algal exudates was tested for P. astreoides. In January and August 2017, thermal effects on microbiomes of M. areolata and adjacent seawater was explored under ambient conditions at seagrass sites in the South Water Caye Marine Reserve with significantly different sea surface temperature, as well as in controlled experiments that exposed corals to a thermal stress event. Algal exudates from two algae, Dictyota sp. and Amphiroa sp., were tested for their impacts on plankton and P. astreoides microbiomes in experiments with the presence or absence of a thermal stress event. Additionally, in August 2017, 13C-labeled exudates from Dictyota sp. were generated and used in experiments to track which bacteria in the plankton microbiome used the exudates for rapid growth.

Coral mucus and plankton metagenomic DNA were extracted from samples collected at ambient sites and in all experiments, and it is in the process of being sequenced to identify taxa of bacteria in each sample. Data will be analyzed to identify conditions of temperature and algal exudates that select for coral pathogens in plankton and mucus microbiomes. These results will contribute to understanding conditions that create the greatest risk to coral resiliency, information that can assist best management practices for coral reef sustainability.

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Biodiversity of symbiotic invertebrates Niko Leisch, Alexander Gruhl, Dolma Michellod, Yui Sato, and Anna Mankowski A variety of marine invertebrates living within sandy bottoms are known to host beneficial bacteria that provide them with nutrition. Researchers from the University of Vienna work at Carrie Bow Cay to explore the diversity of symbioses between marine invertebrates and bacteria in the habitats around the station. One group of them – and the focus of this research trip - are annelid worms of the genus Inanidrilus (see photo).

These worms no longer have a mouth, a gut or an anus and obtain their energy primarily from bacteria that are living under their skin. These bacteria and their storage compounds give these worms their bright white color. Previous field studies showed that the Belize Barrier Reef harbors a wide diversity of such animalbacteria symbioses, and that the actual biodiversity in this area is most likely still underestimated. During this field work stay, the team has successfully broadened the recorded diversity of such symbiotic animals within the Belize Barrier Reef. They collected samples of symbiotic marine invertebrates at different sediment spots around Twin Cayes, Southwater Caye, Carrie Bow Caye and Curlew Caye for morphological- and molecularanalyses. And while analyses of the sampled animals are still ongoing, the researchers have already identified nine different symbiotic host species. The team also collected sediment samples to investigate the presence of closely related, but non-symbiotic bacteria. By pinpointing similarities and differences between symbiotic and freeliving bacteria the scientists hope to understand what makes a certain bacterium capable of successfully colonizing an animal host. Furthermore, the water chemistry within these sandy sediments is being characterized to better understand the habitats these animals live in.

In future studies, the team hopes that the data from this trip will allow them to answer research questions such as ‘How do the host and its symbionts benefit from each other?’, ‘How did the symbiotic lifestyle influence the evolution of both the host and its symbionts?’ and ‘Why do they occur in the Belize Barrier Reef?’.

The symbiotic gutless worm Inanidrilus leukodermatus. The worm no longer has a mouth or a gut, instead it relies on the symbiotic bacteria living within its body.

TMON field campaign Ross Whippo, Emmett Duffy, Janina Seeman, Justin Campbell, Mike Goodison, Scott Jones, Maggie Johnson, and Zach Foltz

MarineGEO transects monitor fish biodiversity over time.

For a third straight year, Smithsonian researchers gathered at Carrie Bow Cay to participate in the Smithsonian’s Marine Global Earth Observatory Network (MarineGEO) annual field campaign. The objectives are to carry out the program’s habitat sampling protocols and to support projects of MarineGEO scientists and postdoctoral fellows.

MarineGEO (www.marineGEO.si.edu), directed by the Smithsonian’s Tennenbaum Marine Observatories Network (TMON), is the first long-term, worldwide research program to focus on understanding coastal marine life and its role in maintaining resilient ecosystems around the world.

In the span of a very busy three weeks, researchers conducted a rigorous set of protocols to examine each important tropical habitat surrounding Carrie Bow Cay, including mangroves, seagrasses, patch reefs, sand flats, and fore reef. Intensive assessments of mangroves and seagrasses measure productivity, growth, and biomass, while an exhaustive survey of fish and invertebrate diversity is conducted at each habitat using Reef Life Survey protocols (www.reeflifesurvey.com).

Important ecological processes like herbivory and predation are measured with fish feeding assays deployed at each habitat. The data generated from these efforts are impressive: thousands of feeding assays have been recorded and hundreds of fish and invertebrate species have been documented. These projects play an important role in advancing MarineGEO’s efforts to monitor coastal ecosystems.

Additionally, the scientific team worked to engage with the public during the campaign by hosting a Facebook Live event with the Smithsonian’s Ocean Portal (www.ocean.si.edu) and by hosting a live presentation for University of Belize students in Dangriga, Belize.

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CCRE South Water Caye Marine Reserve reef assessment Scott Jones, Zach Foltz, Randi Rotjan, Leah Harper, and Alicia Volllmer

This year marks the seventh year Caribbean Coral Reef Ecosystems program (CCRE) staff and collaborators have conducted the South Water Caye Marine Reserve (SWCMR) Reef Assessment Program. At over 100,000 acres, SWCMR is one of the largest marine reserves in Belize and encompasses the waters around the Smithsonian’s Carrie Bow Cay Field Station. The reef assessment project aims to identify effects of the no-take conservation zone around Carrie Bow Cay on the recovery of fish and coral populations. In June 2011, permanent transects were established inside (12 transects) and outside (12 transects) the area’s boundary and have been surveyed bi-annually since then. This amounts to over 336 unique surveys on the reefs around Carrie Bow Cay. Reef monitoring efforts typically measure the diversity, abundance, and biomass of key reef organisms as indicators of reef health. CCRE’s assessment program is designed to evaluate similar ecological metrics, so as to be compatible with other monitoring efforts elsewhere in Belize and the western Atlantic Ocean. But researchers have also added some assessments that yield information about key ecological rates and states that are thought to contribute to reef resistance, resilience, and recovery in the face of negative impacts. One example of the measured rates is the grazing rates of herbivores, such as parrotfishes and surgeonfishes, which help keep algae from overgrowing the reef. Researchers also monitor the “states” of the benthic community, such as the health status of important reef-building corals, as well as coral recruitment and growth dynamics. This approach provides more comprehensive ecological monitoring, and informs models of reef dynamics that will be used to generate new insights into reef community structure in response to different reserve management regimes. This study is designed to take advantage of the strengths and capabilities of the Carrie Bow Cay Field Station and produce important information that will be applied to habitat management in the SWCMR no-take area.

Researchers are keeping a close eye on coral bleaching that has been affecting the reefs for three consecutive years.

Concerns are mounting that this chronic stress could increase coral mortality and reduce the resiliency of the reef to acute disturbances.

A diver surveys corals on a permanent transect in the SWCMR.

What does home smell like?

Skylar Carlson, Zara Cowan, Jennifer Sneed, Audrey Looby, Lane Johnston, Jennifer Joseph, Danielle Dixson, and Valerie Paul

This project seeks to identify cues from the reef that fish and coral larvae use to find their way home. Larval fish are hatched from eggs and enter a planktonic stage where they can travel far from the reef. These fish use chemical cues (as one of many ways) to find their way back to the reef.

This project seeks to identify compounds responsible for guiding these fish home. In the field, we use two channel flow chambers (small two-choice flumes) to test whether chemical cues are important. Chemical cues are prepared by soaking small amounts of individual species from the reef in seawater. We have examined algae, adult coral, cyanobacteria, seagrass, sponges, as well as other fish species for potential attractive and deterrent chemical cues. Juvenile fish are then placed into A light trap is used to collect larval fish for experiments. a two-choice flume, and they can decide between paired seawater choices. Coral larvae are tested in much the same way, but coral only spawn once a year, making the accumulation of data more challenging.

In the laboratory, the same organisms that are tested in the flumes are extracted in order to find sufficient amounts of the attractive or deterrent compounds for further testing and characterization. Additionally, the seawater soaks are passed over solid phase extraction columns to retain compounds dissolved in seawater.

These extracts are then fractionated and individual compounds are identified. During 2017, we learned that most cyanobacteria, macroalgae, and some sponges deter fish and coral recruitment, and corals and crustose coralline algae act as attractants. These efforts are important for determining what an attractive reef smells like and to guide knowledge-based conservation and restoration efforts.

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2017 Scientific Publications

Bok, M. J., M. Capa, D. Nilsson. 2017. Here, There and Everywhere: The Radiolar Eyes of Fan Worms (Annelida, Sabellidae). Integrative and Comparative Biology, 56 (5): 784–795.

Brandl, S.J., J.M. Casey, N. Knowlton, J.E. Duffy. 2017 Marine dock pilings foster diverse, native cryptobenthic fish assemblages across bioregions. Ecology and Evolution, 7: 7069–7079.

Cunha, A., A. Collins, A. Marques. 2017. Phylogenetic relationships of Proboscoida Broch, 1910 (Cnidaria, Hydrozoa): Are traditional morphological diagnostic characters relevant for the delimitation of lineages at the species, genus, and family levels? Molecular Phylogenetics and Evolution, 106: 118-135.

Chak, S.T.C., J.E. Duffy, K.M. Hultgren, D.R. Rubenstein. 2017 Evolutionary transitions towards eusociality in snapping shrimps. Nature Ecology and Evolution, 1: 0096.

D’Aloia, C.C., S.M. Bogdanowicz, R.G. Harrison, P.M. Buston. 2017. Cryptic genetic diversity and spatial patterns of admixture within Belizean marine reserves. Conservation Genetics, 18: 211–223.

Dimond, J.L., S.K. Gamblewood, S.B. Roberts. 2017. Genetic and epigenetic insight into morphospecies in a reef coral.

Molecular Ecology, 26: 5031–5042.

Leisch, N., N. Pende, P. Weber, H. Gruber-Vodicka, J. Verheul, N. Vischer, S. Abby, B. Geier, T. den Blaauwen, S. Bulgheresi.

2017. Asynchronous division by non-ring FtsZ in the gammaproteobacterial symbiont of Robbea hypermnestra. Nature Microbiology, 2: 16182 Marino, C.M., J.R. Pawlik, S. Lopez-Legentil, P. M. Erwin. 2017. Latitudinal variation in the microbiome of the sponge Iricinia campana correlates with host haplotype but not anti-predatory chemical defense. Marine Ecology Progress Series, 565: 53-66.

Meyer, J.L., V.J. Paul, L. J. Raymundo, M. Teplitski. 2017. Comparative metagenomics of the polymicrobial Black Band Disease of corals. Frontiers in Microbiology, 8: 618.

Seah, B. K. B., T. Schwaha, J. Volland, B. Huettel, N. Dubilier, H.R. Gruber-Vodicka. 2017. Specificity in diversity: single origin of a widespread ciliate-bacteria symbiosis. Proceeding of the Royal Society B, 284 (1858): 20170764.

Wulff, J. 2017. Bottom-up and top-down controls on coral reef sponges: disentangling within-habitat and between-habitat processes. Ecology, 98 (4): 1130–1139.

Caribbean Coral Reef Ecosystems|36

2017 Participants * served as station manager Akkaynak, Derya, Interuniversity Institute of Marine Sciences, Eilat, Israel Alanko, Jerry, Tilghman, MD* Alanko, Sandy, Tilghman, MD* Altieri, Andrew, Smithsonian Tropical Research Center, Panama City, Panama Altizer, Nick, University of Central Florida, Orlando, FL Ashur, Molly, University of Delaware, Newark, DE Avelina, Franco, Fragments of Hope, Placencia, Belize Beers, Scott, Smithsonian Environmental Research Center, Edgewater, MD* Belby, Colin, University of Wisconsin- La Crosse, La Crosse, WI Bock, Megan, Nova Southeastern University, Dania Beach, FL Bohnsack, Karen, Florida Department of Environmental Protection, Key Largo, FL Brandl, Simon, Smithsonian Environmental Research Center, Edgewater, MD Branson, David, Smithsonian Marine Station, Fort Pierce, FL Brooker, Rohan, University of Delaware, Newark, DE Bulgheresi, Sylvia, University of Vienna, Vienna, Austria Cardini, Ulisse, University of Vienna, Vienna, Austria Carlson, Skylar, Smithsonian Marine Station, Fort Pierce, FL Carne, Lisa, Fragments of Hope, Placencia, Belize Casey, Jordan, James Cook University, Australia Campbell, Justin, Smithsonian Marine Station, Fort Pierce, FL Cody, Clyde, Boise, ID* Cody, Liz, Boise, ID* Cowan, Zara, University of Delaware, Newark, DE Dimond, Jay, Shannon Point Marine Center, Western Washington University, Anacortes, WA Dimond, Julie, Shannon Point Marine Center, Western Washington University, Anacortes, WA Dodge, Danielle, Harbor Branch Oceanographic Institute, Florida Atlantic University, Fort Pierce, FL Dramer, Greg, Kalispell, MT* Dramer, Joann, Kalispell, MT* Eckert, Ryan, Harbor Branch Oceanographic Institute, Florida Atlantic University, Fort Pierce, FL Felder, Darryl, University of Lousiana at Lafayette, LA Felder, Jennifer, University of Lousiana at Lafayette, LA Foltz, Zachary, Smithsonian Marine Station, Fort Pierce, FL Fogarty, Nicole, Nova Southeastern University, Dania Beach, FL Freeman, Chris, Smithsonian Marine Station, Fort Pierce, FL Gentry, Eric, Smithsonian Institution, Washington, D.C. Gerrish, Gretchen, University of Wisconsin- La Crosse, La Crosse, WI 37 |Caribbean Coral Reef Ecosystems

2017 Participants Gochfeld, Deborah, University of Mississippi, Oxford, MS Godfrey, Dale, Fragments of Hope, Placencia, Belize Goodison, Mike, Smithsonian Environmental Research Center, Edgewater, MD Gruhl, Alexander, Maz Planck Institute for Marine Microbiology, Bremen, Germany Habicht, Kelly, Nova Southeastern University, Dania Beach, FL Haren, Nick, Anacortes, WA* Haren, Marylin, Anacortes, WA* Harper, Leah, Nova Southeastern University, Dania Beach, FL Hightshoe, Morgan, Nova Southeastern University, Dania Beach, FL Hoch, Matthew, Lamar University, Beaumont, TX James, Edwin, Tilgman, MD* James, Bonnie, Tilgman, MD* Janiak, Dean, Smithsonian Marine Station, Fort Pierce, FL Johnston, Lane, University of Delaware, Newark, DE Jones, Scott, Smithsonian Marine Station, Fort Pierce, FL Joseph, Jennifer, University of Delaware, Newark, DE Kintzig, Elizabeth, University of New Hampshire, Durham, NH Koltes, Karen, U.S. Department of the Interior, Washington, D.C. Leisch, Nikolaus, Max Planck Institute for Marine Microbiology, Bremen, Germany Lesser, Michael, University of New Hampshire, Durham, NH Looby, Audrey, Smithsonian Marine Station, Fort Pierce, FL Macartney, Keir, University of New Hampshire, Durham, NH Manglicmot, Claire, University of Toronto-University of St. Maryâ&#x20AC;&#x2122;s College, Toronto, Canada Mankowski, Anna, Max Planck Institute for Marine Microbiology, Bremen, Germany May, Hostin, Lamar University, Beaumont, TX McNab, Mark, University of Belize, Belmopan, Belize Michellod, Dolma, Max Planck Institute for Marine Microbiology, Bremen, Germany Moore, Joel, Shingle Springs, CA* Moore, Linda, Shingle Springs, CA* Moran, Benjamin, Northeastern University, Boston, MA Morrow, Kathy, University of New Hampshire, Durham, NH Opishinski, Tom, Interactive Oceanographics, East Greenwich, RI Ott, JĂśrg, University of Vienna, Austria Ott, Renate, University of Vienna, Austria Paredes, Gabriela, University of Vienna, Austria Parsons, Keith, Atlanta, GA* Paul, Valerie, Smithsonian Marine Station, Fort Pierce, FL Pende, Nika, University of Vienna, Austria Caribbean Coral Reef Ecosystems | 38

Peresta, Gary, Smithsonian Environmental Research Center, Edgewater, MD* Puebla, Oscar, GEOMAR Helmholtz Center for Ocean Research, Kiel, Germany Rabalais, Steve, Baton Rouge, LA Rabalais, Jean, Baton Rouge, LA Radke, Karl, University of Wisconsin- La Crosse, La Crosse, WI Roden, Isabella, Washington, D.C. Sabrina Pankey, Molly, University of New Hampshire, Durham, NH Sanchez, Maria, Washington, D.C. Sato, Yui, Max Planck Institute for Marine Microbiology, Bremen, Germany Scharhauser, Florian, University of Vienna, Austria Scheff, George, Boise, ID* Schile, Lisa, Smithsonian Environmental Research Center, Edgewater, MD* Seemann, Janina, Smithsonian Tropical Research Institute, Panama Serrato, Milena, National University of Colombia, Bogota, Colombia Shatters, Alycia, Harbor Branch Oceanographic Institute, Florida Atlantic University, Fort Pierce, FL Sherwood, Craig, Deale, MD* Slattery, Marc, University of Mississippi, Oxford, MS Smith, J.R., National Museum of Natural History, Washington, D.C. Sneed, Jennifer, Smithsonian Marine Station, Fort Pierce, FL Spiers, Lindsay, University of Florida, Gainesville, FL Sterrer, Wolfgang, Bermuda Zoological Society, Flatts Village, Bermuda Stuart-Smith, Rick, University of Tasmania, Hobart TAS, Australia Studivan, Michael, Harbor Branch Oceanographic Institute, Florida Atlantic University, Fort Pierce, FL Tschirky, John, American Bird Conservancy, Washington, D.C. Viehbรถck, Tobias, University of Vienna, Austria Vollmer, Alicia, Nova Southeastern University, Dania Beach, FL Voss, Josh, Harbor Branch Oceanographic Institute, Florida Atlantic University, Fort Pierce, FL Wallen, Mariko, Fragments of Hope, Placencia, Belize Walczak, Joanna, Florida Department of Environmental Protection, Miami, FL Weber, Phillip, University of Vienna, Austria Whippo, Ross, Smithsonian Tennenbaum Marine Observatories Network, Washington, D.C. Wulff, Janie, Florida State University, Tallahassee, FL

39 |Caribbean Coral Reef Ecosystems

Acknowledgements

Our research is hosted by the Belize Fisheries Department and we thank Ms. Beverly Wade and Mr. Mauro Gongora and staff for collaboration and issuing permits. The owners and dedicated staff of Pelican Beach Resort in Dangriga provided logistical support for our fieldwork. Earl David and his staff provided boat transportation, as well as invaluable advice and support.

Numerous volunteer managers helped run the field station and assisted in research activities; we greatly appreciate their many efforts: Jerry & Sandy Alanko, Scott Beers, Liz & Clyde Cody, Greg & Joann Dramer, Nicky & Marilyn Haren, Raphael Ritson-Williams, Ed & Bonnie James, Joel & Linda Moore, Keith Parsons, Gary Peresta, George Scheff, Lisa Schile, and Craig Sherwood.

In Fort Pierce, we sincerely thank Joan Kaminski for administrative advice and assistance with many fund management tasks. Special thanks to Skylar Carlson for her keen editorial eye.

In Washington, Klaus Ruetzler and Mike Carpenter are always willing to share wisdom stemming from their many years of experience in Belize. A number of people at NMNH are always willing to answer questions: Charmone Williams, Mike McCarthy, Carol Youmans, and JoAnna Mullins among many others. We also thank the office of the Director of the National Museum of Natural History for continued support.

The CCRE program is supported by Federal funding complemented by the Hunterdon Oceanographic Research Fund.

Caribbean Coral Reef Ecosystems | 40

Photo Credits

Cover: Nick Altizer page 1: S. Jones; page 4: (top to bottom) Z. Foltz, Z. Foltz, V. Paul; page 5: A. Wood; page 8: M. Lesser; page 9: D. Felder; page 11: J. Wulff: page 12: G.W. Stoyle; page 13: Z. Foltz; page 15: S. Brandl & J. Casey; page 17: G. Gerrish; page 20: S. Jones; page 21: J. Voss; page 24: Citizen Science GIS; page 25: S. Jones; page 27: T. Opishinksi; page 28 T. Opishinski; page 29: Z. Foltz; page 30: L. Spiers; page 31: S. Jones; page 32: N. Leisch; page 33: Z. Foltz; page 34: Z. Foltz page 35: S. Carlson; page 41: J. Brown; Back cover: S. Brandl & J. Casey

41|Caribbean Coral Reef Ecosystems

Smithsonian Marine Station Fort Pierce, FL www.sms.si.edu Caribbean Coral Reef Ecosystems Program Carrie Bow Cay, Belize www.ccre.si.edu