Sea Grant Final Report: Executive Summary Plus Narrative
Project Title: Symbiont diversity and population dynamics of coral reef sea anemones
Date: 22 November 2010
Project Number: R-101-1-08
Investigators and affiliations:
PRINCIPAL INVESTIGATOR: Nanette E. Chadwick, Auburn University (AU)
CO-PRINCIPAL INVESTIGATOR: Stephen G. Ratchford, University of the Virgin Islands (UVI)
Dates Covered: February 1, 2008 to October 31, 2010
A. Executive Summary of Impacts and Contributions
1. Objectives:
Objective 1: Determine the abundance and diversity of crustacean macrosymbionts and the population dynamics of corkscrew sea anemones Bartholomea annulata on Caribbean coral reefs We completely met this objective, by conducting quarterly censes of mapped anemones at 2 coral reef sites on St. Thomas, USVI, over 2 years. These revealed that the anemone populations are stable among years, but experience rapid turnover of individuals, with most anemone mortality occurring within 1-2 years. Small individuals contribute the most to population growth, and the anemones rely on high rates of juvenile recruitment for maintenance of stable populations. These anemones support a high biodiversity of crustacean associates, including 1 facultative and 5 obligate species, which remain fairly stable in overall abundance among years in unfished populations. The crustacean assemblage on individual anemones varies widely among quarterly censes, indicating high shrimp mobility and population turnover.
Objective 2: Train a graduate student at AU and undergraduate students at UVI in methods for interannual modeling of sea anemone population dynamics and determination of the diversity patterns of crustacean symbionts. We completely met this objective, by training 3 M.Sc. students and 1 Ph.D. student at AU, of which this Sea Grant research was the core of their thesis projects (2 graduate theses completed, 2 in progress). We also trained 4 undergraduate students in research projects at UVI.
Objective 3: Educate youth in the Virgin Islands concerning the ecological importance of this and other symbioses on coral reefs, through the development of educational materials and a hands-on program. We completely met this objective, by developing an educational activity book on Coral Reef Symbiosis, printing 1,700 copies, distributing them to elementary schools and environmental organizations throughout St. Thoma, and posting an electronic copy on the internet for public use. We also conducted 2 hands-on programs for a total of 45 high school students and 7 teachers on coral reefs surrounding St. Thomas. Their responses on program evaluations indicated substantial improvement in their marine environmental awareness.
2. Advancement of the Field: This is the first in-depth description of population dynamics of a coral reef sea anemone, revealing that some reef anemones are short-lived. Their rapid population turnover is in sharp contrast to demographic patterns in reef-building corals, which have lifespans of decades to hundreds of years. These findings advance the field of demographic studies on coral reefs, by showing that anemones can be much more dynamic than their close relatives the stony corals, and as such, are expected to recover much more rapidly from disturbances. A reciprocal field transplant experiment between our 2 field sites indicated that these anemones are extremely plastic in the expression of life history traits, also a first for tropical anemones, and similar to the known strong effect of environment on the expression of traits in stony corals. The crustacean associates of these Caribbean anemones are as biodiverse as those associated with Indo-Pacific anemones, which is surprising given the relatively low biodiversity of most coral reef organisms in the Caribbean compared with the Indo-Pacific region. These results indicate that obligate symbiosis with sea anemones is an important driver of crustacean coevolution and biodiversity on Caribbean coral reefs. Because these anemones host obligate cleanershrimps that are major cleaners of parasites from reef fishes, they also can drive patterns of fish biodiversity on Caribbean reefs. The results of our field experiments, which go beyond the original
objectives of the project, show that reef fishes from 16 families use the large, conspicous anemones as visual cues to locate shrimp cleaning stations. Finally, our field observations and experiments add important information to the field of niche partitioning, in that they reveal distinct and fairly rigid patterns of microhabitat use among the 6 species of crustacean associates of this anemone, which appear to be controlled by both competition and predation. Our methods demonstrate for the first time that large, conspicuous sea anemones on reefs may be efficiently tracked using precise tagging and mapping techniques and frequent census methods.
3. Problems encountered: It was difficult to track the sea anemones, because tags sometimes detached from the chalky reef substrate and disappeared, and also anemones potentially moved among locations on the reef. Thus, we could not always determine if a newly-observed anemone was a recruit, or if it was a prior resident that had moved or lost its tag since the last census. We overcame this problem by constructing detailed maps of our sites, to track the locations of all anemones. We also presented upper and lower estimates of the turnover rates of anemones, which showed that even in under the most conservative scenario, these anemones experienced rapid turnover of individuals among censes. We also experienced some delays in publishing our results, due in part to hospitalization of the PI, and communication problems among widely-dispersed co-authors. In terms of the outreach program, we were unable to distribute our educational book to all elementary schools on St. Thomas as planned, because many teachers were too busy or set in their curricula, to allow class presentations using the book. We solved this problem by distributing the book only to schools and environmental organizations that expressed interest and were likely to use the book effectively to raise awareness among children. This meant that the book reached a narrower, but more motivated audience than originally intended.
4. Research Impacts: Both these anemones and their crustacean associates are collected intensively for the ornamental aquarium trade, and are overfished leading to local extinction on some reefs in Florida. This fishery is not sustainable, and the findings here provide a scientific basis to support better management of the fishery. Based on our demographic results, we recommend a minimum body size for collection of these anemones, and limitation of collecting to populations with rapid growth of individuals, located near MPAs for adequate recruitment to ensure population stability. In addition, our outreach program enhanced the marine environmental experience and awareness of Virgin Islands schoolchildren, and caused some of them to consider careers in marine conservation.
5. Other important impacts or products: Eight students supported: Michael Nelsen, michael.nelsen@gmail.com M.Sc. Thesis title: Population dynamic modeling of the corkscrew sea anemone Bartholomea annulata on Caribbean coral reefs. M.Sc. Degree, December 2008. Supported May-August 2008, $3,300.
Lindsay Huebner, lkh0002@auburn.edu M.Sc. Thesis title: The role of host sea anemones in the cleaning mutualism between anemoneshrimp and client fishes. M.Sc. Degree,December 2010. Supported JuneAugust 2009, $2,200.
Benjamin Titus, bmt0004@auburn.edu M.Sc. research proposal title: Effects of habitat variation on reproductive strategies of the corkscrew anemone Bartholomea annulata on Caribbean coral reefs. M.Sc. Degree expected May 2011. Supported June-August 2010, $2,200.
Ashley Isbell, adi0001@auburn.edu Ph.D. research proposal title: Ensemble structure of crustaceans symbiotic with the Caribbean sea anemone Bartholomea annulata. Ph.D. Degree expected December 2012. Supported July 2010, $1,300.
Anna-Mai Christmas, annafchristmas@gmail.com Undergraduate research project on competition among anemoneshrimps. Supported by synergistic programs: National Institutes of Health (NIH) Minority Biomedical Research Support (MBRS) Research Initiative for Scientific Enhancement (RISE) program May-December 2009, 300 hours, $3,000.
Adam Ringel, admanat@gmail.com Undergraduate research project on anemoneshrimp fidelity to host sea anemones. August-November 2008, 45 hours, received course credits
Eugene Brooks, eugene417@hotmail.com Undergraduate research project on anemone unburial by anemoneshrimps Supported by synergistic program: SSRI (NSF). July 2009-April 2010, 220 hours, $2,000.
Sanlin Robinson, sanlinsky@hotmail.com Undergraduate research project on acclimation of anemoneshrimps to host anemones Supported by synergistic program: SURE (NSF). July-August 2009, 175 hours, $2,000.
Nine presentations at professional meetings: 11th International Coral Reef Symposium, Fort Lauderdale, Florida (2008); Fall Research Symposium, University of the Virgin Islands, St. Thomas, USVI (2008); Annual Biomedical Research Conference for Minority Students (ABRCMS), University of the Virgin Islands, St. Thomas, USVI (2008, 2009); 39th Annual Benthic Ecology Meeting, University of North Carolina at Wilmington (2010, 5 presentations).
Six manuscripts in preparation for submission to the peer-reviewed journals: Marine Biology, Marine Ecology Progress Series, Journal of Experimental Marine Biology and Ecology, Proceedings of the Royal Society of London, and Coral Reefs.
One educational book; pdf posted on website: http://sites.google.com/site/anemonesymbionts/
6. Sources of matching funds: Auburn University, $49,030. University of the Virgin Islands, $26,464
7. New extramual funds in addition to match: “Assessing patterns of distribution and relatedness in Bartholomea annulata”, June 2010-May 2011, PADI Foundation Grant, $4,170. “Reprinting of Marine Educational Book for Virgin Islands Schoolchildren”, April-July 2010, Community Foundation of the Virgin Islands, $1,000.
8. Benefits: This project benefits the ornamental fisheries in Puerto Rico and Florida, in that we provide a scientific basis for sustainable management of the fisheries on these sea anemones and crustaceans, which are among the most heavily-collected organisms for the ornamental aquarium trade. Our demographic data also improve the ability of resource managers to forecast recovery rates of these important reef organisms following disturbances. Our Coral Reef Activity Book is available for printing on our website, and can be used by marine educators worldwide, as well as translated into Spanish for outreach programs in Puerto Rico.
B. Final Report Narrative
Statement of the Problem
The largest and most common sea anemones on Caribbean coral reefs are the rosetip anemone Condylactis gigantea and the corkscrew anemone Bartholomea annulata, some of which may attain tentacle crown diameters in excess of 30 cm (Colin 1978; Kaplan 1982; Humann 1992). Due in part to their large polyp size, fleshy tentacles and toxic nematocysts, these anemones host over 30 species of facultative fish symbionts (Albrecht 1977) and at least 9 species of anemoneshrimps (Colin 1978; Knowlton and Keller 1985; Nizinski 1989). Some of the shrimps clean ectoparasites from free-living reef fish (Sargent and Wagenbach 1975; Nizinski 1989). For example, Periclimenes pedersoni, an obligate shrimp associate of both C. gigantea and B. annulata, is known to remove juvenile parasitic isopods from French Grunt fish hosts (Bunkley-Williams and Williams 1998). Thus, anemone hosts may serve as base stations for fish cleaning activity on Caribbean coral reefs (Herrnkind et al. 1976; Sefton and Webster 1986), and the loss of these sea anemones can lead to cascade effects across multiple trophic levels on the reef.
Despite their potential importance to the reef ecosystem, few quantitative data exist for the Caribbean Sea, and none at all for the Virgin Islands, on patterns of diversity, population size structure, or abundance of the fish and shrimp macrosymbionts of these sea anemones. Qualitative surveys have shown that all of the above 30 fish species associate with C. gigantea (Hanlon and Kaufman 1976; Albrecht 1977), while a small subset of these, only 2 fish species, occur with B. annulata (Colin and
Heiser 1973). In contrast, 2 shrimp species associate with both of the anemone host species, an additional 2 shrimp species occur only with C. gigantea (Sefton and Webster 1986; Nizinski 1989) and 5 species associate only with B. annulata (Colin 1978; Knowlton and Keller 1983; 1985). Thus, B. annulata anemones may host a more diverse shrimp assemblage, while C. gigantea hosts a wider variety of fishes. Only one study has examined the population structure of a Caribbean anemoneshrimp, Periclimenes anthophilus, which occurs with C. gigantea (Nizinski 1989). Quantitative information on the other anemone associates is needed for calculation of diversity indices for this assemblage on coral reefs, and assessment of the impacts of these associations on other reef organisms such as large piscivorous fish.
Demographic processes in Caribbean sea anemones also are poorly understood. Information on patterns of recruitment, growth, mortality and lifespan are important for understanding the potential for their recovery following disturbances on reefs. Giant sea anemones are one of the most frequently-harvested invertebrates for the ornamental aquarium trade in some parts of the Caribbean, and information on their population dynamics is needed to support a sustainable fishery (Chiappone et al. 2001; LeGore et al. 2005). In the Indo-Pacific region, population dynamic patterns have been determined for some solitary reef anemones (Porat and Chadwick-Furman 2004; Chadwick and Arvedlund 2005; Hattori 2006) and solitary stony corals (Chadwick-Furman et al. 2000), and a sustainable yield model was developed for the latter. These studies have revealed that solitary cnidarians on reefs tend to have short lifespans of <20 years and high turnover of populations. The Caribbean anemones C. gigantea and B. annulata are particularly amenable to the application of population dynamic modeling, because individuals are solitary and large, and may be monitored easily for long periods on shallow reefs. Although reef anemones can locomote, they rarely vacate their holes due to a high risk of predation (Porat and Chadwick-Furman 2004; Hattori 2006), making them good candidates for long-term population studies.
Two major types of mathematical models have been applied to analyze the population dynamics of cnidarians. Firstly, standard fisheries models (Beverton and Holt 1957) have been used to examine the demography of some stony and soft corals that grow determinately and rarely shrink in body size (Grigg 1977; 1984; Goffredo et al. 2004; Goffredo and Lasker 2006; Chadwick-Furman et al. 2000; Guzner et al. 2007). They also were applied to sea anemones before stage-based models were developed for cnidarians (Sebens 1983). These models have demonstrated that populations of some reef cnidarians behave similarly to those of many vertebrates, in that individuals have finite lifespans with decreasing rates of mortality and growth as they age. Secondly, Leslie matrix models based on body size rather than age have been applied to species of cnidarians that exhibit substantial body shrinkage during their lifespans due to skeletal fragmentation or partial tissue mortality (Hughes 1984; Hughes and Connell 1987; Figs. 1 and 2). The stage-based Leslie matrix models have been used successfully to understand the complex dynamics of some populations of stony corals (Hughes and Jackson 1985; Babcock 1991; Hughes and Tanner 2000; Lirman 2003) and soft corals (Gotelli 1991; Lasker 1991). They also have been applied to the assess recovery patterns of reef-building corals on reefs (Lirman and Miller 2003), and to effectively design marine protected areas (Gerber and Heppell 2004). These models can incorporate sensitivity analyses which reveal the crucial life stages that most affect population size changes, thus guiding management to focus on the most important life stages in populations and reducing management costs (Lasker 1991; Rose and Cowan 2003; Gerber and Heppell 2004). The use of mathematical models is important for analysis of demographic changes in cnidarians because they may enable reef managers to predict changes in future population structure and size based on current patterns of demographic change.
We focussed our demographic modelling on the corkscrew anemone B. annulata, because it was the most common anemone on coral reefs at St. Thomas, US Virgin Islands, where we conducted this project.
Methods Used
Two to three personnel from Auburn University (PI and graduate students) made 4 visits of about 6 diving days each to St. Thomas, US Virgin Islands during each project year: in March, June, September, and December (every 3 months). This frequency allowed us to track seasonal variation in populations of the sea anemones and shrimps, and provided enough time for maintenance of tags and maps of the research sites. It also allowed sufficient interaction with the Co-PI and the Marine Advisor of UVI for the
development and execution of marine educational programs connected with the project. We collaborated with the Co-PI and UVI undergraduates to travel between UVI and the coral reef field sites on St. Thomas by boat. The PI also traveled to the Sea Grant Symposium on Puerto Rico.
For the sea anemone population study, during each visit to UVI we marked individuals of B. annulata, including newly settled individuals, by attaching a numbered metal tag to a small stainless steel nail driven into the reef adjacent to each anemone, at each of 2 reef sites (see detailed Site Maps in the 2 graduate theses on file). The location of each anemone was marked on a map of each site (after Hirose 1985). We recorded the following data for each marked anemone: diameter of oral disk and tentacle crown, expansion state, microhabitat (reef hole versus sand, angle of orientation), and species, numbers and sizes of associated shrimps (after Hirose 1985; Chadwick and Arvedlund 2005). Each survey area was searched carefully to locate all anemones, especially small and/or recently-settled juveniles (new recruits), as well as the disappearance or movement of tagged individuals. The time period of 2 years (plus the pilot year funded by VI-EPSCoR) was sufficient to determine inter-annual variation in population processes, similar to studies on other species of cnidarians in which demographic models have been applied to 2-3 years of data (Chadwick-Furman et al. 2000; Goffredo and Chadwick-Furman 2003, Goffredo et al. 2004). The sample size of about 70-120 tagged individuals per site also was similar to that used in the above studies, and was large enough for application of population models. Size-specific growth rates were estimated from observed changes in anemone size (after Chomsky et al. 2004). From the population size structure and growth rates, we estimated size-specific mortality rates and population turnover of the anemones. Population dynamic modelling was accomplished using the stage-based matrix models described above. Information on levels of adult fecundity was obtained from Jennison (1981), and combined with observed rates of juvenile recruitment to predict rates of future input of individuals into the populations (after Hughes et al. 2000). Collection of field data was done by teams of divers consisting of the PI, Co-PI, and AU and UVI students. The population modeling was accomplished by an AU graduate student (Michael Nelsen, see thesis on file) under supervision of the PI. The Co-PI supervised the participation of UVI undergraduate students, who developed related mini-projects on the mechanisms underlying changes in the anemone/symbiont populations, such as levels of fidelity of shrimp symbionts to individual anemones.
We also used the population data to develop a sustainable yield model for this anemone species for potential use by fisheries officials in the Caribbean region, modified after methods in Chadwick-Furman et al. (2000) and Shuman et al. (2005).
The diversity patterns of the anemoneshrimp symbionts were assessed using standard formulas to calculate levels of species richness, Shannon diversity indices, and species evenness (Morin 1999). Patterns of diversity, distribution, and abundance of the shrimp symbionts were analyzed for variation both temporally (among seasons and years) and spatially (among individual sea anemone hosts within site, and between sites). At least one of the anemoneshrimps, the snapping shrimp Alpheus armatus, consists of a complex of morphologically-similar sibling species (Knowlton and Keller 1983, 1985). Individuals of this shrimp were collected and sent to a shrimp taxonomists to determine which sibling species occur at our study sites.
We also employed additional field and laboratory methods that were not originally proposed for this project. During some censes, we also collected data on patterns of microhabitat use by the symbiotic crustaceans, and fish visitation to the cleanershrimps. We conducted 2 field experiments: a reciprocal field transplant to examine the phenotypic plasticity of sea anemone life history traits between reef sites, and removal experiments of both anemones and cleaner shrimps, to determine the influence of host anemones as cues for cleaning stations. Related laboratory methods included a molecular genetic analysis of the population genetic structure of the sea anemones, in terms of the relative contributions of asexual and sexual reproduction. These molecular analyses were conducted at Auburn University, from tissue samples collected on St. Thomas. Laboratory behavioral experiments also investigated the aggressive interactions among species of crustacean associates. Details of statistical tests are described in the 2 graduate theses produced.
For the elementary school outreach portion of the project, the PI and Co-PI interacted with the UVI Marine Advisor to design and print an educational activity book patterned after the successful “Trees in
the Seas” coloring book on mangroves that was produced with Sea Grant funding. In this book, we included activities such as crossword puzzles and find-the-object games. We produced an activity book rather than just a coloring book, because it is more interactive and engaging, and allows students to actively learn terms and concepts in coral reef symbioses. The PI, Co-PI, and UVI Marine Advisor wrote the text together, and organized an illustration contest among local elementary school students to produce the illustrations. The students won small prizes for their artwork, and their sketches appeared in the activity book. This contest also created publicity for the book and generated active student involvement and a sense of ownership. For the illustration contest, we sent out packets to elementary schools on St. Thomas with some information on local marine symbioses, what we were looking for in a good sketch, and what we planned to do with the sketches (see materials used, on file). By the end of the first year, we had the books printed and ready to distribute to Virgin Islands schools. During the second year, the UVI marine advisor distributed the books. We printed 1,700 educational books and distributed them to 7 schools and 9 environmental organizations on St. Thomas. For this initial outreach project, we limited book distribution to public elementary school students on St. Thomas, and to environmental organizations, so that we could accomplish a manageable scale of outreach during initial efforts. However, this type of outreach program potentially could be extended in the future to students in more schools on St. Thomas, and schools on the other US Virgin Islands, such as St. John and St. Croix
For the high school program, we recruited high school students and their science teachers on St. Thomas to participate in a hands-on program at the UVI marine laboratory. We presented lectures in the conference room of the marine laboratory to teach the students and science teachers about various types of marine symbioses, and took them snorkeling at nearby coral reef areas so that they could document (via a slate and camera) the types of symbioses they saw. Having teacher involvement (1) assisted us with monitoring a group of students in the water, and (2) got science teachers out in the field as well. We worked together on this high school project during each PI visit, and the Co-PI and Marine Advisor also worked with the high school teachers and students between PI visits. We run 2 programs for the high school students, each with a separate group of students. We limited these programs to a total of 45 students and 7 teachers, so that we could adequately supervise and maintain high quality in this intensive hands-on program. Based on the demand and success of this 2-year program, it potentially can be expanded in future years.
Results and Findings
Our first project objective was to determine the abundance and diversity of crustacean macrosymbionts and the population dynamics of host anemones Bartholomea annulata on Caribbean coral reefs We initially collected data on the physical characteristics of our study sites, showing that our inshore site, Brewers Bay, had significantly lower water motion, light penetration, and percent coral cover, and higher sedimentation than at our offshore site, Flat Cay Abundances of both the anemones and their shrimp symbionts were about 5-10x higher at the inner than outer reef site, and remained stable over the 2 years of study. Population dynamics of the sea anemone hosts also differed significantly between the 2 examined locations, with higher mortality at the outer reef site and higher rates of transition between sizeclasses (growth and shrinkage) at the inner reef site. The anemones were significantly smaller at the outer site, and the larger classes tended to shrink more than did those at the inner site. The anemones at both sites grew more during spring and summer, and shrank more in fall to winter. Both the number of recruits per m2 and recruits per resident anemone per m2 were significantly higher at the inner site, while the number of recruits per resident anemone was significantly higher at the outer site. The differences in site characteristics may influence the demography of B. annulata at each site, in particular rates of anemone growth and mortality. Matrix models based on current population trends projected the survival of these populations at both sites. Population models projected stabilization of the anemone populations, though the equilibrium sizes of the populations varied among models. Elasticity analyses of the matrix models indicated that the smallest individuals contributed the most to population growth, and suggest a need for establishing a minimum body size for the collection for these organisms. When outside recruitment was removed from the models, anemone populations were projected to plummet to zero
within about 3 years, revealing the importance of outside recruitment for the growth and stability of these populations. As such, unfished marine preserves, if located near fished areas of these anemones, are expected to be important sources of outside recruitment to fished populations. Based on this research, we recommend that areas where fishing of this sea anemone is allowed should be located near marine protected areas where the anemones are not collected, to facilitate adequate larval recruitment to fished populations. In addition, a minimum body size for collection of individuals at fished sites needs to be established to support a sustainable fishery. Also, collecting should be limited to reef habitats such as inshore sites, which support high recruitment and growth of these anemones. We conclude that these populations are stable among years, but experience rapid turnover of individuals. Most anemone mortality occurs within 1-2 years, indicating highly dynamic populations compared with those of stony corals, which turn over on a scale of 20-100s of years. Small individuals contribute the most to population growth, thus these anemones rely on high rates of juvenile recruitment for maintenance of stable populations.
We also compiled data from the Fish and Wildlife Research Institute, of the Florida Fish and Wildlife Conservation Commission, which revealed that the fishery for this sea anemone has steadily declined over the past 2 decades. This decline likely is due at least in part to declining numbers of anemones on Florida reefs, as some reefs are fished to local extinction of anemones.
In terms of the biodiversity of crustacean associates, we determied that individuals of this anemone support 1 facultative species (juveniles of the arrow crab Stenorhynchus seticornis) and 5obligate species (Pederson’s cleaning shrimp Ancylomenes pedersoni, spotted cleaner shrimp Periclimenes yucatanicus, red snapping shrimp Alpheus armatus, squat shrimp Thor amboinensis, and anemone mysid Heteromysis actiniae). Populations of these 5 crustacean associates remained fairly stable in overall abundance among the 3 years of study in these unfished populations. Individuals of the cleaner shrimp dominated both assemblages, and occurred in social groups of 2-10 individuals per anemone. The other shrimps occurred as single individuals per anemone, or as mated pairs, and the mysid occurred as large swarms of individuals that hovered among the anemone tentacles. More than 50% of anemones were occupied by shrimps at both sites. The Shannon diversity index for these crustacean assemblages was about 0.8-1.0, and the species evenness was 0.58-0.68, indicating fairly high diversity for a small number of associates, and dominance by the cleaner shrimps. These patterns of biodiversity were similar to those on IndoPacific tropical anemones, which is surprising considering that most reef organisms are much less diverse in the Caribbean than they are in the Indo-Pacific region. The crustacean assemblage on individual anemones varied widely among quarterly censes, indicating high shrimp mobility and population turnover.
In addition to collecting data in the proposed research areas of anemone population dynamics and crustacean biodiversity, we also conducted 4 related studies. Firstly, we examined the role of these anemones as visual cues for client fishes seeking cleaning by anemoneshrimps. Field removal experiments revealed that a wide diversity of client fishes (16 families) rely on the large conspicous anemones rather than the much smaller shrimps as visual cues for cleaning stations. Client fish visitation depends on anemone size and the overall diversity of crustacean associates, while the duration of cleans depends on abundance of the cleanershrimp Periclimenes pedersoni Secondly, we conducted a reciprocal transplant experiment of anemones between the 2 study sites, which showed that transplanted anemones grow and recruit more rapidly on inshore than offshore reefs, regardless of their site of origin. This experiment indicated that reef habitat type strongly impacts the expression of life history traits of these anemones, and that these traits are very plastic. They also confirmed the modeling studies above, in that inshore sites are much more sustain for the collection of these anemones than are offshore areas. Thirdly, we conducted a study of microhabitat partitioning among the 6 crustacean associates, which revealed that each species utilizes a different area on the anemone body, with little niche overlap. Competition experiments showed that these patterns of habitat use do not shift when competitors are removed, but that behavioral interactions such as aggression serve to enforce these patterns. The cleaner shrimp may occupy outer areas on the anemone, in part because it is less susceptible to predation than are the other shrimps, and also because it needs to be in conspicous positions on tentacle tips, for the cleaning of passing fishes.
Finally, molecular genetic analysis of the sea anemones has revealed that individuals in aggregations do not appear to be clonemates, and so most of the reproduction at these sites is via sexual recruits rather than asexual pedal lacerates.
Objectives Accomplished or not and why
The proposed 3 objectives for this Sea Grant program are listed below, with information on what was accomplished for each:
1. Determine inter-annual variation in the abundance and diversity of crustacean macrosymbionts and the population dynamics of the sea anemone Bartholomea annulata, among 3 years: the pilot study year (2006-07) and both Sea Grant project years (2008-09 and 2009-2010). Submit manuscripts to peer-reviewed journals on sea anemone population dynamics and patterns of crustacean macrosymbiont diversity.
We met most of the goals of this first objective. We collected 3 years of data on patterns of abundance and diversity of the crustacean associates of these sea anemones, and on the population dynamics of the anemones. We analyzed those data, and the findings on sea anemone population dynamics are summarized in an M.Sc. Thesis by Michael Nelsen, listed below. The data on abundance and diversity of crustacean associates are part of the Ph.D. thesis in progress of Ms. Ashley Isbell, see also Ph.D. proposal file listed below.
In addition to the stated research topics for this objective, we completed 4 related research projects: (1) Experimental evaluation of the phenotypic plasticity of sea anemone life history traits between reef sites, and (2) Molecular genetic analysis of population genetic structure of this sea anemone: relative contributions of asexual and sexual reproduction. These 2 projects are part of an in-progress M.Sc. Thesis by Mr. Benjamin Titus (see details below on thesis proposal). (3) Niche partitioning and effects of competition on crustacean assemblages of sea anemones. This project is part of the Ph.D. Thesis project of Ms. Ashley Isbell (see details above and below). (4) Patterns of client fish use of anemoneshrimps for cleaning interactions and influence of host anemones as cues for cleaning stations. This project formed the basis of the M.Sc. Thesis of Ms. Lindsay Huebner (see details below).
Two of the students involved in some of these projects (Ben Titus and Ashley Isbell) used this Sea Grant to leverage an additional $4,170 of support from a PADI Foundation Grant. They used these funds for additional fieldwork on St. Thomas in September 2010, plus to pay for additional field and laboratory research supplies, for their collaborative project entitled “Assessing patterns of distribution and relatedness in Bartholomea annulata”.
From all of these related research projects, 6 manuscript are in various stages of completion, but we have not yet submitted them to journals as listed in objective #1. Problems encountered that led to this delay include the departure of the first student (Michael Nelsen) from Auburn after his degree was completed, and problems in communicating with him to finalize revisions of some of the manuscripts. In addition, the P.I. Chadwick was hospitalized and convalescing during part of this grant period due to severe appendicitis surgery. However, final revisions of several of these manuscripts are now in progress, and submissions to journals are expected during Fall 2010 to Spring 2011. The P.I. will inform Sea Grant as each article is published, and will acknowledge this Sea Grant funding in all of these publications. Despite these delays, the large number of publications expected to result from this project exceed the goals of the original research objective.
We also had proposed to explore contacts with fisheries officials in regions where these and other sea anemone and shrimp species are collected commercially (such as in Florida, Chiappone et al. 2001; and in Puerto Rico, LeGore et al. 2005), and to provide them with this initial model for a sustainable fishery on B. annulata Due in part to the above publishing delays, we have not yet done so, but expect to publish this demographic model and communicate it to fisheries officials during the coming year. We also expect to develop future proposals for projects that will involve formal interaction with fisheries officials.
2. Train a graduate student at Auburn University and undergraduate students at the University of the Virgin Islands in field data collection for inter-annual modeling of sea anemone population dynamics and determination of the diversity patterns of crustacean symbionts.
We exceeded the goals of this objective, by training 4 graduate students at Auburn University, and 4 undergraduates at the University of the Virgin Islands:
Auburn University graduate students:
Mike Nelson – M.Sc. 2008 on anemone demographic modelling
Lindsay Huebner – M.Sc. 2010 on anemone role in fish cleaning
Ben Titus – M.Sc. 2011 on anemone life history variation
Ashley Isbell – Ph.D. 2012 on anemoneshrimp habitat partitioning
University of the Virgin Islands undergraduate students:
Adam Ringel – 2008 Independent research credits on shrimp fidelity to hosts
Eugene Brooks – 2010 Independent research on anemone unburial by shrimp
Sanlin Robinson – 2009 NSF program project on acclimation to anemones
Anna-Mai Christmas – 2009 NIH program project on shrimp competition
All of these students participated in field and laboratory research on aspects of the interactions between sea anemones and anemoneshrimps in this symbiosis, and also made research presentations at local and national meetings. Some of them completed graduate theses or undergraduate research projects, and some of them are in process. See below under Students Supported and Presentations, for details. Thus, we accomplished our objectives for student training, and exceeded them. This occurred in part because it was easy to incorporate extra students as diving buddies who could then work on other aspects of the project. Also, by careful budgeting of funds, and through the generous provision of free student lodging during some visits at the home of collaborator Steve Ratchford of UVI, we were able to bring more students to the field sites than originally proposed. Finally, synergistic programs at UVI contributed funds for the undergraduates, allowing several to be involved (see details below).
3. Educate youth in the Virgin Islands concerning the ecological importance of this and other symbioses on coral reefs through development of educational materials and a hands-on program. Print an educational activity book and distribute to elementary schools. Conduct hands-on programs for high school students.
For the elementary school program, we first involved local St. Thomas school children in the creation of illustrations for our activity book, by advertising a marine life art contest (see pdf of contest flyer), with prizes awarded for students who contributed drawings to illustrate the book, and to develop enthusiasm and involvement in the book-making process. The winning student illustrations were included in the book (see pdf of book). We then developed the book content, with 20 pages of crossword puzzles, matching, find the object, word search, maze, and fill-in questions, on aspects of coral reef conservation and ecology. We hired a local artist to design the front and back cover of the book, which illustrated sustainable (front cover) and unsustainable (back cover) practices on coral reefs (see pdf file of book). We then spent months editing and correcting mistakes in the book, and conferring on the final format. Finally, we printed 1,700 copies of the book, and distributed them to schools and environmental educators in the U.S. Virgin Islands, including: Antilles Middle School, Montessori School, Gladys Abraham School, Guy Benjamin School, Gift Hill School, Ulla Muller School, Wesleyan Academy, Tiny Bubbles Snorkel Program, VI Ecotours, Environmental Rangers Program, Coral World, Seagrant Outreach Program on St. Croix, Outreach Proframs of Reef Fest, Earth Day, and Coastweeks, and St. Thomas East Marine Park We also made this book available for free to the public, by posting a PDF file of the book (and outreach photographs) online at: www.sites.google.com/site/anemonesymbionts/ . In 2010, the marine outreach coordinator for the University of the Virgin Islands leveraged additional funds from the Virgin Islands
Community Foundation, to print an additional 500 more copies. These books currently are being used in Saturday Academies for middle school students.
For the hands-on programs for high school students, we completed 2 programs, 1 during each of the 2 years of the Sea Grant. For the first-year program, during December 15-17, 2008, 37 students and 7 teachers from St. Thomas high schools participated: 13 students and 3 teachers from Ivanna Eudora Kean High School (public), 12 students and 1 teacher from Charlotte Amalie High School (public), and 12 students and 3 teachers from the Montessori School (private). All students and teachers participated in reef snorkels and laboratory activities hosted by the MacLean Marine Science Center of the University of the Virgin Islands Each student spent about 4 hours at the marine station, during which they participated in an introductory discussion session on coral reef ecology (facilitated by AU graduate student Ben Titus), a water safety session (UVI water safety officer Steve Prosterman), and in-water guided snorkels on the coral reef. Adult supervision during the snorkels was provided by Lihla Noori (UVI Marine Outreach Coordinator), Ben Titus (AU graduate student), Steve Ratchford (UVI professor), Jackie Calnan (UVI student), and Emily Tyner (Outreach Coordinator for Virgin Islands Marine Advisory Service on St. Croix), and the 7 teachers from the participating schools. Students used disposable underwater cameras to photograph their observations on the coral reef. After the snorkel activity, the students gathered again at the marine station for a post-activity session on food webs on coral reefs. Feedback from the students and teachers was positive, and they gained a fuller understanding of how on-island human activities impact symbioses on local coral reefs. Part of the success of this program was because all of the students had been taught to swim beforehand in public swimming classes, and were selected by their teachers as students who were able to participate fully in water activities on the coral reef. See photographs of the 2008 outreach activity in the pdf file, plus on our program website: http://sites.google.com/site/anemonesymbionts/
For the second year of the high school program, in the springtime we sent a flyer to St. Thomas high schools to advertise the program (see pdf file of flyer). We then screened applications (see file of application form), and selected 8 students who demonstrated high levels of motivation and the basic water skills needed to fully participate in this hands-on educational experience. A group of 10 UVI and AU teaching staff (including faculty members, graduate and undergraduate students, and staff members) planned and organized the program, which was entitled UVI Coral Reef Discovery Week Program, and occurred during July 27-31, 2009, and consisted of the following activities: Monday: Introduction, Team building, Coral Reef Ecology, and Swim and Snorkel Assessment; Tuesday: Coral Reef Health and Monitoring, and Marine Species ID; Wednesday: Mangrove and Seagrass Monitoring; Thursday: GIS Applications to Science, and Friday: Coral Reef and Fish ID Boat Trip, and UVI Undergraduate Research Poster Symposium (see pdf file for detailed daily schedule). The students rated this program as outstanding, as 8.9-10.0 on a scale of 1 to 10. And among other comments, they said that the program substantially raised their awareness and understanding of the conservation issues facing coastal habitats on St. Thomas (see full text of completed evaluation forms and student comments in pdf file). Many of the students expressed interest in this type of educational activity being offered for more than 1 week each summer, and in repeated summers. This type of activity, if well-organized seems to be in high demand among high school students on St. Thomas. Based on this one-year trial, it appears that this type of program would be extremely beneficial for hands-on public education about the ocean on St. Thomas, especially during summers when students do not have to attend school.
The outreach objectives of educating youth in the Virgin Islands concerning the ecological importance of this and other symbioses on coral reefs were completely met, and the hands-on activities generated greater than expected interest and enthusiasm among high school students. The only area where outreach objectives were not fully met was in the distribution of the educational book to a wide range of St. Thomas schools. Problems encountered were that few teachers were interested, and many claimed that they did not have room in their planned curriculum to discuss or use the books. Thus, the books appeared to be more successfully used when distributed to a smaller subset of interested teachers who were able to incorporate them into lesson plans. They also proved useful to distribute through other avenues for reaching youth on St. Thomas (see organizations listed above). The success and educational value of this
book is evidenced in the continued demand and interest in reprinting copies, as described above in the recent grant obtained by UVI. Thus the usefulness of this Sea Grant book extends beyond the original grant period, as a continuing resource for use in educational programs on St. Thomas and for coral reef educational programs worldwide
These outreach programs were designed and executed by a series of 3 Marine Stewardship Coordinaters for UVI (Kemit-Amon Lewis, Lihla Noori, and Christine Settar), in collaboration with the PI, Co-PI, and students at AU and UVI
Discussion of project impacts and products
This project benefits the ornamental fisheries in Puerto Rico and Florida, in that we provide a scientific basis for sustainable management of the fisheries on these sea anemones and crustaceans, which are among the most heavily-collected organisms for the ornamental aquarium trade. Our demographic data also improve the ability of resource managers to forecast recovery rates of these important reef organisms following disturbances. Based on our demographic results, we recommend a minimum body size for collection of these anemones, and limitation of collecting to populations with rapid growth of individuals, located near MPAs for adequate recruitment to ensure population stability
In addition, our outreach program enhanced the marine environmental experience and awareness of Virgin Islands schoolchildren, and caused some of them to consider careers in marine conservation. Our Coral Reef Activity Book is available for printing on our website, and can be used by marine educators worldwide, as well as translated into Spanish for outreach programs in Puerto Rico: Noori L. 2009. Coral Reef Activity Book, 20 pp. Developed for St. Thomas elementary and middle school students. Online copy available at http://sites.google.com/site/anemonesymbionts/ Several graduate and undergraduate students were trained, contributing to future leadership in coral reef conservation. They produced several theses and presentations at national and regional meetings, in addition to several publications in preparation, as listed below.
Students supported
This grant supported 4 graduate students, 2 of which have completed their degrees, and 2 who are still in progress. All were supervised by the P.I. Dr. Chadwick in the Department of Biological Sciences at Auburn University:
Michael Nelsen, michael.nelsen@gmail.com M.Sc. Thesis title: Population dynamic modeling of the corkscrew sea anemone Bartholomea annulata on Caribbean coral reefs. See pdf of entire thesis. Date of entry into graduate program: August 2006. M.Sc. Degree in Biological Sciences granted December 2008. Supported May-August 2008 as a research assistant, $3,300
Lindsay Huebner, lkh0002@auburn.edu M.Sc. Thesis title: The Role of Host Sea Anemones in the Cleaning Mutualism Between Anemoneshrimp and Client Fishes. See pdf of entire thesis. Date of entry into graduate program: August 2008. M.Sc. Degree granted December 2010. Supported JuneAugust 2009 as a research assistant, $2,200.
Benjamin Titus, bmt0004@auburn.edu M.Sc. research proposal title: “Effects of habitat variation on reproductive strategies of the corkscrew anemone Bartholomea annulata on Caribbean coral reefs”. See pdf of thesis proposal. Date of entry into graduate program: August 2008. M.Sc. Degree expected May 2011. Supported June-August 2010 as a research assistant, $2,200.
Ashley Isbell, adi0001@auburn.edu Ph.D. research proposal title: Ensemble structure of crustaceans symbiotic with the Caribbean sea anemone Bartholomea annulata. Date of entry into graduate program: August 2008. Ph.D. Degree expected December 2012. Supported July 2010 as a research assistant, $1,300.
This grant also supported 4 undergraduate students, all supervised by the Co-PI Dr. Ratchford in the Marine Biology Program at the UVI. UVI does not have senior theses or graduate theses, so the projects of these students received recognition in the form of course credits, and salary support and travel funds to present at meetings, from related programs:
Anna-Mai Christmas, annafchristmas@gmail.com
Duration: May to December 2009 Undergraduate research project on competition among anemoneshrimps. This Sea Grant provided the research topic framework, field supplies, and release time for supervisor Dr. Ratchford, but Ms. Christmas also was supported by synergistic programs: National Institutes of Health (NIH) Minority Biomedical Research Support (MBRS) Research Initiative for Scientific Enhancement (RISE) program. Spent 300 hours and earned $3,000.
Adam Ringel, admanat@gmail.com
Duration: August to November 2008. Undergraduate course credits for Directed Independent Research (DIR), spent about 45 hours total during August to November 2008, on his project on anemoneshrimp fidelity to host sea anemones He received course credits instead of pay during this project. This Sea Grant provided field supplies, and release time for supervisor Dr. Ratchford.
Eugene Brooks, eugene417@hotmail.com . Duration: July 2009 – April 2010. Independent research on anemone unburial by anemoneshrimps. Same Sea Grant support as above. Also supported by SSRI (NSF) during summer 2009, and earned 1 credit of DIR in spring 2010. Spent 220 hours on the project, and earned $2,000.
Sanlin Robinson, sanlinsky@hotmail.com . Duration: July to August 2009. Independent research on acclimation of anemoneshrimps to host anemones. Same Sea Grant support as above. Also supported by SURE (NSF), and spent 175 hours to earn $2,000.
Presentations and publications
2010 Huebner, L., Chadwick, N.E. Importance of multi-level symbioses: sea anemones as visual cues in anemoneshrimp cleaning of fish clients on Caribbean coral reefs. 39th Annual Benthic Ecology Meeting, University of North Carolina at Wilmington.
2010 Isbell, A.D., Ratchford, S.G., Chadwick, N.E. Guild structure and microhabitat partitioning among shrimps symbiotic with giant sea anemones on Caribbean coral reefs. 39th Annual Benthic Ecology Meeting, University of North Carolina at Wilmington.
2010 Titus, B.M., Ratchford, S.G., Chadwick, N.E. Effects of habitat variation on of growth, reproduction, and mortality in the corkscrew anemone Bartholomea annulata on Caribbean coral reefs. 39th Annual Benthic Ecology Meeting, University of North Carolina at Wilmington.
2010 Ratchford, S.G., Ringel, A., Chadwick, N.E. Cleaner shrimp symbionts display short term fidelity to host anemones. 39th Annual Benthic Ecology Meeting, University of North Carolina at Wilmington.
2010 Brooks, E. Jr., Ratchford, S.G., Chadwick, N.E. Alpheid shrimp reduce burial time of corkscrew anemones. 39th Annual Benthic Ecology Meeting, University of North Carolina at Wilmington.
2009 Christmas, A.-M., Ratchford, S., Chadwick, N.E. Differences in Aggression May Explain Differences in Numbers of Periclimenes yucatanicus and P. pedersoni Inhabiting Corkscrew Anemones. Annual Biomedical Research Conference for Minority Students (ABRCMS), University of the Virgin Islands, St. Thomas, USVI.
2009 Robinson, S., Ratchford, S., Chadwick, N.E. Snapping Shrimp, Alpheus spp., Instantaneously Acclimate to the Caribbean Corkscrew Anemone Bartholomea annulata Annual Biomedical
Research Conference for Minority Students (ABRCMS), University of the Virgin Islands, St. Thomas, USVI.
2008 Ringel A., Ratchford, S.G., Chadwick, N.E. Cleaner shrimp symbionts display short term fidelity to host anemones Fall Research Symposium, University of the Virgin Islands, St. Thomas, USVI
2008 Nelsen, M., Ratchford, S., Chadwick, N.E. Population dynamics of the corkscrew anemone Bartholomea annulata on Caribbean coral reefs: Implications for anemoneshrimp symbionts and fish cleaning stations. 11th International Coral Reef Symposium, Fort Lauderdale, Florida.
The following 6 manuscripts are in various stages of preparation for submission to journals:
Nelsen MW, Ratchford S, Chadwick NE. 2010. Population dynamics of the corkscrew anemone Bartholomea annulata on Caribbean coral reefs. Marine Biology.
Nelsen MW, Chadwick NE. 2010. Stage-based modeling of demographic processes in the corkscrew anemone Bartholomea annulata Marine Ecology Progress Series
Titus BM, Chadwick NE. 2011 Growth, reproduction, and mortality of the corkscrew anemone Bartholomea annulata. I. Effects of habitat type Journal of Experimental Marine Biology and Ecology
Titus BM, Chadwick NE. 2011. Growth, reproduction, and mortality of the corkscrew Bartholomea annulata II. Effects of feeding regime. Journal of Experimental Marine Biology and Ecology
Huebner LK, Chadwick NE. 2011. Multi-level network effects in cleaning mutualisms: fish clients use sea anemones to locate cleaning stations of anemoneshrimp Proceedings of the Royal Society of London, Series B.
Huebner LK, Ratchford SG, Chadwick NE. 2011. Patterns of client fish use of shrimp cleaning stations on coral reef sea anemones. Marine Biology.
Isbell AD, Ratchford SG, Chadwick NE. 2011. Patterns of biodiversity and abundance of crustacean associates on the corkscrew anemone Bartholomea annulata on Caribbean coral reefs. Coral Reefs
Recommendations
(1) Management of ornamental fisheries in US waters in the Caribbean needs to be re-evaluated, because these anemones and their crustacean associates are overfished and populations are in decline, especially in Florida, but also potentially in Puerto Rico (ornamental collection is not allowed in the US Virgin Islands). Based on our results, managers need to consider limiting the collection of these important anemones to a minimum body size of about 8 cm diameter, which would allow the smallest, fastest-growing individuals to reach sexual maturity. Also, collection needs to be limited to inshore populations that support high abundances and rapid growth rates of individuals, and banned from offshore areas that receive low recruitment of anemones. Finally, collecting needs to be limited to areas near MPAs with abundant anemones, to allow for nearby source populations to replenish these highly dynamic anemones which rely on rapid recruitment to offset their high natural mortality rates. If these measures are not implemented, overall coral reef fish diversity is expected to continue to decline, because these anemones are the major cleaning stations for removal of fish parasites by cleanershrimps on Caribbean coral reefs. Fishes are known to emigrate from reefs that lack cleaning stations.
(2) This complex mutualistic network (zooxanthellae-sea anemone-cleanershrimp-parasites-reef fishes) should continue to be used as a model system to train both undergraduate and graduate students in marine conservation methods on Caribbean coral reefs. This system provides a wealth of important ecological interactions to investigate, and is easily examined by students using lowtech methods of tagging, data recording, census, mapping, and demographic modeling analysis over the short time scales of student projects. It has been used to successfully train 4 graduate students and 4 undergraduates in 2 years, and should be used as a student research training system on coral reefs in the future. Especially, the important links to reef fish biodiversity control should
be examined.
(3) Finally, the outreach programs developed for this project should be modified and expanded to reach more youth in the Caribbean region. The focus on reef symbioses and species relationships was an effective tool that engaged youth to understand reef ecology. The hands-on programs we designed were immensely popular, and all participants expressed an interest in continuation and expansion to expose more children to the field experience. Both the day-long and week-long programs worked well, were inexpensive to run, and resulted in substantial marine environmental experience for middle school and high school students. These hands-on experiences are important, because they plant the seeds for better marine resource awareness and management in future generations. A large number of supporting documents and educational products of this hands-on program are on file with Sea Grant, to support future hands-on programs on coral reefs. The Coral Reef Activity book should continue to be reprinted and used in schools in the US Virgin Islands, Florida, and beyond. It also should be translated into Spanish and used in Puerto Rico outreach programs.
Bibliography
Albrecht, H. 1977. Einige Beobachtungen an Anemonenfischen in der Karibischen See. Bijdrachen tot die Dierkunde 47:109-119.
Babcock, R.C. 1991. Comparative demography of three species of scleractinian corals using age- and size-dependent classifications. Ecol. Monogr. 61:225-244.
Beverton, R.J.H., and S.V. Holt. 1957. On the dynamics of exploited fish populations. Fisheries Investigations of the Ministry of Agriculture, Fisheries and Food (GB) Series II 19:1-553.
Bunkley-Williams, L., and E.H. Williams. 1998. Ability of Pederson cleaner shrimp to remove juveniles of the parasitic cymothoid isopod, Anilocra haemuli, from the host. Crustaceana 71:862-869.
Caswell, H. 2001. Matrix Population Models: Construction, Analysis, and Interpretation, Second Edition. Sinauer Associates, Sunderland, Massachusetts. 722 pp.
Chadwick-Furman, N.E., S. Goffredo, and Y. Loya. 2000. Growth and population dynamic model of the reef coral Fungia granulosa at Eilat, northern Red Sea. J. Exp. Mar. Biol. Ecol. 249:199-218.
Chadwick, N.E., and M. Arvedlund. 2005. Abundance of giant sea anemones and patterns of association with anemonefish in the northern Red Sea. J. Mar. Biol. Assoc. U.K. 85:1287-1292.
Chiappone, M., D.W. Swanson, and S.L. Miller. 2001. Condylactis gigantea- A giant comes under pressure from the aquarium trade in Florida. Reef Encounter 30:29-31.
Chomsky, O., Y. Kamenir, M. Hyams, Z. Dubinsky, and N.E. Chadwick-Furman. 2004. Effects of feeding regime on growth rate in the Mediterranean sea anemone Actinia equina (Linnaeus). J. Exp. Mar. Biol. Ecol. 299:217-229.
Colin, P.L. 1978. Caribbean Reef Invertebrates and Plants. TFH, Hong Kong, 512 pp.
Colin, P.L., and J.B. Heiser. 1973. Associations of two species of cardinalfishes (Apogonidae: Pisces) with sea anemones in the West Indies. Bull. Mar. Sci. 23:521-524.
Ebert, T.A. 1999. Plant and Animal Populations: Methods in Demography. Academic Press, London. 312 pp.
Gerber, L.R., and S.S. Heppell. 2004. The use of demographic sensitivity analysis in marine species conservation planning. Biol. Conserv. 120:121-128.
Goffredo, S., and N.E. Chadwick-Furman. 2003. Comparative demography of mushroom corals (Scleractinia: Fungiidae) at Eilat, northern Red Sea. Mar. Biol. 142:411-418.
Goffredo, S., G. Mattioli, and F. Zaccanti F. 2004. Growth and population dynamics model of the
Mediterranean solitary coral Balanophyllia europaea (Scleractinia, Dendrophylliidae). Coral Reefs 23:433-443.
Goffredo, S., and H.R. Lasker. 2006. Modular growth of a gorgonian coral can generate predictable patterns of colony growth. J. Exp. Mar. Biol. Ecol. 336:221-229.
Gotelli, N.J. 1991. Demographic models for Leptogorgia virgulata, a shallow-water gorgonian. Ecology 72:457-467.
Grigg, R.W. 1977. Population dynamics of two gorgonian corals. Ecology 58:278-290.
Grigg, R.W. 1984. Resource management of precious corals: a review and application to shallow water reef building corals. P.S.Z.N.I. Mar. Ecol. 5:57-74.
Guzner, B., A. Novoplansky, and N.E. Chadwick. 2007. Population dynamics of the reef-building coral Acropora hemprichii as an indicator of reef condition. Mar. Ecol. Prog. Ser. 333:143-150.
Hanlon, R.T., and L. Kaufman L. 1976. Associations of seven West Indian reef fishes with sea anemones. Bull. Mar. Sci. 16:225-232.
Hattori, A. 2006. Vertical and horizontal distribution patterns of the giant sea anemone Heteractis crispa with symbiotic anemonefish on a fringing coral reef. J. Ethol. 24:51-57.
Herrnkind, W., G. Stanton, and E. Conklin. 1976. Initial characterization of the commensal complex associated with the anemone, Lebrunia danae, at Grand Bahama. Bull. Mar. Sci. 26:65-71.
Hirose, Y. 1985. Habitat, distribution and abundance of coral reef sea-anemones (Actiniidae and Stichodactylidae) in Sesoko Island, Okinawa, with notes on expansion and contraction behavior. Galaxea 4:113-127.
Hughes, T.P. 1984. Population dynamics based on individual size rather than age: a general model with a reef coral example. Am. Nat. 123:778-795.
Hughes, T.P., and J.B.C. Jackson. 1985. Population dynamics and life histories of foliaceous corals. Ecol. Monogr. 55:141-166.
Hughes, T.P., and J.H. Connell. 1987. Population dynamics based on size or age? A reef-coral analysis. Am. Nat. 129:818-829.
Hughes, T.P., and J.E. Tanner. 2000. Recruitment failure, life histories, and long-term decline of Caribbean corals. Ecology 81:2250-2263.
Hughes, T.P., A.H. Baird, E.A. Dinsdale, N.A. Moltschaniwskyj, M.S. Pratchett, J.E. Tanner, and B.L. Willis. 2000. Supply-side ecology works both ways: The link between benthic adults, fecundity, and larval recruits. Ecology 81:2241-2249.
Humann, P., and N. DeLoach. 2002. Reef Creature Identification: Florida, Caribbean, Bahamas, Second Edition. New World Publications, Jacksonville, Florida. 420 pp.
Jennison, B.L. 1981 Reproduction in three species of sea anemones from Key West, Florida. Can. J. Zool. 59:1708-1719.
Kaplan, E.H. 1982 A Field Guide to Coral Reefs: Caribbean and Florida. Houghton Mifflin, New York. 289 pp.
Knowlton, N., and B.D. Keller. 1983. A new, sibling species of snapping shrimp associated with the Caribbean sea anemone Bartholomea annulata. Bull. Mar. Sci. 33:353-362.
Knowlton, N., and B.D. Keller. 1985. Two more sibling species of alpheid shrimps associated with the Caribbean sea anemones Bartholomea annulata and Heteractis lucida. Bull. Mar. Sci. 37:893-904.
Lasker, H.R. 1991. Population growth of a gorgonian coral: equilibrium and non-equilibrium sensitivity to changes in life history variables. Oecologia 86:503-509.
LeGore, R.S., M.P. Hardin, and D. Ter-Ghazaryan. 2005. Organization and operation of the marine ornamental fish and invertebrate export fishery in Puerto Rico. Int. J. Trop. Biol. 53:145-153.
Lirman, D. 2003. A simulation model of the population dynamics of the branching coral Acropora palmata: Effects of storm intensity and frequency. Ecol. Model. 161:169-182.
Lirman, D., and M.W. Miller. 2003. Modeling and monitoring tools to assess recovery status and convergence rates between restored and undisturbed coral reef habitats. Restor. Ecol. 11:448-456.
Morin, P.J. 1999. Community Ecology. Blackwell Science, Oxford. 423 pp.
Nizinski, M.S. 1989. Ecological distribution, demography and behavioral observations on Periclimenes anthophilus, an atypical symbiotic cleaner shrimp. Bull. Mar. Sci. 45:174-188.
Porat, D., and N.E. Chadwick-Furman. 2004. Effects of anemonefish on giant sea anemones: expansion behavior, growth, and survival. Hydrobiologia 530:513-520.
Rose, K.A., and J.H. Cowan. 2003. Data, models, and decisions in U.S. marine fisheries management: Lessons for ecologists. Ann. Rev. Ecol. Evol. Syst. 34:127-151.
Sargent, R.C., and G.E. Wagenbach. 1975. Cleaning behavior of the shrimp, Periclimenes anthophilus Holthuis and Eibl-Eibesfeldt (Crustacea: Decapoda: Natantia). Bull. Mar. Sci. 25:466-472.
Sebens, K.P. 1983. Population dynamics and habitat suitability of the intertidal sea anemones Anthopleura elegantissima and A. xanthogrammica. Ecol. Monogr. 53:405-433.
Sefton, N., S.K. Webster. 1986. Caribbean Reef Invertebrates. Sea Challengers, Monterey. 112 pp.
Shuman, C.S., G. Hodgson, and R.F. Ambrose. 2005. Population impacts of collecting sea anemones and anemonefish for the aquarium trade in the Philippines. Coral Reefs 24:564-573.
US Virgin Islands Department of Education. 2006. Planning, Research, and Evaluation. SASI Database.