Patricia Miloslavich

A Census of Marine Biodiversity Knowledge, Resources, and Future Challenges

The resources available for research are always limited. When setting priorities for research funding, governments, industry, and funding agencies must balance the demands of human health, food supply, and standards of living, against the less-tangible benefits of discovering more about the planets biodiversity. Scientists have discovered almost 2 million species indicating that we have made great gains in our knowledge of biodiversity. However, this knowledge may distract attention from the estimated four-fifths of species on Earth that remain unknown to science, many of them inhabiting our oceans [1], [2]. The worlds media still find it newsworthy when new species are discovered [1]. However, the extent of this taxonomic challenge no longer appears to be a priority in many funding agencies, perhaps because society and many scientists believe we have discovered most species, or that doing so is out of fashion except when new technologies are employed. Another symptom of this trend may be that the increased attention to novel methods available in molecular sciences is resulting in a loss of expertise and know-how in the traditional descriptive taxonomy of species [3]. The use of molecular techniques complements traditional methods of describing species but has not significantly increased the rate of discovery of new species (at least of fish), although it may help classify them [4]. At least in Europe, there was a mismatch between the number of species in a taxon and the number of people with expertise in it [5]. Unfortunately, because most species remain to be discovered in the most species-rich taxa [2], [5], [6], [7], there are then few experts to appreciate that this work needs to be done. Evidently, a global review of gaps in marine biodiversity knowledge and resources is overdue. History of discovering marine biodiversity Although the economic exploitation of marine resources dates back to prehistoric times, and historical documentation has existed since the third century B.C. with Aristotles contributions in the Mediterranean Sea (e.g. [8]), the establishment of systematic collections of marine organisms began only during the seventeenth and eighteenth centuries. Global marine biodiversity investigations at these times depended not only on the availability of expertise, but also on foreign policies of the colonial powers of the time. For those reasons, the specimens collected from several regions (e.g., Caribbean, Japan, South America, Africa) were mostly brought to Europe, where they were described, deposited in museum collections, and used for the production of marine biological monographs. These early publications contained descriptions and checklists of many marine species, such as molluscs, crustaceans, fishes, turtles, birds, and mammals (e.g. [9], [10], [11]). The history of research on marine biodiversity can generally be divided into three periods: early exploratory studies, local coastal “descriptive” studies, and large-scale multidisciplinary investigations and syntheses. These periods vary in timing by different seas and countries. The first exploratory studies in several regions (e.g., South America, Caribbean, South Africa, Pacific Ocean) took place from the mid-1700s until the late-1800s, in association with mainly European, North American, and Russian exploration expeditions, such as the Kamchatka Expedition in the 1740s, James Cooks voyages in the 1770s, the cruise of HMS Beagle in the 1830s, the voyage of HMS Challenger in the 1870s, and the first deep-sea investigations in the Mediterranean Sea [8], [9], [12], [13]. Pioneer investigations on deep-sea organisms were conducted in the Aegean Sea, where Forbes [14] noticed that sediments became progressively more impoverished in terms of biodiversity with increasing sampling depth. The azoic hypothesis proposed by Forbes suggested that life would be extinguished beyond 500 m depth, although a work published 68 years earlier provided indisputable evidence of the presence of life in the Gulf of Genoa at depths down to 1,000 m [15]. The taxonomists who described marine species at these times seldom collected specimens themselves in the field and, therefore, had only second-hand information about the distribution and ecology of the samples they received [4], [8]. Some of the early descriptions of tropical species thus do not even have the locality where the holotype or voucher material was collected (some examples in Chenu 1842–1853). The second period of regional studies was initiated by enhanced availability of research resources (experts, institutes, and vessels) in developing countries around the mid-1900s. The earliest institutions and research stations, many of which continue to operate, were founded in some areas as early as the late 1800s and early 1900s (e.g. [11], [16], [17]). Wide-scale establishment of laboratories in several continents (Europe, New Zealand, North and South America) have only been operational since the 1950s–1960s. The third stage, large-scale multidisciplinary investigations, has evolved since the 1990s, and is related to development and application of modern technologies and implementation of large, multinational research projects. Perhaps the largest of such investigations was the Census of Marine Life (Census).

Marine Biodiversity in the Caribbean: Regional Estimates and Distribution Patterns

This paper provides an analysis of the distribution patterns of marine biodiversity and summarizes the major activities of the Census of Marine Life program in the Caribbean region. The coastal Caribbean region is a large marine ecosystem (LME) characterized by coral reefs, mangroves, and seagrasses, but including other environments, such as sandy beaches and rocky shores. These tropical ecosystems incorporate a high diversity of associated flora and fauna, and the nations that border the Caribbean collectively encompass a major global marine biodiversity hot spot. We analyze the state of knowledge of marine biodiversity based on the geographic distribution of georeferenced species records and regional taxonomic lists. A total of 12,046 marine species are reported in this paper for the Caribbean region. These include representatives from 31 animal phyla, two plant phyla, one group of Chromista, and three groups of Protoctista. Sampling effort has been greatest in shallow, nearshore waters, where there is relatively good coverage of species records; offshore and deep environments have been less studied. Additionally, we found that the currently accepted classification of marine ecoregions of the Caribbean did not apply for the benthic distributions of five relatively well known taxonomic groups. Coastal species richness tends to concentrate along the Antillean arc (Cuba to the southernmost Antilles) and the northern coast of South America (Venezuela – Colombia), while no pattern can be observed in the deep sea with the available data. Several factors make it impossible to determine the extent to which these distribution patterns accurately reflect the true situation for marine biodiversity in general: (1) highly localized concentrations of collecting effort and a lack of collecting in many areas and ecosystems, (2) high variability among collecting methods, (3) limited taxonomic expertise for many groups, and (4) differing levels of activity in the study of different taxa.

Marine Biodiversity in the Atlantic and Pacific Coasts of South America: Knowledge and Gaps

The marine areas of South America (SA) include almost 30,000 km of coastline and encompass three different oceanic domains--the Caribbean, the Pacific, and the Atlantic--ranging in latitude from 12∘N to 55∘S. The 10 countries that border these coasts have different research capabilities and taxonomic traditions that affect taxonomic knowledge. This paper analyzes the status of knowledge of marine biodiversity in five subregions along the Atlantic and Pacific coasts of South America (SA): the Tropical East Pacific, the Humboldt Current,the Patagonian Shelf, the Brazilian Shelves, and the Tropical West Atlantic, and it provides a review of ecosystem threats and regional marine conservation strategies. South American marine biodiversity is least well known in the tropical subregions (with the exception of Costa Rica and Panama). Differences in total biodiversity were observed between the Atlantic and Pacific oceans at the same latitude. In the north of the continent, the Tropical East Pacific is richer in species than the Tropical West Atlantic, however, when standardized by coastal length, there is very little difference among them. In the south, the Humboldt Current system is much richer than the Patagonian Shelf. An analysis of endemism shows that 75% of the species are reported within only one of the SA regions, while about 22% of the species of SA are not reported elsewhere in the world. National and regional initiatives focusing on new exploration, especially to unknown areas and ecosystems, as well as collaboration among countries are fundamental to achieving the goal of completing inventories of species diversity and distribution.These inventories will allow accurate interpretation of the biogeography of its two oceanic coasts and latitudinal trends,and will also provide relevant information for science based policies.

Large-scale spatial distribution patterns of echinoderms in nearshore rocky habitats

This study examined echinoderm assemblages from nearshore rocky habitats for large-scale distribution patterns with specific emphasis on identifying latitudinal trends and large regional hotspots. Echinoderms were sampled from 76 globally-distributed sites within 12 ecoregions, following the standardized sampling protocol of the Census of Marine Life NaGISA project (www.nagisa.coml.org). Sample-based species richness was overall low (<1–5 species per site), with a total of 32 asteroid, 18 echinoid, 21 ophiuroid, and 15 holothuroid species. Abundance and species richness in intertidal assemblages sampled with visual methods (organisms >2 cm in 1 m2 quadrats) was highest in the Caribbean ecoregions and echinoids dominated these assemblages with an average of 5 ind m−2. In contrast, intertidal echinoderm assemblages collected from clearings of 0.0625 m2 quadrats had the highest abundance and richness in the Northeast Pacific ecoregions where asteroids and holothurians dominated with an average of 14 ind 0.0625 m−2. Distinct latitudinal trends existed for abundance and richness in intertidal assemblages with declines from peaks at high northern latitudes. No latitudinal trends were found for subtidal echinoderm assemblages with either sampling technique. Latitudinal gradients appear to be superseded by regional diversity hotspots. In these hotspots echinoderm assemblages may be driven by local and regional processes, such as overall productivity and evolutionary history. We also tested a set of 14 environmental variables (six natural and eight anthropogenic) as potential drivers of echinoderm assemblages by ecoregions. The natural variables of salinity, sea-surface temperature, chlorophyll a, and primary productivity were strongly correlated with echinoderm assemblages; the anthropogenic variables of inorganic pollution and nutrient contamination also contributed to correlations. Our results indicate that nearshore echinoderm assemblages appear to be shaped by a network of environmental and ecological processes, and by the differing responses of various echinoderm taxa, making generalizations about the patterns of nearshore rocky habitat echinoderm assemblages difficult.

Spatial relationships between polychaete assemblages and environmental variables over broad geographical scales

This study examined spatial relationships between rocky shore polychaete assemblages and environmental variables over broad geographical scales, using a database compiled within the Census of Marine Life NaGISA (Natural Geography In Shore Areas) research program. The database consisted of abundance measures of polychaetes classified at the genus and family levels for 74 and 93 sites, respectively, from nine geographic regions. We tested the general hypothesis that the set of environmental variables emerging as potentially important drivers of variation in polychaete assemblages depend on the spatial scale considered. Through Morans eigenvector maps we indentified three submodels reflecting spatial relationships among sampling sites at intercontinental (>10000 km), continental (1000–5000 km) and regional (20–500 km) scales. Using redundancy analysis we found that most environmental variables contributed to explain a large and significant proportion of variation of the intercontinental submodel both for genera and families (54% and 53%, respectively). A subset of these variables, organic pollution, inorganic pollution, primary productivity and nutrient contamination was also significantly related to spatial variation at the continental scale, explaining 25% and 32% of the variance at the genus and family levels, respectively. These variables should therefore be preferably considered when forecasting large-scale spatial patterns of polychaete assemblages in relation to ongoing or predicted changes in environmental conditions. None of the variables considered in this study were significantly related to the regional submodel.

Venezuelan Caribbean Sea under the threat of TBT.

Although environmental tributyltin (TBT) contamination is considered a solved problem, imposex occurrence in Plicopurpura patula as well as butyltins (BTs) contamination in sediments and tissues were detected along 700 km of the Caribbean coastal shore. Areas under the influence of five main ports of Venezuela were covered, as well as large marinas and sites located away from expected sources. Marinas were the most contaminated areas, whilst imposex incidence and TBT levels were relatively low in areas nearby commercial harbors. Thus, it is evident that marinas have become the main source of fresh TBT to the region. This might explain why imposex incidence seems to be widely distributed along the Venezuelan coast, since leisure boats are circulating along the whole coastal region. In fact, this could be the pattern for other areas of the Caribbean Sea.

Patterns of Spatial Variation of Assemblages Associated with Intertidal Rocky Shores: A Global Perspective

Assemblages associated with intertidal rocky shores were examined for large scale distribution patterns with specific emphasis on identifying latitudinal trends of species richness and taxonomic distinctiveness. Seventy-two sites distributed around the globe were evaluated following the standardized sampling protocol of the Census of Marine Life NaGISA project (www.nagisa.coml.org). There were no clear patterns of standardized estimators of species richness along latitudinal gradients or among Large Marine Ecosystems (LMEs); however, a strong latitudinal gradient in taxonomic composition (i.e., proportion of different taxonomic groups in a given sample) was observed. Environmental variables related to natural influences were strongly related to the distribution patterns of the assemblages on the LME scale, particularly photoperiod, sea surface temperature (SST) and rainfall. In contrast, no environmental variables directly associated with human influences (with the exception of the inorganic pollution index) were related to assemblage patterns among LMEs. Correlations of the natural assemblages with either latitudinal gradients or environmental variables were equally strong suggesting that neither neutral models nor models based solely on environmental variables sufficiently explain spatial variation of these assemblages at a global scale. Despite the data shortcomings in this study (e.g., unbalanced sample distribution), we show the importance of generating biological global databases for the use in large-scale diversity comparisons of rocky intertidal assemblages to stimulate continued sampling and analyses.

Current Patterns of Macroalgal Diversity and Biomass in Northern Hemisphere Rocky Shores

Latitudinal gradients in species abundance and diversity have been postulated for nearshore taxa but few analyses have been done over sufficiently broad geographic scales incorporating various nearshore depth strata to empirically test these gradients. Typically, gradients are based on literature reviews and species lists and have focused on alpha diversity across the entire nearshore zone. No studies have used a standardized protocol in the field to examine species density among sites across a large spatial scale while also focusing on particular depth strata. The present research used field collected samples in the northern hemisphere to explore the relationships between macroalgal species density and biomass along intertidal heights and subtidal depths and latitude. Results indicated no overall correlations between either estimates of species density or biomass with latitude, although the highest numbers of both were found at mid-latitudes. However, when strata were examined separately, significant positive correlations were found for both species numbers and biomass at particular strata, namely the intertidal ones. While the data presented in this paper have some limitations, we show that latitudinal macroalgal trends in species density and biomass do exist for some strata in the northern hemisphere with more taxa and biomass at higher latitudes.

Marine biodiversity in Venezuela: Status and perspectives

Venezuela se encuentra entre los primeros 10 paises con la mayor biodiversidad en el mundo, tanto en el ambiente terrestre como en el marino. Dada su posicion biogeografica, la flora y fauna marina venezolana esta compuesta por especies de biorregiones muy distintas como lo son el Caribe y el Delta del Orinoco. En el Caribe, los ecosistemas han recibido una atencion considerable, sin embargo, debido al tremendo impacto de actividades humanas tales como el turismo, sobreexplotacion de recursos marinos, alteracion fisica, la industria petrolera y contaminacion, entre otras, estos ambientes se encuentran bajo un gran riesgo y su biodiversidad esta altamente amenazada. Los ecosistemas mas representativos de esta region incluyen las playas arenosas, litorales rocosos, praderas de fanerogamas marinas, arrecifes coralinos, comunidades de fondos blandos y bosques de manglar. El Delta del Orinoco esta constituido por un grupo muy complejo de ecosistemas marinos, estuarinos y dulceacuicolas, los habitats son muy diversos pero hay muy poca informacion disponible acerca de este sistema. En este trabajo resumimos lo conocido, lo cual es toda la informacion disponible en Venezuela acerca de la investigacion cientifica en biodiversidad, los diferentes ecosistemas y el grado de conocimiento que ha sido generado a traves de diversos tipos de publicaciones, las colecciones biologicas, la importancia y el alcance de las areas protegidas como reservas de biodiversidad y el marco legal institucional dirigido hacia su proteccion y uso sustentable. Igualmente, para lo desconocido, proponemos como prioridad de investigacion la estimacion de area, el listado completo de las especies y el estado de salud de los principales ecosistemas a una escala a nivel nacional. Esta nueva informacion debe ser integrada y resumida en bases de datos de sistemas de informacion geografica, accesible a la comunidad cientifica asi como a las agencias encargadas de los planes de manejo. A largo plazo, un inventario genetico deberia incluirse como una necesidad para establecer un mejor conocimiento de los recursos biologicos. Proponemos posibles proyectos a futuro en una escala local (Venezuela), regional (Caribe Sur: Colombia, Venezuela y las Antillas) y global (America del Sur).

The Census of Marine Life—evolution of worldwide marine biodiversity research

This paper discusses the origin and development of the 10-year Census of Marine Life, describing the way in which a visionary idea developed into a program involving over 80 nations. The time was ripe to engage in a large-scale marine biodiversity program incorporating the newest technology for exploration, along with the traditional approach of reviewing and synthesizing the known. We discuss the planning workshops, the development of the suite of projects as well as the management and support structures. The result was a international program with globally distributed responsibilities, but supported by a strong secretariat, national and regional organizations, an highly interactive outreach and education program, and the database, Ocean Biogeographic Information System. Scientific results are highlighted in 2,600+ publications, and the program, now completed, is expected to promote and influence biodiversity research and conservation for the long-term future.