2016 CCRE Annual Report

Smithsonian Institution

2016 CCRE Annual Report Caribbean Coral Reef Ecosystems • National Museum of Natural History

CCRE Fiscal Year 2016

Table of Contents The CCRE program continued moving forward in 2016. Carrie Bow Cay hosted nearly 80 individual scientific visitors that contributed to almost 1000 research days in the field. Carrie Bow continues to be a venue for a diverse spectrum of research into biodiversity, ecology, and conservation. Additionally, the station made important facility improvements to reduce fossil fuel consumption: increased solar capacity has reduced dependence on a power generator and new four-stroke outboard engines have significantly increased the fuel efficiency of the vessels. The research taking place at Carrie Bow Cay is more critical now than ever as coastal marine environments undergo rapid changes. The station continues to be an important site for coral reef studies for Smithsonian researchers and their colleagues from all over the world.

4 Carrie Bow Cay Field Station 5 Research Highlights 21 Research Briefs 30 Scientific Publications 32 Visitors and Station Managers 35 Acknowledgements

0

km

$BSSJF #PX 3FTFBSDI "SFB

100

SFWJTFE

XJUI NPTU $BZT OBNFE

Columbus Cay

Mexico

Beli z e C i ty

D an g r i g a

$ BS JCC F BO 4FB

. .

Hutson Cay

17˚00'N

Mosquito Cay Sandfly Cay Cross Cay

Dangriga

Garbutt Cay $PMVNCVT 3FFG

1 7ºN

16˚55'N

5PCBDDP 3BOHF Tobacco Cay G ua te mala

Coco Plum Cay

Honduras

5PCBDDP 3FFG

Man-o'-War Cay

8 8 ºW

Ragged Cay Twin Cays

#MVF (SPVOE 3BOHF

South Water Cay

Sittee Point

Carrie Bow Cay $VSMFX #BOL

4BQPEJMMB -BHPPO

Stewart Cay Wee Wee Cay

1BUDI 3FFGT 4BOE #PSFT

Spruce Cay

16˚45'N

4PVUI $VU

Douglas Cay Riversdale

Manatee Cay

Jonathan Point

N mag.

Elbow Cays

1FMJDBO $BZT

Quamino Cays

Cat Cay Channel Cay

Lagoon Cays 1BUDI 3FFGT 4BOE #PSFT

False Cay Crawl Cay

False Point

16˚35'N

Tarpum Cay

5 km

Bakers Rendezvous Rendezvous Cay 88˚15'W

Gladden Cays 88˚05'W

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 and highly functional field laboratory boasts a flow-through seawater system, wet and dry laboratory space, full SCUBA facilities, research vessels, and living quarters.

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

Coral larval ecology

Jennifer Sneed, Justin Campbell, and Valerie Paul

Modern and future coral reefs face an unprecedented combination of biotic and abiotic threats. Two of the most prominent threats to coral reefs are increasing coral-algal competitive interactions and ocean acidification. In the Caribbean, depressed herbivory rates due to overfishing and the massive die-off of the sea urchin Diadema antillarum have increased macroalgal abundance and the frequency of coral-algal competitive interactions. As carbon dioxide increases in the atmosphere, the amount of carbon dioxide in the oceans also increases, causing a decrease in the pH of seawater.

This phenomenon is known as ocean acidification. Both macroalgal presence and ocean acidification have been found to have detrimental impacts on the heath of adult corals and on the recruitment of future generations, however, these stressors will not occur in isolation and understanding the implications of these factors in combination is critical for the development of efficient and effective management and conservation strategies.

Over the past two years, we have been examining how corals will respond to the combined threats of algal overgrowth and ocean acidification by setting up a field-based ocean acidification system at Carrie Bow Cay. This system allows us to control the carbon dioxide levels in the seawater in order to replicate conditions that are predicted to occur within the next 100 years if carbon emissions continue as they are today. We have determined that the effects of OA and macroalgae are complex and depend heavily on the algal species and coral species involved. Based on an experiment using the OA system at Carrie Bow Cay last summer, we determined that neither OA nor exposure to the brown alga Stypopodium zonale had any effect on the settlement behavior of the elkhorn coral, Acropora palmata. However, the presence of S. zonale significantly affected the health (measured as photosynthetic ability) of the crustose coralline alga (CCA) the corals use as a preferred settlement surface. The effects of S. zonale were exacerbated by future ocean acidification conditions (pH 7.8) as compared to present day levels (pH 8.0). This summer we set out to determine if the harmful impacts of S. zonale on the health of CCA could be attributed to defensive chemicals produced by the algae. We conditioned pieces of CCA in seawater at either present day pH (8.0) or future pH (7.8) for 8 days. Then we exposed them to either organic surface extracts from S. zonale, the pure compound stypoldione (a known defensive compound from S. zonale), or a control with no extract. We added A. palmata larvae to all of the treatments and allowed them the opportunity to settle on the CCA for 24 hours. Neither the presence of S. zonale compounds nor changes in the seawater pH had any impact on the photosynthetic capabilities of the CCA or on the settlement behavior of A. palmata. However, we had some difficulties testing the extracts and pure compound on the CCA and need to develop better methods to test these effects, a project that we will tackle next year. While the presence of S. zonale on the reef might not directly impact larval settlement in the spawning coral A. palmata, it could cause a reduction in the amount of healthy CCA that is necessary to provide an appropriate habitat for new coral recruits. Through our continued investigation of the interactive effects of macroalgae and OA on the reproductive success of corals at Carrie Bow Cay, we have discovered that these effects are extremely complex and species dependent.

Smithsonian researcher Justin Campbell tends to an experiment in the ocean acidification system at Carrie Bow Cay.

Caribbean Coral Reef Ecosystems | 6

Does biodiversity benefit ecosystem stability?

Simon Brandl and Jordan Casey

The present project examines the effect of biodiversity on the stability of communities in the wake of a severe disturbance. To do so, the project takes advantage of two frequently overlooked components, dock pilings and cryptobenthic fishes. 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. To implement the experiment, cryptobenthic fish communities are sampled from dock pilings at the start of the experiment and one year after a severe habitat disturbance is administered to the pilings (by scraping off the sessile community). By replicating this experiment at six locations from Maine to Panama, including Carrie Bow Cay, the experimental framework utilizes a natural biodiversity gradient to understand the impact of biodiversity on communitiesâ&#x20AC;&#x2122; responses to disturbance.

Initial results from implementing the experiment at docks around Carrie Bow Cay suggest that dock pilings are a viable habitat for cryptobenthic fishes and that communities show significant variation both at regional and local scales. In addition, the sampling revealed that dock pilings serve as important habitat for species with conservation concerns, such as the black grouper Mycteroperca bonaci. Overall, these preliminary results are promising for the outcome of the experiment.

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.

7 |Caribbean Coral Reef Ecosystems

An assortment of cryptobenthic fishes sampled from dock pilings in the vicinity of Carrie Bow Cay.

How are populations of porcellanid crabs connected in the West Atlantic and East Pacific?

Alexandra Hiller and H.A. Lessios

Porcellanidae is a morphologically and ecologically diverse family of marine, crab-like anomuran crustaceans. This taxon contains 278 species in 30 genera, with littoral or sublittoral distribution throughout the tropical and temperate regions of all oceans. Porcellanidae comprises one of the most abundant groups of crustaceans in rocky and coral habitats, and are located at the base of the marine food web because they filter feed on water-borne detritus.

The morphological diversity within the family reflects ecological diversity. Most porcellanid species live on hard substrates, but some are involved in symbiotic associations with marine invertebrates (e.g. echinoderms, polychaetes and sponges), and a few are found in muddy burrows in mangrove swamps and estuaries.

The principal aim of this project is to generate phylogeographies of West Atlantic and East Pacific porcellanid species in order to reveal the genetic connectivity of their populations, as well as current and historical barriers to gene flow. Phylogeographic analyses are based on comparison of DNA sequences of mitochondrial genes, and depend on densely sampling a species throughout its geographic range. Belize lies in a key location of the geographic range of West Atlantic species with wide and restricted distributions (e.g. from South Carolina to Brazil vs. endemic to the Caribbean). The most abundant species around the Carrie Bow Cay area are Petrolisthes caribensis, P. galathinus, P. quadratus (see left) and Pachycheles susanae. Sampling these crabs is difficult but fun.

They typically live in areas where currents and waves are strong because they need water movement to optimally filter-feed.

The porcelain crab, Petrolisthes quadratus, collected from the waters around Carrie Bow Cay.

Caribbean Coral Reef Ecosystems | 10

Using 3D models to measure carbonate production in coral reefs Andrew Mogg and Martin Sayer

Carbonate cycling processes may exert a constructive or destructive influence on reef-related carbonate accumulation. These processes operate at the scale of the individual coral colony but aggregate to influence reef accretion over larger spatial units. The ReefBudget project quantifies net rates of biologically-derived reef framework production encompassing estimates of carbonate production by corals and calcareous encrusters (usually dominated by crustose coralline algae) and framework erosion by internal borers and substrate grazers. This is achieved using an intensive, in-situ, census-based approach. This approach yields a planar surface area for each organism or substrate investigated, which is then corrected for rugosity by measuring the topographic complexity of the reef.

SfM-Multiview Stereophotogrammetry (SfM-MVS) is the technique of creating three dimensional digital models from successive images. These models provide a permanent in-silico record which may be analysed for any specific physical component, such as surface area and volume, depending on resolution. Though it was developed for terrestrial projects such as aerial survey or archaeological recording, it is increasingly being used in underwater environments, as it significantly increases the amount of data recovered in a limited survey time.

This study, undertaken in March 2016, sought to investigate whether scaled high-resolution photographic transects could augment or replace the current in-situ measurement methodology. Sites were chosen to provide replicate topographic and habitat complexities and slope aspects, ranging from reef flats to vertical drop-offs. At each site, in-situ assessments and photogrammetric surveys were performed successively along a 10m transect (see top right). Following data collection, images were processed on a dedicated photogrammetric workstation to produce digital models of the surveyed transects (see bottom right) which are currently being used to quantify carbonate production.

The resulting models can be â&#x20AC;&#x2DC;divedâ&#x20AC;&#x2122;, and measurements taken at leisure. Investigation of community interactions on scales from sub-centimeter to meter are achievable. As dimensional and orientation data were collected during the survey process, additional confounding processes, such as slope effects, shading and vertical topography can be incorporated into analyses. From a logistical standpoint, actual survey time was reduced by up to two thirds compared with current in-situ assessment methods.

11 | Caribbean Coral Reef Ecosystems

Right, Above: Diver conducts photogrammetric survey Right, Below: Various corals (carbonate producers) are measured via photogrammetry

Cephalocarida

Martin Schwentner and Gonzalo Giribet The enigmatic Cephalocarida (Crustacea) have never been easily collected. Although they are globally distributed most of the twelve known species are reported from a single locality and from only a handful of specimens. Therefore the Carrie Bow Cay Field Station, located on a small Caribbean island off the coast of Belize, seemed a perfect choice for a collection campaign. Here the local cephalocarid species Lightiella incisa had been reported in relatively high abundances from one of the islandâ&#x20AC;&#x2122;s sand bars at a water depth of less than 30 cm. Apparently easy to access, easy to sample and all in reach of a fully equipped marine field station in the Caribbean. Perfect!

Cephalocarida are interesting and fascinating for a range of reasons. They were first discovered in 1955 and constitute one of the five main taxa of Crustacea. Due to a range of potentially ancestral morphological characteristics they were long thought to represent the most basal crustaceans. However, more recent molecular analyses suggest the opposite. They are potentially the sister taxon to all Hexapoda (we have known for a few years that Hexapods are in fact crustaceans) and thus closely related to insects. Relatively little is known about the biology of these tiny crustaceans. All species are found in organic rich marine sediments and their distribution is very patchy.

Sampling at Carrie Bow Cay was a good as imagined: Snorkeling in the shallow, warm and clear Caribbean waters with a diverse range of habitats. But there was a small problem. The sand bar from which the species had been reported has been washed away in a storm a few years ago. The same had happened to a large sandy beach on the neighboring island of South Water Cay, where Lightiella had also been collected. Therefore we collected sandy sediments from all types of suitable looking habitats at different depth. Finding sandy patches was no problem, but finding Cephalocarida was. The sediments featured a rich and very diverse meiofauna - including a wide range of Ostracoda, Copepoda, Oligochaeta, Polychaeta, Nematoda, Mollusca, Nemertea and many others - but for nearly four days we found no Cephalocarida. Late afternoon on the fourth day we found the first cephalocarid specimen of the sampling trip. And where did we collect it? Only ten meters from the lab door, in 30 cm water depth and about one meter behind the tidal zone, it was the most accessible place on the island. Once we knew where to collect, collecting more individuals was relatively simple and did not require much effort. But it also emphasized how patchy the distribution of Cephalocarida can be, as we had unsuccessfully sampled locations less than five meters on either side of the site.

In the end, collecting Cephalocarida was as exciting and easy as expected- right at your feet in front of the lab. But first you had to know exactly where to place your feet. Next time we will know where to look, at least if the island does not change again.

An example of the Cephalocarid species Lightiella incisa, collected at Carrie Bow Cay.

Caribbean Coral Reef Ecosystems | 14

Do predators affect how far herbivores venture from patch reefs?

Bart Difiore, Valerie Paul, Steve Box, Simon Queenborough, and Audrey Looby

Predators dramatically shape marine ecosystems by consuming prey and altering prey behavior. These changes in behavior, or risk effects, influence where fish graze and can cascade to lower trophic levels. Predator-prey behavioral interactions are particularly important in coral reef and seagrass ecosystems. Researchers in Shark Bay, Australia have shown that seagrass herbivores (sea turtles and dugong) concentrate grazing in lower risk environments in order to avoid tiger shark predators. Predators also change the location and amount of macroalgae grazing by critical reef herbivores, like parrotfish and surgeonfish. Therefore, fear of predators can alter basic ecosystem structure, like the balance of coral cover to macroalgae, or ecosystem services, like carbon sequestration by seagrasses.

Last summer, researchers with the Smithsonian Marine Station and Yale University used Carrie Bow Cay to examine how predators alter herbivory at coral patch reefs. In the waters of Belize, patch reefs are coral oases in lush, shallow seagrass plains, and act as refuges for herbivorous fish and urchins. Each patch reef is surrounded by a ring of sand, known as a grazing halo, formed by herbivores foraging close to the safety of the refuge. Using stationary video cameras, fish surveys, grazing assays, and other measures of reef characteristics, they explored how predator abundance and other factors impact herbivore foraging distance and the size of grazing halos.

Preliminary analysis of the grazing assays shows that grazing decreases with distance from the patch, and that grazing distance is correlated with halo size.

Not only does this research provide insight into basic ecological questions on predator-prey behavioral relationships, it may offer a unique technique to monitor predator populations. Grazing halos are readily visible in satellite imagery (see right). If foraging distance is inversely correlated with predator abundance, then changes in halo area could be used as an indirect indicator of local abundances of predator species, like reef sharks, barracuda, jacks, grouper, and large snapper. Using a time series of images taken over Carrie Bow Caye (2005, 2009, 2015), this study hopes to track changes in grazing halo size and see if these changes are related to historic shifts in fish community structure.

15 | Caribbean Coral Reef Ecosystems

A satellite image of inshore patch reefs near Carrie Bow Cay. Each circular patch reef is surrounded by a light-colored â&#x20AC;&#x153;grazing haloâ&#x20AC;? formed by herbivores.

Hybridization: the key to threatened coral species survival or the harbinger of extinction?

Nicole Fogarty, Ilina Baums, Hunter Noren, Morgan Hightshoe, Megan Bock, Alicia Vollmer, and Leah Harper

The once dominant staghorn coral (Acropora cervicornis) and the elkhorn coral (A. palmata) have decreased by more than 90% since the 1980s, primarily from disease. Their continuing decline jeopardizes the ability of coral reefs to provide numerous societal and ecological benefits. Despite their protection under the U.S. Endangered Species Act, threats to the survival of reef-building acroporid corals remain pervasive and include disease and warming ocean temperatures that may lead to further large-scale mortality. However, hybridization among these closely related acroporid species is increasing and may provide an avenue for adaptation to a changing environment. While hybrids were rare in the past, they are now thriving in shallow habitats with extreme temperatures and irradiance and are expanding into the parental species habitats. Additional evidence suggests that the hybrid is more disease resistant than at least one of the parental species. Hybridization may therefore have the potential to rescue the threatened parental species from extinction through the transfer of adapted genes via hybrids mating with both parental species, but extensive gene flow may alter the evolutionary trajectory of the parental species and drive one or both to extinction.

Dr. Fogarty and her graduate students from Nova Southeastern University in collaboration with Dr. Baumsâ&#x20AC;&#x2122; laboratory from Penn State University are examining the likelihood of these potential outcomes. Highlights from their work include the identification of F2 hybrids and A. palmata backcross (formed when A. palmata mates with hybrids). Morphological analysis showed that at both gross and fine scales F2 hybrids and A. palmata backcross are morphologically similar to F1 hybrids. The ability for hybrids to tolerate thermal stress during the earliest life history stages depends upon the direction of the cross. Those crosses between species with A. cervicornis eggs do worse than the reciprocal. Although the number of hybrid genets that showed signs of disease did not differ from the parental species, the location of disease transmission did. Hybrids are less likely to get disease in the shallow, warm hybrid zone than the parental species. This collaborative project will collect genetic and ecological data in order to understand the mechanisms underlying increasing hybrid abundance. The knowledge gained from this research will help facilitate more strategic management of coral populations under current and emerging threats to their survival.

Members of the Fogarty Lab, from L to R: Hunter Noren, Morgan Hightshoe, Megan Bock, and Nicole Fogarty

Caribbean Coral Reef Ecosystems | 18

Phenotypic plasticity in reef-building corals Jay Dimond

All species on the planet show variation, whether you are talking about people, trees, bacteria, or corals. Some variation you can see with your own eyes, like color or shape, while some of it may be less readily obvious, like disease resistance or the ability to tolerate different temperatures. Some of this variation has a genetic basis, meaning that certain genes are either present or absent, but some is the result of how genes are used, or expressed. Variation in gene expression ultimately leads to phenotypic plasticity, which is a means for organisms to adjust to new environments, or to changes in their existing environment.

For my PhD work at the University of Washington, I am studying phenotypic plasticity in reef-building corals. I focus my work on corals in the genus Porites, which are fairly common in a variety of habitats. Corals are great models for studying phenotypic plasticity because a single individual can be divided into two or more pieces, creating genetically identical fragments that can be moved to different environments and assessed for phenotypic change.

Corals cannot move themselves to a more favorable location if conditions change, so the are especially reliant on phenotypic plasticity.

I am interested in whether the relatively new field of epigenetics can help uncover the basis of phenotypic plasticity in corals. Epigenetics deals with additional information that is layered on top of DNA. I am specifically interested in DNA methylation, an epigenetic mark that influences how that DNA is expressed. Interestingly, DNA methylation can be influenced by the environment, making it a good candidate for involvement in phenotypic plasticity.

I have collected corals from a variety of habitats to assess their phenotypic and epigenetic variation, and to see if these are related. I have also fragmented some of these corals, leaving half the coral in its original habitat while bringing the other half to a new environment. After about a year, I will return to these sites to assess the phenotypic and epigenetic change of the fragments. Iâ&#x20AC;&#x2122;ll be looking at levels of DNA methylation in addition to things like growth, color, and the size and shape of the individual coral polyps.

Aside from simply being convenient research models, corals are also under threat around the world for numerous reasons, so much of this research is driven by an interest in how corals cope with these threats. The current intensity and pace of environmental change makes phenotypic plasticity especially important for the persistence of corals, as well as many other species.

Common shallow-water coral Porites porites in the waters near Carrie Bow Cay. 19 | Caribbean Coral Reef Ecosystems

Testing the sponge-loop for Caribbean reefs

Joseph Pawlik, Steve McMurray, Amber Stubler, and Lindsay Deignan

A new concept called the â&#x20AC;&#x153;sponge-loop hypothesisâ&#x20AC;? proposes that sponges are important cyclers of carbon on coral reefs, feeding on dissolved compounds exuded by seaweeds and returning cellular debris to particle feeders on the reef. The sponge-loop was tested by sampling seawater from the outside (incurrent) and inside (excurrent) surfaces of vase, tube and barrel sponge species while using a sophisticated device to measure flow through the sponge (acoustic doppler velocimeter).

Chemical analyses of water samples will reveal the extent to which sponges feed on dissolved compounds, and the degree to which they produce cellular debris. The sponge-loop may help to explain why Caribbean coral reefs have been less resilient than reefs elsewhere.

This tube sponge is one species studied by the authors at Carrie Bow Cay.

21 | Caribbean Coral Reef Ecosystems

Connectivity and gene expression analysis of Montastraea cavernosa Michael Studivan, Joshua Voss, and Amanda Alker PhD candidate Michael Studivan and lab technician Amanda Alker from the Voss Lab at FAU Harbor Branch returned to Carrie Bow in March 2016 to continue a coral monitoring project begun in March 2014. The first objective was to relocate mapped reef sites and 45 tagged shallow corals. The three sites named Raphâ&#x20AC;&#x2122;s Wall, South Reef, and Tobacco Caye each have shallow (55 ft) and mesophotic (130 ft) depth zones. The first dives at each site were spent exploring the shallow reef crest and deep walls to redeploy new light and temperature data loggers.

The shallow Montastraea cavernosa colonies were then located, despite high algal overgrowth on the cattle tags.

The team located all but one of the original colonies, the majority of which showed a healthy appearance and colony growth, with a few cases of algal overgrowth and bleaching.

The next steps were to resample the shallow corals and scout mesophotic depths for deep conspecifics. These sites are typical of mesophotic reef habitats in the Caribbean, where the shallow reef crest falls off to a vertical wall.

Light levels deeper than 100 feet are greatly diminished, causing relatively low coral growth compared to shallower reefs. Most deep colonies were much smaller than the shallow conspecifics and were found in plating and encrusting morphologies rather than the usual mounding growth form. However, there was a diverse array of color morphotypes including red fluorescence. These brightly colored individuals are suspected to benefit from nitrogen fixation and additional light absorption due to bacterial symbionts.

Over eighteen dives, 90 samples were collected from shallow (n=45) and mesophotic (n=45) depths. The data generated from this project will be used to compare genetic connectivity and gene expression across depths and reefs in the Gulf of Mexico and Caribbean for Michaelâ&#x20AC;&#x2122;s dissertation research. The data collected from the loggers will allow comparisons among gene expression trends to environmental conditions.

Additionally, this will be the first temporal study examining basal gene expression profiles of shallow corals in the Caribbean, and is expected to uncover the genetic mechanisms behind coral adaptation to depth.

The author descending to mesophotic reef habitat.

Genetic connectivity in the sea cucumber Isostichopus badionotus Giomar Helena Borrero-Perez and Harilaos Lessios

A juvenile sea cucmber, Isostichopus badionotus, found near Carrie Bow Cay.

To examine connectivity in populations of the sea cucumber Isostichopus badionotus, the authors collected samples along its entire geographical range of distribution, which currently includes all the Atlantic Ocean (Gulf of Guinee, Cape Verde Islands, Ascension Island, Gulf of Mexico, Caribbean Sea and South Atlantic). The Mesoamerican Barrier Reef System is a significant area of biodiversity concentration, harboring important populations of I. badionotus. Therefore, understanding patterns of connectivity in this region could be of particular relevance for management and conservation.

Sampling was conducted in June 2016, through the facilities of the Carrie Bow Cay Field Station. However, only a few specimens of I. badionotus were located, and more individuals in this area will be needed for accurate analysis. During samplings all the sea cucumbers species belonging to the order Aspidochirotida and previously reported in Carrie Bow Cay (nine species) were observed, plus Holothuria (Semperothuria) surinamensis, a previously unreported species.

Collection of I. badionotus specimens is made by snorkeling or SCUBA, and in most cases photos in situ of each specimen are taken and a tissue sample of body wall is removed and preserved in absolute ethanol. Each sample is processed in order to get DNA information (mt COI gene and nuclear microsatellites), which allows examination of the historic and recent genetic connectivity of the populations. Early results of this project showed that what is considered I. badionotus, actually includes more than one species. In order to define the taxonomic status of them, some complete specimens are collected for morphological revision including external characteristics (color patterns, size and organization of the dorsal papillae) and skin ossicles (using light microscopy and scanning electron microscopy).

Sea cucumbers and particularly I. badionotus have gained considerable economic interest due to fisheries for trepang (a market term for sea cucumber). Efforts are underway to characterize natural populations and to farm it in aquaculture ponds. Correct knowledge of the species involved and information on the degree of genetic connectivity, are essential data for the success of these efforts and the management and conservation of the species.

23 | Caribbean Coral Reef Ecosystems

Chemical cues in habitat selection Danielle Dixson, Rohan Brooker, and Molly Ashur 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 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 coral reef peppermint cleaner shrimp utilizes chemical cues to distinguish between different sponge habitats, selecting the preferred habitat based on chemical cues alone (led by Molly Ashur). Coral reef fishes of various species use chemical cues in locating reefs, and the importance of chemical cues produced by mangroves was identified (led by Rohan Brooker). Free-swimming coral larvae also use chemical signals to identify reef habitat and can distinguish between different benthic components indicative of reef quality through chemical cues alone (led by Danielle Dixson, Jennifer Sneed and Valerie Paul). While each individual project has identified specific components, the overall findings indicate the significance of sensory signals in marine systems.

Additionally, research conducted highlights the importance of incorporating animal behavior into studies focused on marine connectivity.

A peppermint cleaner shrimp receives a harmless elastomer tag used to track habitat preferences near Carrie Bow Cay.

A 15-year retrospective survey of fishery species in the SWCMR Charles Acosta, Marisa Derenzo, Alyssa Frank, Anna Snowball, Rachel Prokopius, and Kris Howard

The authors conduct spiny lobster surveys on patch reefs in the SWCMR near Carrie Bow Cay.

No-take conservation areas in marine reserves are now widely considered essential to fisheries management.

This is a stated purpose of the official management plan of the South Water Cay Marine Reserve (SWCMR).

However, the effectiveness of any given conservation area for sustaining and enhancing fisheries is influenced by many factors, such as habitat area and quality, recruitment dynamics, and practical enforcement of conservation zones. In 2016, we conducted a beforeafter control-impact (BACI) study of the same sites initially surveyed in 2001 in the SWCMR, as well as in the Glover’s Reef Marine Reserve (GRMR). Both marine reserves were designated in 1996, but management plans and enforcement were only implemented several years later (2008 for SWCMR and 2004 for GRMR).

The “before-after” component was our surveys in 2001 and again in 2016, whereas the “control-impact” component was the conservation zone (no-take area) versus the general use zone (fishing area).

We conducted surveys of essential habitats at the same sites for spiny lobsters, queen conch, and target finfish species (Nassau grouper, mutton snapper, hogfish, queen triggerfish). We also recorded habitat composition and quality along video transects to compare to original transect data from 2001. Preliminary analysis of our 15-year retrospective surveys indicates that little or no changes have occurred in these populations at SWCMR. This may be due to lack of essential habitat in the conservation zone for some species; for example, sparse patch reefs for spiny lobsters and groupers. This may also be due to continued intense fishing pressure in the general use zone and poaching in the conservation zone.

We also studied sea cucumber species that became a target of commercial fishing in Belize in 2015. Our markrecapture and tracking data shows that sea cucumbers are patchily distributed at low densities that may not be resilient to commercial fishing pressure. Monitoring and experimental data are crucial to fisheries management to determine the relative effectiveness of conservation zones. Only through these means will managers be able to assess whether a marine reserve contributes to sustainable fisheries or whether changes in design are warranted.

25 |Caribbean Coral Reef Ecosystems

The evolution of bioluminescence in ostracods Emily Ellis, Nicholai Hensley, and Trevor Rivers The patch reefs surrounding Carrie Bow Cay are home to many species of bioluminescent ostracod. Males display species-specific luminous courtship, and females intercept males to mate. The scientists collected various species (five new to science) and preserved them for genetic study. One experiment studied the biochemical differences between species, and another studied the femalesâ&#x20AC;&#x2122; response to simulated bioluminescence.

Carrie Bow Cay ostracods collected in trap.

How does the long spined sea urchin affect algae on coral reefs?

Lindsay Spiers, Tom Frazer, and Chuck Jacoby In 1983 the long spined sea urchin Diadema antillarum experienced a massive Caribbean wide mortality event that killed between 90-99% of all Diadema. Before this, Diadema were considered the herbivore primarily responsible for controlling algae. The die off combined with overfishing allowed algal abundance on many reefs to increase, contributing to the decline of these reefs.

In the past decade, Diadema populations have started to increase in many places, which prompted the question of how the return of Diadema might affect algae on coral reefs. To look at this question, two different types of experiments were conducted in Belize: feeding experiments and caging experiments. From the feeding experiments it is apparent that Diadema The sea urchin, Diadema antillarum. have a preference for certain types of algae. They avoid tough leathery algae like Turbinaria, but consume algae like Dictyota even though they produce compounds designed to keep organisms from eating them. Additionally a long term caging experiment was set up to see the difference in the abundance and type of algae in three types of plots. Some plots allow both fish and urchins in, others only allow fish in, and the third exclude all herbivores. After seven weeks, plots that excluded all herbivores were 50% covered in algae, plots that allowed only fish were 21% covered algae, and plots that allowed both fish and urchins were covered in 25% algae. After 12 weeks there was even more algae in the plots that exclude all herbivores while the amount of algae in the other types of cages stayed approximately the same. This indicates that on these patch reefs in Belize, fish alone or fish and urchins together may be capable of keeping algae at a steady level. Between these feeding experiments, current cages, and cages to be deployed soon it may be possible to predict how coral reefs may change in the future as urchin and fish abundances change. As the abundance and type of algae change so do the abundance of other important organisms such as corals and sponges.

27 | Caribbean Coral Reef Ecosystems

CCRE South Water Caye Marine Reserve reef assessment program Scott Jones, Zach Foltz, Randi Rotjan, Sean Marden, Jay Dimond, Sam Herman This year marks the sixth year that staff from the Caribbean Coral Reef Ecosystems program (CCRE) and collaborators from the New England Aquarium have implemented 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 264 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 newly formed SWCMR no-take area.

Over the course of the project, researchers have documented alarming declines in local populations of groupers and snappers, as well as an unusual winter coral bleaching event in 2015.

Time will tell if the marine reserve has any influence on the recovery rates of these fish and coral populations, or on reef resilience and recovery overall.

A diver surveys corals on a permanent transect.

CARICOMP 2016 Karen Koltes and John Tschirky Monitoring of physical and biological variables under the Caribbean Coastal Marine Productivity (CARICOMP) program continued at Carrie Bow Cay (CBC) in 2016. The CARICOMP Program is a long-term, Caribbean-wide initiative to determine the dominant influences on coastal productivity, to monitor for ecosystem change and, ultimately, to discriminate human disturbance from long-term natural variation in coastal systems over the range of their distribution. Continuously monitored physical variables at CBC include air and water temperature, water transparency (measured by Secchi disk), salinity, and rainfall. Ecological variables include seagrass productivity (biomass and growth) and coral reef community structure based on repeated sampling of 10 permanent transects established in 1993 at a depth of about 13 m on the forereef.

The 20+ year record of repeated measurements at Carrie Bow Cay likely represents the longest continuous record of in situ environmental data for the Meso-American Barrier Reef and one of the longest in the CARICOMP network that was established in 1992 with 23 research institutions/laboratories in 19 Caribbean countries and territories. In combination with other CARICOMP sites, it allows for investigation of the extent of global and local changes in coastal habitats in the Caribbean Basin. To quantify the extent of these changes over the past two decades, we collaborated with other CARICOMP scientists to analyze water quality/transparency (measured by Secchi disk) and temperature trends using data from CARICOMP sites that had collected at least 3 years of data.

Trend analyses showed that water transparency decreased at 42% of the sites, including Carrie Bow Cay, indicating that local-scale chronic stressors are widespread. The analyses also indicated that decreases in water quality are linked to increased human density; however, the effect is modulated by environmental factors, with areas that are getting drier and/or characterized by vigorous water movement showing a smaller loss of water quality. On the other hand, only 18% of the stations showed an increase in water temperature that would be expected from rising global temperatures. This may result from the timeframe of 3 - 20 years being insufficient to provide enough statistical power to assess longterm changes in temperature because the magnitude of the trend is small, the memory (i.e. temporal autocorrelation) is high, or the temperature is especially variable. The paper resulting from this network-wide collaboration has been submitted for publication in Marine Pollution Bulletin.

29 | Caribbean Coral Reef Ecosystems

The author conducts a reef survey near Carrie Bow Cay.

Fiscal Year 2016 Scientific Publications Open access articles are indicated with clickable link Capper, A., A. A. Erickson, R. Ritson-Williams, M. A. Becerro, K. A. Arthur, and V. J. Paul. 2016. Palatability and chemical defenses of benthic cyanobacteria to a suite of herbivores. Journal of Experimental Marine Biology and Ecology 474: 100 – 108.

Duffy, J.E., S.L. Ziegler, J.E. Campbell, P.M. Bippus, J.S. Lefcheck. 2015. Squidpops: A simple tool to crowdsource a global map of marine predation intensity. PLoS ONE 10(11): e0142994. link DeBose, J. L., R. P. Kiene and V.J. Paul. 2015. Eggs and larvae of Acropora palmata and larvae of Porites astreoides contain high amounts of dimethylsulfoniopropionate. Journal of Experimental Marine Biology and Ecology 473: 146 – 151.

Franklin, A., N.J. Marshall, S. M. Lewis. 2016. Multimodal signals: ultraviolet reflectance and chemical cues in stomatopod agonistic encounters. Royal Society Open Science 3: 160329. link Leisch, N., N. Pende, P. M. Weber, H. R. Gruber-Vodicka, J. Verheul, N. O. E. Vischer, S. S. Abby, B. Geier, T. den Blaauwen, and S. Bulgheresi. 2016. Asynchronous division by non-ring FtsZ in the gammaproteobacterial symbiont of Robbea hypermnestra. Nature Microbiology 16182.

Maldonado, M., R. Aguilar, R. Bannister, J. Bell, J. Conway, P. Dayton, C. Diaz, J. Gutt, M. Kelly, E. Kenchington, S. Leys, S. Pomponi, H. Tore Rapp,K. Rützler, O. Tendal, J. Vacelet, Jean and C. Young. 2016. Sponge grounds as key marine habitats: A synthetic review of types, structure, functional roles, and conservation concerns. In: Rossi, Sergio, Bramanti, Lorenzo, Gori, Andrea and Saco del Valle, Covadonga Orejas, Marine Animal Forests: The Ecology of Benthic Biodiversity Hotspots. Berlin: Springer International Publishing, pp.1-31.

Meyer,J.L., S.P. Gunasekera, R.M. Scott, V.J. Paul, and M. Teplitski. 2016. Microbiome shifts and the inhibition of quorum sensing by black band disease cyanobacteria. ISMEJ. 10, 1204–1216. doi:10.1038/ismej.2015.184 Meyer, J.L., J. M. Rodgers, B. A. Dillard, V.J. Paul, M. Teplitski. 2016. Epimicrobiota associated with the decay and recovery of Orbicella corals exhibiting dark spot syndrome. Frontiers in Microbiology 7: 893. link Montanaro, J., D. Gruber, N. Leisch. 2016. Improved ultrastructure of marine invertebrates using non-toxic buffers. PeerJ 4:e1860 link Olsen K., J.M. Sneed, V.J. Paul. 2016. Differential larval settlement responses of Porites astreoides and Acropora palmata in the presence of the green alga Halimeda opuntia. Coral Reefs 35(2): 521-525.

Caribbean Coral Reef Ecosystems | 30

2016 Scientific Publications Palacios Theil, E., J. A. Cuesta, D.L. Felder. 2016. Molecular evidence for non-monophyly of the pinnotheroid crabs (Crustacea : Brachyura : Pinnotheroidea), warranting taxonomic reappraisal. Invertebrate Systematics 30, 1-27.

Robles, R. and D. L. Felder. 2015. Molecular phylogeny of the genus Lepidophthalmus (Decapoda, Callianassidae), with re-examination of its species composition. Zootaxa 4020 (3): 453–472. link Sneed, J.M., R. Ritson-Williams, V.J. Paul. 2015. Crustose coralline algal species host distinct bacterial assemblages on their surfaces. The ISME Journal 9: 2527-2536. link Zeidler, W., W. E. Browne. 2015. A new Glossocephalus (Crustacea: Amphipoda: Hyperiidea: Oxycephalidae) from deepwater in the Monterey Bay region, California, USA, with an overview of the genus. Zootaxa 4027 (3): 408–424. link Zimmermann, J., Wentrup, C., Sadowski, M., Blazejak, A., Gruber-Vodicka, H. R., Kleiner, M., Ott, J. A., Cronholm, B., De Wit, P., Erséus, C. and Dubilier, N. 2016. Closely coupled evolutionary history of ecto- and endosymbionts from two distantly related animal phyla. Molecular Ecology, 25: 3203–3223. link

31|Caribbean Coral Reef Ecosystems

2016 Participants * served as station manager Acosta, Charles, Northern Kentucky University, Newport, KY Alanko, Jerry, Tilghman, MD* Alanko, Sandy, Tilghman, MD* Alker, Amanda, Harbor Branch Oceanographic Institute, Florida Atlantic University, Fort Pierce, FL Ashur, Molly, University of Delaware, Newark, DE Baums, Iliana, Penn State University, University Park, PA Beers, Scott, Smithsonian Environmental Research Center, Edgewater, MD* Bennett, Sue, Smithsonian Marine Station, Fort Pierce, FL Bock, Megan, Nova Southeastern University, Dania Beach, FL Bohnsack, Karen, Florida Department of Environmental Protection, Fort Lauderdale, FL Borrero, Giomar, Smithsonian Tropical Research Institue, Panama City, Panama Brandl, Simon, Smithsonian Environmental Research Center, Edgewater, MD Brooker, Rohan, University of Delaware, Newark, DE Bulgheresi, Sylvia, University of Vienna, Austria Cardini, Ulisse, University of Vienna, Austria Carpenter, Mike, Ellijay, GA* Casey, Jordan, James Cook University, Australia Campbell, Justin, Smithsonian Marine Station, Fort Pierce, FL Canty, Steven, Smithsonian Marine Station, Fort Pierce, FL Clark, Abigail, University of Florida, Gainesville, FL Cody, Clyde, Boise, ID Cody, Liz, Boise, ID Deignan, Lindsey, University of North Carolina at Wilmington, NC Derenzo, Marisa, Northern Kentucky University, Newport, KY DiFiore, Bart, Yale University, New Haven, CT Dimond, Jay, Shannon Point Marine Center, Western Washington University, Anacortes, WA Dixson, Danielle, University of Delaware, Newark, DE Dramer, Greg, Kalispell, MT* Dramer, Joann, Kalispell, MT* Ellis, Emily, University of California, Santa Barbara, CA Felder, Darryl, University of Lousiana at Lafayette, LA Felder, Jennifer, University of Lousiana at Lafayette, LA Feller, Candy, Smithsonian Environmental Research Center, Edgewater, MD Fieseler, Clare, University of North Carolina at Chapel Hill, Chapel Hill, NC Foltz, Zachary, Smithsonian Marine Station, Fort Pierce, FL Fogarty, Nicole, Nova Southeastern University, Dania Beach, FL Caribbean Coral Reef Ecosystems | 32

2016 Participants Frank, Alyssa, Northern Kentucky University, Newport, KY Geyer, Laura, Smithsonian Tropical Research Institue, Panama City, Panama Giribet, Gonzalo, Harvard University Museum of Comparative Zoology, Cambridge, MA Gouge, Daniel, Williston, FL* Haren, Nick, Anacortes, WA* Haren, Marylin, Anacortes, WA* Harper, Leah, Nova Southeastern University, Dania Beach, FL Hensley, Niko, University of California, Santa Barbara, CA Herman, Sam, New England Aquarium, Boston, MA Hightshoe, Morgan, Nova Southeastern University, Dania Beach, FL Hiller, Alexandra, Smithsonian Tropical Research Institue, Panama City, Panama Horning, Reginald, Traverse City, MI* Howard, Kristafer, Northern Kentucky University, Newport, KY Jaekle, Oliver, Max Planck Institute for Marine Microbiology, Bremen, Germany James, Edwin, Tilgman, MD* James, Bonnie, Tilgman, MD* Janiak, Dean, Smithsonian Marine Station, Fort Pierce, FL Jensen, Paul, Scripps Institution of Oceanography, La Jolla, CA Johnston, Cora, University of Maryland, College Park, MD Jones, Scott, Smithsonian Marine Station, Fort Pierce, FL Koltes, Karen, U.S. Department of the Interior, Washington, D.C. Kowalewski, Michal, Florida Museum of Natural History, Gainesville, FL Leisch, Nikolaus, University of Vienna, Austria Looby, Audrey, Smithsonian Marine Station, Fort Pierce, FL Marden, Sean, New England Aquarium, Boston, MA McMurray, Steven, University of North Carolina at Wilmington, NC Mogg, Andrew, Scottish Association for Marine Science, Oban, Argyll, Scotland Moore, Joel & Linda, Shingle Springs, CA* Mullins, Charlie, Pearisburg, VA* Noren, Hunter, Nova Southeastern University, Dania Beach, FL Opishinski, Tom, Interactive Oceanographics, East Greenwich, RI Paredes, Gabriella, University of Vienna, Austria Parsons, Keith, Atlanta, GA* Paul, Valerie, Smithsonian Marine Station, Fort Pierce, FL Patin, Nastassia, Scripps Institute of Oceanography, La Jolla, CA Pawlik, Joseph, University of North Carolina at Wilmington, NC Pende, Nika, University of Vienna, Austria Peresta, Gary, Smithsonian Environmental Research Center, Edgewater, MD* 33 |Caribbean Coral Reef Ecosystems

Prokopius, Rachel, Northern Kentucky University, Newport, KY Rivera, Nelson, Smithsonian Marine Station, Fort Pierce, FL Rivers, Trevor, University of California, Santa Barbara, CA Sayer, Martin, Scottish Association for Marine Science, Oban, Argyll, Scotland Scheff, George, Boise, ID* Schile, Lisa, Smithsonian Environmental Research Center, Edgewater, MD* Schwentner, Martin, Harvard University Museum of Comparative Zoology, Cambridge, MA Seemann, Janina, Smithsonian Tropical Research Institute, Panama Sheehy, Sandy, Albuquerque, NM Sherwood, Craig, Deale, MD* Simpson, Loraeâ&#x20AC;&#x2122;, Smithsonian Environmental Research Center, Edgewater, MD Sneed, Jennifer, Smithsonian Marine Station, Fort Pierce, FL Snowball, Anna, Northern Kentucky University, Newport, KY Spadaro, Angelo, Old Dominion University, Norfolk, VA Spiers, Lindsay, Univeristy of Florida, Gainesville, FL Stubler, Amber, University of North Carolina at Wilmington, NC Studivan, Michael, Harbor Branch Oceanographic Institute, Florida Atlantic University, Fort Pierce, FL Thacker, Cheryl, University of Florida, Gainesville, FL* Toscano, Maggie, Smithsonian Environmental Research Center, Edgewater, MD Truelove, Nathan, Smithsonian Marine Station, Fort Pierce, FL Tschirky, John, American Bird Conservancy, Washington, D.C. Walczak, Joanna, Florida Department of Environmental Protection, Fort Lauderdale, FL Weber, Phillip, University of Vienna, Austria Whippo, Ross, Smithsonian Tennenbaum Marine Observatories Network, Washington, D.C. Wulff, Janie, Florida State University, Tallahassee, FL

Caribbean Coral Reef Ecosystems | 34

Acknowledgements

Our research is hosted by the Belize Fisheries Department and we thank Ms. Beverly Wade and Mr. James Azueta 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, Mike Carpenter, Liz & Clyde Cody, Greg & Joann Dramer, Daniel Gouge, Nicky & Marilyn Haren, Reg Horning, Ed & Bonnie James, Joel & Linda Moore, Charlie Mullins, 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. Many thanks to Laura Diederick for her editorial eye, sharing her expertise in science communication, and lending valuable advice.

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, Marty Joynt, 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.

35 |Caribbean Coral Reef Ecosystems

Photo Credits

Cover: Zach Foltz page 1: Zach Foltz; page 4: (top to bottom) Abby Wood, Zach Foltz, Zach Foltz; page 5: Zach Foltz; page 8: Simon Brandl & Jordan Casey; page 9: Alexandra Hiller; page 12: Martin Sayer & Andew Mogg; page 13: M. Schwentner & G. Giribet; page 16: Digital Globe Foundation; page 17: Zach Foltz; page 20: Scott Jones; page 21: Joseph Pawlik; page 22: Michael Studivan; page 23: Giomar Borrero; page 24: Zach Foltz; page 25: Charles Acosta; page 26: Emily Ellis; page 27: Scott Jones; page 28: Zach Foltz; page 29: Karen Koltes; page 36: John Brown; Back cover: John Brown

Caribbean Coral Reef Ecosystems | 36

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