2013 CCRE Annual Report

Smithsonian Institution

CCRE Annual Report 2013 Caribbean Coral Reef Ecosystems • National Museum of Natural History

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CCRE ANNUAL REPORT 2013

National Museum of Natural History Smithsonian Marine Station at Fort Pierce Caribbean Coral Reef Ecosystems Program Fort Pierce, FL 34949

November 2013

Table of Contents CCRE 2013.........................................................................................................................................................................1 Flashbacks...........................................................................................................................................................................2 Acknowledgements ........................................................................................................................................................5 Projects.............................................................................................................................................................................6

Outreach.......................................................................................................................................................6 Long Term Ecological Research ............................................................................................................................9 Ecology and Evolution..........................................................................................................................................14

Corals........................................................................................................................................14 Sponges.....................................................................................................................................20 Crustaceans...............................................................................................................................23 Mangroves................................................................................................................................26 Fish...........................................................................................................................................26 Biodiversity and Community Ecology.....................................................................................27 Other Invertebrate Studies........................................................................................................30

Contributions 2013 .......................................................................................................................................................35 Participants 2013 ..........................................................................................................................................................36

Photograph & Art Credits ..........................................................................................................................................38

CCRE 2013

This past year was another busy one for CCRE program staff and the Carrie Bow Cay Field Station. With over 75 scientific visitors contributing to over 1,000 scientific visitor days, the station continues to be well-utilized and an important site for Caribbean coral reef research. The program's continued support for long-term reef observations through continuous monitoring systems, the CARICOMP program, and reef monitoring becomes especially relevant as Carrie Bow Cay joins the Smithsonian's Global Tenenbaum Marine Observatory Network (TMON). This exciting new initiative places the CCRE program at the heart of what will be the world's first global network of coastal ecological field sites, standardizing measurements of biological change. The network has the potential to provide an unprecedented understanding of how marine biodiversity is affected by local human activities and global change. When Klaus Ruetzler and his colleagues formed the CCRE program, they intended to create a site that would seek to understand a complex ecosystem through long-term observations. It is their hard work that laid the foundation for such endeavors as a global observatory network.

Station manager Daniel Gouge has a close encounter with a hawksbill sea turtle near Carrie Bow Cay.

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Flashbacks 1971

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1978 1979

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1983

• National Museum of Natural History’s I.G. Macintyre (geology & sedimentology), W. Adey, P. Kier, T. Waller (paleobiology), A. Dahl (botany), A. Antonius (postdoctoral fellow, invertebrate zoology), M. Rice, and K. Ruet- zler (invertebrate zoology) found the program Investigations of Marine Shallow Water Ecosystems (IMSWE).

• IMSWE search party identifies Carrie Bow Cay on the barrier reef of Belize as ideally located and affordable site for long-term, collaborative field research on tropical coastal ecosystems • Establishment of principal reference transect across the Belize barrier reef just north of Carrie Bow Cay • Hurricane Fifi destroys laboratory structures, uproots coconut trees, and reduces the surface area of Carrie Bow Cay by about one third, to 0.4 hectare.

• EXXON Corporation provides grant for study of the coral reef ecosystem at Carrie Bow Cay. • Marine and terrestrial post-hurricane surveys.• Establishment of all-manual meteorological station.

• Refinement and calibration of profiles and maps with the aid of vertical aerial photographs taken by Royal Sig- nals Detachment helicopter • Introduction of aerial photography by helium balloon for community mapping • Submersible tide recorder installed at Carrie Bow Cay concrete dock.

• Field trip to Carrie Bow Cay by participants of the Third International Coral Reef Symposium.• Aerial and underwater surveys expanded to cover the entire barrier reef of Belize • Geology team drills first cores to determine reef history • EXXON’s The Lamp publishes article on company-sponsored research at Carrie Bow Cay (“Where seaworms glow..”).

• Hurricane Greta destroys Carrie Bow Cay field station.

• Post-hurricane survey and rebuilding of laboratory with several improvements • Count of participating scien- tists and of published scientific contributions both pass the 50 mark; 23 scientific institutions are now collabora- ting with NMNH. • EXXON Corporation funds new initiative: comprehensive study of a western Atlantic mangrove swamp ecosys- tem, now known as SWAMP (Smithsonian Western Atlantic Mangrove Program) • Mapping of Twin Cays, principal site of SWAMP, by aerial photography and ground truthing.

• Initiation of Art in a SWAMP project where scientific illustrators and scientists collaborate in analysis and picto- rial rendition of mangrove communities in time and space • Employment of H. Edgerton underwater time-lapse camera with strobe light (on loan from the inventor) to record day-night activity in benthic communities • Vibracoring at Twin Cays to determine internal structure and development.

• Publication of The Atlantic Barrier Reef Ecosystem at Carrie Bow Cay, Belize, 1: Structure and Communities.

Smithsonian Institution Press (K. Ruetzler & I.G. Macintyre, eds.).

• New weather protected and enlarged seawater system for laboratory experiments installed on Carrie Bow Cay • Series of extremely low tides at noon time were observed to have catastrophic effects on reef

and mangrove organisms.

1984 • First automated weather station installed at Twin Cays • Cooperation with Belize Government identifying

coastal marine areas suitable for natural resource conservation • Busiest year since program start: 8 months con-

tinuing laboratory operation for 45 research staff.

1985 • First year of operation of Caribbean Coral Reef Ecosystems (CCRE), a new program of the National Museum

of Natural History. It replaces the old IMSWE project and supplements the ongoing SWAMP program which is

supported by a renewed annual grant by the EXXON Corporation.

1986 • Renovations on Carrie Bow Cay to accommodate dry-laboratory space, added living quarters, and boat, diving,

and laboratory equipment • Mangrove vegetation map for Twin Cays completed • Published scientific contribu tions pass the number 200.

1987 • Record visitation of Carrie Bow laboratory, 120 total: 90 scientists and assistants; others dignitaries, including

the Prime Minister of Belize, Smithsonian administrators, and media people working on documentaries and

news-related productions • Continued facility renovation, including addition of solar photovoltaic system, large

seawater tank, two fiberglass whalers, fluorescence microscope, and time-lapse video recorder with underwater camcorder.

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1988

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2001

• Mangrove workshop for 37 EXXON-SWAMP scientists at Solomons, Maryland, entitled A Mangrove Ecosystem: Twin Cays, Belize.

• Science as Art exhibit at the Smithsonian’s S. Dillon Ripley Center displays scientifically important and aesthetically pleasing products from SWAMP mangrove research, such as community drawings, paintings, photo- graphs, and sculpture-like epoxy casts of soft-bottom animal burrows • Vandalized and malfunctioning weather station reconditioned and relocated to the Carrie Bow field laboratory • Increasing problems with anthropogenic stresses at research sites, such as heavy tourist visitation, garbage dumping, and clear-cutting mangrove trees.

• CCRE-SWAMP program represented at first Caribbean Coastal Marine Productivity workshop, Jamaica, CARICOMP is a program for Caribbean-wide monitoring of environmental quality in reefs, mangroves, and seagrass meadows.

• Belize Forestry Department helps stopping disturbances to SWAMP research sites. Belize Department of Natural Resources reviews legislation with intention of declaring Carrie Bow Cay - Twin Cays area protected research site • CCRE-SWAMP program staff participates in developing Belize Tropical Forestry Action Plan and helps designing Institute for Ecology to be based in Belmopan.

• CCRE-SWAMP researchers produce video documentary on mangrove swamp biology • Unprecedented, severe problem with hydrozoan stings to snorkelers and divers in the Carrie Bow area traced to microscopic siphonophorans • CCRE-SWAMP staff and Belize Fisheries Department and Agriculture representatives conduct first workshop for Belize high-school teachers entitled Mangrove Conservation through Education • CCRE-SWAMP lecture series started in Belize City, co-hosted by Belize Audubon Society • CCRE officially joins the CARICOMP network and initiates monitoring program.

• Belize Ministry of Natural Resources grants rights to Twin Cays for mangrove research • Launching of new 8 m (25 ft) research vessel Physalia, funded by a grant from the U. S. National Science Foundation, extends research radius over most of central and southern Belize • Ivan Goodbody pioneers surveys of Pelican Cays, a tunicate heaven at SSW of Carrie Bow. • Start of collaborative surveys and experimental projects in the Pelican Cays • Pelican Cays workshop, co-hosted

by Candy Feller (SERC), at Edgewater, Maryland.

• Finalized lease with the Villanuevas of Placentia to southern portion of Northeast Cay, Pelican group, to establish a field base for future studies • Malcolm Spaulding develops plans for new integrated environmental sensing system with radio- telemetry link to the University of Rhode Island’s COASTMAP network.

• Installation by Tom Opishinski of self-contained Endeco-YSI-Campbell monitoring station of meteorological and oceanographic parameters and hookup to Internet • Visit of field party from 8th International Coral Reef Symposium, Panamá.

• Celebration of the 25th birthday of the Carrie Bow Marine Field Station • New U. S. National Science Foundation grant allows purchase of a second 8-m (25 ft) boat to back up the heavily used Physalia (under construction) • International team of seven expert systematists conducts workshop at Carrie Bow Cay to quantify the unusually high sponge diversity of the Pelican Cays • Number 500 reached in CCRE scientific contributions • Carrie Bow Field Station, including laboratories, weather station, kitchen, and living quarters is consumed by an accidental electrical fire which was apparently sparked by a short in the wiring and aided by dry, termite-riddled lumber and strong northerly winds. Luckily, no-one was hurt.

• Island clean-up and design for new field station completed. Construction work initiated but delayed by flooding and coastal erosion from hurricane Mitch • Completed editorial work on CD-ROM containing over 100 represen- tative CCRE scientific papers that resulted from research at Carrie Bow Cay • Cosponsored Smithsonian (STRI) exhibit Our Reefs –Caribbean Connections in Belize City. Contributed large poster describing 25 years of CCRE coral reef research in Belize • Serious coral bleaching and die-off on reefs off Carrie Bow and Pelican Cays observed, partly caused by hurricane Mitch.

• Rededication ceremony for the new Carrie Bow Marine Field Station, in August • BBC team (Bristol, UK) films segments for its Blue Planet TV series, including (with E. Duffy) eusocial shrimps living in sponges.

• Publication of Natural History of Pelican Cays, Belize, in Atoll Research Bulletin (Macintyre & Ruetzler, eds, 2000) • Replacement of environmental monitoring station lost in the 1997 fire • Initiation of Twin Cays Biocomplexity Study funded by an NSF grant (to I. Feller & colleagues).

• Completion of 3-room cottage over the eastern shore of Carrie Bow Cay • Hurricanes Michelle and Iris (October) barely miss Carrie Bow Cay, causing some damage to buildings and heavy beach erosion and devastate

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2002

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2008

(Iris, in particular) large areas in southern Belize • Signing of MoU with Belize Fisheries Department officially acknowledging the Carrie Bow Marine Field Station as a nationally recognized laboratory • Publication of Golden (50-year anniversary) issue of Atoll Research Bulletin recognizing prominent coral reef scientists through their autobiographies, several of them participants in the CCRE Program.

• Founding of the Smithsonian Marine Science Network (MSN), incorporating the CCRE Program and the Carrie Bow Marine Field Station • Number 600 reached of CCRE scientific contributions • Ranger Station established on southeast Twin Cays by Belize Fisheries Department to oversee South Water Cay Marine Reserve.

• Cristián Samper, recently appointed director of the Smithsonian’s Natural History Museum, visits the Carrie Bow station in July, dives on the barrier reef, and snorkels in mangroves habitats • Hurricane Claudette threatens Carrie Bow (July) and necessitates temporary evacuation • Smithsonian Secretary Larry Small visits the Carrie Bow lab in December and dives on the reefs • Twin Cays Mangrove Biodiversity Conference is held at Ft. Pierce, Florida (December), convened by Klaus Ruetzler, Ilka Feller, and Ian Macintyre, and cosponsored by Valerie Paul of the Smithsonian Marine Station at Ft. Pierce.

• CCRE Postdoctoral Fellowship established • Hurricane Ivan causes substantial coastal erosion of Carrie Bow Cay • Atoll Research Bulletin volume dedicated to Twin Cays Mangrove Biodiversity goes to press • Number 700 reached of CCRE scientific contributions • Carla Dietrich takes over from Michelle Nestlerode as CCRE research assistant • Addendum to MoU with Belize Fisheries Department signed, clarifying intellectual property rights and issues of bioprospecting sponges in particular • CCRE Program Administrator Marsha Sitnik (recently, administrative advisor) retires.

• A total of 13 hurricanes formed this season. Three category five hurricanes (Katrina, Rita and Wilma) caused substantial coastal erosion and damage to the Carrie Bow facilities. The record number of 25 named storms in the Caribbean broke the previous record (from 1933) of 21 named storms • An external scientific review of the CCRE Program was conducted and resulted in a strong endorsement of the program’s mission and accomplishments • Over 50 new CCRE scientific contributions were published.

• The first Belize National Marine Science Symposium, cosponsored by Belize Fisheries and Forestry departments and the Hugh Parkey Foundation, took place and CCRE was represented with 4 talks and 8 posters, including a review of 35 years of Smithsonian Marine Science in Belize • CCRE hosted the U. S. Ambassador and 35 Embassy staff for a picnic, including a tour of the Carrie Bow lab facilities • More than 130 Smithsonian Asociates, North Carolina teachers, and members of the Sierra Club visited Carrie Bow for guided tours of facilties and ongoing projects • A film crew for a Discovery channel in The Netherlands worked at Carrie Bow to document Gordon Hendler’s work on newly discovered brittle-star light-sensing organs • The CCRE program and the Carrie Bow Marine Field Station, along with all other Smithsonian marine programs and facilities, took part in an external review ordered by the Smithsonian Undersecretary for Science; The efficiency and scientific productivity of the program and its field station received excellent marks.

• Hurricane Dean strikes Northern Belize and Yucatan, Mexico (August), Felix passed over Honduras

south of Belize (September); both cause major beach erosion at Carrie Bow Cay but no damage to buildings.

• The Belize Minister of Natural Resources and his staff visit our facilities and tour the Pelican Cays to view dam- age caused by mangrove clear-cutting in this part of the Southwater Cay Marine Reserve.

2009 • Ilka “Candy” Feller was again offered use of Light Hawk, a volunteer pilot-based organization

at Lander, WY, to observe and photograph environmental damage to mangrove coast and cays. •Pro- ceedings of the first Smithsonian Marine Science Symposium highlight CCRE’s diverse contributions to knowledge of the biology and geology of the Mesoamerican Barrier Reef, Belize •Mike Carpen- ter retired after 25 years of service as CCRE Operations Manager and will build a new home in the woods of Georgia •Klaus Ruetzler resigned as CCRE Director after 25 years in this position (and a total

37 years as leader of the IMSWE, SWAMP, and CCRE programs). He will be followed by Valerie Paul of SMSFP.

2010

• Director Valerie Paul and new staff at Fort Pierce assume responsibility for CCRE • Michael Carpenter, Zach

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Foltz, and Woody Lee spend three weeks on Carrie Bow Cay, for training and transition • A new CCRE website is launched: www.ccre.si.edu • U.S. Ambassador Vinai Thummalapally and five others from the U.S. Embassy in Belize visit Carrie Bow Cay on August 30, 2010 • Belize Fisheries establishes the South Water Caye Marine Reserve Conservation Zone, a no-take zone encompassing the area around Carrie Bow Cay (www.swcmr.org).

2011 • Carrie Bow Cay recieved major infractructure improvements, including 10 kw diesel generator, improved photovoltaic system, air compressor for SCUBA, and composting toilets • CCRE contibutions

list reached #900 • Randi Rotjan, Peter Gawne, Jay Dimond, Scott Jones, and Zach Foltz initiated 24 permanent

reef transects, establishing a long-term reef monitoring program to assess the effects of the SCWMR no-take

zone • CCRE director, Valerie Paul, along with Raphael Ritson-Williams, Scott Jones, and Nicole

Fogarty receive an award from the Smithsonian Endowment Program for “Population dynamics of

threatened Caribbean acroporid corals at Carrie Bow Cay, Belize.” • Tropical Storm Harvey forces evacuation

and makes landfall in Belize, no damage was caused to the station.

2012 • The CCRE program celebrated its 40-year anniversary since Drs. Klaus Rutlzer and Arnfried Antonious happened upon Carrie Bow Cay and secured an agreement to use it for field operations • Hurricane Ernesto tracked near Belize in early August, theatening to force evacuation of the island; the storm tracked north and caused no damage to the island. • Sherry Reed assumed responsibilities as Dive Safery Officer for the CCRE program • Over 30% of dives logged at the Smithosonian were completed in the waters surrounding Carrie Bow Cay, a total of 875 dives.

2013 • In October 2012, the CCRE program welcomed members of the Summit Foundation and Wildlife Conservation Society (WCS) to Carrie Bow Cay for a tour of the facilities and a visit to the Acropora-dominated reef adjacent to the island. Participants included Summit Foundation Chairman Roger Sant and WCS president Cristián Samper.

• Several photographers and videographers from National Geographic, the BBC, and Public Television used the island as a venue for their work • On-site tours of CBC continued to reach a large public audience, with 1556 people touring the lab in FY2013. • The Smithsonian Institution launched the Tenenbaum Marine Observatory Network, a world wide network of coastal ecological field sites, and Carrie Bow Cay was named one of the first five participating sites.

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 staff of Pelican Beach Resort in Dangriga provided logistical support for our fieldwork.; Earl David and his fine staff provided boat transportation as well invaluable advice and support.

Numerous volunteer managers helped run the field station and assisted in research activities; we greatly appreciate their many efforts: Daniel Gouge, Joel Moore, Linda Moore, George Scheff, Jeanne Scheff, Gary Peresta, James Taylor, Tanya Ruetzler, Jonathan Hootman, Jerry Alanko, Sandy Alanko, Ed James, Bonnie James, Craig Sherwood, Carl Hansen, Ginger Hansen, Greg Dramer, JoAnn Dramer, Raphael Ritson-Williams, Keith Parsons, and Shirley Parsons

In Fort Pierce, we sincerely thank Joan Kaminski for administrative advice and assistance with many fund management tasks. CCRE Dive Officer Sherry Reed was very helpful in assisting dive operations at Carrie Bow. 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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Outreach Crabs & Hurricanes

lines according to size, all biding their time until the right sized crab turns up to unlock the chain – rather like the home owners on a housing ladder, waiting for the family at the top of the ladder to get their mortgage approved.

Sometimes this waiting is orderly; sometimes it disintegrates into a mass brawl, with multiple lines forming and John Brown tug-of-war battles developing between rival lines – while The following is an excerpt from John Brown’s blog on tiny crabs rush from the end of one queue to another trying June 25, 2013 (http://www.johnbrownimages.co.uk/news/ to guess which line is going to win (Figure 1). crabs-hurricanes/). John is a freelance photographer and videographer on assignment with the BBC to film animal When the move finally happens the speed is incredible.

Ten or more crabs can switch up in shell size in a matter behavior unique to hermit crabs. of a few seconds, usually leaving a tiny empty shell at the end as everyone has moved up one size. Occasionally the Shells are everything in the world of the hermit crab, and chain would break down as an individual would move up an individual’s ability to grow is limited by the size of the in shell size but be reluctant to let go of his/her old shell shell it inhabits. Hermit crabs therefore rely on finding a and you’ll end up with a nude crab charging around desshell slightly bigger and better than their own in order to perately trying to figure out what to do, like the loser in a move up the housing ladder. Sometimes these shells are game of musical chairs. It was great behaviour but surprisoccupied by another crab, sometimes not, and sometimes ingly tricky to film – small and sensitive creatures and a a small crab comes across an empty shell that is too big behaviour that can go from nothing to completion in a few for it to move into. What’s really fascinating is that the seconds, but I think we got a really strong sequence. crab then ‘knows’ that waiting next to the empty shell is a good strategy as, sooner or later, the presence of that big We were lucky to be on the island with the nicest bunch of empty shell will probably set off a chain of ‘house moves’ people you could imagine. Randi Rotjan (who discovered that will result in an empty shell of a suitable size for it to the synchronous vacancy chain behavior) was absolutely move in to. fantastic, a brilliant advisor and great fun to work with.

It’s a really incredible behaviour and possibly unique to Within hours a large empty shell can have dozens of crabs hermit crabs and humans. We certainly couldn’t think of patiently waiting next to it, sometimes arranged in neat another species that forms these ‘vacancy chains’ – individuals queue in order to move up from a limiting resource to a more suitable resource.

The island was so lovely to work on; you wake up at sunrise, pull on swimming shorts, get some coffee brewing, and could be filming within five minutes. In addition to the very cool hermit crabs there were pelicans, a pair of ospreys, frigate birds and the bath-warm sea was filled with fantastic marine life.

Figure 1- Hermit crabs assemble around an empty shell.Photo: John Brown

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The BioCube Project David Liittschwager, Chris Meyer, and Seabird McKeon Few of us take the time to observe the variety of creatures that can be found on close inspection. But Earth teems with life, much of it largely unseen and small in scale, yet spectacular under magnification. Look carefully at a small corner of forest floor or a coral reef. Carefully turn over rocks lining a streambed, or watch flowers in a meadow,

alone manage, functioning systems when we only know a third of the pieces? Describing this diversity, documenting life on the planet, is the role of natural history museums.

Documenting complete ecosystems, however, is a daunting task. How can scientists study every species in a forest, on a reef, in a stream, or within a meadow? The scale is too large, but if you get too small, you lose important pieces of the big picture. So what scale captures enough variation, while accounting for the significant functions of the ecosystem? What are manageable, representative subsets to tackle?

Figure 2- The BioCube deployed on the reef near Carrie Bow Cay. Photo: David Liittschwager

and you’ll be amazed by what you see. The creatures in each of these small environments are interacting players that form the parts of vast machines—or ecosystems— upon which the health of the planet and its inhabitants depend.

The answer is “about one cubic foot”—a BioCube. Most of the world’s biodiversity occurs at small scales; organisms hidden in leaf litter, soil, and the nooks and crannies of environments. By focusing on a cubic foot of space, scientists can fully characterize complete representative communities to understand the interactions and predict Studying the species that make up an ecosystem is the first impending impacts on the larger environment (Figure 2). step in understanding how biological systems function and predicting the impact of change. Scientists have identified The concept of a BioCube—a cubic foot of space and and named only about one-third of the planet’s species, time observed over 24 hours—springs from collaborative and they estimate that at least 10 million more species Smithsonian research aimed at helping scientists develop await discovery. How are we supposed to understand, let 7

Figure 3- Just a few of the many fish and invertebrates found inside one cubic foot of coral reef. Photos: David Liittschwager

a better understanding of our biological warehouse so that we can make informed decisions about essential resources. By gaining a detailed picture one cubic foot at a time, scientists can begin to chart relationships between organisms and environments, infer what is not known or seen, model the impact of changes on those ecosystems, and build a body of data to compare with other environments.

In the past, scientists relied primarily on direct observation to understand ecosystems. Now, using DNA analysis, scientists can get a picture of the genetic makeup and diversity of an ecosystem, including organisms that are not visible to the naked eye. Computer modeling allows scientists to create, run, and manipulate simulations to predict the health and impacts on ecosystems due to loss or changes in biodiversity, environmental degradation, climate change, and other impacts.

Smithsonian scientists are actively involved in deploying and analyzing BioCubes, contributing to a body of data and knowledge that will help us understand and preserve life on earth. Working in conjunction with partner organizations, the Smithsonian is also pioneering the devel8

opment of BioCubes for education so that students and individuals can study their own backyards and local environments. The BioCube Project visited Carrie Bow Cay in November 2012 as a part of exhibit development in the Museum of Natural History’s Ocean Hall (Figure 3).

Long Term Ecological Research CARICOMP Report 2013 Karen Koltes and JohnTschirky Monitoring surveys and data collection were conducted in December 2012 and July 2013 under the Caribbean Coastal Marine Productivity Program (CARICOMP).

CARICOMP was launched at Carrie Bow Cay (CBC) in 1993 as part of a collaborative regional scientific effort among 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.

tion to the standard CARICOMP measurements taken at CBC, enhancements to the protocols continue with photodocumentation of coral reef transects, octocoral surveys to improve observations of population dynamics, in situ light intensity measurements and current flow monitoring in shallow and deep sites.

Over the past year, several of the laboratories in the CARICOMP network collaborated on the first regional synthesis of the nearly two-decades long record of measurements on growth and biomass of the dominant Caribbean seagrass, Thalassia testudinum (Figure 4). The analyses included 52 sampling stations at 22 sites (mostly adjacent to reef systems) across the Caribbean region. At Carrie Bow Cay, the semi-annual CARICOMP measurements are conducted at two shallow seagrass beds: a relatively low-energy site just east of Twin Cays (TC; depth = 1m) and a highenergy, back-reef area located just west of CBC (CBC; depth = 1.2m). Following the CARICOMP protocols, these sites were selected as representative of “high productivity” (TC) and “average productivity” (CBC) seagrass habitats for the central Belize barrier reef platform.

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. In addi- The region-wide analyses revealed wide variations among the CARICOMP sites. Annual productivity of leaves of Thalassia testudinum varied by an order of magnitude, from <200 g-dry/m2/y at Long Key (FL) to >2100 g-dry/ m2/y at Puerto Rico and Tobago. The two Belize sites fell mid-range at 1102 g-dry/m2/y (TC) and 858 g-dry/m2/y (CBC). Total community above-ground biomass also varied by an order of magnitude among stations, from 15 g-dry/m2 in Bermuda to 325 g-dry/m2 in Puerto Morelos, Mexico, with the Belize sites again falling mid-range at 136 (TC) and 83 (CBC) g-dry/m2. The highest total (above- and below-ground) biomass of T. testudinum was recorded from Barbados (2193 g-dry/m2) followed closely

by Twin Cays (2063 g-dry/m2). Seasonal variations in T. testudinum leaf productivity were observed at all latitudes > 16°N, including the two Belize sites.

Figure 4- Sorting seagrass samples for productivity analysis.

Photo: Karen Koltes

More than half (58%) of the seagrass communities at the long-term study stations, including Belize, showed changes consistent with degradation of the environment during the CARICOMP monitoring period. One measure of this is the density of short shoots (Figure 5). At TC, the density of short shoots has steadily declined since monitoring began. Decreases in the density of short shoots typically occur is response to declines in light levels and/or nutrient enrichment. Declining light levels are now well documented for Belize through the CARICOMP program. By contrast, short shoot density has increased at the CBC site 9

time to a base station located in Dangriga on the Belize mainland. The data is processed at the base station and assembled to form continuous time series data sets that are then uploaded via the Internet where it is immediately available for visualization and analysis on our web portal.

Due to a historical lack of monitoring over the entire Mesoamerican Barrier Reef, the environmental monitoring system (EMS) realizes a vision of Klaus Ruetzler, the founder of the CCRE program, to monitor conditions existing on the reef to serve not only as a baseline for comparisons of future conditions but also as an immediate resource for researchers, scientists, environmental managers and the public. The EMS is completely automated and requires no human interaction excepting quarterly maintenance and service visits to calibrate sensors, perform repairs, and implement upgrades.

Figure 5- Short Shoot Density at Twin Cays (1994 â&#x20AC;&#x201C; 2013) and Carrie Bow Cay (1997 â&#x20AC;&#x201C; 2013). Densities are based on the means of six 10x20cm quadrats deployed for 8-12 days twice yearly.

since monitoring began there in 1997. The increase may be due to recovery from extensive scouring of these beds following Hurricane Mitch in 1998, as short shoot density appears to have leveled off since reaching a peak around 2008-09.

In 2013, specific updates to the EMS included replacement of the datalogger battery as well as the entire lightning protection and electrical grounding system. In addition a new radio antenna and RF cables were installed to replace aging components. Oceanographic probes that measure water temperature, conductivity, and turbidity were replaced. An overhaul of the wind monitor (Figure 6) that began in 2102 was completed with the replacement of vertical shaft bearings and rotor, potentiometer (wind direction) and coil assembly (wind speed). These upgrades were performed as part of the regular maintenance program that is followed to maintain the highest quality data possible and to address any issues before they arise.

The environmental degradation over a relatively short time-span (6-18 years) at many sites is a worrying trend because many of these sites, including those in Belize, A significant improvement is the establishment of a VPN were considered to have received little or moderate human- (virtual private network) connection to the base station computer. This advance allows us to access and operate induced impacts when monitoring began in the 1990â&#x20AC;&#x2122;s. the computer remotely to check the status of data transmissions and reestablish transmissions in the event of CCRE Meterological and Oceanographic power outages or other events (such as automatic updates Monitoring Program requiring computer restarts) that may stop the computer from processing and disseminating the data. Previously Tom Opishinsksi we relied on employees at the local The meteorological and oceanographic monitoring pro- business where the gram initially established on Carrie Bow Cay in 1996 computer and base continued operation through 2013. A combination of station are located oceanographic (temperature, salinity, turbidity, water lev- to restart the sysel, pH, and dissolved oxygen) and meteorological sensors tem. This however (air temperature, wind speed/direction, relative humidity, was not always barometric pressure, rainfall, and solar radiation) operate convenient for the continuously to provide measurements of environmental employees and if conditions every 10 minutes. A datalogger records and an outage occurred Figure 6- Wind monitor at CBC. transmits the measurements by radio frequency in real 10

itoring program with a new platform for sea level monitoring. The new system is designed to meet requirements established by the international Global Sea Level Observing System (GLOSS) program for sea surface water level measurements to monitor sea level rise. As part of this effort we performed an analysis of 10-plus year record of water level data (>450,000 samples) to correct for water density and atmospheric pressure changes. A two-year time series of the corrected data set has been submitted to NOAA for a comprehensive analysis that precludes analysis of the entire data record. The data set is also being utilized Figure 7- Wind rose plot for December 2010.

by Smithsonian scientist Marguerite Toscano to benchmark peat cores taken on the weekend then the system would not be restarted unon Twin Cays with the goal of advancing our understandtil the next Monday when they returned. This also allows ing of historical mangrove response to sea level change. direct access to the datalogger for internal assessments and updates.

This exciting expansion of monitoring capabilities, supported by Smithsonianâ&#x20AC;&#x2122;s MarineGEO program, will include Data collected by the system continues to be analyzed to construction of a new offshore platform early in 2014. The expand the products available to users of the web porplatform will host multiple state-of-the-art vented water tal (http://nmnhmp.riocean.com). One such data prodlevel sensors and will be equipped with a satellite transmituct, introduced in 2011 and updated regularly as new ter to send data in real time to NOAA and to our web portal. data becomes available is the presentation of monthly Measurement sampling will be increased from the present wind rose charts (http://nmnhmp.riocean.com/windrose.

10-minute rate to 6 minutes. In addition, the system design php?siteIndex=0). A wind rose is a graphic chart used to will meet protocols for tsunami warning systems providing give a succinct view of how wind speed and direction are a crucial need for the Central American region. distributed at a particular location and for a specific time period. Viewed successively in chronological order the wind rose charts clearly illustrate seasonal patterns of the trade winds for the areas. In general the wind blows from a northeasterly to easterly direction from March through September and then transitions to northwest to north-northwesterly direction from October to February. Figures 7 and 8 illustrate these patterns for the months of December 2010 and July 2011, respectively.

Following the tradition initiated by Klaus Ruetzler to establish the first operational oceanographic and meteorological monitoring system on the Mesoamerican barrier reef we have initiated activities to expand our mon-

Figure 8- Wind rose plot for July 2011.

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Carrie Bow Acroporid Demographics

types after disease and coral bleaching episodes. Additionally, putative new sexual recruits, rare snail predation, and Nicole Fogartty, Scott Jones, Zach Foltz, limited 3-spot damselfish damage have been documented and Hunter Noren at this site. This unique data set allows us to better understand the processes that drive population dynamics of Acropora palmata and A. cervicornis were dominant shal- these threatened habitat-building corals, an important step low-water corals in the Caribbean for millions of years, in appropriately managing degraded reefs. yet over the past 30 years losses exceeding 97% of the population have led to the listing of these species as threatCCRE South Water Caye Marine Reserve ened under the U.S. Endangered Species Act. The losses of these species have profound effects on shallow Carib- Reef Assessment Program bean reef ecosystems and their associated biodiversity because of their rapid growth and the three dimensional Scott Jones, Randi Rotjan, Zach Foltz, Peter Gawne, structure they create for other reef organisms. Quantifying and James Dimond demographic traits is critical to understanding the ecology and evolution of an organism. Despite the ecologi- This year marks the third full year that CCRE staff and cal importance and evolutionary complexity of threatened collaborators from the New England Aquarium have hybridizing acroporid corals, their demographics are not implemented the South Water Caye Marine Reserve well understood, particularly in the Western Caribbean. In Reef Assessment Program. This project is directed June 2011, we established seven circular plots on a reef at assessing effects of the no-take conservation zone in Belize where every acroporid coral was tagged, pho- around Carrie Bow Cay on recovery of fish and coral tographed, measured, sampled for genotypic analysis, populations. Permanent transects were established in and assessed for threats (Figure 9). To document intra- June 2011 inside (12 transects) and outside (12 tranannual variation in demographic processes, these plots sects) the areaâ&#x20AC;&#x2122;s boundary. were resurveyed every four months and assessed for new asexual fragments and sexual recruits. In late summer, we Most monitoring plans measure the diversity and recorded annual reproductive effort and have documented abundance of key reef organisms; some of the best over 100 observations of tagged colonies spawning. Mic- programs also assess biomass of benthic reef builders rosatellite data revealed extensive genotypic diversity in and fishes. We have designed our program to assess A. palmata, low genotypic diversity in A. cervicornis and similar ecological metrics, so as to be cross-compatiA. prolifera (hybrid), and the overall loss of several geno- ble with historical and simultaneous efforts elsewhere in Belize and the western Atlantic Ocean. However, we have also added some innovative 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 (Figure 10).

Figure 9- Diver performing individual colony assessments on Acropora cervicornis. Photo: Scott Jones

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To date, 24 permanent transects have been surveyed six times, for a total of 144 transects, and results to date show that: • Hard coral cover is holding steady at ~10%, supported by data collected via 2 methods: transects and photoquadrat analysis • As of yet, there are no obvious reserve-level effects on benthic structure or fish populations.

Figure 10- Divers conducting coral transect assessments inside the South Water Caye Marine Reserve. Photo: Z. Foltz

Ecology & Evolution Corals Establishing a Captive Population of Caribbean Acroporids: Developing Ex Situ Conservation Techniques Mike Henley, Abby Wood, Mary Hagedorn and Alan Peters Zoos and aquariums serve as live genetic repositories for threatened and endangered species around the world, and the organisms maintained in these populations are educational ambassadors to their wild counterparts. With the well-documented decline in Caribbean coral populations and the subsequent addition of elkhorn coral (Acropora palmata) and staghorn coral (Acropora cervicornis) to

the endangered species list, it is imperative that zoos and aquariums help these struggling coral communities in much the same way that they aid declining mammal, bird, reptile, amphibian, plant, etc. populations.

While coral bleaching, ocean acidification, overfishing, pollution, runoff and other anthropogenic-induced environmental changes continue to stress reefs, coral disease – likely fueled by these stressors – has the potential to quickly wipe out coral populations within weeks to months of an outbreak. At the time of this writing, during the 2013 coral spawning field season, much of the staghorn coral on the Carrie Bow reef was ravaged by coral disease. It is important to secure this genetic diversity (from here and other parts of the Caribbean) before it is lost. Some of this work has already been completed. In 2011, Dr. Mary Hagedorn was able to successfully cryopreserve the embryonic stem cells of these threatened corals. However, to date we do not have any Belizean elkhorn or staghorn coral in captivity.

This year’s field season began in January 2013 when Abby Wood (photographer and NZP volunteer) and the author traveled to Carrie Bow Cay (CBC) to begin the conditioning of our coral recruit settlement tiles. In addition to placing the tiles in seawater six to seven months in advance to “cure,” we also implemented a new strategy – harvesting a known preferred settlement cue, the crustose coralline algae (CCA) Hydrolithon boergesenii from the reef – and gluing it to our settlement tiles. The grids of tiles were then secured in two pvc/mesh crates and tied to the reef in two locations – one on the CBC reef and the other in the lagoon area on the east side of the island (See Figure 11). This was done with the hope that a known settlement cue – the CCA Hydrolithon – would have a “head start” and grow on/encrust our settlement tiles to make those tiles an “ideal” location for larval coral settlement. Upon our return to CBC this July, we found that in many cases the Hydrolithon had taken hold and began encrusting our tiles. However, the tiles placed in the lagoon area east of the island had a much higher rate of turf algae coverage (these coral larvae often avoid turf algae). If this experiment is repeated again, both crates will likely be placed on the CBC house reef or on the reef wall.

This year, the full moon (and anticipated possible early spawn) had us returning to CBC for the acroporid spawn in late July. At day five after the full moon, we finally collected our first samples of Elkhorn larvae (See Figure 13).

Night six saw more elkhorn spawning and collection, with very minimal staghorn. Since the staghorn bundles were 13

spawning on the CBC reef, so part of our team spent nights three through eight monitoring Curlew Reef for spawning.

Night eight after the August full moon saw staghorn and elkhorn corals spawning, but only a few hundred bundles of each were collected, and both were from a single colony of elkhorn and staghorn. Therefore, we mixed the two together and settled them as the hybrid fused staghorn coral (A. prolifera). After rearing the larvae for four days, we placed approximately 200,000 elkhorn larvae (A. palmata) and a few hundred fused staghorn larvae into separate settlement bins with our conditioned tiles.

The recruits from the late July spawn remained at CBC in the seawater system the entire time and, happily, have begun to acquire their endosymbiotic zooxanthellae, without which they cannot live (Figure 12). With the extra time spent in “captivity” in the CBC seawater system, we are hoping that since they will be more established before making the long journey back to the zoo in Washington, D.C., they will be slightly more robust and able to survive the journey, while the settled larvae from the August spawn will have about two weeks to settle in to their new homes. All settlement tiles will be counted at three months

Figure 11 - A PVC crate housing settlement tiles being conditioned in the lagoon behind the Carrie Bow lab. Photo: Abby Wood

from the same clone (the same genotype), none of these larvae survived; however, staghorn eggs were crossed with elkhorn sperm that night to create larvae of the hybrid, fused staghorn coral (A. prolifera). Four days after fertilization, the larvae from the two species were placed in separate settlement bins with the tiles from the reef, and approximately 2,000 elkhorn and 300 fused staghorn larvae settled.

Unfortunately, the corals did not spawn nearly as much as we had hoped, leaving us with fewer larvae than needed (and no Staghorn larvae) and believing this spawning season might be a “split spawn.” Rearing corals past settlement to growing juveniles and eventually thriving adults is a “numbers game.” Mortality is extremely high postsettlement, and one ideally needs to begin with thousands of recruits to possibly ensure that there will be survivors after the three to four month initial die-off. Therefore, we returned to CBC for the late August full moon where the elkhorn corals on the CBC house reef spawned on the second night after the full moon, leaving us rearing approximately 500,000 larvae. The staghorn corals were still not 14

Figure 12- Newly settled Acropora corals on CCA substrate.

Photo: Abby Wood

Twilight Reefs May Usher In a New Dawn for Depauperate, Shallow Reefs Nicole Fogarty and Hunter Noren Coral reefs are among the most diverse and productive ecosystems on our planet.

Unfortunately, over the last few decades, many shallow water coral reefs have experienced a drastic decline. Due to their proximity to populated coastlines and exposure to extreme temperatures and storms, shallow reefs are declining at a greater rate than their deep water counterparts. This increased mortality likely limits shallow reefs capacFigure 13- Large numbers of gametes are in the collecting tube as well as floating ity to reproduce and recover from humanin the water column during a spawning event. Photo: Abby Wood induced stress. In order to maintain biomass, it has been proposed that shallow reefs may to assess survival rates. Only time will tell. require an outside reproductive source of larvae, such as deep water (mesophotic) reefs. This idea, We owe thanks to several people who continue to make termed the ‘deep reef refugia’ hypothesis (DRRH) has rethis project a reality. The CCRE and Smithsonian Marine cently gained popularity and due to advances in SCUBA Station personnel, Zach Foltz (station manager), Val Paul, diving techniques, we now have the ability to explore the Scott Jones, Jenny Sneed, and Nikki Fogarty (Assistant complex interactions that occur between deep and shallow Professor at NOVA Southeastern University) were a tre- reefs. Mesophotic (or “twilight”) reefs defy this definition; mendous help to us as always. My unbelievably patient, they are coral assemblages that inhabit depths beginning understanding and supportive supervisor, Alan Peters, and around 100 feet deep and extending down to the limit of coworkers Tamie Dewitt, Donna Stockton, Michael Miller light penetration, which can be deeper than 300 feet. and Ish Ganame, who held down the fort while I was away – for TWO spawning seasons this year. I always rely on Despite low light conditions, many corals appear to thrive Mary Hagedorn for answers to questions and knowledge in the mesophotic environment, and in many locations, regarding coral spawning and various techniques. Thanks these mesophotic reefs are healthier than their shallower to Abby Wood, an amazing photographer and diver, who is responsible for all the images and video collected during this project and for working with the National Zoo’s Communications department (Pamela Baker-Mason, Devin Murphy and Jen Zoon) to spread the word and help tell the story of our work. And finally, to our supporters Dr. Ken Hintz of George Mason University and WAMAS (Washington Area Marine Aquarist Society) for their continued funding of this project: without your support, this project would simply not be possible.

Figure 14- Authors N. Fogarty and H. Noren conduct fertilization experiments in the dark to prevent disturbing captive corals that have yet to spawn.

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spawned? This study has focused on the boulder star coral, Orbicella franksi (previously Montastraea). (Figure 15) Preliminary results demonstrate the shallow and deep O. franksi are compatible, but larvae generated from deep O. franksi corals (100’) prefer to settle on tiles conditioned at shallower depths (60’). This supports the DRRH and provides hope that depauperate shallow reefs may be seeded by deeper corals. (Figure 14)

Investigating the Role of Bacteria in the Recruitment Ecology of Coral Larvae

Figure 15- Orbicella sp. coral ready to release gamete bundles.

neighbors. There are two ways mesophotic corals can assist in the recovery of shallow water corals: 1) provide gametes to mix with limited shallow water gametes resulting in enhanced fertilization success, or 2) provide larvae that recruit to the shallows. Because of the relatively easy access to the upper limits of the mesophotic zone (100130’), and its proximity to shallower reefs, we chose to start our study at Carrie Bow Cay to try and answer the following questions: (1) Are corals in the mesophotic zone “healthier” than their shallow counterparts? (2) How closely related are mesophotic and shallow water corals?

(3) Are mesophotic coral gametes viable and capable of fertilizing conspecifics within the mesophotic and at shallower depths? (4) Is fecundity related to depth? (5) Do the resulting larvae generated from mesophotic and shallow corals prefer their parent’s habitat? (6) Are larvae better adapted to survive in the habitat from which they were

Jennifer Sneed, Koty Sharp, Jay Houk, and Valerie Paul Coral reefs are declining worldwide and one key to the survival of endangered coral species is their ability to recruit to appropriate surfaces during the larval settlement stage of their life cycle. Over the past several years we have been investigating the ways that coral larvae choose settlement substrata and have determined that bacterial biofilms may be important in the selection process. We have recently identified a chemical cue, tetrabromopyrrole (TBP), produced by the biofilm bacterium Pseudoalteromonas sp. PS5, that induces settlement in multiple Caribbean coral species. At Carrie Bow Cay we tested this compound for its effects on the settlement of two spawning corals, Acropora palmata and Orbicella (formerly Montastraea) franksi.

We found that the compound induced as much larval settlement as the crustose coralline alga (CCA) Hydrolithon boergesenii, which has been identified as a facilitator of settlement for some corals. O. franski larvae responded to concentrations of TBP ranging from 125 – 250 ng/ml. A. palmata larvae were more sensitive to the compound than O. franksi, responding to concentrations as low as 12.5 ng/ml. We monitored the settled A. palmata larvae for four weeks and determined that exposure to TBP did not affect the post-settlement survival of the juvenile corals. After four weeks, many of the juvenile corals had taken up zooxanthellae and were beginning to develop new polyps.

Figure 16- Experimental chambers are placed on the reef to investigate patterns in coral larval settlement.

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Because many coral reefs worldwide are undergoing phase shifts from coral-dominated to algal-dominated ecosystems, our lab has also been investigating the effects of this shift on the

of macroalgae on the reef will impact corals during early life history stages.

High-Definition Benthic Image Map Surveys: A Giga-view of the Ocean Laurie Penland Coral reef health assessment has relied on benthic photographic surveys as an essential measurement tool for decades. The emergence of gigapixel (one billion pixel) image technologies makes possible the creation of high-definition benthic image map surveys (HDBIMS). These image maps provide the traditional overall percent coverage data. In addition, they allow zoom capabilities in Figure 17- Settled coral larvae, called â&#x20AC;&#x153;spat,â&#x20AC;? begin to resemble adult coral within days. such detail that scientists can, for example, count the polyps on a coral head. While the recruitment of coral larvae. This summer at Carrie Bow image maps are easily viewed over the internet, they we set up experiments looking at the effects of macroalgae on the bacterial flora associated with newly settled corals are challenging to produce. Numerous previous studies and their settlement substrata. We settled A. palmata lar- have contributed to the advancement of high-definition vae on pieces of the CCA H. boergesenii (Figure 17) and benthic survey methods. This ongoing HDBIMS study is then attached clumps of either Dictyota sp. or Halimeda focused on production methods that 1) produce the best opuntia. We exposed the settled larvae and CCA to algal image quality for the lowest cost, 2) provide accurate and treatment for 48 hours in settlement chambers on the reef repeatable results at any depth over time, and 3) utilize (Figure 16). After 48 hours, we took samples of the larvae inexpensive off-the-shelf (OTS) stitching software that and the CCA biofilms and submitted them for next-gen- allows accurate results that can be reviewed in the field. eration sequencing to determine whether these macroal- This structured approach to image acquisition, integrated gae alter larval and CCA associated bacterial communi- with the OTS grid-oriented stitching software produces ties. These data will help us understand how the presence highly accurate benthic image maps.

Figure 18- Top: A.) Overall section of reef with ARMS installation shortly after deployment. Bottom: Detail images from A.), B.) Transect tape next to coral head, C.) Lettuce Coral and algae, D.) Polyps detail on Boulder Star Coral, E.) Soft Corals and cryptic Goby, F.) Small Fish and soft coral near newly deployed ARMS.

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The first trial of HDBIMS methods occurred at Carrie Bow in October of 2012. These initial tests were conducted at Autonomous Reef Monitoring System (ARMS) deployment sites on the lagoon side of Carrie Bow Cay (Figure 18). Four transect tapes were placed in a 5x5 meter perimeter that surrounded deployed ARMS. Two weighted belts with surface signals and dive computers to measure depth were deployed at the west end of the north and south sides. The surface signals were raised to a depth where their base was two meters above the bottom. A dive line was run between the bases of the surface signals. The diver with the camera followed this dive line from the south end to the north end of the site, photographing the reef in a downward facing position. Once photography of a row was completed, the weighted belts were moved 1/2 meter to the east, and the photographic process was repeated.

This method required two divers and one dive to complete. The entire process, from the laying of the transect tapes to site clean-up, was completed in approximately 60 minutes.

problems were identified to allow for corrections in image acquisition methods while still in the field.

Results of these initial HDBIMS tests proved both that the concept works and that the image maps are achievable within reasonable costs. However, one test determined that it is difficult to keep the dive line on target in a very strong current. This directly affected the image stitching. It was decided a more structured approach should be pursued. The next set of increased structured trials will occur in October of 2013.

See http://www.si.edu/dive/hdbims.htm for ongoing results of this study.

Ecology of Coral Disease and MicrobeMicrobe Interactions on Coral Surfaces Max Teplitski

Corals are crucial to the health of reef ecosystems and Once back at the lab, images were downloaded onto sustainability of the surrounding human communities. an external drive for storage and processing. To vali- Coral reefs around the world, and especially in the Caribdate results while in the field, multiple OTS stitching bean, are under increasing stress. Global climate change, applications were tested on the images with the field overfishing, and terrestrial run-off are just a few of the exlaptop. While the field laptop proved too slow to cre- amples of such stressors. When stressed, corals become ate an entire image map, sections were constructed and susceptible to infections with pathogens, which may result in dramatic, ecosystem-wide outbreaks of coral diseases. While coral diseases are common in ecosystems around the world, there are uncertainties associated with the question of what exactly causes them. Most scientists, however, agree that coral diseases are similar to those of other organisms and can be explained by the “Disease Triangle” model. This model postulates that the host must be in a physiological state that makes it more susceptible to the infection, a pathogen must be present and the environmental conditions must favor the disease progression.

As it relates to corals, the Disease Triangle model is complicated by the fact that corals are “holobionts”. Holobionts are multi-partite symbiotic Figure 19 - Two photos of the same Mustard hill coral, exhibiting symptoms of disease, taken 8 months apart, showing progression of disease and tissue mortality. organisms formed by the animal (coral polyp), dinoflagellate algae 18

that reside within coral cells (and supply it with carbon fixed through photosynthesis), bacterial and viral associates of polyps and dinoflagellates. Over the last decade, significant advances have been made in characterization of the microbial interactions on coral surfaces. It is now clear that microbes can have both positive and negative effects on coral health and resistance to various stressors.

The goal of this project is to characterize how interactions between coral pathogens and native bacteria play out under natural conditions.

The Carrie Bow Cay Field Station is perfectly positioned to study coral diseases and also interactions between native coral-associated beneficial bacteria and potential pathogens. In fact, some of the most devastating coral diseases were first characterizing there. The goal of this project is to continue the characterization of interactions between pathogens, corals and their associated native microbial communities.

BBD spreads fast, devastating boulders within only a few months. Images of tagged corals were take eight months apart: the black band is apparent in the image on the top, on the border of the denuded skeleton and healthy tissue.

Eight months later, almost the entire colony is consumed by the disease consortium. Thus, a better understanding of what causes this disease is needed in order to develop more effective pro-active management approaches for controlling it.

The goal of this project is to characterize chemical interactions within the BBD consortium to determine how

A novel disease of Mustard Hill Coral (Porites astreoides) Mustard hill coral is commonly considered a “weedy” coral, often colonizing surfaces that are unsuitable for other corals. In fact, some have hypothesized that once stands of most other corals have declined due to environmental stresses and diseases, reefs would be dominated

by Porites spp. However, this discovery of a disease on P. astreoides indicates that this coral may be more vulnerable to infections than previously thought. As shown in Figure 19, the disease begins as a yellow biofilm (narrow band), preceded by a large bleached zone. The coral tissue appears completely removed behind the band. The two images of the same coral colony were taken 8 months apart. Our current research focuses on understanding whether a specific pathogen causes the disease symptoms, or whether this is a consortium of pathogens or whether the observed symptoms are due to the members of the native microbial communities “switching” from the benign (commensal) existence to cause a disease due to environmental stress.

Interactions within the Black Band Disease consortium

Figure 20 - The same colony of boulder star coral, Orbicella faveolata, taken 8 months apart., showing the progression of BBD.

pathogens within the consortium communicate with each other, with native coral microorganisms and with the coral Black band disease (BBD), a multi-species consortium itself. To this end, we have collected samples of the disdominated by cyanobacteria, was first described in Carrie ease consortium from a dozen corals at various stages of Bow Cay in the 1970s. Since its discovery there, BBD the diseases. Molecular and chemical characterization of was found world wide, affecting corals in the Caribbean, these samples is currently ongoing.

Red Sea and the Indian Ocean. As shown in Figure 20, 19

we could, although an overly friendly (and very hungry) nurse shark patrolling the reefs just off the station sometimes made lionfish collections difficult.

Developing a Model for Transmission of an Infectious Disease of Marine Sponges Deborah J. GocIfeld, Julie B. Olson, Julia Stevens

Figure 21- Barrel sponge (Xestospongia muta) exhibiting disease and tissue mortality.

Sponges Developing a Better Understanding of Symbiotic Interactions in Marine Sponges

Sponge diseases are increasing worldwide, but no models of sponge disease dynamics have been produced. The increasing prevalence and diversity of diseases affecting marine systems highlight the need to develop new tools to test hypotheses related to disease spread and impacts on populations and communities. We aim to develop a disease transmission model for Aplysina Red Band Syndrome. Our specific aims are to: (1) characterize the pathogen(s) responsible for ARBS, (2) identify potential environmental reservoirs and/or vectors for transmission of pathogens to the sponge Aplysina cauliformis, and (3)

Christopher Freeman In the marine environment, symbiotic interactions are exemplified by mutualisms between diverse benthic invertebrates and microbial and algal symbionts. Surprisingly, our understanding of these interactions and factors structuring them or leading to their disruption is largely restricted to certain taxa. With their nutritional diversity and flexibility, marine sponges are crucial to nutrient cycling and productivity in the benthic environment. In recent years, however, reports of disease outbreaks, bleaching events, and unexplained mortality in sponges have increased, suggesting that, under certain conditions, these symbioses may be shifting or breaking down. To determine how anthropogenic change through human development is impacting these symbioses, I am assessing these interactions in 10 common Caribbean sponges across a Caribbean-wide gradient of impacted to pristine reefs. Using stable isotopes, I am able to determine whether host benefit (in the form of symbiont-derived C or N) increases or decreases under certain conditions. Interestingly, during recent collections at Carrie Bow, one of my pristine sites, I observed the remnants of recently deceased and collapsed giant barrel sponges (Xestospongia muta) and colorless or bleached Callyspongia plicifera on reefs close to the station and surrounding Gloverâ&#x20AC;&#x2122;s atoll (Figure 21). Research into whether this mortality is due a breakdown or shifts in symbiotic interactions at these sites is underway. In our free time, we speared and consumed as many lionfish as 20

Figure 22- Aplysina Red Band Syndrome on Aplysina cauliformis.

the abundance of its primary host, A. cauliformis, but is not correlated with other measures of sponge, coral or gorgonian diversity. In spite of a reported sponge mortality event on the Carrie Bow Cay forereef in 2011, our surveys on patch reefs indicated that overall sponge number and diversity did not differ significantly between 2008, 2009 and 2012. In fact, A. cauliformis and A. fulva density increased significantly between 2009 and 2012. ARBS was slightly more prevalent in 2012 than during our earlier surveys.

We also established a 10 x 10 m2 grid on each of two patch reefs and the whole grid was photographed in 1 x 1 m2 increments to create a photomosaic. Within each grid, every A. cauliFigure 23- Every A. cauliformis within a 100 m2 grid was measured in situ to formis was mapped and measured (Figure 23), determine frequency of contact with neighboring sponges. and the number of ARBS lesions was recorded on a map, so that spatial statistics can be used use spatial demographic data to develop a conceptual to characterize the dispersion pattern and transmodel of ARBS transmission at the population level. missibility of the disease on the reef. These data will be Aplysina Red Band Syndrome (ARBS; Figure 22) is an in- compared to a model developed with similar data from the fectious disease affecting Caribbean sponges of the genus Bahamas to determine whether it is possible to model the Aplysina. ARBS is widespread throughout the Caribbean, prevalence of ARBS across the Caribbean basin. and we previously reported it from the patch reefs near Carrie Bow Cay (CBC), Belize, in 2008 and 2009. The Using SCUBA, spongivorous fishes (angelfishes, filefishpresent study enabled us to revisit and re-survey several es, pufferfishes) were collected with hand nets and transpatch reefs near CBC for the presence and abundance of ferred to large plastic bags. In the boat, swabs of the oral this disease, and assess the potential mechanisms for dis- cavities of the fish were taken and placed into RNALater ease transmission in the environment. Samples of Aply- for molecular microbiological analyses. All fish were then sina sponges affected by ARBS, as well as sediment, am- returned to the reef. Samples of the ambient water and bient water, and swabs of the oral cavity of spongivorous sediment were also collected and preserved to determine fishes were collected for molecular, microbiological and whether these may serve as reservoirs for potential pathochemical analyses to identify potential reservoirs and/or gens. vectors for pathogen transmission.

Six 10 x 2 m transects were previously established on each of three patch reefs near Carrie Bow Cay and biodiversity surveys were performed for comparison with surveys conducted in 2008 and 2009. On each transect, a combination of point intercept and band transects were performed to assess percent cover of all substrata, and abundance and diversity of sponges, corals and gorgonians. In addition, the condition of each Aplysina sponge was recorded. ARBS was found to affect both A. cauliformis and A. fulva on the survey reefs, but at a lower frequency than at our study sites in the Bahamas. For example, we found ARBS on 3.2% of A. cauliformis in Belize compared to 6.6% in the Bahamas in the same period. Preliminary analyses suggest that ARBS abundance is correlated with

Sponge Mortality and Meager Recovery on the Belize Barrier Reef Janie Wulff

We have been mapping, identifying, and measuring (volume) all sponges on a set of shallow patch reefs in the Blue Ground Range at yearly intervals beginning in 2006, allowing us to quantify sponge community dynamics with respect to sponge biomass, number of individuals, and species. Embedded in these data are also population dynamics of 54 sponge species. Sponge mortality associated with a dense phytoplankton bloom on the southern portions of the Belize Barrier Reef in late summer 2011 was extreme, with 71% of the sponge volume lost (Figure 24) 21

size as they reorganized around the wounds we inflicted, and other individuals did not regenerate at all. Although sponges are masters of regeneration and recovery of sponge populations after environmental disasters is definitely more rapid by regeneration than by recruitment of larvae, our data indicate that regeneration is not cost-free or fool-proof.

Crustaceans Decapod Biodiversity of Carrie Bow Cay and Vicinity; Surveys and Guidebook Production Figure 24- This vase sponge (Niphates digitalis) is regenerating after partial mortality thought to be caused by a harmful phytoplankton bloom.

In the course of analyzing the data related to this mortality event we discovered that a significant mortality event had also occurred in 2008, when 49% of the sponge volume had been lost. Rapid healing of partially killed sponges, combined with rapid disarticulation and utter disappearance of skeletons of dead sponges, had entirely obscured this substantial earlier mortality. Recovery after the 2008 mortality was only 52% before the 2011 mortality, resulting in an overall decline in the sponge volume of 74% between 2006 and 2011. Evaluation of very early recovery after the 2011 mortality suggests that because a large proportion of the mortality consisted of partial mortality of large massive sponges, recovery may be aided by regeneration of these sponges. Differences in response among sponge species, ranging from complete loss to no effect, have resulted in striking changes in community structure, and consequently changes in the degree to which various key ecosystem roles are played by sponges.

Darryl Felder, Rafael Lemaitre, Heather BrackenGrissom, Thomas Shirley, Brent Thoma, Jana Thoma, Jennifer Howell Felder Field work was limited to a one week trip October of 2012. Collections were focused primarily on and immediately around Carrie Bow, Twin Cays, and shoals along South Water Cay. Targeting previously under-sampled substrates and microhabitats and broadening methodological approaches, the investigators substantially augmented collection holdings required for production of a proposed regional color-illustrated checklist, originally begun by Darryl Felder and the late Raymond Manning in the early 1980â&#x20AC;&#x2122;s.

Growth and Regeneration of Sponges on Coral Reefs and Mangroves Janie Wulff and Kelly Vasbinder Motivated by the importance of regeneration in the recovery of sponges that have suffered partial mortality, we wounded sponges of five common species and compared their regeneration and growth rates on coral reefs vs. mangroves (Figure 25). Regeneration rates varied by species, and although for one species they were as rapid as full recovery within one week, the wounds were still evident for other species after two and a half months. Regeneration was not limited to replacement of the removed tissue, and sometimes involved production of new oscules at the wound site, especially by individuals on the reef. Some individuals diminished in 22

Figure 25 - Diverse assemblage of sponges inhabiting mangrove prop roots.

ples of which are attached to this report (Figures 26 & 27). As to be expected, a number of systematic problems have arisen in the course of identifying collections from the area, some of which have been resolved in recent publications.

Others require additional work, such as currently underway on regional materials of Hexapanopeus, Lobopilumnus, Pagurus, Tumidotheres, several genera of mithracid spider crabs, gebiidean mud shrimp, and several groups of caridean shrimp.

Progress was also made on other project elements, including the continued accrual of sequence-quality tissue samples for molecular phylogenetic analyses of Figure 26 - Small porcelain crab, Petrolisthes jugosus, from the reef crest in front of burrowing axiidean mud shrimp, paguCarrie Bow Cay roid anomuran crabs, intertidal porcelain crabs, majoid spider crabs, xanthoid mud Following a long haitus after the original effort, materi- crabs, and pinnotherid commensal crabs, all under conals accumulated slowly through additional field efforts by tinuing study even though initial results are appearing in the late Brian Kensley, though they for the most part re- publication. Return to several sites near Carrie Bow also mained and sometimes unsorted on holding stacks of the allowed continued monitoring of the non-indigenous porNMNH. Over the last year, through the efforts of Rafael tunid crab, Charybdis helleri. While populations of this Lematire, these have now been entered into the EMu da- aggressive species appeared to expand rapidly after initial tabase, at least to family level. Our own field work on discovery, 2012 observations indicated that populations the project was reinitiated in 2002, and trips that followed have not resurged from a decline first noted in 2011. in 2007, 2009, 2011, and 2012 have contributed extensively to a collection of color photographs specifically from the Carrie Bow Cay vicinity. These are proving to be of tremendous value in comparative study of decapod crustacean populations throughout the western Atlantic, as well as for potential use in the regional guidebook for Belize decapods. The latter effort is now being undertaken as a collaboration between Darryl Felder and Rafael Lemaitre and Sam De Grave, and almost 4000 color photographs have been accumulated for use specifically from the Carrie Bow Cay region. Over 800 of these photographs were added by Figure 27- Small spider crab Mithrax tortugae, collected from rubble near Carie Bow Cay. This species is under revision, generic reassignment currently in press.

Darryl Felder in 2012, sam23

Additional work is required on and around Twin Cays and Carrie Bow Cay to more comprehensively represent the decapod fauna in the envisioned guidebook. Additional intertidal arrant collections (day and night), seine sampling of appropriate shallow substrates, shallow subtidal snorkeling, and shallow SCUBA sampling will be required.

This is essential in part to assure adequate coverage of caridean fauna, now that we have committed to inclusion of this group in the field guide. For all the accessible decapods, however, we seek to reach asymptotic levels in species richness measures, though for now we continue to add taxa higher than anticipated frequency. Work underway continues to include description and naming of new taxa, as this must be completed in advance of the regional guidebook.

Investigating the Influence of Refuge Availability on Mangrove Herbivory Dynamics Megan Riley and Ilka C. Feller Foraging behavior is often influenced by a combination of food quality and environmental constraints, such as predation pressure and refuge availability. For instance, organisms experiencing high levels of perceived predation risk may elect to remain close to shelter, potentially compromising the quality of their diet in order to lower the possibility that they will encounter a predator. On the other hand, individuals under low predation threat may forage further afield in search of higher quality food items. In

Figure 28- Mangrove tree crab, Aratus pisonii.

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Figure 29- Mangrove root crab, Goniopsis cruentata, potential predator of A. pisonii.

habitats with high predation risk, variation in refuge availability can significantly affect consumer diet choices and lead to cascading impacts on community dynamics.

We were interested in how spatial heterogeneity in refuge availability influences patterns of herbivory by the mangrove tree crab Aratus pisonii (Figure 28). This species of arboreal grapsid crab is a major consumer in neotropical mangrove systems. It is amongst the most abundant animals found in Caribbean and Floridian mangroves, where it is the dominant folivore of the red mangrove Rhizophora mangle. As such, its herbivory is a key link between primary production and the detrital food web. However, these crabs do not feed exclusively on plant material. Like many other mangrove crabs, they are omnivores and preferentially consume high quality food items such as insects and other crabs rather than the plant material abundant in their habitat. Recent evidence indicates that this opportunistic inclusion of animal material in their diet significantly improves their physiological condition and reproductive effort.

We investigated the potential impact of refuge availability on the intensity of nearby herbivory by A. pisonii. The dwarf mangroves on Twin Cays provide an excellent opportunity to investigate this topic. A. pisonii in tropical mangroves such as those on Twin Cays face intense predation pressure from a variety of terrestrial and marine sources, including birds, fishes, and other crabs (Figure

29). However, herbivory by beetles and other wood-boring insects, which girdle branches and cause extensive loss of yield, has left trees riddled with tree holes that serve as potential refuges for crabs. We set up 10m x 10m experimental plots, measured tree characteristics, and categorized the presence, absence, and proximity of tree hole refuges for all R. mangle within the plots. We also surveyed A. pisonii density and collected leaves from trees for image analysis of leaf herbivory. As an additional ongoing component of this study, we experimentally manipulated refuge availability by deploying artificial â&#x20AC;&#x153;tree holeâ&#x20AC;? refuges in dwarf red mangroves with no lifetime evidence of A. pisonii folivory. Preliminary analyses indicate that the presence of a tree hole refuge significantly increases A. pisonii folivory on that tree and adjacent red mangroves. The results of this study will elucidate the mechanisms underlying spatial folivory patterns of a dominant herbivore in neotropical mangroves. Because mangrove herbivores can shape forest structure, influence nutrient dynamics, and alter primary productivity, this work also has broader implications for the entire mangrove community.

Mangroves Carbon budgets of Caribbean Mangrove forests LoraĂŠ Simpson and Ilka Feller Mangrove forests are important sinks of carbon throughout the tropics and subtropics due to their high carbon stores and high carbon burial rates. These observations have led to a heightened level of interest in conserving and restoring mangroves for their carbon values. However, there are very few detailed carbon budgets available for mangrove forests. Over the past several years, we have been studying the carbon dynamics of Twin Cays in efforts to formulate a carbon budget for the mangrove forests of Belize. Our aim is to increase the knowledge of the global variation in mangrove carbon budgets and the understanding of the factors giving rise to variation in carbon stocks, rates of carbon burial and the role of mangrove forests in supporting productivity of the coasts on which they occur.

Figure 30- The author recording soil respiration data at Twin Cays, Belize.

ing habitats (Figure 30). Nitrogen and sucrose had little to no effect on soil respiration, however phosphorus (P) increased CO2 efflux by 60% in both scrub and fringing forest habitats, indicating phosphorus limitation of the microbial community. Phosphorus limitation of the microbial community has been suggested previously in other mangrove forests and addition of phosphorus increased decomposition of standardized cotton strips at this site.

The addition of excess phosphorus may lead to increased decomposition of soil carbon and thereby reduce rates of carbon burial. Our experiment provides some evidence that decomposition may be limited by the availability of phosphorus at this site which may reduce decomposition and enhance carbon burial.

Soil respiration, the total CO2 efflux from the soil surface, is an integral part of any carbon budget and will likely be altered by nutrient enrichment brought about by global climate change. We used short term experiments to test for variation in soil respiration with the addition of nutrients and a labile carbon source in both scrub and fring25

Fish Conservation Status of Halichoeres socialis, the Most Threatened Marine Fish in the World.

Luiz Rocha and Carole Baldwin Note: Dr. Rocha was invited by the New York Times to blog for their series "Scientists at Work." He submitted five posts before, during, and after his trip, the following is an excerpt from his first post (http://scientistatwork. blogs.nytimes.com/2012/12/12/to-save-a-coral-reef-enabler/): "Belize is home to a portion of the largest barrier reef in the Caribbean, the Mesoamerican Barrier Reef System.

Hundreds of species of fish inhabit this diverse coral reef system, many of them unique to the region. This week I will conduct field work there, joining forces with a team from the Smithsonian Institution led by fish curator Carole Baldwin.

Our team will look specifically at the population status and habitat conditions of the social wrasse, Halichoeres socialis. (Figure 31) But why pick this one species from the hundreds to be found there? The social wrasse is currently listed as “critically endangered” (the highest threat category) in the International Union for Conservation of Nature Red List of Threatened Species. There are two reasons the social wrasse is listed as critically endangered: it has a very small geographical range, and the quality of its habitat has continued to decline in the face of acceler-

Figure 32- Invasive Pacific Lionfish, Pterois volitans

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Figure 31- The Social Wrasse, Halichoeres socialis, an endemic species to the Pelican Cays, Belize.

ated coastal development.

Now a new threat looms, the invasive lionfish (Figure 32). This voracious predator is native to the Indo-Pacific, but during the mid to late 1990s the first lionfish were spotted in Florida…[and quickly spread throughout the Caribbean].

In December 2012 we speared 51 invasive Pacific lionfish in the Pelican Cayes and surrounding areas and analyzed stomach contents using a combination of morphological and genetic techniques. Halichoeres socialis represented 46% of the prey items investigated, and was present in 18 (41%) of the 44 stomachs with contents. Numbers of social wrasses in individual lionfish stomachs ranged from one to 18, with many stomachs containing 2-4 wrasses.

Lionfish are voracious predators and are known to consume up to 20 reef fishes in 30 minutes.

Our results suggest that the critically endangered social wrasse is the most important item of the lionfish diet in the Pelican Cayes area of Belize’s inner barrier reef. Similar studies conducted throughout the Caribbean suggest that wrasses and gobies are often among preferred lionfish prey, especially species that, like social wrasse, school, hover just above the bottom and range in size from 10 to 30mm. Although most other Caribbean wrasses are consumed by lionfish only as juveniles due to their large adult sizes, both adults and juveniles of Halichoeres socialis are within the preferred size range of lionfish prey. In addition, lionfish are present in the entire depth range (1-9 m) and in all habitats (reefs, sea grass, and mangrove) where social wrasses are found. The combination of negative

impacts caused by invasive species and habitat degradation has been identified as a leading cause of extinctions of fishes, and both agents of environmental change are currently impacting Belize. The social wrasse is endemic to the Pelican Cays, Belize, and such a restricted distribution may heighten the negative impacts on this species.

I seek to better understand how boring and fouling invertebrates affect mangrove growth and morphology in brackish and marine systems. Using surveys of red mangrove shorelines, I am presently examining how the presence of woodborers and fouling invertebrates relates to mangrove root breakage and morphology. In brackish systems, I am comparing the growth rates of Dr. Rocha's remaining blog posts can be viewed here: roots open to colonization by boring isopods and caged roots designed to exclude isopods. In marine mangrove http://scientistatwork.blogs.nytimes.com/2012/12/17/for- sites, I am testing how root growth and morphology the-social-wrasse-news-good-and-bad/ may be related to colonization by fouling invertebrates. http://scientistatwork.blogs.nytimes.com/2012/12/18/em- Furthermore, I am replicating these surveys and experibracing-the-pain-for-science/?_r=0 ments in multiple sites throughout Florida, Belize, and http://scientistatwork.blogs.nytimes.com/2012/12/28/a- Panama to investigate how these biotic interactions fish-with-nowhere-to-hide/ may vary with latitude. Broadly, this work will reveal http://scientistatwork.blogs.nytimes.com/2013/01/10/a- how animals modify the structure of a critical marine persistent-foreign-predator-dangerous-but-delicious/ habitat and elucidate the importance of these interac-

Biodiversity and Community Ecology How do Root-Boring and Fouling Invertebrates Affect the Habitat Structure of Red Mangroves in the Caribbean?

Timothy Davidson By altering the physical structure of habitats, animals may have cascading effects to other members of marine communities. Diverse assemblages of species inhabit the submerged root systems of red mangroves (Rhizophora mangle) in the Caribbean including numerous root-boring and fouling invertebrates. Within brackish creeks and lagoons in the Caribbean, the non-native pillbug Sphaeroma terebrans is an important structuring agent of mangroves. This woodborer attacks the hanging roots of red mangroves, which can stimulate the creation of root tips or facilitate root breakage and alter root morphology. These isopods are absent from marine mangroves, however. Instead, diverse fouling invertebrates, such as sponges and oysters, live on mangrove roots. While sponges may enhance root growth, other species such as oysters and barnacles may reduce growth by blocking pores used by mangroves for gaseous exchange. Thus, boring isopods and fouling species may have variable effects to the morphology of this shoreline habitat.

Figure 33- The author inspects hanging prop roots from red mangroves at Twin Cays, Belize.

tions across broad biogeographic areas.

Understanding the Role of Competition at Structuring Assemblages of Marine Invertebrates in Reef Communities Along a Latitudinal Gradient Matthieu Leray The latitudinal gradient in species diversity is one of the best recognized patterns, with species richness increasing from the tropics to the poles for most metazoan taxonomic groups in both terrestrial and marine ecosystems. Yet despite the robustness of the pattern, its cause remains one of the most debated topics in biology. One hypothesis is that these patterns are the result of an increased gradient in the strength of biotic inter27

bile and sessile members of reef communities. A set of nine ARMS will be collected every six months at each of the two temperate locations and every year at each of the two tropical locations.

First samples were obtained from Fort Pierce and the Chesapeake shore in May 2013 and a first set of ARMS will be sampled in Bocas late September 2013 and in Carrie Bow early October 2013. DNA barcoding and metabarcoding data are being generated to infer the role of competitive interactions using community phylogenetic tools.

Biodiversity of Coral Associated Decapods Sea McKeon Work by McKeon et al. at Carrie Bow Cay has focused on the role of biodiversity in the ecology of reef invertebrates. The Mesoamerican barrier reef is home to large numFigure 34- Autonomous Reef Monitoring Structures (ARMS) deployed in the bers of decapod (crabs, shrimp, etc.) taxa that reef environment. are symbiotic with structural reef organisms such as corals and anemones. Frequently, actions leading to higher rates of ecological speciation. these exosymbiotic decapods are closely reIn support of this, lower intensities of predator-prey lated groups that have been historically assumed to play interactions and plant-herbivore interactions have been similar ecological roles on the reef. The work to date observed in higher latitudes. Yet, despite being a highly has focused on understanding the similarities and differcommon and important biological interaction in nature, ences in ecological services provided by closely related very few studies have specifically looked at the role of competitive interactions across latitudes. Moreover, community-level studies remain scarce.

We are conducting a large-scale experiment to investigate latitudinal patterns in the role of competition at structuring assemblages of marine invertebrates in reef communities. Twenty-seven Autonomous Reef Monitoring Structures (ARMS) were deployed at each of the four Tenenbaum Marine Observatory Network (TMON) Sites: on coral reefs near Carrie Bow Cay and Bocas del Toro (Panama), on oyster reef in Fort Pierce and on the Eastern Shore of the Chesapeake Bay. ARMS are long-term collecting devices of cubic shape composed of stacked PVC layers designed to mimic the structural complexity of a reef habitat (Figure 34). They allow organisms to settle or shelter within the structure and provide an ideal opportunity to study both the mo28

Figure 35- Porites divaricata, host to the crab M. sculptus.

Figure 36- Coral-inhabiting crab Mithraculus sculptus..

groups of organisms. One example is the Majid crab genus Mithraculus, a group of small algae feeding crabs that are found living in association with reef corals and anemones. Despite overall similarity to its congeners, Mithraculus sculptus (Figure 36) has been documented providing more effective defense from algal overgrowth to the host coral Porites divaricata (Figure 35) and favoring Porites thickets with higher stem densities. Similar comparisons of services provided to exosymbiont crustaceans (Perclimenes yucatanicus) by a variety of host cnidarians continue to reveal critical differences among even close relatives. The work is important to ongoing reef conservation in that it highlights how species level taxonomic differences can have ecosystem level impacts.

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Figure 37- Blue water diving.

Other Invertebrate Studies

pelagic realm, but we don’t yet understand how transparent animals structure their tissues to appear invisible; absence of pigment is insufficient for transparency Clearly Camouflaged Crustaceans at as tissues also must not scatter light. Our goal was to Carrie Bow Cay collect transparent hyperiid amphipods – pelagic crustaceans often associated with gelatinous zooplankton – Laura Bagge, William Browne, Jamie Baldwin Fergus, Stephanie Bush, Brad Seibel, Sönke to answer questions about their transparency and their visual ecology. We traveled to Pelican Cayes, where Johnsen On our last day of blue-water diving to collect oceanic plankton, four members of our research team descended into the clearest water imaginable; our only reference point in this featureless environment was the orange safety-line to which we were tethered. The fact that there was no place to hide became frightfully clear when an 8 ft. long shark suddenly approached from the blue depths, causing us to hastily ascend back to our boat.

Wearing our conspicuously dark wetsuits, dangling like bait from the blue-water diving rig as we waited to climb the dive ladder, we wished that we could become as invisible as any of the transparent organisms we had come to Carrie Bow Cay to study (Figure 37).

Transparency is a common camouflage strategy in the 30

Figure 38- The comb jelly Mnemiopsis is host to transparent hyperiid amphipods.

(Thor amboinensis) from the same microhabitat for comparison, and we are currently using transmission electron microscopy to investigate whether morphological and ultrastructural modifications for transparency are present (Figures 39 & 40).

Binary Fission in Supersized Nematode Symbionts Slivia Bulgheresi and Niko Leisch

Figure 39- Periclimenes yucanticus shrimp on anemone host.

Mnemiopsis ctenophores with clear Glossocephalus hyperiid hitchhikers were rumored to wash over submerged coral ledges in multitudes (Figure 38). Though we were able to find plenty of Mnemiopsis to answer questions about genetic variability in these transparent pelagic creatures, we didn’t catch any symbiotic hyperiids. For clear crustaceans, we turned our attention to the Periclimenes shrimp inhabiting our backyard near the Carrie Bow Cay dock. Despite having a benthic, commensal existence with anemones and a relatively large (>10 mm) body with conspicuous color markings, these shrimp were clear enough to read a newspaper through their abdomen. We collected three transparent species of Periclimenes (P. rathbunae, P. yucatanicus, and P. pedersoni) and a more opaque shrimp species

Figure 40- Periclimenes yucanticus shrimp as seen under a microscope..

The molecular basis of cell division is well studied only in cultivable, average-sized microorganisms. Yet, microbial cell size ranges over three orders of magnitude and how extraordinarily long prokaryotes divide is poorly understood. Our recent work on longitudinally dividing Gammaproteobacteria associated to marine nematodes (see CCRE Annual Report 2012) revealed that cells have unanticipated capabilities to segregate their chromosomes and divide. Moreover, it suggested the existence of undiscovered mechanisms for spatial regulation of cell division. In our 2013 field trip, we collected Eubostrichus fertilis and E. dianeae nematodes from Twin Cays to investigate how their filamentous aseptate symbionts reproduce. The symbiont coating E. fertilis is crescent-shaped and can be 4 - 45 µm long (Figures 41 & 42), whereas the E. dianeae symbiont can be up to 120 µm-long (Figure 43). Despite their unusual length, they both appear to reproduce by symmetric binary fission based on ultrastructural, morphometric and immunocytochemical analysis. This implies the existence of undiscovered mechanisms for temporal regulation of cell division. These probably evolved as a consequence of the symbiotic lifestyle, linking microbial ecology to the fundamental biological process

Figure 41- Scanning electron micrograph of a Eubostrichus fertilis nematode covered with crescent- shaped symbiotic bacteria.

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meters long and often worm-shaped. Several of these animals and protists can reach very high local abundances and some live in a tight symbiotic association with thiotrophic chemosynthetic bacteria. In the absence of light these bacteria can fix carbon by using the oxidation of reduced sulfur compounds as an energy source. The optimal energy yield can be reached with oxygen as an electron acceptor, but these interstitial waters usually exhibit a characteristic chemical gradient from the oxic surface to anoxic and sulfidic layers where oxygen and sulfide rarely meet. By ‘hitching a ride’ with the much larger and highly motile meiofaunal hosts, the bacteria are able to bridge this gap and access both oxygen and sulfide. In return, several host groups completely rely on their symbionts for nutrition and lost their mouth and gut. The hosts Figure 42- Scanning electron micrograph of a of a Eubostrichus of chemosynthetic bacteria are phylogenetically highly fertilis nematode (central region) covered with crescent-shaped diverse and include members of the ciliates, flatworms, symbiotic bacteria. roundworms and annelids, and we sampled a wide range of cell growth. Given that Gammaproteobacteria are of them during our 2013 field-work campaign not only ecologically but also medically important and many engage in both beneficial and pathogenic associa- Paracatenula tions with plants and animals, our findings will likely The members of the genus Paracatenula are mouthenlarge the understanding of other microbial associa- and gut-less catenulid flatworms that have intracellular alphaproteobacteria as thiotrophic symbionts in spetions such as those involving humans. cialized cells – the bacteriocytes. Their body is structured in a transparent and symbiont-free front end with a brain – the rostrum, and the rest of their body is a white colored region that houses the symbionts in numerous bacteriocytes. Nine different species of Paracatenula occur in the waters around Carrie Bow Cay, several still undescribed. One of our projects focused on Paracatenula galateia from the Southwater Cay southern sandbar, a large and common species (several mm in length) that we recently described. Paracatenula galateia, as all Paracatenula species we investigated so far, has the capability to regenerate their rostrum when

Figure 43- Scanning electron micrograph of a Eubostrichus dianeae nematode covered with long filamentous symbiotic bacteria.

Thiotrophic Meiofauna Christer Erseus, Harald Gruber-Vodicka, Jörg Ott, Cecilia Wentrup and Judith Zimmermann Shallow water sands appear empty and lifeless at the first glance, yet they host a very diverse micro-fauna that lives in the pore space between the sand grains. This so-called meiofauna is between 30 micrometers and several milli32

Figure 44- Numerous specimens of a new species of Paracatenula flatworms (scale 1mm) collected from Southwater Cay.

the genus Stilbonema, for example, are associated with a multilayer of coccoid bacteria, while members of other genera are covered by rods or filamentous bacteria (Figure 45). Molecular analyses of the ectosymbiotic bacteria based on the 16S rRNA gene have confirmed the morphological observation that each nematode host is associated with a specific strain of C D gammaproteobacterial ectosymbiont.

Our knowledge of the symbiotic interaction and the mutual benefits is still limited. While the host is assumed to benefit nutritionally from the ectosymbionts, the bacteria should benefit from the mobility of the host, facilitating a regular substrate supply from both the oxidized surface Figure 45- Stilbonematinae ectosymbiotic bacteria with different morphologies. layers and the deeper reduced sediment Bacteria of rod- (A), rice- (B), round (C) and filamentous shape (D) found on layers.

A

B

different Stilbonematid nematodes species around Carrie Bow Cay.

a part of the worm is ripped off. In a controlled experiment we cut the worms and allowed them to regenerate to certain rostrum development states, and we will test possible links between host development and symbiont physiology.

To address the undescribed diversity of Paracatenula we sampled another large species of Paracatenula in a second project (Figure 44). This largest species so far found around Carrie Bow Cay is several mm long, 0.5 mm wide and the worms can easily be seen with the naked eye. We collected all necessary morphological data as well as fixed specimens to describe this species.

We visited Carrie Bow Cay in 2013 to investigate the diversity of nematode species and the specificity of their ectosymbiotic bacteria in different shallow water sediments around Carrie Bow Cay. We identified different nematode species in the field and transported them to the Shallow Water Symbiosis Group lab in the Max Planck Institute for Marine Microbiology in Bremen for molecular analyses of the host and the symbionts. We are especially interested in the evolutionary history of these ectosymbioses and will compare our results to those from previously sampled

â&#x20AC;&#x2DC;Stilbosâ&#x20AC;&#x2122; Marine nematodes of the subfamily Stilbonematinae (Desmodorida, Desmodoridae) are highly abundant in the shallow water sands of the Mesoamerican reef.

To date, nine genera with multiple species have been described worldwide, but the majority of the diversity might still be unknown. Many species are very difficult to distinguish based on morphology alone and we use a combination of morphology and molecular analyses to characterize our samples.

The characteristic feature of stilbonematid nematodes are ectosymbiotic bacteria that cover almost their entire cuticle, leaving only the mouth region and the tail tip symbiont-free. The morphology of these ectosymbiotic bacteria varies from species to species, and general patterns are often genus-specific. Nematodes of

FIgure 46- Inanidrilus leukodermatus, a very common gutless oligochaete collected just off the dive-shack of CBC (scale 1mm).

33

species from different geographical regions. We further collected nematodes for experiments to investigate the potential nutritional benefit the host gains from its ectosymbiotic bacteria. Experiments are currently underway.

Gutless oligochaetes Gutless oligochaetes comprise another group of thiotrophic meiofauna that inhabits the oxic-anoxic interphase of shallow water sediments. These animals are relatively large for meiofauna (~ 0.2 mm diameter and ~ 2 cm long) and, as relatives of earthworms, are segmented worms that belong to the Annelida (Clitellata, Naididae, Phallodrilinae) (Figure 46). Gutless oligochaetes have no digestive or excretory system (i.e. they lack a mouth, gut, and nephridia, which are kidney-like excretory organs) and instead rely on bacterial symbionts for nutrition and waste recycling.

Our studies on the phylogeny of the bacterial symbionts have revealed a remarkable diversity, with up to 6 different symbionts within one worm. Nevertheless, these symbiotic associations are highly specific, since each worm species harbors only one specific symbiont community.

Because a wide variety of gutless oligochaete species has already been described from several sites around Carrie Bow Cay, the main goal of our survey at CBC was to collect as many different gutless oligochaete species as possible to analyse their symbiotic community. Genomic and proteomic comparisons of the symbionts will provide information of how these remarkable symbioses function today and might additionally give insights into how they evolved.

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CCRE Contributions Fiscal Year 2013 Baldwin, C.C. 2013. The phylogenetic significance of color patterns in marine teleost larvae. Zoological Journal of the Linnean Society 168(3): 496–563.

Bucher, K.E., J.N. Norris, and J.R. Sears. 2013. Gloiotrichus vermiculatus sp. nov. (Liagoraceae, Rhodophyta) a new species from the Caribbean Sea. Caribbean Journal of Science 47(1):98-113.

Engene, N., S.P. Gunasekera, W.H. Gerwick, and V.J. Paul. 2013. Phylogenetic inferences reveal large extent of novel biodiversity in chemically rich tropical marine cyanobacteria. Applied Environmental Microbiology 79 (6): 1882-1888.

Feller, I.C., A.H. Chamberlain, C. Piou, S. Chapman, and C.E. Lovelock. 2013. Latitudinal patterns of herbivory in mangrove forests: consequences of nutrient over-enrichment. Ecosystems 16: 1203-1215.

Frable B.W., C.C. Baldwin, B.M. Luther, and L.A. Weigt. 2013. A new species of western Atlantic lizardfish (Teleostei: Synodontidae: Synodus) and resurrection of Synodus bondi Fowler, 1939, as a valid species from the Caribbean with redescriptions of S. bondi, S. foetens (Linnaeus, 1766) and S. intermedius (Spix and Agassiz 1829). Fishery Bulletin 111: 122–146.

Hurt, C., S.H.D. Haddock, and W.E. Browne. 2012. Molecular phylogenetic evidence for the reorganization of the Hyperiid amphipods, a diverse group of pelagic crustaceans. Molecular Phylogenetics and Evolution 67(1): 28-37.

Jörger, K.M., J.L. Norenburg, N.G. Wilson, and M. Schrödl. 2012. Barcoding against a paradox? Combined molecular species delineations reveal multiple cryptic lineages in elusive meiofaunal sea slugs. BMC Evolutionary Biology 12: 245.

Leisch, N., J. Verheul, N.R. Heindl, H.R. Gruber-Vodicka, N. Pende, T. den Blaauwen, and S. Bulgheresi. 2012. Growth in width and FtsZ ring longitudinal positioning in a gammaproteobacterial symbiont. Current Biology 22 (19): R831 - R832.

Martínez, A., M. Di Domenico , K. Jörger , J. Norenburg, and K. Worsaae. 2013. Description of three new species of Protodrilus (Annelida, Protodrilidae) from Central America. Marine Biology Research 9(7): 676-691.

Mathis, W.N. and T. Zatwarnicki. 2012. A Revision of the New World Species of Polytrichophora Cresson and Facitrichophora, New Genus (Diptera: Ephydridae). Zookeys 231: 1–116.

Morrow, K.M., M.R. Liles, V.J. Paul, A.G. Moss, and N. Chadwick. 2013. Bacterial shifts associated with coral-macroalgal competition in the Caribbean Sea. Marine Ecology Progress Series 488: 103-117.

Taylor, D.S. 2012. Twenty-four years in the mud: what have we learned about the natural history and ecology of the mangrove rivulus, Kryptolebius marmoratus? Integrative and Comparative Biology 52 (6): 724-736.

Vaslet, A., C. France, C. C. Baldwin, and I.C. Feller. 2012. Dietary habits of juveniles of the Mayan cichlid, Cichlasoma urophthalmus, in mangrove ponds of an offshore islet in Belize, Central America. Neotropical Ichthyology 10 (3): 667674.

Weigt, L.A., C.C. Baldwin, A. Driskell, D.G. Smith, A. Ormos, and E.A. Reyier. 2012. Using DNA barcoding to assess Caribbean reef fish biodiversity: Expanding taxonomic and geographic coverage. PLoS ONE 7(7): e41059.

Wulff, J. 2013. Recovery of sponges after extreme mortality events: morphological and taxonomic patterns in regeneration versus recruitment. Integrative and Comparative Biology 53 (3): 512-523.

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2013 Participants * served as station manager

Alanko, Jerry & Sandy, Tilghman, MD* Atherton, Sarah, University of Massachutsetts, Lowell, MA Bagge, Laura, Duke University, Durham, NC Baker, David, National Museum of Natural History, Washingotn, D.C. Baldwin, Carole, National Museum of Natural History, Washington, D.C. Baldwin-Fergus, Jamie, National Museum of Natural History, Washington, D.C. Bodart, Jake, Univeristy of Maryland, College Park, MD Bracken-Grissom, Heather, Florida International University, Miami, FL Brightwater, Franklin, Oakland, CA Brown, John, John Brown Images, Oxfordshire, England Browne, William, University of Miami, Miami, FL Bulgheresi, Silvia, University of Vienna, Austria Bush, Stepanie, National Museum of Natural History, Washington, D.C. Campbell, Justin, Smithsonian Marine Station, Fort Pierce, FL Castillo, Cristina, National Museum of Natural History, Washington, D.C. Davidson, Timothy, Smithsonian Tropical Research Inst., Panama Dimond, James, Western Washington University, Shannon Point Marine Center, Anacortes, WA Ducket, Lisa, Smithosnian Environmental Research Center, Edgewater, MD Elliot, Alexa, WPBT2, Miami, FL Erseus, Christer, Univeristy of Gothenburg, Gothenburg, Sweden Felder, Darryl, University of Louisiana, Lafayette, LA Felder, Jennifer, Lafayette, LA Feller, Ilka, Smithsonian Environmental Research Center, Edgewater, MD Feuerstein, Amanda, National Museum of Natural History, Washington, D.C. Fogarty, Nicole, Nova Southeastern University, Dania Beach, FL Foltz, Zach, Smithsonian Marine Station, Fort Pierce, FL Forde, Alex, University of Maryland, College Park, MD Franklin, Amanda, Tufts University, Medford, MA Freeman, Chris, University of Alabama, Birmingham, Birmingham, AL Fuller, Kathryn, Summit Foundation, Washington, D.C. Gawne, Peter, New England Aquarium, Boston, MA Gibson, Janet, Wildlife Conservation Society, Dangriga, Belize Gochfeld, Deborah, University of Missippi, Oxford, MS Gray, Ian, BBC Natural History Unit, Bristol, England Gruber, Harald, Max Planck Institute of Marine Biology, Bremen, Germany Gouge, Daniel, Williston, FL* Halloran-Fagan, Maggie, National Museum of Natural History, Washington, D.C. Hansen, Carl & Ginger, Springfield, VA Henley, Michael, Smithsonian Institution National Zoological Park, Washington, D.C. Hickey, Sean, WPBT2, Miami, FL Houk, Jay, Smithsonian Marine Station, Fort Pierce, FL Hootman, Jonathon, Whitesburg, KY* James, Edwin & Bonnie, Tilgman, MD* Johnsen, Sonke, Duke University, Durham, NC Jones, Scott, Smithsonian Marine Station, Fort Pierce, FL Kobrinsky, Zach, Natural History Photographer, San Francisco, CA Koltes, Karen, Office of Insular Affairs, Dept. of Interior, Washington, D.C. Lemaitre, Raphael, National Museum of Natural History, Washington, D.C. Leray, Matthieu, National Museum of Natural History, Washington, D.C. Littshcwager, David, Natural History Photogrpaher, San Francisco, CA

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Lovelock, Catherine, University of Queensland, Brisbane, Australia Massi, Joe, New England Aquarium, Boston, MA McClennan, Caleb, Wildlife Conservation Society, Dangriga, Belize McField, Melanie, Healthy Reefs for Healthy People, Belize City, Belize McKeon, Seabird, Smithsonian Marine Station, Fort Pierce, FL Meyer, Chris, National Museum of Natural History, Washington, D.C. Moura, Carlos, University of the Azores, Portugal Moore, Joel & Linda, Shingle Springs, CA* Noren, Hunter, Nova Southeastern University, Dania Beach, FL Olsen, Kevin, Smithsonian Marine Station, Fort Pierce, FL Opishinksi, Thomas, Interactive Oceanographics, East Greenwich, RI Ott, Joerg, University of Vienna, Austria Pandolfi, John, University of Queensland, Brisbane, Australia Paul, Valerie, Smithsonian Marine Station, Fort Pierce Parsons, Keith & Shirley, Atlanta, GA* Pende, Nika, University of Vienna, Austria Penland, Laurie, National Museum of Natural History, Washington, D.C. Peresta, Gary, Smithsonian Environmental Research Center, 647 Contees Wharf Rd., Edgewater, MD* Pitassy, Diane, National Museum of Natural History, Washington, D.C. Riley, Meghan, University of South Carolina, Columbia, SC Rocha, Luiz, California Academy of Sciences, San Francisco, CA Ross, Clifford, University of North Florida, Jacksonville, FL Rotjan, Randi, New England Aquarium, Boston, MA Saavedra, Carlos, Summit Foundation, Washington, D.C. Samper, CristiĂĄn, Wildlife Conservation Society, New York, NY Sant, Roger, Summit Foundation, Washington, D.C. Seibel, Brad, University of Rhode Island, Kingston, RI Shirley, Thomas, Texas A&M University-Corpus Christi, Corpus Christi, TX Simpson, Lorae, Smithsonian Marine Station/Smithsonian Environmental Research Center, Fort Pierce, FL Scheff, George, 4092 Norris Rd., Bellville, OH* Sherwood, Craig, Deale, MD* Sneed, Jennifer, Smithsonian Marine Station, Fort Pierce, FL Spathias, Hanae, University of Puerto Rico, MayagĂźez, Puerto Rico Stango, Frank, Compressed Air Supplies and Equipment, Dania, FL Stevens, Julia, University of Alabama, Tuscaloosa, AL Tarabochia, Alex, University of Florida, Gainesville, FL Taylor, Jim & Tanya, Oxford, MS* Teplitski, Max, University of Florida, Gainesville, FL Thacker, Cheryl, University of Florida, Gainesville, FL Thoma, Brent, University of Louisiana, Lafayette, LA Tschirky, John, Washington, D.C. Vasbinger, Kelly, Florida State Univeristy, Tallahassee, FL Weber, Michelle, University of California, Berkeley, CA Weigt, Lee, National Museum of Natural History, Washington, D.C. Wells, Christopher, University of New Hampshire, Durham, NH Wentrup, Cecilia, Max Planck Institute of Marine Biology, Bremen, Germany Wood, Abby, Smithsonian Institution National Zoological Park, Washington, D.C. Wulff, Colin, Talahassee, FL Wulff, Janie, Florida State University, Tallahasee, FL Zimmerman, Judith, Max Planck Institute of Marine Biology, Bremen, Germany

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Photograph & Art Credits: Front Cover: Scott Jones, p. 1 A. Wood, p.6 J. Brown, p.7 D. Liitschwager, p.8 D. Liitschwager, p.9 K. Koltes, p.10 T. Opishinski, p.12 S. Jones, p.13 Z. Foltz, p.14 A. Wood, p. 15 A. Wood (both), p. 16 H. Noren (top), S. Jones (bottom), p.17 R. Ritson-Williams(top), A. Wood (bottom), p. 18 L. Penland, p. 19 M. Teplitski, p. 20 M. Teplitski (top), R. Ritson-Williams (bottom), p. 21. D. Gochfeld (both), p. 22 J. Wulff, p.23 R. Ritson-Williams (top), D. Felder (bottom), p.24 D. Felder, p. 25 M. Riley (both), p. 26 L. Simpson, L. Rocha (right), p. 27 A. Wood, p. 28 L. Penland, p. 29 C. McKeon (both), p. 30 M. Lombardi (top), B. Browne (bottom), p. 31 Laura Bagge (both), p. 32 Nikolaus Leisch, p. 33 H. Gruber (both), p. 33 H. Gruber, Back Cover: A. Wood.

Smithsonian Marine Station Caribbean Coral Reef Ecosystems Program Fort Pierce, FL 路 Carrie Bow Cay, Belize www.ccre.si.edu www.sms.si.edu CCRE Staff: Valerie Paul, Director Zach Foltz, Station Manager Scott Jones, Program Coordinator

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