Review

Marine Biodiversity in the Caribbean: Regional Estimates

and Distribution Patterns
Patricia Miloslavich1,2*, Juan Manuel Dı́az3, Eduardo Klein1,2, Juan José Alvarado4, Cristina Dı́az5, Judith
Gobin6, Elva Escobar-Briones7, Juan José Cruz-Motta1,2, Ernesto Weil8, Jorge Cortés4, Ana Carolina
Bastidas9, Ross Robertson10, Fernando Zapata11, Alberto Martı́n1,2, Julio Castillo2,3, Aniuska
Kazandjian2,9, Manuel Ortiz12
1 Departamento de Estudios Ambientales, Universidad Simón Bolı́var, Caracas, Venezuela, 2 Centro de Biodiversidad Marina, Universidad Simón Bolı́var, Caracas,
Venezuela, 3 Universidad Nacional de Colombia, Bogotá, Colombia, 4 Universidad de Costa Rica, El Centro de Investigación en Ciencias del Mar y Limnologı́a (CIMAR), San
José, Costa Rica, 5 Museo del Mar, Margarita, Venezuela, 6 Department of Life Sciences, University of West Indies, St. Augustine, Trinidad and Tobago, 7 Universidad
Nacional Autónoma de México, Instituto de Ciencias del Mar y Limnologı́a, Mexico City, Mexico, 8 Department of Marine Sciences, University of Puerto Rico, Lajas, Puerto
Rico, 9 Departamento de Biologı́a de Organismos, Universidad Simón Bolı́var, Caracas, Venezuela, 10 Smithsonian Tropical Research Institute, Balboa, Ancón, Panamá,
11 Department of Biology, Universidad del Valle, Cali, Colombia, 12 Centro de Investigaciones Marinas, Universidad de La Habana, La Habana, Cuba

This paper provides an analysis of the distribution patterns of from the Atlantic Ocean and acts as a sieve for the inflow of
marine biodiversity and summarizes the major activities of the Atlantic water [1], whereas toward the northwest the Caribbean is
Census of Marine Life program in the Caribbean region. The linked to the Gulf of Mexico by the Yucatan Channel. The
coastal Caribbean region is a large marine ecosystem (LME) Caribbean seafloor is divided into five basins (Grenada, Vene-
characterized by coral reefs, mangroves, and seagrasses, but zuela, Colombia, and Yucatan Basins and the Cayman Trough)
including other environments, such as sandy beaches and rocky separated from each other by underwater ridges and sills. Half of
shores. These tropical ecosystems incorporate a high diversity of the waters in the Caribbean are deeper than 3,600 m, and 75%
associated flora and fauna, and the nations that border the are deeper than 1,800 m [2]. The average seafloor depth is about
Caribbean collectively encompass a major global marine biodi- 2,400 m, while the Cayman Trough, between Cuba and Jamaica,
versity hot spot. We analyze the state of knowledge of marine reaches more than 7,500 m [3]. Volcanic activity and earthquakes
biodiversity based on the geographic distribution of georeferenced are common in the Caribbean, as are destructive hurricanes, most
species records and regional taxonomic lists. A total of 12,046 of which originate in the central Atlantic.
marine species are reported in this paper for the Caribbean region. The Caribbean has an overall counterclockwise circulation
These include representatives from 31 animal phyla, two plant (Figure 1). The Caribbean Current enters the southeast corner of
phyla, one group of Chromista, and three groups of Protoctista. the basin through several passages of variable sill depth between the
Sampling effort has been greatest in shallow, nearshore waters, Lesser Antilles and, to a lesser extent, the Windward Passage, and
where there is relatively good coverage of species records; offshore slightly increases its velocity as it flows west-northwesterly into the
and deep environments have been less studied. Additionally, we Gulf of Mexico through the Yucatan Channel, where it forms the
found that the currently accepted classification of marine Gulf Stream (see [4]). Caribbean waters are mostly clear and warm
ecoregions of the Caribbean did not apply for the benthic (22–29uC), and the tidal range is very low (,0.4 m) [5]. The water
distributions of five relatively well known taxonomic groups. column is highly stratified in the upper 1,200 m because of the sill
Coastal species richness tends to concentrate along the Antillean depths of the Antilles Islands arc, which prevents the flow of deep
arc (Cuba to the southernmost Antilles) and the northern coast of water into the Caribbean Basin [6]. The Caribbean geology was
South America (Venezuela – Colombia), while no pattern can be recently reviewed by Jackson [7]. The deep Caribbean Sea evolved
observed in the deep sea with the available data. Several factors by seafloor spreading since the Jurassic, but the key aspects of the
make it impossible to determine the extent to which these tectonic history have been subject to controversy [8,9]. Two models
distribution patterns accurately reflect the true situation for marine explain the late Mesozoic formation and the evolution of the
biodiversity in general: (1) highly localized concentrations of
collecting effort and a lack of collecting in many areas and
Citation: Miloslavich P, Dı́az JM, Klein E, Alvarado JJ, Dı́az C, et al. (2010) Marine
ecosystems, (2) high variability among collecting methods, (3) Biodiversity in the Caribbean: Regional Estimates and Distribution Patterns. PLoS
limited taxonomic expertise for many groups, and (4) differing ONE 5(8): e11916. doi:10.1371/journal.pone.0011916
levels of activity in the study of different taxa. Editor: Simon Thrush, NIWA, New Zealand
Received March 11, 2010; Accepted June 16, 2010; Published August 2, 2010
Introduction Copyright: ß 2010 Miloslavich et al. This is an open-access article distributed
under the terms of the Creative Commons Attribution License, which permits
Physical and geological description of the Caribbean unrestricted use, distribution, and reproduction in any medium, provided the
The Caribbean Sea is a semienclosed basin of the western original author and source are credited.
Atlantic Ocean, bounded by the coasts of Central and South Funding: The Alfred P. Sloan Foundation, the Centro de Biodiversidad Marina
America on two sides and by the Antilles island chain on the other CBM and the Decanato de Investigación y Desarrollo of the Universidad Simon
Bolivar provided funds for this work. The Smithsonian Marine Sciences Network
two (Figure 1). It has an area of about 2,754,000 km2, a volume of provided financial support of the fish work. The funders had no role in study
nearly 6.56106 km3, and over 13,500 km of coastline, and is design, data collection and analysis, decision to publish, or preparation of the
home to 26 countries as well as 19 dependent territories of France, manuscript.
the Netherlands, the United Kingdom, and the United States. Competing Interests: The authors have declared that no competing interests
Toward the east and northeast, the closely spaced chain of islands, exist.
banks, and sills of the Antilles Islands arc separates the Caribbean * E-mail: [email protected]

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 Caribbean Marine Biodiversity

Figure 1. Bathymetry, main currents, and ecosystems of the Caribbean Sea. Arrows representing average surface ocean currents were
derived from the Hybrid Coordinate Ocean Model, or HYCOM (http://hycom.org). Coral reef data were obtained from the World Resources Institute
(http://www.wri.org/publication/reefs-risk-caribbean). Data on seagrasses were extracted from version 2.0 of the global polygon and point dataset
compiled by UNEP World Conservation Monitoring Centre (UNEP-WCMC), 2005. Mangrove data were extracted from version 3.0 of the global polygon
dataset compiled by UNEP-WCMC in collaboration with the International Society for Mangrove Ecosystems (ISME), 1997.
doi:10.1371/journal.pone.0011916.g001

Caribbean Plate. The first suggests that the Caribbean crust was oceanic water masses in the region. The Orinoco plume spreads
formed between the South American and North American plates widely over the Caribbean affecting significantly the optical
(model reviewed in Meschede and Frisch [10]). The second suggests a properties of the water in the eastern Caribbean Sea by
late Mesozoic origin of the Caribbean crust in the Pacific region as a introducing large amounts of colored dissolved organic matter
result of a flood basalt event at the Galapagos hot spot and a later drift and nutrients and thus increasing primary productivity [16].
to the east during the Cenozoic times [11–13]. Meschede and Frisch Elevated pigment concentrations are visible within the southern
[14], concluded from geological, geochronological, and paleomag- Caribbean where the shoaling of the deep chlorophyll maximum
netic evidence that the Caribbean crust was originally formed in an and dispersal of the water mass occur [17]. The sediment and
inter-American position (adjacent to the northwestern margin of organic matter particles transported from the Orinoco and
South America) during the middle to upper Cretaceous, not in the Amazon rivers by the northward moving Guiana current enter
Galapagos hot spot, and that the source for the Caribbean flood and disperse in the Caribbean Sea and the near Atlantic [18] and
basalt must be a plume between the two Americas that was active are deposited on the western flank of the Aves Ridge. Higher
during the middle and upper Cretaceous. The Eocene basalt and the zooplankton production in the southeastern Caribbean may also
pelagic cover formed a relatively deep floor in which arc-derived enhance transport of organically rich suspended matter into fecal
turbidites and pelagic sediments have accumulated over 25–30 pellets that have accelerated sinking rates (Richardson et al 1995).
millions of years. This labile organic matter raining from the overlying water is
The ratio of continental margin to total open ocean area in the tightly coupled with the benthic assemblages in the Venezuela
Caribbean basin is larger than in the major ocean basins, meaning Basin [19]. Based on penetration profiles done with an
that the margins have greater potential importance to physical, echosounder, a continuous sedimentation from the water column
geological, and biological processes. Major river systems and to the seafloor characterizes the Puerto Rico Trench. The top
associated features characterize the seafloor on the continental 10 cm of this sediment is brown to brownish gray and shows
shelf and influence the offshore habitats with sediment input. The evidence of both coastal and pelagic input [20].
coastal ecosystems in the Intra Americas Sea (IAS) are highly The most characteristic ecosystems in the Caribbean are coral
productive in contrast to the oligotrophic offshore waters, and are reefs covering about 26,000 km2 [21], seagrass beds with an area
mainly characterized by particulate organic carbon (POC) flux. In of about 66,000 km2 [22], and mangroves at nearly 11,560 km2
offshore waters the pelagic deposition and turbidity currents have [23]. Although the Caribbean has been considered as oligotrophic,
been correlated with the benthic macrofaunal standing stock [15]. it can be better defined as mesotrophic, depending on the time of
With the exception of restricted turbid coastal areas near rivers, the year [24]. The intrusion of the Orinoco River during autumn
the most salient feature of the IAS is its warm, transparent water, generates large concentrations of chlorophyll a in the eastern
compared to other large ocean systems. This water clarity is a Caribbean, which can be carried up to the island of Puerto Rico
function of the oligotrophic conditions and strong influence of [24]. Moreover, strong trade winds during winter and spring are

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 Caribbean Marine Biodiversity

responsible for coastal upwelling along much of the coastline of in the region, our present knowledge about Caribbean marine
northeast Colombia and Venezuela, bringing nutrients to the biodiversity and species distribution does not satisfy the needs for
surface and increasing the concentration of phytoplankton objectively defining geographic conservation priorities and design-
biomass in that area [1,25]. The deep-sea habitats in the ing management plans at a regional scale. This is one of the
Caribbean Sea and surrounding areas include typical abyssal reasons why conservation planners often make use of surrogates of
soft-sediment extensions, numerous small canyons [26], and wide species diversity (e.g., presence of habitats, bottom topography,
(10 km) and low-relief (,5 m) channels over the Orinoco deep-sea wave exposure) to offset uncertainty and lack of detailed
fan, an accretionary prism near Barbados [27], seamounts (e.g., information (see [52,53]), as has been the case in various recent
Niobe, Chı́a, Ubaté, Calima), ridges (e.g., Tayrona, Aves), hills attempts to determine the relative importance of sites for
(e.g., Aracataca, Tumaco, Pijao), tablemounts (Explorer) where conservation in the Caribbean (e.g., [54–56]).
encrusting coralline algae have been recorded at 268 m depth in Although the first scientific expedition to the New World did not
the Bahamas [28], knolls (e.g., Naquı́, Nectier), and escarpments occur until 1799, species discoveries and descriptions of marine
(Hess). According to the latest marine biogeographic classification organisms from the Caribbean started several years earlier from
system into marine ecoregions (Marine Ecoregions of the World or preserved fishes, coral skeletons, and mollusk shells collected
MEOW) [29], the Greater Caribbean is part of the Tropical during exploration voyages. These samples were transported to
Northwestern Atlantic Province which comprises nine ecoregions: Europe, where they were described and deposited in museum
Western Caribbean, Southwestern Caribbean, Eastern Caribbean, collections. With a few exceptions, such as Charles B. Adams
South Caribbean, Greater Antilles, Bermuda, Bahamian, South- (1814–53) and William Stimpson (1832-72), who spent several
ern Gulf of Mexico, and Floridian. In this paper, we will focus on years collecting and studying marine mollusks in the Caribbean,
the first five ecoregions, which include the entire Caribbean basin most of the taxonomists who described marine species from the
and the north of the islands of the Greater Antilles. The other four Caribbean until the end of the nineteenth century were land
ecoregions are developed in another article in this collection [30]. based, working in museums or universities. Such taxonomists
seldom collected specimens themselves in the field and had a
History of exploration of marine biodiversity in the limited knowledge of the distribution and ecology of the samples
Caribbean they received. With only a single specimen of each species, a shell,
Species inventories are the most elementary data in ecology, or a fragment of a colony, these naturalists worked with a
biogeography, and conservation biology. Species records are magnifier, a lamp, paper, ink, and a pen on a bench, with
mostly used to determine the number of species occurring in a approximate information about the locality where the specimen
given area, but they can also be employed to determine was found. Local and geographic morphological variability could
distribution patterns, for the identification of biodiversity ‘‘hot not be assessed. Nevertheless, they did a remarkable job with their
spots’’ or for designing conservation strategies [31,32]. descriptions and drawings. By the beginning of the twentieth
Species extinction has reached unprecedented rates on both century, about half of the marine species known today from the
land and ocean [33,34], and these rates are much higher than Caribbean had already been described.
those of new species discovery [35,36]. This suggests that there is a A remarkable impulse to the knowledge of Caribbean species
crisis in global information or, in other words, a critical weakness diversity, particularly from deep waters, stemmed from several
in the world’s ‘‘knowledge economy’’ [37]. The increasing human scientific cruises conducted in the late nineteenth century. In
impacts on marine biodiversity and the need to optimize and set particular, the cruises of the U.S. Coast Survey vessel Blake (1877-80),
priorities among limited resources for implementing conservation under the scientific supervision of Alexander Agassiz, became a
measures have impelled the description of diversity patterns and, pivotal event in the exploration of the Gulf of Mexico and the
consequently, have encouraged the use of taxonomic inventories Caribbean; hundreds of species of hydroids, corals, antipatharians,
[38,39]. However, the use and comparability of species inventories crustaceans, echinoderms, annelids, mollusks, fishes, and other
are limited by the extent of their completeness and the organisms from depths of up to 3,000 m were described based on the
heterogeneity of sampling effort between sites or areas [40]. collections obtained from the Blake expeditions. A second impetus in
The Caribbean contains the greatest concentration of marine Caribbean species inventories occurred in the 1970s with the advent
species in the Atlantic Ocean and is a global-scale hot spot of of scuba diving and more extensive collections that greatly helped to
marine biodiversity [32]. Because the Caribbean is regarded as a refine the taxonomical classifications and increase the knowledge of
distinct biogeographic province of the Tropical Western Atlantic the taxonomy, ecology, and variability of many groups.
Region, several authors (e.g., [29,41–46]) have proposed more
detailed biogeographic regionalizations within the Caribbean, Research capacity in the Caribbean region
using a variety of criteria for defining divisions. Most Caribbean countries (with the exception of Haiti,
The growth of human population, particularly in coastal zones, Honduras, Guatemala, Nicaragua, and some of the small insular
and the environmental pressures imposed by economic growth states) have well-known marine research stations and laboratories,
and climate change pose great challenges to the future which are usually tied to academic institutions with long-standing
conservation of marine ecosystems and species diversity. In traditions in the study of marine organisms. The majority of them,
particular, the Caribbean Sea has large population densities, a despite different cultures, financial resources, and capabilities, have
long history of human use of marine resources, and remarkable developed a common interest in cooperation and networking since
land-based sources of pollution associated with oil production, port the 1980s, through national and local government departments and
and tourism development, deforestation, and agriculture [45,47]. nongovernmental organizations (NGOs); universities and other
The areal coverage of mangroves in the Caribbean has decreased tertiary learning institutions; regional intergovernmental organiza-
by about 1% per year since 1980 [47]. Live coral cover has already tions (IGOs); UN organizations; and international NGOs.
declined by as much as 80% in many areas of Caribbean reefs The first regional marine science organization in the Caribbean,
over the last two decades because of various human activities and the Association of Marine Laboratories of the Caribbean (AMLC),
global warming [48,49], and 35% of the region’s fish stocks are was established in 1957 by nine research institutions. It evolved into a
overexploited [50,51]. Despite a long history of scientific research confederation of more than 30 marine research, education, and

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 Caribbean Marine Biodiversity

resource management institutions and more than 300 individual across the Caribbean seafloor. Besides these projects, the region
members. Its main objective is to encourage the production and also participated in Antarctic research with the Census of
exchange of research and resource management information, to Antarctic Marine Life (CAML) project. The Caribbean region
advance the cause of marine and environmental education in the also contributed substantial amounts of data to the Ocean
region, and to facilitate cooperation and mutual assistance among its Biogeographic Information System (OBIS) database and proposed
membership (www.amlc-carib.org/). One of the most successful a sister project to the established Census of Coral Reef Ecosystems
research programs developed on the strength of the AMLC was the (CReefs), aimed to update and clarify the taxonomy and
Caribbean Coastal Marine Productivity Program (CARICOMP), distribution of the major benthic coral reefs groups. In addition,
which was a regional scientific program supported by UNESCO and it established a network of researchers associated with the
the U.S. National Science Foundation. The aims of this program International Census of Marine Microbes (ICoMM) project.
included the monitoring of long-term changes in the three main Besides contributing significantly to the knowledge of marine
coastal ecosystems in the Caribbean region—mangroves, seagrass biodiversity in the Caribbean region, the Census established
beds, and coral reefs, while it left the offshore and deep-sea habitats regional networks for scientific cooperation.
remaining poorly documented. Monitoring activities and data In 2005 the United Nations General Assembly endorsed the
collection began in 1992 at 29 sites in 22 countries and territories, need for a regular process for global reporting and assessment of
using standard research methods, building regional capacity the state of the marine environment. The ‘‘Assessment of
and shared expertise (http://www.unesco.org/csi/act/caricomp/ Assessments,’’ begun during the start-up phase of the process,
summary14.htm). Data was archived at the CARICOMP Data has as its main objective an overview of the geographic and
Centre at the University of the West Indies in Jamaica. While this thematic coverage of existing assessments on oceans and coastal
program has formally ended, at present, CARICOMP monitoring areas at regional and global levels. The assessment established the
activities still take place in Colombia, Panama, Costa Rica, and relative importance of issues being assessed in the region and
Venezuela, among other sites. Currently, discussions are being held analyzed the capability of the region to undertake future
within the AMLC about the need to continue a regional monitoring assessments of issues that have clear links to neighboring regions.
program. These future assessments include biodiversity, ecosystems (corals,
Another remarkable regional scientific initiative in the region mangroves, seamounts), mammals, genetic resources, and invasive
includes the Cooperative Investigations of the Caribbean and alien species. The spatial framework developed for the Assessment
Adjacent Regions (CICAR) dating back to the 1970s. Its aim was of Assessments is based on both biogeographic factors and
to develop capabilities among the participating countries to carry administrative structures conducive to an ecosystem approach.
out marine scientific research and the understanding of oceano- The Caribbean Sea was recognized as such an entity for that
graphic processes in the Caribbean region [2]. As a successor assessment.
organization to CICAR, in 1982 IOCARIBE (the Sub-Commis- Here we analyze the state of knowledge of Caribbean marine
sion for the Caribbean and Adjacent Regions, of the Intergov- biodiversity using georeferenced species-record data and species
ernmental Oceanographic Commission (IOC) of UNESCO) was lists for localities within that region. Our first goal is to analyze
created, with 19 member states. spatial heterogeneity of the data to determine gaps in knowledge
A Protocol of the Convention for the Protection and and the effect of biases in the distribution of geographical data
Development of the Marine Environment of the Wider Caribbean within the established ecoregional biogeographical divisions in
Region came in effect into 1986 to protect the endangered marine the Caribbean. Our second goal is to assess patterns in the
life of the Caribbean by prohibiting human activities that would distribution of members of these five groups of marine organisms
result in the continued destruction of such marine life in various and test if species distribution actually fits to the biogeographic
areas. The protocol has been ratified by 15 countries and diverse model of the five ecoregions proposed. The paper also discusses
NGOs, such as The Nature Conservancy, the World Wildlife the role of the Census of Marine Life program in advancing
Fund, and the Caribbean Conservation Corporation, that have knowledge about marine biodiversity in the Caribbean as well as
been involved in the preservation of Caribbean marine life. The the major threats to marine biodiversity in the region. Our hope
Census of Marine Life (Census) program became involved in the with this paper is to increase awareness of the value of taxonomic
region in 2004 with the Caribbean Marine Biodiversity Workshop. inventories and of how much and where scientific sampling is
In this workshop, 10 of the largest Caribbean countries reviewed needed to understand better the large-scale geography of
the status of knowledge of marine biodiversity within their Caribbean marine biodiversity.
boundaries (Venezuela, Colombia, Panama, Costa Rica, Mexico,
Bermuda, Cuba, Jamaica, Puerto Rico, and the Dominican Methods
Republic), resulting in the production of a regional report (see
[39]). The workshop also led to a productive interaction between To compile available data on marine species diversity in the
researchers, conservation agencies, and oil companies, which Caribbean, we used two approaches. The first approach was to
established links for international collaboration and future summarize the number of species for all taxonomic groups using
partnerships within the Census umbrella. The main projects that georeferenced species records from open-access databases (espe-
the Census advanced in the Caribbean region were History of cially OBIS) and from local, country, territory, and regional
Marine Animal Populations (HMAP), Natural Geography in checklists. The second approach was to produce revised species
Shore Areas (NaGISA), Continental Margin Ecosystems on a lists for the relatively well known taxonomic groups (sponges, stony
Worldwide Scale (COMARGE), and Biogeography of Deep- corals, polychaetes, mollusks, amphipods, and echinoderms) by
Water Chemosynthetic Ecosystems (ChEss). These projects carried country or subregions (where there is information available). Only
out field work in several sites in the region and the data can be taxonomically valid species were included, based on the expertise
found in the Ocean Biogeographic Information System (OBIS). of taxonomist authors of this paper. Introduced and invasive
The most recent of these expeditions (April 2010) was the British species were also incorporated. We also reviewed records of the
cruise on the Royal Research Ship James Cook to the Cayman distribution of shallow-water shore fishes within the Caribbean, as
Trough, the world’s deepest undersea volcanic rift, which runs well as deep-sea records (below 200 m depth) for all taxonomic

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 Caribbean Marine Biodiversity

groups. The main data sources used for constructing these known as Hispaniola Island), Cayman Islands, (5) Eastern Caribbean:
matrices are presented in Table 1, which lists the essential Barbados, Virgin Islands, and combined information from several
literature for marine biodiversity studies in the Caribbean. of the islands comprising the Lesser Antilles. To analyze the
In order to test the hypothesis of different species composition relative contribution of each ecoregion to the Caribbean regional
assemblages for each of the five marine ecoregions of the diversity (gamma diversity), we used the contribution partition
Caribbean area (as proposed by Spalding et al. [29]), we used a analysis proposed by Lu et al. [59]. Each ecoregion’s species list
permutational multivariate ANOVA [57] as implemented in R (richness) represents the ecoregional diversity. According to the
package ‘‘vegan’’ [58]. Using the country presence-absence matrix partition of species diversity, where the regional (gamma) diversity
for each taxonomic group, we estimated a dissimilarity matrix is the sum of the local (alpha) and interlocal (beta) diversity, an
based on Sorensen’s index, and then each country was recoded as index of relative contribution of each term could be estimated. For
a member of its particular ecoregion. If the ecoregional pattern for each ecoregion, the greater the number of species that are listed,
a particular taxa represents different species assemblages, a the higher its alpha diversity. However, depending on the number
statistically different community ordination should result in the of endemic or exclusive species in an ecoregion, the relevance of
analysis. A graphical representation of the ordination was made this ecoregion to the relative contribution to the gamma diversity
using a non-metric multidimensional scaling, so countries within could change. The same analysis was done for individual countries
the same marine ecoregion would be expected to group closely in to determine which of the countries within each ecoregion
the MDS. Countries or territories considered within each of the contributed more to the gamma diversity. For example, a country
marine ecoregion were: (1) Western Caribbean: Mexico, Belize, or subregion with few species, many of which are endemic (or
Honduras, Guatemala, (2) Southwestern Caribbean: Nicaragua, Costa exclusive), contributes more to the regional diversity than a
Rica, Panama, Colombia, San Andres Island, (3) Southern Caribbean: country with many but wide-ranging species.
Venezuela, the Netherland Antilles (Aruba, Bonaire and Curacao), Additionally, to assess whether or not the rate of discovery of a
Trinidad and Tobago, (4) Greater Antilles: Cuba, Jamaica, Puerto particular type of fauna shows a tendency to decline, thus
Rico, Dominican Republic, Haiti (these last two together are also indicating that we are approaching its full description, we

Table 1. Sources of data used to estimate total number of marine species for different taxa and for the deep sea.

Taxa/Environment Literature, museum and database sources

Algae [159–162]
Museums: HNV, MMM
Databases: www.obis.org
Porifera [72,89–92,114,163–187]
Databases: www.marinespecies.org/porifera / www.spongeguide.org / www.obis.org
Scleractinia [95,186,188,189–202]
Databases: www.reefbase.org
Polychaeta [203–207]
Mollusca [137,208–220]
Museums: MHNMC, NMNH
Databases: www.malacolog.org / www.sealifebase.org / www.marinespecies.org
www.cephbase.utmb.edu / www.redciencia.cu/cdbio/Contenido
www.jaxshells.org/cayman.htm / www.jaxshells.org/abc.htm
Amphipoda [221–239]
Museums: GCCAS, USB-ANF, UMML, MNCN, MBUCV, ZMA, BMNH
Databases: www.obis.org
Echinodermata [82,105,107,109,240–279]
Museums: GCCAS
Databases: www.itis.gov
Pisces [115,280–289]
Museums: NMNH
Databases: www.obis.org / Personal database of coauthors DRR and FAZ
Deep sea (*) [251,261,263,274,279,290-297]

GCCAS: Geology Collection of the California Academy of Sciences, San Francisco, USA.
USB-ANF: Collection of Peracaridean Crustaceans – Amphipods from Museo de Ciencias Naturales – Universidad Simón Bolı́var, Caracas, Venezuela.
UMML: Marine Invertebrate Museum, Rosenstiel School of Marine and Atmospheric Science, University of Miami, USA.
MNCN: Museo Nacional de Ciencias Naturales, Madrid, Spain.
MBUCV: Museo de Biologı́a de la Universidad Central de Venezuela, Caracas, Venezuela.
ZMA: Zoological Museum of Amsterdam, Amsterdam, The Netherlands.
BMNH: British Museum of Natural History, London, UK.
HNV: Herbario Nacional de Venezuela, Caracas, Venezuela.
MMM: Museo del Mar, Isla de Margarita, Venezuela.
MHNMC: Museo de Historia Natural Marina de Colombia, INVEMAR, Santa Marta, Colombia.
NMNH: National Museum of Natural History, Washington D.C., USA.
(*)The deep-sea review encompasses 1,530 species grouped in 12 phyla [Porifera, Cnidaria, Chaetognata, Mollusca, Sipunculida (still considered separate from
Annelida), Annelida (subdivided into Polychaeta and Echiura), Bryozoa/Ectoprocta, Brachiopoda, Pycnogonida, Crustacea, Echinodermata, and Cephalochordata
(demersal fish only)].
doi:10.1371/journal.pone.0011916.t001

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 Caribbean Marine Biodiversity

established the number of new species described per year and and Bermuda. Since the Caribbean shares many species with these
plotted accumulation curves for fishes, mollusks, and echinoderms. adjacent regions, each of which has its own endemics, estimates of
Since the quality of taxonomic inventories depends strongly on the endemism for the Greater Caribbean are likely to be higher.
availability of identification guides and taxonomic experts, our With the exception of mangroves, seagrasses, mammals, birds,
review also included an account of these resources for each and reptiles, we can expect that the number of species recorded in
taxonomic group (Table 1). the Caribbean will increase in the future for the majority of taxa,
particularly for those groups scored lower than 3 for ‘‘state of
Results knowledge’’ in Table 2 and Table S1. However, even for relatively
well known groups, such as mollusks, echinoderms, and fishes, the
Taxonomic inventories inventories have by no means been completed, and further
At least 12,046 species have been reported to occur in the discoveries (descriptions of new species or first Caribbean records
Caribbean Sea (Table 2, Table S1). These include representatives of known species) ought to be expected. For relatively well known
from 31 animal phyla, two plant phyla (green and red algae and and not very species-rich groups, such as echinoderms, the
Angiospermae: mangroves and seagrasses), one group of Chro- accumulation curve of species discovery in the Caribbean shows
mista (brown algae), and three groups of Protoctista (Foraminifera, that it is approaching an asymptote. In contrast, the accumulation
Dinoflagellata and Amoebozoa). The quality of information curves of species-rich groups, including mollusks and fishes
available differs considerably among these taxa, and only poor (Figure 2), suggest that a full inventory of these taxa is still far
information is available on bacteria, Cyanophyceae, and diatoms from being completed and that, despite the long history of
(Chrysophyta). For the Dinoflagellate (Pyrrhophyta), 85 inverte- collecting in a relatively small area, there are still many species to
brate species within the Anthozoa, Hydrozoa, Scyphozoa, be discovered. As an example that supports this assertion, the map
Actinaria, Gorgonacea, Zoanthidae, Corallimorpharia, and Gas- on Figure 3 shows the spatial distribution of 161,000 datapoints
tropoda have been reported to have one or more clades of the representing historical fish records in the Greater Caribbean,
symbiont dinoflagellate Symbiodinium, with a total of 31 different which represent 2,927 areas or localities of 10610 km. That
clades (Table 3, Table S2). For many taxonomic groups, the distribution indicates that within this region, large areas, even
number of known species is constantly increasing as new species along the coastal zones, are seriously undersampled. Those areas
are described or are recorded for the first time in the region. include a large portion of Cuba, the large area of continental shelf
Knowing the taxonomic background (availability and expertise) of off Nicaragua and Honduras, the ocean banks between Nicaragua
the region, we had not expected to be able to produce species lists and Jamaica and between Honduras and the Caymans, all of
of the same quality for the different taxonomic groups. However, Hispaniola, the extreme northeastern Lesser Antilles, and some of
for most of the groups, our review can be considered satisfactory. the reefs offshore from Venezuela. In general, sampling effort has
We consider only 16 of the 78 (about 20%) species counts at the been best for shallow nearshore waters, where there is relatively
phylum to order level (Table 2 and Table S1) deficient in quality good coverage of species records, especially along the southern
or incomplete: Fungi, Placozoa, Entoprocta, Brachiopoda, Phor- Caribbean coasts (Belize, Costa Rica, Panama, Colombia, and
onida, Nemertea, Gnathostomulida, Pogonophora, Rotifera, Venezuela), in Puerto Rico, and much of the Lesser Antilles.
Priapulida, Kinorhyncha, Tardigrada, Nematoda, Branchiopoda The collecting effort in settings deeper than 200 m has been
(Cladocera), Ostracoda, and Urochordata. Species in these taxa concentrated along the Mexican and Colombian continental
represent probably less than 5% of the species reported in Table 2. slopes and abyssal plains, the north and south coasts of the eastern
The counts for the remaining groups should be considered two-thirds of Cuba, the south coast of Jamaica, and the Lesser
satisfactory, with a presumable error margin of less than 5%. Antilles arc. Elsewhere in the Caribbean, records are much more
However, about half of these counts would greatly benefit from sparse and scattered. Very few records exist for areas between
further taxonomic review. No species were reported from four Honduras and Panama, along the shelf north of Venezuela, and
phyla (Nematomorpha, Loricifera, Micrognathozoa, and Cyclio- off western Cuba (Figure 4). The Caribbean basin deep-sea species
phora), which is probably because of a lack of taxonomic attention database includes 1,530 species grouped in 12 phyla: Porifera,
rather than the absence of these groups from Caribbean waters. By Cnidaria, Chaetognata, Mollusca, Sipunculida, Annelida, Bryo-
far, the most speciose taxa are Mollusca (3,032 species), Crustacea zoa/Ectoprocta, Brachiopoda, Pycnogonida, Crustacea, Echino-
(2,916 species), and Pisces (1,336 species), which together account dermata, and Cephalochordata (demersal fish only). Further, the
for about 60% of the total biota. Mollusks are also the most diverse data derived from these distributions of sampling effort in the deep
group for all countries and ecoregions (Table 4). sea, even in relatively heavily sampled areas, are limited by the fact
The number of endemic species could be established with that different sampling methods were used in different areas and
relatively high confidence for only 21 of the 78 higher taxa (27%) that the long history of collecting has occurred in bursts of activity
(Table S1). The total number of endemic species for those taxa is in different places at different times.
1,563, which represents 25.6% of the species for these groups. For many species groups in the Caribbean, the only currently
However, this estimate of endemism cannot be extrapolated to the active taxonomists work in universities, museums, or research
whole Caribbean biota, because the relative contribution of the institutions outside the region. Current local expertise is
different taxa varies strongly. For example, about 45% of the fish completely lacking for several important taxa, particularly those
species are considered Caribbean endemics, whereas endemism in with small body sizes and little economic significance, such as
mollusks amounts to about 26% and in copepods to only 2%. Mesozoa, Nemertea, Phoronida, Brachiopoda, Pogonophora,
Notable differences are also apparent between closely related Kinorhyncha, and Chelicerata. The best-covered taxa with local
groups, such as the proportions of endemics among the bivalves expertise are Angiospermae, Aves, Reptilia, and Pisces, and
(17.9%) and Gastropoda (29.3%), as well as those among moderate capacity exists for Porifera, Polychaeta, and some groups
Amphipoda (1.3%), far lower than that among Copepoda of Algae, Crustacea, Mollusca, and Cnidaria (Table 2). Moreover,
(9.2%). Note that these estimates hold only for the Caribbean only a small fraction of the local experts are employed as full-time
Sea as defined above and not for the so-called Greater Caribbean, systematists or taxonomists. For several groups, the coverage of
which also encompasses the Gulf of Mexico, Florida, the Bahamas, available guides and identification keys for known species is good

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 Caribbean Marine Biodiversity

Table 2. Diversity, state of knowledge, and expertise of the main taxonomic groups within the Caribbean region.

State of No. introduced

Taxonomic group No. species1 knowledge2 species No. experts No. identification guides3

Domain Archaea ND ND ND ND
Domain Bacteria (including 5 1 ND ND
Cyanobacteria)
Domain Eukarya
Kingdom Chromista
Phaeophyta 71 4 ND 10 1
Kingdom Plantae
Chlorophyta 170 4 2 10 1
Rhodophyta 320 3 3 10 1
Angiospermae 14 5 1 13 2
Kindom Protoctista (Protozoa)
Dinomastigota (Dinoflagellata) .31 (*1) 2 ND
Foraminifera 704 2 ND 1
Kingdom Animalia
Porifera 519 4 1 7 4
Cnidaria 994 1–3 5 20 8
Platyhelminthes 129 3 ND 2 1
Mollusca 3032 1–4 6 20 8
Annelida 658 3 2 31 1
Crustacea 2916 2–4 7 57 10
Bryozoa 131 2 2 2 0
Echinodermata 438 3–4 ND 5 2
Urochordata (Tunicata) 62 3 1 ND 1
Other invertebrates 402
Vertebrata (Pisces) (*2) 1336 3–5 15 ,55 16
Other vertebrates 59 4–5 0 .150 10
SUBTOTAL 11,991
TOTAL REGIONAL DIVERSITY4 12,046 45 388 67

Notes:
1
Sources of the reports: databases, scientific literature, books, field guides, technical reports.
2
State of knowledge: 5 = very well known (.80% described, identification guides ,20 years old, and current taxonomic expertise); 4 = well known (.70% described,
identification guides ,50 years old, some taxonomic expertise); 3 = poorly known (,50% species described, identification guides old or incomplete, no present
expertise within region); 2 = very poorly known (only few species recorded, no identification guides, no expertise); 1 = unknown (no species recorded, no identification
guides, no expertise). 3Identification guides cited in Table 1 and in References.
4
Total regional diversity including all taxonomic groups as reported in Appendix 1.
(*1) At least 31 clades of the genus Symbiodinium are found in 85 species of invertebrates.
(*2) Shore fish species that occur in the upper 100 m of the water column.
ND = No data.
doi:10.1371/journal.pone.0011916.t002

(marine mammals, fishes, turtles, birds, reef corals, reef sponges, ecological factors change abruptly. We expected to find species
ascidians, mollusks, amphipods, algae), although some are composition to be more similar between countries within one
outdated. However, for many other groups, such guides are either ecoregion in relation to countries within a different ecoregion or
inadequate or completely lacking (Table 2). One of the most with areas located farther apart, however, this was not observed
recent regional taxonomic guides in the region is on shallow-water (Figure 5). The MDS ordination of the species by country within
ascidians and includes descriptions and photographs of living ecoregions is very different from one taxonomic group to the
animals [60]. other, and no signicant differences were found in species
composition between ecoregions for any of the taxonomic
Geographic patterns of species richness groups. MDS stress values for the figures were very low (0.005–
The species of sponges (Table S3), scleractinian corals (Table 0.129), indicating that the 2-dimensional plots are a good
S4), polychaetes (Table S5), mollusks (Table S6), amphipod representation of the data [61].The species composition of
crustaceans (Table S7) and echinoderms (Table S8) were sponges throughout the Caribbean is relatively homogenous with
compiled for the different countries or subregions within the the exception of Curacao, Puerto Rico, Virgin Islands, and
Caribbean. Spatial patterns of species diversity usually exhibit Barbados. Barbados and the Virgin Islands are both from the
relatively definitive gradients or shift progressively in space, unless Eastern Caribbean region, and despite being different in

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 Caribbean Marine Biodiversity

Table 3. Summary of Symbiodinium clades (Dinoflagellata) found in invertebrates sampled in the Caribbean.

Taxonomic group Clade designation of symbiont Reference

Anthozoa Scleractinia (47) A, A3, A4a, B, B1, B5a, B6, B7, B9, C, C1, C1a, C2, [298–312]
C3a, C3c, C3e, C4, C9, C11, C12, D, D1a,
Anthozoa Actinaria (5) A3, A4a, B1, C1 [301,305]
Anthozoa Zoanthidae (3) A3, A4, B1, C1, C3, D1 [301,305,313]
Anthozoa Corallimorpharia (3) C1, C3c [301,305]
Scyphozoa (2) A1, A3, B1, C1 [301,305]
Hydrozoa (3) A3, A4, A4a, B1 [301,305]
Gorgonaceae (21) B1, B1a, B1b, B8, B9, B19, C1, C3 [301,305]
Gastropoda (1) B1, C4 [305]
Total species = 85 Total clades = 31 Total references = 17

Note:
Numbers in parentheses beside the taxonomic group represent the number of species within that group reported to have symbiosis with Symbiodinium clades (See
Table S2 for the complete list of species known to have different clades of Symbiodinium as symbionts).
doi:10.1371/journal.pone.0011916.t003

composition from the rest, they are also different from each other of Hispaniola island), for the Western Caribbean, for the
(Figure 5a). The same tendency of species homogeneity Southwestern Caribbean (with the exception of San Andres
throughout the Caribbean can be observed for corals, with the Island), and for the Southern Caribbean. The Eastern Caribbean
exception of Trinidad and Tobago and Guatemala (Figure 5b). was grouped closely with all of the ecoregions except for the
For mollusks, species composition was similar within several Southern Caribbean (Figure 5c). In the case of amphipods, Cuba,
countries from the Greater Antilles ecoregion (with the exception Mexico, and Venezuela are closely grouped together which is

Table 4. Number of Caribbean species of sponges (Spon), scleractinian corals (Cor), mollusks (Moll), amphipods (Amph), and
echinoderms (Echi), per kilometer of coast per country within the five ecoregions.

Coastline length Species/

Ecoregion/country Spon Cor Moll Amph Echi Total species (km) 100 km

WESTERN CARIBBEAN 243 73 938 142 268 1664 2089 80

Mexico (Yucatán) 118 63 733 133 182 1229 911 120
Belize 193 51 580 24 134 982 386 248
Honduras 62 580 95 737 644 114
Guatemala 27 23 148 34
SOUTH-WESTERN 222 81 1451 91 284 2129 3880 55
CARIBBEAN
Colombia 142 65 1168 63 180 1618 1880 83
Panama 146 62 587 21 155 971 1295 73
Nicaragua 41 129 65 235 493 48
Costa Rica 64 47 638 21 23 793 212 364
SOUTHERN CARIBBEAN 225 87 944 208 151 1615 3444 47
Venezuela 144 79 664 195 124 1206 2722 37
ABC* 113 68 239 20 440 360 117
Trinidad & Tobago 41 55 96 362 27
GREATER ANTILLES 335 91 1943 164 248 2781 8477 33
Jamaica 169 72 824 86 1151 1022 113
Cayman Islands 82 62 477 621 160 388
Puerto Rico 40 72 1078 25 121 1336 501 262
Cuba 255 72 1300 131 145 1903 3735 47
Hispaniola 71 72 572 16 117 848 3059 27
EASTERN CARIBBEAN 126 71 1119 46 79 1441 1322 109
Lesser Antilles

*(ABC = Aruba, Bonaire, Curacao).

doi:10.1371/journal.pone.0011916.t004

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 Caribbean Marine Biodiversity

ecoregion (Figure 5d). In the case of echinoderms, species

composition was relatively similar within the Greater Antilles
ecoregion, and within the Western Caribbean ecoregion
(Figure 5e). In terms of absolute species richness by ecoregion,
for these groups, the most speciose ecoregion was the Greater
Antilles with 2781 species, followed by the Southwestern
Caribbean with 2129, the Western Caribbean with 1664, the
Southern Caribbean with 1615, and finally the Eastern
Caribbean with 1441 species (Table 4). The Greater Antilles is
also the most speciose region for sponges, corals, and mollusks,
while amphipods were more diverse in the Southern Caribbean,
and echinoderms in the Southwestern Caribbean. A very large
proportion of the species in this compilation is from coastal
shallow waters, therefore, coastal length was considered within
each of the ecoregions. When the species richness is viewed in
terms of species per 100 kilometers of coast, the situation is
different: the Eastern Caribbean has the highest number of
species per coastal length (109 species/100 km of coast), followed
by the Western Caribbean (80), the Southwestern Caribbean (55),
the Southern Caribbean (47), and finally the larger area, the
Greater Antilles (33 species/100 km of coast) (Table 4). When
looking in detail at biodiversity richness within each of the
ecoregions, the Porifera are clearly more species rich (165–255
Figure 2. Species-description accumulation curves for Carib- species) in Cuba, Belize, and Jamaica than elsewhere in the
bean mollusks, echinoderms and fishes. Caribbean. This group is significantly less diverse (40–85 species)
doi:10.1371/journal.pone.0011916.g002 in Hispaniola, Puerto Rico, and the Lesser Antilles, as well as
along the Nicaraguan and Costa Rican coasts. Intermediate
probably an artifact due to the fact that these three countries are richness values (113–146 species) occur in Yucatan, southern
the best sampled in the Caribbean with extensive species list for Central American, and northern South American coasts,
amphipods (these countries list more than 130 amphipod species, including the Leeward Antilles (Aruba, Bonaire, and Curacao,
while the rest list between 16 to 63 species only). For this group, or ABC Islands, and Venezuelan offshore islands). The Cayman
species composition is relatively similar within the Western Islands have only 82 reported species, however, the Cayman
Caribbean ecoregion and within the Southwestern Caribbean Islands are small coral islands, and as measured by the number of

Figure 3. Geographic distribution of shallow water bony fishes and elasmobranchs. Geographic distribution of 161,000 records of shallow
water bony fishes and elasmobranchs in the Greater Caribbean (Caribbean proper plus the Bahamas, the Gulf of Mexico, Florida, and Bermuda). Data
were drawn from 20 museum databases, 9 Web databases, and 98 publications.
doi:10.1371/journal.pone.0011916.g003

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 Caribbean Marine Biodiversity

Figure 4. Distribution of deep-water species records (.200 m) in the Caribbean Sea.

doi:10.1371/journal.pone.0011916.g004

sponge species per kilometer of coastline the Cayman Islands and The highest numbers for all-taxa species richness are found in
the ABC Islands rank as the most species-diverse areas in the Cuba, Colombia, the Lesser Antilles, and Puerto Rico, with
Caribbean (Table 4). With regard to zooxanthellated hard corals, intermediate richness in Venezuela, Yucatan, Jamaica, Belize, and
species-rich areas (containing more than 70% of all Caribbean Panama, and relatively low richness in the other countries.
species) occur throughout the region, but Hispaniola and However, when the number of species of sponges, corals, mollusks,
Venezuela clearly stand out with 63 and 68 species, respectively. and echinoderms is combined and standardized by length of
On the contrary, Guatemala, Nicaragua, Costa Rica, and coastline (Table 4), the highest numbers of coastal species per
Trinidad and Tobago are less diverse areas. Again, considering kilometer of coastline occur in the Cayman Islands, followed by
the number of species per kilometer of coastline, the Cayman the ABC Islands, Costa Rica, the Lesser Antilles, and Puerto Rico.
Islands and ABC Islands are by far the most species-diverse areas. While counts of species numbers may reasonably reflect the
On the other hand, azooxanthellate corals, most of which occur biological richness of a given area, they do not reflect its
in deeper waters and have not been thoroughly surveyed in many uniqueness. The latter is an equally significant measure of an
areas, are apparently more diverse in Cuba, Jamaica, and area’s importance in a wider context. A useful measure of an area’s
Trinidad and Tobago. uniqueness is the number of endemic species it contains or of
Among the Mollusca, the Gastropoda appear to be more diverse species that are likely to occur only in this area within the region
(more than 750 species) in Cuba, the Lesser Antilles, and Colombia. but are more or less widely distributed in other regions outside the
The Bivalvia exhibit a similar trend but seem by far more diverse in evaluated region. To measure uniqueness, the relative contribu-
Puerto Rico (308 species) than in the Lesser Antilles (248 species). The tion of local (by country or subregion) diversity (alpha diversity) to
Polyplacophora are conspicuously more diverse (23–28 species) along the regional diversity (gamma diversity) was assessed. Figure 6
the Greater and Lesser Antilles and in Colombia than along the presents for five taxa: sponges (Figure 6a), hard corals (Figure 6b),
Central American coast and in other Caribbean islands (fewer than mollusks (Figure 6c), amphipods (Figure 6d), echinoderms
18 species). Species numbers of Scaphopoda and Cephalopoda vary (Figure 6e), and for all taxa combined (Figure 6f) the relative
greatly between countries, but in both cases they appear to be more contribution of species diversity from the five Caribbean
diverse in Puerto Rico (33 species) and Colombia (23 species). In ecoregions to the whole species diversity in the Caribbean region
general, mollusk species richness seems to be highest (more than (gamma diversity). For each taxonomic group in the figure, the
1,000 species) in Cuba, Colombia, the Lesser Antilles, and Puerto ecoregions are ordered by alpha diversity. For all of the five groups
Rico. Intermediate richness occurs in Jamaica, Yucatan, Belize- (Figure 6a–6e), the regions that had the higher alpha biodiversity
Honduras, Costa Rica, Panama, Venezuela, and Hispaniola, and were also those that contributed more to the regional (gamma)
least species richness occurs in Nicaragua and around ABC, the diversity, however, the contribution by ecoregion was different
Cayman Islands, and other oceanic small islands in the central depending on the taxonomic group. The Greater Antilles is the
Caribbean. Species richness among Echinodermata is high in ecoregion that contributes more to the region’s diversity when all
Yucatan and Colombia (more than 180 species), intermediate species from the five taxonomic groups are combined, a trend that
(117–155 species) in Venezuela, Panama, Belize, Cuba, Hispaniola, was also observed for sponges and mollusks. For corals and for
Mexico (Yucatan coast) and Puerto Rico, and rather low (more than amphipods, the Southern Caribbean was the most contributing
95 species) in Trinidad and Tobago, the Lesser Antilles, and Jamaica ecoregion, while for echinoderms, it was the Southwestern
and along the Central American coast. Caribbean. The ecoregion with the lowest contribution to the

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 Caribbean Marine Biodiversity

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 Caribbean Marine Biodiversity

Figure 5. MDS for various taxa between the different Caribbean countries or subregions. SCar: Southern Caribbean (red), SWCar:
Southwestern Caribbean (blue), ECar: Eastern Caribbean (green), GAnt: Greater Antilles (purple), WCar: Western Caribbean (orange).
doi:10.1371/journal.pone.0011916.g005

region’s gamma diversity was the Eastern Caribbean. These whether these species are endemic, invasive, or simply distributed
ecoregional trends, however, may hide important contributions over wide ranges.
from smaller areas. When smaller areas within ecoregions were
studied in detail, some countries also showed particular endemisms Discussion
(Figure 7). In general, countries with a higher number of species
also contribute more to the regional diversity (e.g., Cuba for Taxonomic inventories
sponges, Venezuela for amphipods, Mexico and Colombia for Biodiversity assessments are fundamental not only for basic
echinoderms). Nevertheless, there are some exceptions. In diversity science from the ecological, biogeographical, and
Barbados, for example, the number of sponge species (alpha evolutionary perspective, but also for ecosystem and ocean
diversity) is not very high, and as a country, it ranks in the bottom management as well as for the establishment of conservation
30% of Caribbean countries for this group. However, its species policies. A recent regional example of a biodiversity assessments
seem to contribute significantly to the regional, gamma diversity, was carried out at the Saba Bank (Netherland Antilles) in fish
even more than Panama and Venezuela, which rank among the [62,63], macroalgae [64], sponges [65], hard corals [66], and
top 30% of countries with high diversity. octocorals [67]. Results of this research highlight the importance
Cuba not only is the most diverse country for the Porifera but of habitat heterogeneity and the relative richness of the marine
also has the most unique sponge composition by far (Figure 7a). flora and fauna of the Saba Bank as targets for conservation [68].
Regarding zooxanthellate corals, despite Cuba not having the Despite a long history of taxonomic research in the Caribbean,
highest diversity, it is the most important contributor to the the marine biota of the region remains far from well known. The
regional diversity, closely followed by Jamaica, Panama, Trinidad current record of approximately 12,000 marine species is clearly
and Tobago, and Venezuela, the last of these being the most an underestimate for such a large and environmentally diverse
diverse in species number (Figure 7b). For Mollusca, the plot tropical region. The same number of marine macroscopic species
exhibits a nearly straight correlation between alpha diversity and has been recently estimated for the Mediterranean Sea [69,70], a
its contribution to gamma diversity. Cuba (north and south), the temperate marine region of similar size to the Caribbean. The
Lesser Antilles, and Colombia, are not only the most diverse ability to develop a more accurate inventory of Caribbean species
countries or subregions but also the major contributors to is hampered by the lack of comprehensive regional identification
Caribbean mollusk diversity (Figure 7c). Venezuela, Cuba, and guides for most taxa, limiting the ability to make accurate species
the Mexican Caribbean are clearly the major contributors to the inventories and more thorough revisions of most taxa. In addition,
regional species diversity of Amphipods, whereas the contribution the ability to make revisions is limited by the fact that many of the
of the remaining countries is rather low (Figure 7d). In collected specimens are not deposited in local collections but
Echinodermata, alpha diversity and its contribution to regional remain scattered worldwide. In this sense, the Caribbean is no
diversity are highly correlated; the Mexican and the Colombian exception to the general problem of limited taxonomic expertise.
Caribbean are the most diverse as well as being the major The main goal of the Census of Marine Life program was to study
contributing subregions (Figure 7e). the diversity distribution, and abundance of marine life. For this,
A major problem with these data on more than 12,000 species is the program used two approaches, the first was through
that spatial locations are unknown for many, and thus species exploration to new areas and ecosystems, and the second was
distributions cannot be mapped. To visualize marine diversity through a review of the known. In both cases, the program
distribution patterns in the Caribbean, we relied on the OBIS achieved to coordinate and centralize all the information that was
database, which includes about 50% of the species reported here scattered all over the world, largely in unavailable formats and
for the Caribbean (Figure 8). This map shows very clearly that sources. Regardless of the approach used, taxonomic expertise was
biodiversity is concentrated around areas with a long history of a need, and this has been one of the major limits to knowledge. In
research: Cuba, Colombia, Belize, Panama, Puerto Rico, and the last decade, molecular techniques have been refined and
Tobago. certainly provided a method to address many of the challenges of
assessing diversity. In coral reefs around the world, including in the
Threats to biodiversity: Invasive species Caribbean, the Census CReefs project coupled the use of
Except for a couple of species—the green mussel (Perna viridis) Autonomous Reef Monitoring Structures or ARMS with envi-
and the red lionfish (Pterois volitans)—little is known or documented ronmental genomics to assess the enourmous diversity in these
on the status of marine alien species. A total of 45 alien species systems as well as to monitor understudied coral reef invertebrate
belonging to 17 of the 78 taxa groups are known to date (Table 2). biodiversity, along with the effects of climate change and ocean
The most important introduced taxa in numbers of species are the acidification [71]. Monitoring and biodiversity assessments will
Pisces (15 species), Crustacea (7 species), and Mollusca (6 species). allow us to better understand diversity patterns and will improve
The absence of records of introduced species in other groups is the effectiveness of management strategies for marine ecosystems.
indicative of the poor level of taxonomic knowledge and does not To do so, capacity building in taxonomy through molecular
necessarily signify a lack of introduced species. In addition, there is techniques and monitoring is essential. Inevitably, given the
often difficulty in deciding whether newly reported marine species limited number of active taxonomists within the Caribbean region,
are introduced aliens, or native species that had not been formerly while some taxa have received much attention (for example, fish,
recorded. In sponges for instance, 10% of the species listed here mollusks, corals, sponges, and some crustacean groups), many taxa
have dubious taxonomic status because they were described have been completely neglected (most of the meiofaunal groups,
originally from other biogeographic regions (Mediterranean, the bacteria, and most of the protoctista). Sampling effort has also
Northern Atlantic, Arctic, or Pacific). Only careful taxonomic been strongly biased toward certain habitats in coastal and shallow
comparisons, and in some cases genetic studies can help to discern waters, particularly coral reefs, with very little collecting of benthic

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 Caribbean Marine Biodiversity

Figure 6. Contributions from Caribbean ecoregions to regional species diversity (gamma diversity) for five taxa. For each taxonomic
group, the ecoregions are ordered by alpha diversity, from higher to lower. SCar: Southern Caribbean, SWCar: Southwestern Caribbean, ECar: Eastern
Caribbean, GAnt: Greater Antilles, WCar: Western Caribbean.
doi:10.1371/journal.pone.0011916.g006

organisms in waters deeper than 500 m, which cover more than consequence of the significant deep-water exploration mentioned
75% of the region. In addition, certain countries or subregions earlier (Figure 8).
have been more exhaustively surveyed than others. For example, A good example is the recently published compilation of Costa
the apparently low species richness of most taxa in Hispaniola, Rica’s marine biodiversity, which includes exhaustive lists of all
Guatemala, Nicaragua, and several oceanic islands probably is an recorded species of many groups [73]. Detailed mapping of habitat
artifact of low sampling intensity. All of these factors contribute to types on national scales have also been undertaken in most of these
taxonomic, regional, and habitat biases in the current state of taxonomically best-known areas: Colombia [74,75], Guadalupe
knowledge of Caribbean biodiversity. Such biases are probably [76], Puerto Rico and the Virgin Islands [77], and Panama [78].
responsible in large part for the marked variations of species Conservation planning has also benefited greatly from both the
richness between countries or ecoregions and the apparent spatial relatively good knowledge of the species and the availability of
inconsistencies in some of our similarity analyses. Most deep-sea habitat maps, for example, in Colombia [55], and Venezuela [56].
studies in the Caribbean Basin have been carried out historically Many non-Caribbean researchers either participate in regional
by scientific groups from other regions in the world. Deep-sea sampling through collaborative projects and international pro-
research capacity in the Caribbean is limited to laboratories that grams or conduct work of their own. Because researchers resident
have the infrastructure and vessels to sample at the depths in a particular Caribbean country may not be aware of research
required. In the Caribbean, only Mexico, Colombia, and being done locally by external institutions, quantifying diversity
Venezuela have such capabilities. Outside the Caribbean, becomes difficult if available data are not published. Much of the
additional countries include France, Germany, Great Britain, work done by non-Caribbean researchers is encountered only in
and the United States. Thus, many historical records were the primary literature and is disconnected from regional plans.
obtained through large international research efforts. Examples With the highly welcome development of OBIS, however, this is
of these records are the sponge surveys in Barbados. The Barbados rapidly changing as more institutions develop georeferenced digital
data were obtained mostly from Soest and Stentoft [72] and are databases of their collections and contribute those databases to this
restricted to a collection from sponges dredged at deep waters. clearinghouse for global data.
Another unprecedented collection effort in the Caribbean was the An example of the power of databases to provide maps of
shallow-water and submersible collections (with the Argus in 1984 biodiversity distribution and to visualize the areas where more
and RV Seward Johnson in 1997) of Hexactinellida and Lithistid effort is needed is illustrated with fishes (Figure 3). The continuing
(Demospongiae) in Cuba. upward trend of the curve of new species descriptions (Figure 2)
The number of scientists who have expertise in deep-sea clearly demonstrates that we have a long way to go yet regarding
Caribbean taxa does not exceed 15. As many of these experts work new species descriptions, even in a relatively well known group
at major museums in the United States and Europe, the local and such as fishes. Further discoveries will not only take place in the
regional scientific capacity for such research is very low. deep sea, which has been a less explored area but also in shallow
Sampling effort has clearly been best for shallow, nearshore water reefs. As an example of this, there are three recent papers
waters, especially along the southern Caribbean coasts (Belize, describing new shallow water cryptic fish species (gobies and
Costa Rica, Panama, Colombia, and Venezuela), off Mexico, in blennioids, the two most speciose groups of fishes) from Honduras,
Puerto Rico, and in some of the Lesser Antilles (Figures 2 and 8). Saba, and Belize [62,79,80]. Some of those species appear to have
Figure 8 shows that the areas with the highest known biodiversity very limited ranges, and there are substantial parts of the
in the region are in Belize and central Colombia. This pattern, Caribbean that have had very little sampling (e.g. Cuba and the
however, may not reflect the true situation for regional Caribbean large shelf east of Nicaragua). Forensic barcoding has been
marine biodiversity for the following reasons: (1) the lack of important in revealing this under-appreciated diversity. Barcoding
collecting exhaustively in many areas or ecosystems (such as the requires the use of freshly collected material and assessment of that
deep sea and even coastal rocky shores), (2) the high variability diversity requires comparison of bodies and DNA that will be
between collecting methods, (3) the limited taxonomic expertise for available mostly through new collected material.
many groups in the Caribbean, and (4) the very limited or
inconsistent effort to make the data available through open-access Geographic patterns of species richness
digital databases. So, in the example of Belize and Colombia, the The Caribbean as a whole constitutes one distinctive subregion
high species richness shown in Figure 8 is most likely a sampling of the Tropical North Western Atlantic Province [41,44,45,81].
artifact as the U.S. National Museum of Natural History (US- However, the Caribbean is far from being homogeneous
NMNH) for Belize, and Colombia’s Institute of Marine and biogeographically. Its complex geological history and the pres-
Coastal Research (INVEMAR), have carried out excellent surveys ent-day geographic diversity in hydrologic, morphologic, and
and made the data publicly available. Similar, sampling-intensity habitat regimes, have led to the recognition of several distinct
biases undoubtedly contributed to high relative diversity evident at biogeographic sectors. Several criteria have been used to define
other locations, including Puerto Rico and the Virgin Islands, Los these sectors, ranging from purely taxonomic comparisons of the
Roques (Venezuela), the Cayman Islands, Panama and Costa present-day biota between subregions [41,43,82,83], paleobiogeo-
Rica, the Colombian islands offshore from Nicaragua, and tiny graphic considerations [84], arrays of ecoregions according to
Navassa Island, a U.S. territory between Jamaica and Hispaniola. habitat distribution patterns and biogeochemical factors [44,45],
Cuba provides a particularly instructive example, with enormous to expert-derived systems without a rigorous core definition [29].
variation in apparent diversity around different parts of this large Taxonomic-based regionalizations have mostly focused on differ-
island. For example, Cuba has a high diversity of sponges (255 ences in composition of single groups at the class to family taxa
described species), but such high diversity is most probably a levels. For example, the relatively detailed records that already

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 Caribbean Marine Biodiversity

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 Caribbean Marine Biodiversity

Figure 7. Contributions from individual Caribbean countries to regional species diversity (gamma diversity) for five taxa. For each
taxonomic group, the countries are ordered by alpha diversity, from higher to lower.
doi:10.1371/journal.pone.0011916.g007

exist of crinoid echinoderms, selected families of reef fishes, certain interacting environmental factors, the effect of which appears to
gastropod families, and porcellanid crabs from the Caribbean have be variable depending on the different life histories of the
allowed reasonable assessments of their spatial patterns as well as taxonomic groups. Sandin et al. [87] found that diversity of reef-
zoogeographic affinities [43,82,85-88]. Even the relatively widely associated fishes around the Caribbean islands is highly dependent
adopted system proposed by Briggs [41] was based primarily on on island area and isolation, though nearshore productivity might
the degree of endemism among shore fishes. However, at present play an important role as well. Endemism and distribution
there is no biogeographic regionalization system for the Caribbean patterns of many gastropods along the southern Caribbean shelf
that is based on exhaustive comparative analyses of the are thought to be controlled by high productivity and low
distributions of all taxonomic groups, nor even of a single group temperatures linked to upwelling areas [43,84]. These results
at the phylum level. highlight complex, but fundamental, mechanisms that underlie
Despite the absence of common geographic patterns in the spatial patterns of biodiversity within the Caribbean.
studied groups, it can be noticed that, in general, species richness The ecoregion system of classification proposed by Spalding
in the Caribbean tends to concentrate along the Antillean arc et al. [29], which we tested here, defined ecoregions as ‘‘areas of
(Cuba to the southernmost Antilles) and the northern coast of relatively homogeneous species composition and likely determined
South America (Venezuela, Colombia). General support for such a by the predominance of a small number of ecosystems and/or
pattern comes from the comparatively greater contribution of the distinct oceanographic or topographic features’’. While we have
alpha diversity of these subregions to the regional diversity. no doubt that the ecoregions proposed for the Caribbean have
However, that statement must be qualified by the recognition that indeed distinct oceanographic and topographic features (e.g.
apparently lower numbers of species on the Central American upwelling in the Southern Caribbean, geologically recent
continental coast and oceanic islands and banks in the central topographic barrier in the Southwestern Caribbean, the Orinoco
Caribbean are probably at least partially due to reduced sampling influx in the Eastern Caribbean, etc), it is unlikely that they can be
effort in those areas and the overall geographic distribution of defined by species composition. To our knowledge, this paper is
sampling effort (Figure 8). Either way, analysis of biogeographic the first attempt to review all known marine biodiversity in the
patterns of the Caribbean marine biota taken as a whole, or even Caribbean and to produce comprehensive species lists. Moreover,
at the phylum to order level, is still difficult and limited, owing to this collection is the first global effort to compile and organize all
insufficient and geographically biased sampling and knowledge. known information about marine biodiversity in the world’s
Within the relatively small and densely packed Caribbean basin, oceans. In this way, it is not surprising that species distribution was
spatial patterns are seemingly controlled by a number of not consistent with the ecoregional approach in most of the cases.

Figure 8. Spatial distribution of sites (small dots) and number of species recorded (squares) in the Caribbean. Based in data contained
in the OBIS (Ocean Biogeographic Information System) database. Taxa included in the OBIS database were: bacteria, protozoa, microalgae,
macroalgae, angiosperms, sponges, cnidarians, gnathostomulids, nematodes, kinorynches, sipunculans, mollusks, annelids, pogonophorans,
arthropods, brachiopods, chaetognaths, echinoderms, tunicates, lancelets, fishes, reptiles, birds, mammals.
doi:10.1371/journal.pone.0011916.g008

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 Caribbean Marine Biodiversity

The patterns we observed may be explained differently, depending Cuba, Venezuela, and Mexico. In these three localities, the
on the taxonomic group and can be due to a combination of number of species reported surpasses 130, therefore, the
variables as described above. probability of sharing species between these three sites increases,
Sponges. The pattern of sponge diversity is best explained by and this is probably the reason why they are grouped together. To
two facts. The first is the extension of the collecting effort and the have a better idea of the real distribution pattern of amphipod
second is the taxonomic follow-up on the collected samples. In species, more assessments are needed, especially in the Eastern and
collection effort, several countries have been explored not only in the Western Caribbean, as well as in the rest of the Greater Antilles.
coastal zone but also in deep areas (e.g. Barbados by Soest and With this new information, different groups would possibly form in
Stentoft [72]; Puerto Rico by Laubenfels [89]; Virgin Islands as the MDS that would reflect the true similarity in species
described by Schmidt in the 1800s and dispersed in several composition between localities.
publications), therefore, their taxonomic composition is different Echinoderms. The Caribbean seems to be relatively
than in those countries in which only shallow water samples have been homogeneous in echinoderm species composition possibly due to
collected. On the other hand, in Curacao, almost no deep sea sponges the current patterns in this semi-enclosed basin. Ophiuroidea is
have been reported but collecting effort in shallow waters and the most diverse class which can be explained by the variety of
taxonomic descriptions has been significant [90–92]. In taxonomic cryptic habitats that this region provides for the development and
follow-up, Cuba and Belize have benefited from outstanding speciation of this group (Table S1). There has been a marked bias
taxonomic experience. To have a clear and correct picture of in the sampling effort throughout the Caribbean, and
regional biodiversity, both facts are essential. For instance, in Panama, consequently, the countries that have carried out more research
sponge collection up to 30 m in depth has been significant at Bocas del are those that have the highest species diversity (Mexico, Belize,
Toro, but taxonomic identification of these samples has not been Panama, Colombia and Cuba). Efforts have also been dissimilar
completed. Once this identification is completed, the number of within the different classes. In Belize, for example, the ophiuoroid
sponges at this locality will probably increase by at least 100 species, of fauna is rich and well known [105–107], and the holothuroids are
which about 20 will be new descriptions. Recently, 13 new species of well known in the Eastern Caribbean and the Greater Antilles
sponges were described from coral reefs of the Netherlands Antilles [108–112]. The Southwestern Caribbean ecoregion is the richest
and the Colombian Caribbean [93]. ecoregion, closely followed by the Western Caribbean, in which
Corals. Coral composition seems to be similar throughout the the Mesoamerican Reef could be a hot spot.
Caribbean regardless of the ecoregion with the exception of The countries or subregions contributing most to the regional
Trinidad and Tobago, and Guatemala. These two localities have diversity, while not necessarily the most diverse in all taxa, are also
fewer species than the rest of the Caribbean, as well as a more apparently the most rich in endemic or geographically restricted
limited development and cover. In Guatemala, for example, the species (Figures 6 and 7). In this regard, Cuba and the southern
coral reef area is very small, and under the influence of sediments Caribbean, especially the Venezuelan coast, stand out. Owing to
(Punta Manabique). In this area, live species cover is low, and its location on the northern edge of the region, the northern coast
species composition has been reported to be atypical for the of Cuba has a rich marine biota that includes not only typical
Caribbean [94–96], mostly dominated by sediment-resistant Caribbean species but also elements from the biogeographically
species [97]. Trinidad and Tobago, on the other hand, are the somewhat different Gulf of Mexico and eastern North America
most southerly of the eastern Caribbean islands, on the edge of the (Carolinian Province of Briggs [41]). Moreover, in northern Cuba
South American continental shelf, and under the influence of the we see the persistence of many species of mollusks that, during the
Orinoco River. Trinidad has marginal coral communities with Miocene to Pliocene, had more widespread Caribbean distribu-
only sediment tolerant coral species (Siderastrea and Porites), while tions [113]. Another area regarded as a refuge, probably related to
Tobago reefs, despite being more remote, are also threatened by the occurrence of cold and nutrient-enriched upwelling waters, lies
nutrient and sediment runoff from land clearing and coastal on the northern South American coasts of eastern Colombia and
development, sewage pollution and climate change [98]. Venezuela [43,114]. In addition, the extreme southeast corner of
Mollusks. Except for the coasts of Yucatan in Mexico, and the Caribbean, which includes eastern Venezuela, has the greatest
Belize in the Western Caribbean, no consistent pattern was potential to receive immigrants moving northward along the east
observed in the distribution of mollusks (gastropods and bivalves), coast of South America, and is known to host significant numbers
suggesting that the geographic distribution of these groups in the of such species. Such refuges, as well as island chains like the
Caribbean is mostly controlled by habitat type and distribution Antillean arc, represent areas rich in endemism and of active
(coral reefs, seagrass beds, mangroves, rocky shores, estuaries, etc.). speciation, particularly for taxa with limited dispersal capability
However, some lower level molluscan taxa (genus, family) do show [113]. Smith et al. [115] analyzed GIS (geographic information
some clear trends in their distribution patterns. Such is the case for systems) data on the distributions throughout the Greater
the families Volutidae and Conidae, which have a series of Caribbean (the Caribbean plus the Gulf of Mexico, Florida, the
allopatric species that are distributed along the coasts of Central Bahamas, and Bermuda) of 987 species of fishes and 144 species of
America and the north of South America [99–101]. Another invertebrates (mollusks and crustaceans). For fishes they found two
example can be observed in species of the genera Cypraeidae, peaks in species richness, one at southern Florida and northern
Marginellidae, Olividae and Columbellidae which have many Cuba, and the other along the northern coast of South America.
endemic species in the Southern Caribbean [43,102,103] that For the invertebrates, richness was greatest in those same two
apparently originated through several vicariant events related to areas plus the Lesser Antilles. They attributed the fish pattern to
the evolution of the Caribbean Sea [84,104]. In this way, the the abundance at those two hot spots of both local endemics and
eventual biogeographic patterns due to vicariance events that can species that occur primarily in the northern and southern reaches
be observed in certain taxa, can be masked when trying to analyze of the Greater Caribbean.
spatial patterns for the whole group of mollusks.
Amphipods. The amphipod distribution pattern is clearly Threats to biodiversity and conservation of marine life
biased due to sampling effort and taxonomic expertise. This is a Rising population densities and associated coastal development,
group that is poorly known in the Caribbean with the exception of increasing fishing pressure, agricultural and industrial activities,

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 Caribbean Marine Biodiversity

increased river sediment loading, introduction of alien species, and of Mexico Studies regarding Gulf of Mexico and Caribbean
climate change are among the major identified sources of marine invasive species. This workshop had a more scientific focus
anthropogenic pressure on Caribbean marine life (see [21,47]). and provided a list of key issues, priorities and future directions for
Caribbean coral reefs are already greatly degraded, having research and management in the subject at the regional level
declined in some cases from more than 50% live cover to less than [127]. A recent book edited by Rilov and Crooks [128] provides a
10% cover over the last two decades [48]. This degradation is due to detailed compilation and revision of several issues related to
a combination of impacts, including damage by hurricanes, diseases, biological invasions in marine ecosystems in terms of conservation
bleaching, pollution, sediment runoff, overfishing, climate change, as issues, vehicles, ecological understanding, and establishment of
well as more directly through boat anchoring, setting of fish traps, invaders, as well as discusses management and geographic
groundings of ships, dredging activities, collecting of corals, and perspectives. Many areas have substantial information about
dynamite fishing. The effects of climate change are particularly invasive species and processes (e.g. South Africa, New Zealand,
dramatic for coral reefs, particularly through ocean acidification and Australia, Europe, China, Korea, and Brazil), but there is very
increased temperature [116–118]. These changes will lead to an limited information when it comes to the Caribbean. The
increased frequency and severity of coral bleaching events as well as Caribbean Sea has many potential vectors for the introduction
to problems in the calcification process of many organisms [119,120]. of alien species. These include the Panama Canal, a major global
Temperature increases have also been related to an increase in coral crossroads for ship traffic, and many active ports that provide links
diseases in Acropora, as well as in Diadema antillarum. The disappearance for movement of species in ballast water or ship hulls. On the other
of these two structural species leads to changes in the structure, hand, the most publicized marine invasive species that arrived to
composition, and dynamics of coral reefs. Diseases are also known to the Caribbean, the lionfish, was introduced through other
lower coral fecundity affecting the potential of natural recovery mechanisms (aquarium trade activities). Our account records only
[121,122]. Terrestrial runoff has been reported to cause eutrophica- 44 introduced marine or estuarine species in the region. However,
tion gradients in Barbados, increase bacterial biomass in the Grand not all introduced species are known or have been documented as
Cayman Island, and sedimentation in Costa Rica. These changes invasive. Indeed, the compilation by the International Union for
have induced alterations in the community structure, reduced species Conservation of Nature (IUCN) Global Invasive Species Specialist
diversity and live coral cover, and increased bioerosion (see review by Group database (ISSG, http://www.issg.org/database) only lists
Fabricius, [123]). Most of the examples about the effects of terrestrial for the Caribbean Sea a total of 12 alien or invasive species (4
runoff in the Caribbean are very localized, as the examples fishes, 3 bryozoans, 1 mussel, 1 crab, 1 coral, 1 jellyfish, and 1
mentioned above, and in occasions fail to communicate their dinoflagellate). Venezuela, as the major exporter of unrefined
significance to environmental managers. In this sense, the region hydrocarbon products in the Caribbean, imports about 96 million
would greatly benefit from (1) a large scale ecological study along t of ballast water every year. Although only five marine invasive
different water quality gradients and (2) addressing science within a alien species have been recently reported from this country [129],
framework that is scientifically rigorous, but that can be understood four of those are not yet included in the ISSG database. Here
by a broader public. A successful implementation of this approach again regional deficiencies in taxonomic inventories are evident.
was carried out at the Great Barrier Reef in Australia [124]. Additionally, the actual identification of species as native or
High population pressure in coastal areas has also led to the introduced and the difficulty in determining whether newly
conversion of many mangrove areas to other uses, including reported marine species are introduced or cryptogenic natives
infrastructure, aquaculture, rice, and salt production. Mangrove represents a major constraint.
loss has been occurring at about 1% per year in areal cover since Marine ecosystems in the Caribbean region are interlinked
1980. In other words, about 413,000 ha of mangroves have been through the movement of pollutants, nutrients, diseases, and other
lost in the Caribbean since then [47]. In many areas of the stressors, which will undoubtedly cause further degradation. There
Caribbean, seagrass beds are being removed to ‘‘improve’’ bathing is considerable change occurring within the region, and solutions
beaches and to allow access to shipping, or to lay pipes and other require analyzing pros and cons of networks of marine protected
submarine structures. They are also being buried by sediments areas (MPAs), studying connectivity issues, the cooperation of
from nearby dredging and filling activities and in many enclosed neighboring countries, as well as a better understanding of stressors
bays are severely affected by excessive organic loading and and measures that can be taken to ameliorate them [130]. Currently
hydrocarbons [125]. Such loss is important because those there are at least 600 MPAs in the Caribbean region. These areas
ecosystems are the most symbolic and species-rich shallow-water include, among the IUCN categories of protected areas, 22 strict
ecosystems in the Caribbean [45,47]. In fact, coral reefs, nature reserves, 103 national parks, and 350 managed nature
mangroves, and seagrass beds represent an integrated and reserves (http://cep.unep.org/caribbeanmpa). Most of the region’s
interacting set of ecosystems [126], and it is therefore necessary MPAs are coastal or nearshore and are intended to provide some
to consider them as one large, interdependent marine ecosystem coastal zone management while allowing varying levels and types of
with shared biodiversity [47]. extractive activity within them [131]. These MPAs incorporate
The problem of marine invasive species has been recognized samples of most major marine and coastal ecosystem types, of which
only recently in the Caribbean. In 2006, the Venezuelan Institute three of the most important—coral reefs, mangroves, and seagrass
of Aquatic Spaces (INEA), which is the focal point for the beds—are particularly well represented. However, coral reefs in
International Maritime Organization (IMO) organized the first many MPAs have been and remain degraded by human impacts,
regional workshop for the Caribbean regarding ballast water including overfishing, sedimentation from land-based development,
control with the goal of establishing a plan of action. In this land-based nutrient pollution, and anchoring [132].
workshop, the situation of Venezuela, Bahamas, Colombia, Cuba,
Panama, Suriname and the Netherlands was presented from a Role of the Census of Marine Life in the Caribbean
political perspective, and it was summarized in the report of the Although all of the Census projects involved in this region
GloBallast program in Venezuela and the Caribbean, prepared by produced scientific advances, the contributions of the historic
the INEA (http://globallast.imo.org/). In 2007, another regional (HMAP), nearshore (NaGISA), and database (OBIS) projects can
workshop was carried out at the Harte Research Institute for Gulf be especially highlighted. The HMAP project in the Caribbean

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 Caribbean Marine Biodiversity

was focused on the early human impact on mollusk populations uniqueness (i.e., high degree of endemism, biodiversity hot spot,
and aimed to understand ancient human–mollusk interactions at a distinctive geological history, and oceanographic conditions).
global scale. This initiative produced a special volume of the The Census project NaGISA represents the first attempt to
British Archaeological Reports (Antczak and Cipriani [133]) study these rocky systems on a large-scale basis, especially at this
comprising 19 papers focused on two major themes: environmen- time when these systems are likely to increase in cover, owing to
tal and bioecological aspects of human–mollusk relationships, and the sharp decrease of coral reefs. It is comparable in scope to other
sociocultural aspects of this relationship. The 19 papers are global regional initiatives centered on coral reefs and the potential
in scope and include data from several mollusk species from changes that they might undergo, for example, the Atlantic and
around the world. In the Caribbean, these historical and Gulf Rapid Reef Assessment (AGRRA, http://www.agrra.org)
archaeological studies were focused on the early exploitation and and the Caribbean Coastal Marine Productivity (CARICOMP)
symbolic use of the queen conch (Strombus gigas) [133,134]. programs.
Another major contribution of the Census program in the The third significant contribution of the Census in the
Caribbean has been the NaGISA project, aimed to study hard- Caribbean has been the input of regional data in the Ocean
bottom algal and soft-bottom seagrass communities worldwide by Biogeographic Information System (OBIS). One of the major
using a series of well-distributed standard transects from the high problems identified during the Caribbean Marine Biodiversity
intertidal zone to a depth of 20 m. In the Caribbean Sea, rocky Workshop in 2004 was that only some data in the Caribbean
shores had been commonly neglected, as coral reefs have been the existed in electronic format and that much of the data required
main research focus. The few studies in rocky shore biotas have taxonomic revision. The idea of incorporating data into an open-
focused on specific groups, such as algae [135], sponges [136], access biogeographic information system, such as OBIS, was well
mollusks [137], or crustaceans [138]. Few studies have addressed received by the scientific community because it could become a
patterns of spatial or temporal distribution of rocky-shore powerful tool to better protect and manage biodiversity in a region
organisms at the community level [139–144]. heavily dependent on tourism and fisheries. Currently, OBIS has
Tidal ranges in the Caribbean are small (20–75 cm) and, 184,796 records for 6,040 species from the Caribbean. Among the
consequently, the typical zonations reported elsewhere do not records of Caribbean species, 27,000 records for nearly half those
occur in this region. In addition, changes of assemblages across species were contributed to OBIS during the last three years by
rocky shores occur over short horizontal distances (2–6 m, INVEMAR in Colombia, and the Universidad Simon Bolivar in
depending on the slope). For different parts of the Caribbean, Venezuela. Despite these significant contributions, however, there
three distinct vertical zones have been described by different are still about 6,000 known Caribbean species for which data are
authors (Good [141] for the British Virgin Islands, Nuñez et al. not yet included in the OBIS database; hence, much work remains
[142] for Colombia, and Miloslavich et al. [145] for Venezuela), to be done. A critical example is data on the deep sea. Data in
although species composition varies geographically within those OBIS for species in the deep Caribbean basins represents only
zones, which have geographically consistent features. From the about 10% of the records included in this synthesis.
few studies that exist for the Caribbean region, it can be A tremendous amount of work is still needed in the Caribbean
generalized that rocky shores in this region are dominated by to get a clearer picture of species richness and marine biodiversity
foliose algae (but see [146] for exceptions reported outside the patterns. The Census has made a first effort to compile the
Caribbean in Bermuda). This distinct pattern contrasts with available information and to make this information more
previous studies in tropical shores, which report a dominance of accessible to the scientific community. In this way, it has also
herbivore-resistant algal forms, such as turf-forming algae (e.g., been able to indicate where there are the gaps in knowledge in this
Wallenstein and Neto [147] and encrusting algae [148–152]). It region, including knowledge regarding taxonomic groups, inven-
has been proposed that this distinct pattern in the Caribbean tories, geographical areas, and different habitats. The legacy of the
(rocky shores dominated by foliose algae) might be due to a Census in the Caribbean, as well as the international cooperation
negligible effect of herbivores on these assemblages [140], a it has established, will continue after the first phase of the program
situation very different from that thought to exist on the rocky ends in 2010, as we expect many scientific accomplishments and
shores of other tropical regions [141]. discoveries in the next years. As data are produced from the
About 300–320 different species of benthic macroorganisms different projects, OBIS will also continue to grow, facilitating
(.2 cm) are commonly found in rocky shores across the more research and providing a conservation tool that will allow the
Caribbean, of which 50–60% are macroalgae. Most of these development of new approaches to regional management of these
belong to the genera Acantophora, Bryopsis, Caulerpa, Dyctiota, coastal environments for future generations. As Fredrick Grassle,
Laurencia, Padina, Polysiphonia, and Sargassum. Despite the founder of the Census of Marine Life program and chair of its
minimal attention that these systems have received in the Scientific Steering Committee for many years, said in his foreword
Caribbean, the importance of understanding the structure and to the book Caribbean Marine Biodiversity: The Known and the Unknown,
dynamics of rocky systems is growing as a consequence of massive ‘‘The Caribbean Census of Marine Life plans to increase
understanding of the species and populations that historically live
changes that coral reefs have suffered over the past several decades
in these seas. This will expand the expectations for a richer and
[48], including an 80% drop in live coral cover in 25 years [49].
more diverse marine environment—a return to the paradise that
Such decreases in live coral cover have increased the availability of
once was’’ [37].
hard substrata, which consequently may result in a phase shift
from coral-dominated communities, to hard-bottom systems
dominated by algae (e.g., [153–155]). In addition, understanding
Supporting Information
these rocky systems in the Caribbean is important because the Table S1 Diversity, state of knowledge, and expertise of all
traditional models proposed to explain the underlying mechanisms taxonomic groups within the Caribbean region. Sources of the
that determine and structure these communities (e.g., Lubchenco reports: databases, scientific literature, books, field guides,
[156]; Menge and Sutherland [157]; others reviewed in Menge technical reports. State of knowledge classified as: 5 = very well
and Branch [158]) might not work in this region because of its known (.80% described, identification guides ,20 years old, and

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 Caribbean Marine Biodiversity

current taxonomic expertise); 4 = well known (.70% described, Table S6 List of mollusk (Mollusca) species of the Caribbean
identification guides ,50 years old, some taxonomic expertise); and countries by ecoregion where the species have been reported.
3 = poorly known (,50% species described, identification guides Data compiled by Juan Manuel Dı́az and Patricia Miloslavich.
old or incomplete, no present expertise within region); 2 = very Found at: doi:10.1371/journal.pone.0011916.s006 (0.57 MB
poorly known (only few species recorded, no identification guides, XLS)
no expertise); 1 = unknown (no species recorded, no identification
Table S7 List of amphipod (Amphipoda) species of the
guides, no expertise). Taxonomic experts were defined as people
Caribbean and countries by ecoregion where the species have
with expertise in the description and identification of particular
been reported.
groups of marine species (i.e., taxa).
Found at: doi:10.1371/journal.pone.0011916.s007 (0.08 MB
Found at: doi:10.1371/journal.pone.0011916.s001 (0.03 MB
XLS)
XLS)
Table S8 List of echinoderm (Echinodermata) species of the
Table S2 Summary of free-living and symbiont clades of
Caribbean and countries by ecoregion where the species have
Symbiodinium spp. sampled in the Caribbean.
been reported. Data compiled by Juan José Alvarado.
Found at: doi:10.1371/journal.pone.0011916.s002 (0.16 MB
Found at: doi:10.1371/journal.pone.0011916.s008 (0.10 MB
DOC)
XLS)
Table S3 List of sponge (Porifera) species of the Caribbean and
countries by ecoregion where the species have been reported. Data Acknowledgments
compiled by Cristina Dı́az.
Found at: doi:10.1371/journal.pone.0011916.s003 (0.12 MB Klaus Rützler (Smithsonian Institution), Rob van Soest (Zoologish
Museum, Amsterdam University), Adriana Perez (Universidad de Oriente),
XLS) who provided data on sponges.
Table S4 List of zooxanthelate coral (Scleractinia) species of the Ernesto Peña for preparation of data on fishes.
Caribbean and countries by ecoregion where the species have Myrna Martı́nez and Guillermo Sánchez, PCML, for assistance with
putting together the database for the deep sea.
been reported. Data compiled by Ernesto Weil, Jorge Cortés, and
Adriana Humanes for providing information on dinoflagellate clades.
Carolina Bastidas. Yusbelly Dı́az (Universidad Simón Bolı́var) for assistance with data files.
Found at: doi:10.1371/journal.pone.0011916.s004 (0.03 MB César Paz (Universidad Simón Bolı́var) for formatting the references.
XLS) Alana Jute (University of West Indies at Trinidad & Tobago) for
assistance with polychaete species list.
Table S5 List of polychaete (Polychaeta) species of the
Michele DuRand (Census of Marine Life Synthesis Group), Charles
Caribbean and countries by ecoregion where the species have Griffiths (University of Cape Town), and Dale Langford for reviewing and
been reported. Data compiled by Judith Gobin. providing editorial coments on the manuscript.
Found at: doi:10.1371/journal.pone.0011916.s005 (0.11 MB Two anonymous reviewers from PLoS ONE for their valuable
XLS) suggestions to improve the manuscript.

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