2015 CCRE Annual Report

Smithsonian Institution

2015 CCRE Annual Report Caribbean Coral Reef Ecosystems • National Museum of Natural History

CCRE 2015

2015 was yet another busy and productive year for the CCRE program. Carrie Bow Cay hosted over 80 individual scientific visitors that contributed to more than 1000 research days in the field. The station hosted the second annual field campaign for the Tennenbaum Marine Observatory Network (TMON), which collected baseline data at important marine habitats around the station (see page 12). Additionally, MarineGEO scientists installed a permanent instrument platform that will collect vital long-term sea level data well into the future (see page 31). 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.

Table of Contents 4 Carrie Bow Cay Field Station 5 Research Highlights 21 Research Briefs 32 Scientific Publications 34 Visitors and Station Managers 37 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 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

Smithsonian researcher Justin Campbell calibrating sensors in an ocean acidification experiment at Carrie Bow Cay.

Coral Larval Ecology

Jennifer Sneed, Justin Campbell, Lane Johnston, and Valerie Paul

Modern and future coral reefs face an unprecedented combination of biotic and abiotic threats. Given limited resources, managers are faced with the difficulty of developing management strategies that most effectively address these environmental stressors. 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 ocean also increases, causing a decrease in the pH of water. 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.

We set out to gain a better understanding of 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. This summer we focused on the potential impacts of algal overgrowth and ocean acidification on the settlement behavior of the spawning elkhorn coral, Acropora palmata. We exposed pieces of crustose coralline algae (CCA) to the brown alga Stypopodium zonale and conditioned them in seawater at either present day pH (8.0) or future pH (7.8) for 5 days. We added A. palmata larvae to all of the treatments and allowed them the opportunity to settle on the CCA for three days. Neither the presence of S. zonale, nor changes in the seawater pH had any effect on the settlement behavior of A. palmata. This is contrary to our previous results with the brooding coral Porites astreoides. For P. astreoides, larval settlement significantly decreased in the presence of S. zonale under low pH conditions. However, without algae, settlement increased under low pH conditions for this brooding coral. These results demonstrate that for some corals the combination of stressors can have different implications than individual stressors on their own and that different corals will likely respond differently in the face of current and future threats. Continuing to investigate these complex interactions is critical to understanding how these stressors are likely to impact coral reefs today and in the future.

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Examinging microbial communities and coral diseases

Max Teplitski, Julie Meyer, Valerie Paul

Corals are holobionts- complex multi-partite organisms that consist of the invertebrate animal host, dinoflagellate endosymbionts, and microbial communities associated with them. Coral-associated microbes play important roles in the health of the holobiont and contribute to nutrient acquisition. Displacement of the beneficial members of coral microbial communities with microbes from the environment or with minor members of the normal community have been linked with the appearance of coral disease signs. The focus of our work is the Black Band Disease (BBD) of boulder and brain corals. BBD was the first reported coral disease and it was first described from Carrie Bow Cay. It is thought to be the most widely distributed disease of corals, affecting at least 40 species worldwide. The disease is recognized by the appearance of a dense, very dark-purple (black) mat that is the visible accumulation of filamentous cyanobacteria. BBD migrates across the surface of the coral at a rate of up to one cm per day, leaving behind bare coral skeleton. BBD spikes in warmer, sunnier months, and once a BBD outbreak takes place within a given ecosystem, it tends to re-occur each year.

Individual coral colonies in which BBD has halted are 3.5 times more likely to develop signs of the disease in subsequent years. Analyses of the within-ecosystem, spatio-temporal patterns of appearance of BBD point to various models, including transmission by water currents, stochastic appearance of lesions, and direct colony-to-colony transmission.

Meta-analysis of published studies of BBD microbial communities revealed that the same cyanobacterium (now classified as Roseofilum reptotaenium) was detected in over 70% of the samples, indicating that this organism is critical for the appearance or progression of BBD. There are several notable uncertainties, however. The composition of BBD has not been unambiguously determined. It is not clear to what extent the microbial community associated with BBD differs from that of the healthy corals. Microbe-microbe interactions within BBD remain only partially understood. Therefore, with this study we focused on differences in the composition of microbial communities of healthy corals and those afflicted with BBD. To better understand interactions within BBD, we characterized secondary metabolites from the mat.

We found distinct bacterial communities in the surface microbial communities of healthy corals, in seawater, and in the BBD consortia. Microbial communities of healthy corals were remarkably conserved; they were also less diverse than the microbial communities found in the seawater or in the BBD. Interestingly, healthy microbial communities from Orbicella annularis, Montastrea cavernosa and O. faveolata tested in Belize and in the Florida Keys were very closely related, suggesting that the composition of healthy coral microbial communities is conserved. Importantly, all samples (including those collected from depths ranging from ~12 to 21 meters, where BBD is not known to occur) contained R. reptotaenium, the cyanobacterium associated with BBD. Up to 0.3% of sequencing reads from healthy corals were identified as Roseofilum. These observations clearly establish that healthy coral communities are stable across temporal and spatial gradients. Furthermore, these observations support the hypothesis that R. reptotaenium is a normal, albeit minor, member of the coral microbiota, even at depths where BBD does not occur.

As the black band layer migrates across the surface of infected corals, Roseofilum and its associated heterotrophic bacte7 |Caribbean Coral Reef Ecosystems

Author Max Teplitski samples microbial communities from diseased coral near Carrie Bow Cay.

ria continually invade the adjacent healthy surface mucus layer. Our deep sequencing results show that Roseofilum and other members of the polymicrobial disease consortia are present at low levels in healthy tissues and uninfected corals and that 63% of genera were shared between the two sample types. Together, this suggests that interactions between healthy microbiota and BBD consortia members may ultimately determine the overall health of the coral host.

To better understand interactions within the BBD consortium, secondary metabolites present within the extracts of the BBD mats were purified. Lyngbic acid was identified as one of the major secondary metabolites in BBD extracts. Subsequent experiments established that lyngbic acid plays an important role in inhibiting cell-to-cell signaling in Vibrios, which are normal members of coral microbial communities, that tend to get displaced by Roseofilum as the BBD progresses.

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Black Band Disease (BBD) can progress across a colony at a rapid rate. A colony of boulder star coral with BBD (top), photographed 8 months later (bottom).

Comprehensive assessments of habitats like seagrasses are a core component of the MarineGEO sampling strategy.

MarineGEO Field Campaign

Ross Whippo, Scott Jones, Justin Campbell, Valerie Paul, Emmett Duffy Carrie Bow Cay Field Station has been an important research site for over 40 years and continues to be a part of new directions in marine science for the Smithsonian. Researchers from Fort Pierce, Panama, and Washington converged at the station this fall for a two-week field campaign as a part of the Smithsonian’s Tennenbaum Marine Observatory Network and Marine Global Earth Observatory (MarineGEO). MarineGEO is the first and only worldwide network to examine marine biodiversity in coastal waters and measure the ways it may be changing, as well as to identify the drivers of that change. This is accomplished by assessing key biological parameters that indicate the health of different habitats, such as coral reefs, mangroves, and seagrass beds. Working out the methods that MarineGEO will replicate on a global scale is a formidable challenge. Experiments must be simple, inexpensive, and use materials that can be found or shipped anywhere in the world. Chief among these challenges is finding an efficient way to assess herbivory by marine fishes. Ecologically speaking, this simple process can have profound effects on the whole biological community. Grazing intensity plays a vital role in maintaining healthy and resilient coral reefs by limiting fastergrowing algae and giving corals space to compete. Corals, in turn, provide structure and habitat for hundreds of species of fish and invertebrates. In their effort to find a standardized feeding assay, experienced marine ecologists Dr. Emmett Duffy and Dr. Valerie Paul settled on a method akin to offering fish a “smorgasbord� of algae that have different levels of palatability. Algal defenses can be both chemical and physical, and researchers chose examples of each. The feeding assays were deployed in different habitats and checked after one hour and again after 24 hours. Preliminary findings suggest the method worked well, and elucidated interesting patterns within each habitat. Future deployments in new environments will determine if algal smorgasbords will go global.

An array of algae is used to assess grazing activity near Carrie Bow Cay.

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Hydroid Diversity in Belize

Allen Collins and Antonio Marques

The following is an excerpt from Dr. Allen Collins’ post to the NMNH Invertebrate Zoology blog, “No Bones,” written during his trip to Carrie Bow in the fall of 2014: Here we are at Carrie Bow Cay, a somewhat remote and really wonderful marine field station operated by the Smithsonian Marine Station (SMS) at Fort Pierce, Florida. We are two fortunate scientists, one Brazilian and one from the USA, who share a love for tiny animals known as hydroids, which are relatives of the generally much larger anemones and corals.

We have now spent a few days studying the biodiversity (basically hunting for, identifying and documenting) of animals that we find fascinating. As scientists, we are aware of the papers that have been written earlier on topics that are relevant to our interests. Charles Darwin, in 1842, called this region “the most remarkable reef in the West Indies”. For hydroids, besides scattered and somewhat imprecise records in old literature, there have been just two papers written about the hydroids of Belize, one by an American researcher in 1982 and one by a Canadian in 1991. It has been 172 years since Darwin visited, and at least 23 years after the Canadian Dale Calder published his report on the hydroids near Carrie Bow. Since then, no other scientists have published any new findings. The marin environments in this region provide food, income from tourism as well as pride and joy for Belizeans. Hydroids are ubiquitous and integral players in these environments here and in many others around the world, and yet it is just a handful of scientists who study them.

We know that part of our collections will reside in Belize for potential study, and those that make it back into the collections of the Department of Invertebrate Zoology of NMNH (Smithsonian Institution), including DNA and RNA extracts, will be available for any researcher from around the world to either visit or borrow. These scientific resources represent one tangible contribution of our work here for the future. We are also documenting and photographing as many species as possible during our short visit, thereby providing observations that can used to assess change through time. In addition, today we have tentative plans to share some of our work and findings with a nearby eco-adventure/education outfit. But both of us would like nothing more than to be collaborating with one or more Belizean researchers who could understand the joy we feel in studying hydroid biodiversity.

The word hydroid actually refers to one life stage, the benthic polyp stage of the class Hydrozoa of the phylum Cnidaria (stony corals, soft corals, anemones, jellyfish, siphonophores, etc.), which include all animals that contain microscopic stinging organelles known as nematocysts. Many hydrozoans undergo what is called an alternation of generations, involving a benthic polyp stage (hydroid) and a free-swimming jellyfish stage (hydromedusa). This polyp stage can be solitary, but often hydroids form colonies, by which we mean that a single polyp, with a gut and mouth, often surrounded by tentacles, buds additional polyps that are connected with the first polyp. These polyps tend to be very small, usually less than 1 mm in dimension, and in many species polyps can be specialized to serve different functions for the colony, such as defense, feeding, and reproduction. Despite their small these, hydroids can be voracious predators of small plankton.

In just a few days of work we have found about 20 different species of hydroid. World diversity exceeds 3,000 different species. Much of the diversity we have documented is fairly common, and already recorded from the area in prior work.

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An assortment of the hydroid diversity found near Carrie Bow Cay.

However, we have had some exceptions, finding animals that have never been reported from Belize before, such as a species of Dicoryne or Hydrodendron. One other exciting discovery for us has been finding the reproductive polyps (gonothecae) of Symmetroscyphus intermedius. Such reproductive structures are commonly used in taxonomy and so our finding provides information that helps better characterize this species.

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An assortment of the hydroid diversity found near Carrie Bow Cay.

A diverse array of marine hosts to symbiotic bacteria found near Carrie Bow Cay.

Diversity and Ecophysiology of Chemosynthetic Symbioses

Harald Gruber-Vodicka, Nikolaus Leisch, Brandon Seah, Oliver Jaeckle and Manuel Liebeke

In the absence of light, where photosynthesis is impossible, chemosynthetic bacteria use chemical energy from reduced compounds such as sulfide to fix carbon. This process also depends on oxygen for optimal energy yield, but oxygen is usually well separated from the reduced compounds and the bacteria need to bridge this gap. One solution to this problem is to team up with a much larger partner, such as animals, which can help traverse the chemical gradients or buffer the needed reactants. These symbioses were first discovered in the deep sea at hot vents, but can be found in many more habitats in shallow waters.

The location of the Carrie Bow Cay Field Station allows the unique access to reef environments, seagrass habitats and mangrove islands. In these environments an incredible high diversity of these symbioses between eukaryote hosts and sulfur oxidizing bacteria can be found.

Two symbioses between ciliates and chemosynthetic bacteria are known, in very different habitats. While the colonial ciliate Zoothamnium niveum occurs on hard substrates with rotting organic material such as mangrove peat, the single celled Kentrophoros lives in the pore water space of shallow water sands. We employed glass slides to investigate the dispersal capabilities of Zoothamnium and found Zoothamnium growing several meters away from the next peat source. Surprisingly, the growth form of these specimens was different from the usual elongated form of Zoothamnium (top left, page 17) and we are currently analyzing the data with Prof. Monika Bright at the University of Vienna. Other non-symbiotic fauna that settled on our slides typically included placozoa, sessile ctenophores, sea anenomes and serpulid polychetes.

We also explored the diversity of Kentrophoros in several habitats around Carrie Bow Cay and Twin Cays. In contrast to Zoothamnium and like most ciliates, Kentrophoros are single eukaryotic cells, but they can be very large (length > 1 mm) and worm-like in appearance and behavior (top right, page 17). This genus is defined by having a densely-packed coat of ectosymbiotic bacteria on one side of their ribbon-shaped cell bodies. This is the first time that these ciliates are being studied in the Caribbean. We are using traditional morphological methods to describe the ciliates, and genome sequencing to compare the symbiotic bacteria from Belize to related species that we have found elsewhere.

Another interstitial host for chemosynthetic bacteria in the sands of the Belize Barrier reef are flatworms belonging to the genus Paracatenula. They can be found in high numbers around Carrie Bow Cay, Southwater Cay and Twin Cays, in habitats ranging from clean sandbars to stinky sand and peat mixtures. These flatworms, which can reach a length of up to 15 mm, lack a mouth and a gut and live in an ancient association with intracellular symbiotic alphaproteobacteria of the genus Cand. Riegeria. During our stay at least seven different Paracatenula species were sampled on Twin Cays, including new species such as the conspicuous P. sp ‘schlauchi’ that feaCaribbean Coral Reef Ecosystems | 18

tures a prominent duct that runs along the whole worm and likely is a protonephridium (see page 17, bottom).

We characterized the worms morphologically with light microscopy and are currently analyzing them using electron microscopy, genome sequencing, and molecular phylogenetics. Additionally, we conducted incubation experiments using stable isotope labelled substrates to better understand the nutritional relationship between the endosymbionts and their hosts.

Another prominent host group are the Stilbonematinae nematodes that harbor chemosynthetic bacteria on their cuticle. We are continuing our effort to assess the biodiversity of them around Carrie Bow Cay and adjacent islands and we have been able to identify a new species, belonging to the genus Eubostrichus. A striking feature is red inclusions along its whole body length (see photo, right), something that has not been previously observed so and gives the worm a reddish hur in contrast to the typical bright white coloration due to the symbiotic coat.

Back in the lab we are working on identifying these structures as well as on the phylogenetic placement of the species in the Eubostrichus diversity.

One major problem for many of the habitats we sampled is their ephemeral nature. Sand patches in one year can be overgrown by seagrass, or completely eroded to the stony substrate below. As part of our stay we tested an aerial photography system to better document sampling sites. A kite-mounted camera was deployed, which allowed a detailed bird’s view of the microhabitats we are working on (see below).

An aerial view of Carrie Bow Cay.

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The nematode worm, Eubostrichus, coated in bacterial symbionts.

Symbiotic Organism: The Shrimp Periclimenes rathbunae Antonio Baeza and L. John Ambroisio

The adoption of a symbiotic lifestyle is one of the most important adaptations among organisms from terrestrial and marine environments. Some degree of dependence between pairs or among assemblages of species has evolved independently numerous times. Most commonly, symbiotic associations are comprised of small organisms (hereafter symbionts) and large partners that serve as hosts. Usually, hosts vary considerably in their biology and ecology (body plan, abundance, distribution, and habitat) and a wide diversity of host-use patterns has been described for symbionts. For example, symbiotic species might inhabit hosts solitarily, as heterosexual pairs, highly structured groups, or unstructured aggregations. This diversity offers a unique opportunity to understand the conditions driving anatomical, physiological and behavPericlemes rathbunae and its anemone host. ioral traits of resource-specialist organisms.

The Baeza Lab at Clemson University is particularly interested in using several symbiotic species commonly found near Carrie Bow Cay to test predictions that are fundamental to sexual selection, mating systems, and sex allocation theories. During the summer of the year 2015, Dr. J. Antonio Baeza and his graduate student L. J. Ambrosio visited Carrie Bow Cay to conduct research on Periclimenes rathbunae, a shrimp that lives among the tentacles of the sun sea anemone, Stichodactyla helianthus.

At various shallow, back-reef subtidal localities, P. rathbunae were found dwelling in male-female pairs in sea anemones more frequently than expected by chance alone. While these observations indicate monogamy in P. rathbunae, there is evidence to suggest that males are moderately promiscuous. Solitary female shrimp often were brooding embryos, and males were considerably smaller than females. This suggests that males might be roaming among host individuals in search of, and fighting for, females. Dr. Baeza believes symbiotic species like Periclemenes that exhibit disparity in terms of host ecology represent a model group to understand the evolution of mating systems and male mating tactics in resourcespecialists, including symbiotic species. He hopes to return to Carrie Bow to carry out further investigations.

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Coral Larvae Behavior in Response to Chemical Cues in the Environment Molly Ashur and Danielle Dixson

The Dixson Lab at University of Delaware focuses on the sensory capabilities of reef organisms, and Carrie Bow Cay has become the ideal location for this research. It was only recently discovered that coral larvae are able to respond to chemical cues in their environment and use these cues to pick a suitable habitat (Dixson et al. 2014). This research was performed by placing the coral larvae into a two-chamber choice flume with water flowing from two sources that the larvae could choose between. It was discovered that corals are attracted to the smell of healthy reefs and repelled by the smell of degraded reefs, using different species of algae as the degraded cue. The initial study was conducted in the Indo-Pacific with limited numbers of species. Over the past two years, the Dixson Lab has expanded our understanding of coral larvae behavior at Carrie Bow Cay. Beginning in August of 2014, lab members have come to Carrie Bow to participate in the coral spawn collection of Acropora cervicornis, A. palmata, and others. With only a short window of time while the larvae are mobile, Dr. Danielle Dixson ran experiments using a flume to test the larvae’s ability to choose, and swim towards cues from preffered habitats. To address concerns that coral larvae, particularly small ones, are too weak to swim in the flow of a choice experiment flume . The author developed a method to test the smallest of larvae in still water with added chemical cues. While the results are still being analyzed, preliminary findings suggest that corals with small larvae (such as Orbicella annularis and Pseudodiploria strigosa) respond to similar chemical cues as their larger relatives. Other work being done at Carrie Bow Cay involves understanding the chemical preferences of the brooding species, Porites porites, and aiming to classify the behavioral relationship among several reef fish species.

Citation: Dixson, D.L. D. Abrego, M.E. Hay. 2014. Chemically mediated behavior of recruiting corals and fishes: A tipping point that may limit reef recovery. Science. 345(6199):892897

The author observing coral larvae in the lab.

Is Predation Greater in the Tropics?

Brian Cheng

One of the most well known patterns on Earth is called the “latitudinal diversity gradient� (LDG). In other words, for most animals and plants, the tropics have greater biodiversity than the temperate zone or the poles. But why? This question has perplexed scientists for over a century.

One potential explanation for the LDG is the hypothesis that interactions among species (e.g., predation, competition) are stronger in the tropics, which could result in greater coexistence between species, as well as the creation of new species. However, it is extremely difficult to measure species interactions across large areas and few studies have conducted this type of work.

Mithraculus sp.

MarineGEO (Global Earth Observatory) is a network of marine laboratories that aims to facilitate research over large expanses of the oceans. Carrie Bow Cay is a MarineGEO site that I visited in June 2015 for my postdoctoral fellowship, during which I examined predation rates in the Atlantic Ocean. For this question, I am using tunicates and bryozoans, marine invertebrates that are common in the tropics and temperate zone. These are great species for studying predation because they are easily manipulated and many predators consume them. In June, I collected the tunicate Didemnum psammatodes from mangrove roots at Twin Cays and put them into a predator exclusion experiment in seagrass beds.

I allowed the tunicates to grow in the absence of predators for 35 days and then exposed them to predators in the field.

Quickly, the tunicates were consumed by predators, such as spider crabs (see above). In addition to Belize, I have replicated these experiments in Panama, Florida, Virginia, and Connecticut. Initial results suggest that predation is very intense in the tropics as well as the temperate zone. Indeed, the story is more complicated than previously thought. It might be that there is a strong seasonal component to predation in the temperate zone. I am conducting additional experiments to address this idea and to determine if predation truly is stronger in the tropics.

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Mantis Shrimp Signals and Camoflauge Amanda Franklin

Stomatopods (mantis shrimp) are marine crustaceans found mostly in tropical waters around the world. They have a complex visual system with up to 20 photoreceptor classes. This allows them to see UV, visible, and polarised light; however, we know little about what they are using this vision for. Stomatopods are also known for being highly aggressive. They have a powerful punch which they can use during contests over refuges. I am researching how they may use chromatic and achromatic signals during these contests to assess their opponents.

On previous trips to Carrie Bow Cay, I have demonstrated that stomatopods do use chromatic signals in agonistic encounters. In 2015, I investigated how stomatopods may perceive the signal in the natural environment. To do this I recorded the spectra of different backgrounds (e.g. seagrass, rubble). These spectra can be compared to spectral measurements of the signal, which I recorded previously at Carrie Bow. Back at Tufts, I will process these data to compare the signal colour with the background colour.

I also investigated how stomatopod body coloration may provide camouflage from fish predators. This involved more spectral measurements, this time of stomatopod body coloration. The spectral measurements of body color will be compared with the spectral measurements of the background to determine conspicuousness to a fish predator.

From the data collected in Belize, I hope to address whether some body colours act as effective signals whereas others can provide camouflage from predators. This will provide a better understanding of stomatopod signalling systems and why stomatopods are colored as they are.

Mantis shrimp near Carrie Bow Cay.

Marine Chemical Ecology in a Caribbean Reef System Natassia Patin, Paul Jensen, Joe Pawlik, Greg Rouse, Lindsey Deignan, Robert Tuttle

For the second consecutive year, an interdisciplinary team from Scripps Institution of Oceanography (led by Dr. Paul Jensen) and the University of North Carolina, Wilmington (led

by Dr. Joe Pawlik) visited Carrie Bow Cay for a week to pursue various questions in marine chemical ecology.

The coral reef environment is home to many chemically active organisms. Dr. Pawlik’s work on Caribbean sponges has shown that the chemical defenses of sponges directly affect the ecology of the reef, and Dr. Jensen’s group has shown how secondary metabolites affect the competitive differentiation The fluorescent fireworm Hermodice carunculata. of closely-related bacterial species. However, the vast majority of marine natural products do not have well-understood functions. During their time at Carrie Bow, Dr. Jensen and his students collected samples and performed experiments to look at potential ecological functions of microbial secondary metabolites.

In addition to guiding the collection of nematodes and polychaetes for the chemical ecology experiments, Dr. Rouse (Scripps Institution of Oceanography) also collected annelids for transcriptomic analysis and documented many of the organisms used for the studies.

Finally, Dr. Pawlik and his student explored the idea of invertebrate feeding deterrence through bioaccumulation of toxic compounds. The evolutionary loss of shells is thought to be associated with the acquisition of dietary defenses, but many shelled gastropod species are known to eat chemically deterrent prey. They performed wet-lab feeding assays using giant hermit crabs (Petrochirus diogenes) to determine if three species of gastropod gain deterrent compounds from their prey.

The crabs did not show a feeding preference for any species during the feeding assays, suggesting that prey defenses are not passed on to these snails.

Carrie Bow Cay offers the ideal setup for these types of chemical ecology experiments. Direct access to the reef environment makes it possible to collect ecologically relevant organisms and test behavioral responses like feeding deterrence.

The excellent wet lab setup and the expertise of the station manager provide top-notch facilities to perform well-controlled experiments and collections. The only complaint from this group was that the stay should have been longer!

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Ecology of Herbivorous Crabs Jason Sparado

Only recently have we begun to truly appreciate the importance that herbivory plays in structuring coral reef communities. Large herbivorous fishes and echinoid grazers have long been thought of as the most important members of this functional group on coral reefs. A long history of overfishing has left many reef communities, particularly those of the Caribbean region, largely devoid of large herbivorous fishes. In 1983, an unidentified pathogen swept through the Caribbean and resulted in the nearly complete (~98%) mortality of the long spine sea urchin, Diadema antillarum, thought by some to be the region’s keystone herbivore species. Coupled with the loss of grazing function in the Caribbean ecosystem, there has been a substantial (>80%) decline in live coral cover throughout the region. With such a reduction in grazing and an increase in available substrate, the abundance of algae in the region has seen a profound increase. Thus studies of grazers and grazing as an ecosystem function are increasing in frequency and scope. In light of this trend, it is surprising to note that the effects of grazing crabs on coral reefs are still virtually unknown. Recent studies of the Caribbean king crab, Damithrax spinosissimus, the largest crab in the Western Atlantic, demonstrated that the species’ grazing rate meets or exceeds that of all but one species of Caribbean parrotfish, the terminal phase of the stoplight parrotfish (Sparisoma viride).

Therefore, the effect of crab density on the abundance and distribution of benthic macroalgae on coral reefs is substantial.

These large spider crabs are only one species in a large and diverse family, however.

Here, we began a study of the grazing ecology of several members of the family Mithracidae. By determining how these crabs differ in their preference of algae, rates of algal consumption, and potential multiple consumer effects, we will shed light on the complex effects of a cryptic guild of herbivorous crustaceans on coral reef community structure and function. The results of these studies will not only help improve our understanding of these species’ role in Caribbean reef community ecology, but may also help inform future restoration and management efforts.

The author with a Caribbean king crab, Damithrax spinosissimus

TMON Mangrove Ecology Lisa Schile During the two week research campaign at Carrie Bow between February 18th and March 4th, 2015, we accomplished multiple objectives related to establishing the MarineGEO mangrove plots and also initiate my postdoctoral research through the Tennenbaum Marine Observatories Network. My field assistant C. Scott Beers and I took seven deep soil cores in the mangroves at Twin Cays, ranging in depth from 191 to 500 cm. We also collected six soil cores that were up to 1m long within seagrass beds – one near Carrie Bow Cay and five in a lagoon at Twin Cays. We initiated a three month long decomposition experiment that used teabags – green and rooibos tea – and deployed bags within the fringe and interior of the Soil core taken at Twin Cays, near Carrie Bow Cay. mangroves at Twin Cays and within a seagrass bed near Twin Cays. We also collected tidal water samples every two hours over a 24 hour period at the mouth of a channel draining Twin Cays to examine dissolved carbon flux. This project involved us staying on the boat overnight in the mangroves, which was quite an adventure.

We assisted Dr. Candy Feller (Smithsonian Environmental Research Center) and her team in establishing the long term mangrove monitoring plots at Twin Cays. We resurveyed the trees within six 10x10 m plots – three along the fringe and three in the interior dwarf mangroves. All trees within each plot were counted and measured to tree height, stem width, and crown area. Tree bands were installed on some of the mangrove trees within the plots. We also helped Dr. Feller with adding more fertilizer to her long term fertilization experiment. On one calm day, the entire crew went to the Pelican Cays to collect mangrove leaf samples and explore the mangroves from both on land and snorkeling.

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Genetic Assessment of the Temporal Variation in Spiny Lobster Recruitment Iris Segura The Caribbean spiny lobster, Panulirus argus, is one of the most harvested species by both commercial and recreational fishers in the region. To ensure the sustainability of this fishery we require an accurate knowledge of population dynamics at a regional scale and connectivity patterns among local Caribbean populations. Adults of this species reproduce year round and have long planktonic larval duration, which gives it a great amount of dispersal ability- larvae can travel thousands of miles over the course of months. The larval phase consists of 11 stages of phyllosoma larva (leaf-like body shape) that travel with the ocean currents for 5-11 months. The larvae have little horizontal swimming ability, but they are active feeders. The final stage of phyllosoma metamorphoses into a non-feeding puerulus, which is a transparent postlarva similar to the adult shape that actively swim towards coastal areas. The settlement of postlarvae (PL) onto coastal benthic habitats is an important process in the population dynamics of the Caribbean spiny lobster and potentially for the further recruitment into the fishery. Monitoring the PL settlement in the natural habitats is quite challenging, as they are scattered in small and cryptic habitats. To assess the variation in the PL settlement we used artificial collectors, which are floating substrates that resemble local marine vegetation where PL settle after a long swim from the offshore waters. In collaboration with CCRE staff we deployed six collectors along the west coast of the Carrie Bow Cay (CBC). Collectors are checked monthly during the first half of the lunar phase by shaking them to detach PL and associated fauna of the collecting fibers.

Postlarvae are counted and samples are collected for further genetic analyses. The aim of this study is to genetically characterized PL recruits collected in distinct locations across the Caribbean Sea to assess the extent of variation of PL recruitment at spatial and temporal scales, as well as estimated local retention rates, exchange rates among local populations, and connectivity patterns along the Caribbean Sea. This study will have an immediate impact in the management of the Caribbean spiny lobster fishery and securing the local fisher livelihood.

The author with a spiny lobster postlarva.

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 fifth full year that CCRE staff and collaborators from the New England Aquarium have implemented the South Water Caye Marine Reserve Reef Assessment Program. This project is directed at assessing effects of the no-take conservation zone around Carrie Bow Cay on recovery of fish and coral populations. Permanent transects were established in June 2011 inside (12 transects) and outside (12 transects) the area’s boundary.

Most monitoring plans measure the diversity and abundance of key reef organisms; some of the best programs also assess biomass of benthic reef builders and fishes. We have designed our program to assess similar ecological metrics, so as to be cross-compatible with historical and simultaneous efforts elsewhere in Belize and the western Atlantic Ocean. We have also added some innovaThe monitoring team in December 2015. tive and critically important 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. Rates include the grazing rates of herbivorous parrotfishes and surgeonfishes. Benthic states include scleractinian coral health status as well as recruitment and growth dynamics. This plan will enable more comprehensive ecological monitoring, and inform 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.

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CARICOMP Report

Karen Koltes, John Tschirky, and Joanna Walczak

Monitoring surveys and data collection were conducted in July 2015 under the Caribbean Coastal Marine Productivity Program (CARICOMP). CARICOMP was launched at Carrie Bow Cay in 1993 as part of a collaborative scientific effort among the region’s marine laboratories to study land-sea interaction processes, to monitor for change on local and regional scales and distinguish anthropogenic change from natural variation, and to provide appropriate and reliable scientific information for natural resource management.

Standardized, synoptic measurements are made in the three primary Caribbean coastal ecosystems of coral reefs, seagrass beds and island mangroves, together with relevant and simple oceanographic and meteorological measurements. Ecological variables include seagrass productivity (biomass and growth) and coral reef community structure based on annual surveys of 10 permanent, 10m transects at 10-13m depth on the forereef. Here we report on preliminary data on one of those variables, the octocoral populations on the 10 permanent transects. The surveys, which began in 1994, consist of counting all colonies of octocorals that intersect the permanent transect lines (a total area of approximately 50m2) and identifying them to species. Colonies are sorted by form into fan, feather, or rod.

More than 20 species of octocorals have been identified in the survey area. While the data on individual species are still being compiled, the most common species, by number, are feathers in the genus Pseudopterogorgia. The majority of rods are from the genus Eunicea and the majority of fans are Gorgonia.

Preliminary results of the surveys indicate that the total population of octocorals has approximately doubled over the 21year survey period, from about 21 to 53 colonies/m2. However, the increase has differed among the three groups. The total population of rods has remained fairly constant at about 14 colonies/m2. By contrast the populations of fans and feathers have increased significantly. Fans have increased about ten-fold, from about 0.4 to 3.8 fans/m2. A low of about 4.4 colonies/m2 for feathers was reached in July 2001. The decline was due to the lingering effects of the El Nino bleaching event and a Category 5 hurricane (Hurricane Mitch) in 1998. Since 2001, the population of feathers has increased about seven-fold to a total of about 29.6 colonies/m2 in the survey area, and constitutes the majority of octocoral community. The increase in soft corals is in contrast to the loss and/or lack of recovery of hard corals in this zone.

The total population of octocorals has approximately doubled since 1994.

Geodetic Surveying at Carrie Bow Cay Marguerite Toscano

The Smithsonian Institution’s Marine Global Earth Observatory (MarineGEO) is a network of coastal marine research sites designed to advance our understanding of ecological phenomena governed by latitude and anthropogenic activity, focused on landsea interactions, coastal marine ecology, geology, and anthropology. One important consequence of locating the observatory in shallow coastal water at the land-sea margin is the need to measure and understand the most dynamic physical feature of coastal systems – sea level.

Tides and sea level have profound effects on the biodiversity, community structure, The newly-installed instrument platform at Carrie Bow Cay. and ecosystem function of marine systems, particularly those attached to the sediment surface such as coral reefs, sea grass beds, and tidal wetlands. Relative sea level – the elevation of water compared to “land” (i.e. submerged sediment, wetland soil or upland soil) – controls physical features such as light availability, thermocline depth, and O2 flux, and biological processes such as recruitment and propagule dispersal. Increasing rates of sea level rise, coupled with stable or subsiding land elevation, results in deeper water and reduced light to support photosynthetic organisms such as plankton, corals, and sea grasses. In tidal wetlands, deeper water eventually causes emergent plants to drown. In all cases, rising sea level relative to land level makes ecosystems vulnerable to permanent decline or loss.

MarineGEO seeks to operate a long-term observing network (>30yr) designed to explain spatial and temporal change in the coastal environment. The network is instituting long-term monitoring observations and repeated manipulative field experiments to detect, explain, and forecast the effects of global climate change and anthropogenic impacts on ecological structure, function, and biodiversity. This sea level monitoring project was motivated by the need to establish a robust system of tide gauges, land elevation benchmarks, and data analysis protocols as a foundational data set required to meet the scientific goals of MarineGEO.

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2015 Scientific Publications Open access articles are indicated with clickable link Bracken-Grissom, H. D. and D. L. Felder. 2014. Provisional revision of American snapping shrimp allied to Alpheus floridanus Kingsley, 1878 (Crustacea: Decapoda: Alpheidae) with notes on A. floridanus africanus. Zootaxa 3895 (4): 451–491. doi: 10.11646/zootaxa.3895.4.1 link Bracken-Grissom, H. D., R. Robles, and D. L. Felder. 2014. Molecular phylogenetics of American snapping shrimps allied to Alpheus floridanus Kingsley, 1878 (Crustacea: Decapoda: Alpheidae). Zootaxa 3895 (4): 492–502. doi: 10.11646/ zootaxa.3895.4.2 link Engene, N., A. Tronholm, L. A. Salvador-Reyes, H. Luesch, and V. J. Paul. 2015. Caldora penicillata gen. nov., comb. nov. (Cyanobacteria), a pantropical marine species with biomedical relevance. Journal of Phycology, 51 (4): 670-681. doi: 10.1111/jpy.12309. link Freestone, A.L. and B. D. Inouye. 2015. Non-random community assembly and high temporal turnover promote regional coexistence in tropics but not temperate zone. Ecology 96 (1): 264-273. doi: 10.1890/14-0145.1 link Kemp, D.W., D.J. Thornhil, R.D. Rotjan, R. Iglesias-Prieto, W.K. Fitt, G.W. Schmidt. 2015. Spatially distinct and regionally endemic Symbiodinium assemblages in the threatened Caribbean reef-building coral Orbicella faveolata. Coral Reefs 34(2): 535-547. link Longo, G.O., and M. E. Hay. 2015. Does seaweed-coral competition make seaweeds more palatable? Coral Reefs 34 (1): 87-96. doi: 10.1007/s00338-014-1230-6. link Mclean, E. and K. Rutzler. 2015. Competing for space: factors that lead to sponge overgrowth when interacting with octocoral. Open Journal of Marine Science 5: 64-80. doi: 10.4236/ojms.2015.51007. link Rocha, L.A., C. R. Rocha, C. C. Baldwin, L. A. Weigt, and M. McField. 2015. Invasive lionfish preying on critically endangered reef fish. Coral Reefs 34 (3): 803-806. doi: 10.1007/s00338-015-1293-z. link Sneed, J. M., R. Ritson-Williams and V. J. Paul. 2015. Crustose coralline algal species host distinct bacterial assemblages on their surfaces. The ISME Journal 9: 2527-2536. doi: 10.1038/ismej.2015.67.

Soares, A. R., N. Engene, S. P. Gunasekera, J. M. Sneed, and V. J. Paul. 2014. Carriebowlinol, an antimicrobial tetrahydroquinolinol from an assemblage of marine cyanobacteria containing a novel taxon. Journal of Natural Products 78 (3): 534-538. doi: 10.1021/np500598x.

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2015 Scientific Publications Vaslet A., D. L. Phillips, C. A. M. France, I. C. Feller, and C. C. Baldwin. 2015. Trophic behaviour of juvenile reef fishes inhabiting interlinked mangrove-seagrass habitats in Caribbean offshore mangrove islets. Journal of Fish Biology 87 (2): 256-273. doi: 10.1111/jfb.12715. link

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2015 Participants * served as station manager Alanko, Jerry & Sandy, Tilghman, MD* Altieri, Andrew, Smithsonian Tropical Research Institute, Panama Ambrosio, John, Clemson University, Clemson, SC Ashur, Molly, University of Delaware, Newark, DE Baeza, Antonio, Clemson University, Clemson, SC Barkel, Karen, Ferris State University, Big Rapids, MI Barshis, Dan, Old Dominion University, Norfolk, VA Beers, Scott, Smithsonian Environmental Research Center, Edgewater, MD Booker, Rohan, University of Delaware, Newark, DE Boose, Kayleigh, Stony Brook University, NY Brightwater, Franklin, San Carlos, CA Brooks, Barrett, National Museum of Natural History, Washington, D.C. Bulgheresi, Sylvia, University of Vienna, Austria Campbell, Justin, Smithsonian Marine Station, Fort Pierce, FL Cheng, Brian, Smithsonian Tropical Research Institute, Panama Collins, Allen, National Museum of Natural History, Washington, D.C. Craig, Catherine, University of Louisiana at Lafayette, LA Crawford, Drew, Washington, D.C. Deignan, Lindsaay, University of North Carolina at Wilmington, NC Dimond, Jay, Shannon Point Marine Center, Western Washington University, Anacortes, WA Dixson, Danielle, University of Delaware, Newark, DE Dramer, Greg & Joann, Kalispell, MT* Duckett, Lisa, Smithsonian Environmental Research Center, Edgewater, MD 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 Franklin, Amanda,Tufts Unviversity, Medford, MA Gawne, Peter, New England Aquarium, Boston, MA Gouge, Daniel, Williston, FL* Gruber-Vodicka, Harald, Max Planck Institute for Marine Microbiology, Bremen, Germany Haren, Nick & Marylin, Anacortes, WA* Harper, Leah, Nova Southeastern University, Dania Beach, FL Herman, Sam, New England Aquarium, Boston, MA Horning, Reginald, Traverse City, MI* Caribbean Coral Reef Ecosystems | 34

2015 Participants Hunt, Nicholas, Stony Brook University, NY Jacobwitz, Beth, Stony Brook University, NY Jaekle, Oliver, Max Planck Institute for Marine Microbiology, Bremen, Germany James, Edwin & Bonnie, Tilgman, MD* Janiak, Dean, Smithsonian Marine Station, Fort Pierce, FL Jensen, Paul, Scripps Institution of Oceanography, La Jolla, CA Johnston, Lane, Smithsonian Marine Station, Fort Pierce, FL Jones, Scott, Smithsonian Marine Station, Fort Pierce, FL Koltes, Karen, U.S. Department of the Interior, Washington, D.C. Komoroske, Lisa, NOAA Southwest Fisheries Science Center, La Jolla, CA Lamb, Norlan, Earthwatch Institute, Dangriga, Belize Leisch, Nikolaus, University of Vienna, Austria Lee, Woody, Smithsonian Marine Station, Fort Pierce, FL Levine, Amanda, Stony Brook University, NY Liebeke, Manuel, Max Planck Institute for Marine Microbiology, Bremen, Germany Liebert, Emily, Stony Brook University, NY Marden, Sean, New England Aquarium, Boston, MA Marques, Antonio, University of S達o Paulo, S達o Paulo, Brasil Masi, Joe, New England Aquarium, Boston, MA McKeon, Seabird, Smithsonian Marine Station, Fort Pierce, FL Meyer, Julie, University of Florida, Gainesville, FL Miranda, Ashbert, Earthwatch Institute, Dangriga, Belize Moore, Joel & Linda, Shingle Springs, CA* Noren, Hunter, Nova Southeastern University, Dania Beach, FL Nunez, Mayra, Center for Marine Studies, Tegucigalpa, Honduras Opishinski, Tom, Interactive Oceanographics, East Greenwich, RI Palacios-Theil, Emma, University of Lousiana at Lafayette, LA Parsons, Keith & Shirley, 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 Penland, Laurie, National Museum of Natural History, Washington, D.C. Peresta, Gary, Smithsonian Environmental Research Center, Edgewater, MD Rouse, Greg, Scripps Institute of Oceanography, La Jolla, CA Scharer, Lukas, University of Basel, Switzerland Schile, Lisa, Smithsonian Environmental Research Center, Edgewater, MD Schleiger, Doug, Smithsonian Dive Office, Washington, D.C. 35 |Caribbean Coral Reef Ecosystems

Scioli, Justin, University of Louisiana at Lafayette, LA Seah, Brandon, Max Planck Institute of Marine Microbiology, Bremen, Germany Seeman, Janina, Smithsonian Tropical Research Institute, Panama Segura-Gracia, Iris, Smithsonian Marine Station, Fort Pierce, FL Sherwood, Craig, Deale, MD* Sievers, Brittany, Stony Brook University, NY Simpson, Lorae’, Smithsonian Environmental Research Center, Edgewater, MD Sneed, Jennifer, Smithsonian Marine Station, Fort Pierce, FL Spadaro, Angelo, Old Dominion University, Norfolk, VA Spathias, Hanae, Interamerican University of Puerto Rico, San Juan, PR Spiers, Lindsey, Univeristy of Florida, Gainesville, FL Teplitski, Max, University of Florida, Gainesville, FL Thacker, Cheryl, University of Florida, Gainesville, FL Tschirky, John, American Bird Conservancy, The Plains, VA Toscano, Maggie, National Museum of Natural History, Washington, D.C. Tuttle, Robert, Scripps Institution of Oceanography, La Jolla, CA Valentin-Albanese, Jasmine, Stony Brook University, Stony Brook, NY Vasbinder, Kelly, Florida State University, Tallahassee, FL Walczak, Joanna, Florida Department of Environmental Protection, Fort Lauderdale, FL Weber Michelle, National Museum of Natural History, Washington, D.C. Whippo, Ross, Smithsonian Tennenbaum Marine Observatories Network, Washington, D.C. Wulff, Janie, Florida State University, Tallahassee, FL Yockachonis, T.J., San Francisco State University, CA

Caribbean Coral Reef Ecosystems | 36

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: Reg Horning, Craig Sherwood, Greg & Joann Dramer, Gary Peresta, Jim Taylor, Tanya Ruetzler, Joel & Linda Moore, Jerry & Sandy Alanko, Ed James, Keith & Shirley Parsons, Nicky & Marilyn Haren, and Daniel Gouge.

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 Smithsonian offices of the Undersecretary for Science and 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.

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Photo Credits

Cover: Zach Foltz page 1: Clare Fieseler; page 4: (top to bottom) Abby Wood, Zach Foltz, Zach Foltz; page 5: Zach Foltz; page 8: Cheryl Thacker; page 10: Max Teplitski; page 11: Valerie Paul; page 12: Valerie Paul; page 14: Allen Collins; page 16: Allen Collins; page 17: Harald Gruber-Vodicka; page 19 -20: Harald Gruber-Vokicka; page 21: Zach Foltz; page 22: Zach Foltz; page 23: Seabird McKeon; page 24: Scott Jones; page 25: Greg Rouse; page 26: Scott Jones; page 27: Lisa Schile; page 28: Zach Foltz; page 29: Jason Sparado; page 31: Tom Opishinski; page 38: Scott Jones; Back cover: Scott Jones

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