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AQUATIC CONSERVATION: MARINE AND FRESHWATER ECOSYSTEMS

Aquatic Conserv: Mar. Freshw. Ecosyst. (2008)

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Published online in Wiley InterScience (www.interscience.wiley.com) DOI: 10.1002/aqc.993

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Diversity, conservation status and threats to native oysters (Ostreidae) around the Atlantic and Caribbean coasts of South America

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ALVAR CARRANZAa,*, OMAR DEFEOa and MIKE BECKb a

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ABSTRACT

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1. Despite the extensive literature on the ecology, systematics and culture of oysters worldwide, an assessment of their diversity, distribution and conservation status for the Atlantic and Caribbean coasts (i.e. depth 550 m) of South America is lacking. Such information is crucial because of the increasing coastal development that threatens most nearshore habitats throughout the region. 2. The available information on oysters on Atlantic and Caribbean coasts is reviewed with a focus on identifying regional conservation priorities based on ecological and socio-economic importance, as well as the magnitude of current or potential threats faced by oyster populations. The current status of a´- taxonomy within the Ostreidae was also examined. 3. Ten species of native Ostreidae (plus three introduced species) inhabit the coastal waters of the Atlantic and Caribbean coasts of South America. 4. Oyster species were ranked according to their biological/ecological and socio-economic value and conservation status within 10 distinct ecoregions. Crassostrea gasar in the Eastern Brazil ecoregion, C. rhizophorae in the Central Caribbean ecoregion and Ostrea puelchana in the North Patagonian Gulfs ecoregion should receive the highest priority for immediate conservation action due to extensive loss of mangrove habitat in the two former regions and evidence of decline of one of the most important populations for the latter. The need for a standardized methodology to assess the status of oyster populations throughout the ecoregions is identified. 5. On a local scale, the allocation of territorial use rights for fisheries under a collaborative/voluntary community framework is strongly advocated to fulfil management, conservation and poverty alleviation goals in these developing countries. Copyright # 2008 John Wiley & Sons, Ltd.

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UNDECIMAR; Facultad de Ciencias, Igua´ 4225, CP11400, Montevideo, Uruguay The Nature Conservancy and Institute of Marine Sciences, 100 Shaffer Road–LML, University of California, Santa Cruz, California 95060, USA

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Received 21 September 2007; Revised 16 April 2008; Accepted 25 May 2008

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KEY WORDS:

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Crassostrea; Ostrea; Ostreola; Lopha; oyster beds; ecoregions; South America

49 *Correspondence to: Alvar Carranza, UNDECIMAR; Facultad de Ciencias, Igua´ 4225, CP11400, Montevideo, Uruguay. E-mail:

51 [email protected]

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A comprehensive and definitive systematics of living oysters has been difficult to achieve because of the xenomorphic postlarval growth patterns, the lack of diagnostic anatomical characteristics and the widespread translocation of species across the globe (Yamaguchi, 1994; Carlton and Mann, 1996; Kirkendale et al., 2004). Modern molecular techniques are only now beginning to unravel the complex systematic of the group (Jozefowicz and O’Foighil, 1998; Lape`gue et al., 2002; Kirkendale et al., 2004; Shilts et al., 2007; Varela et al., 2007). According to Malacolog 4.1.0: A database of Western Atlantic Marine Mollusca1 (last access: 10 May 2007), 11 species of native Ostreidae are found in the coastal waters (i.e. depth 550 m) of the Atlantic and Caribbean coasts of South America. These oysters are Crassostrea rhizophorae (Guilding, 1828), Crassostrea brasiliana (Lamarck, 1819), Crassostrea gasar (Dautzenberg, 1891), Crassostrea virginica (Gmelin, 1791), Lopha (?) gibsonsmithi (Macsotay and Campos, 2001), Dendrostrea frons (Linnaeus, 1758), Ostrea cristata (Born, 1778), Ostrea libela (Weisbord, 1964), Ostrea lixula (Weisbord, 1964), Ostrea puelchana (d’Orbigny, 1842) and Ostreola equestris (Say, 1834). In addition, Crassostrea gigas (Thunberg, 1793) and Ostrea edulis Linnaeus, 1758 are known to have been introduced in the region (Orensanz et al., 2002; Ruesink et al., 2005). Recently, Varela et al. (2007) regarded C. brasiliana as a synonym of C. gasar and recorded an unidentified exotic species from north-eastern Brazil. Distribution ranges for the native species are summarized in Figure 1.

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DIVERSITY AND DISTRIBUTION

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Mollusc shells introduce complexity and heterogeneity into benthic environments and are key elements of habitat structure, affecting a variety of processes from population structure to ecosystem quality (see Gutierrez et al., 2003 for a review). In particular, oyster beds can directly or indirectly affect local biodiversity, population dynamics, food webs and nutrient cycling in nearshore marine and estuarine habitats from temperate to tropical latitudes worldwide (Dame et al., 1986; Newell, 1988; Thomsen et al., 2007). In addition, several oyster species are of significant commercial importance (Carriker and Gaffney, 1996). The decline of wild oyster populations has been increasingly commented upon since at least the first half of the 20th century (Gross and Smyth, 1946), and there is evidence that in some regions this loss happened centuries ago (Airoldi and Beck, 2007). For instance, commercially harvested Tasmanian oyster populations have been in decline since at least the end of the 19th century (Edgar and Samson, 2004), and the Australian east coast oysters were decimated by imported diseases between 1880 and 1900 (Ogburn et al., 2007). Chesapeake Bay’s oyster populations declined dramatically during the 20th century, mainly due to harvesting pressure, combined with loss of reef habitat, pollution, and disease (Kennedy and Breisch, 1981; Ford and Tripp, 1996; Jackson et al., 2001). In Europe, Ostrea edulis beds at the Wadden Sea nearly vanished due to overfishing (see Wolf, 2000 and references therein). In part because of declines in native species, non-native oysters have been introduced worldwide in 73 countries with many known untoward ecological consequences and many others not yet fully understood (Ruesink et al., 2005b). Consequently, there has been increasing concern expressed about the need for conservation and restoration of structured shellfish habitats such as oyster reefs and beds (Coen and Luckenbach, 2000). The condition of native oysters on the Atlantic and Caribbean coasts of South America may not as yet be as dire as that in many other regions, but there is cause for significant concern that oysters along these coasts are following the same trends as populations elsewhere. Although there is a large body of general literature on the ecology, systematic and culture of oysters, an assessment of diversity, distribution and conservation status of native oyster species on South American coasts is lacking. The aims of this paper are: (a) to review existing information of diversity and distribution of South Atlantic and Caribbean oysters (Ostreidae) in South America; and (b) to suggest regional conservation priorities based on species ecological and socio-

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economic importance and the magnitude of the current or potential threats faced by oyster populations.

INTRODUCTION

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Mangrove oysters The taxonomic status of mangrove oysters (genus Crassostrea) is the most complex among oysters. The American oyster C. virginica seems to occur exclusively in the northern portion of South America, though some authors extend its distribution range southwards into coastal regions of Brazil, thus overlapping the range of C. rhizophorae (Gunter, 1951). The latter lives attached to the roots of mangrove trees (rhizophores), whereas C. virginica adults are found mainly attached to hard, solid substrata. Several authors do not recognize these two forms as separate species (Menzel, 1973; Newball and Carriker, 1983). More recently, Lape`gue et al. (2002) showed that these species yielded the lowest genetic

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Information provided with permission from The Academy of Natural Sciences, Philadelphia, PA.

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O. lixula, O.libela, O. cristata and L. gibsonsmithi are represented by single records. Note that the southernmost record for C. rhizophorae is probably based on a fossil specimen.

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27 Figure 1. Literature records for Ostreidae species in the Caribbean and Atlantic coasts of South America. No precise records for D. frons were found.

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distance estimates (Kimura’s two-parameter model) among the 33 seven oyster species studied. In a relatively recent taxonomic list of Brazilian molluscs, Rios (1994) recognized only one 35 Brazilian mangrove oyster (C. rhizophorae), explicitly stating that C. virginica does not occur in Brazil. Later, Ignacio et al. 37 (2000) demonstrated, on the basis of allozyme data, that two distinct biological species, C. brasiliana and C. rhizophorae, 39 occur along the coast of Brazil. In agreement, Pie et al. (2006) discriminated between three oyster species on the Brazilian 41 coast (C. brasiliana, C. rhizophorae and C. gigas) through a simple PCR-RFLP method. Lape`gue et al. (2002) have also 43 suggested that there is a fourth mangrove oyster on the Atlantic coast, C. gasar, which has a transatlantic distribution. 45 However, it has been suggested that gene sequences from C. brasiliana (GenBank DQ839413) and C. gassar (GenBank 47 AJ312937) are identical (Melo et al., 2007), a fact that was confirmed by Varela et al. (2007). These authors performed 49 mitochondrial DNA (16S rRNA gene) analyses from 120 specimens collected at nine different sites distributed along 51 the Brazilian coast. They identified two native species (C. gasar, distributed from the Amazon to the Parnaı´ ba Copyright # 2008 John Wiley & Sons, Ltd.

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delta; and C. rhizophorae, from the north-east Fortim to the south of Brazil) and an exotic Crassostrea species, closely related to Indo-Pacific Crassostrea, which was restricted to one location in the north of Brazil. The southernmost records for a living Crassostrea species belong to Uruguayan waters (C. rhizophorae praia; see Scarabino (2003), and references therein), but they are more likely attributable to Holocene fossil specimens of C. rhizophorae praia (Figure 1).

Flat oysters Ostrea cristata, O. libela, O. lixula, O. puelchana and Ostreola equestris are the currently used names for South American flat oysters (Rios, 1994; Scarabino, 2003) whose distributions are shown in Figure 1. Ostrea libela and O. lixula are highly endemic species, apparently restricted to the Caribbean Sea (Venezuela: Isla Margarita; Macsotay and Campos Villarroel, 2001). In turn, O. cristata, a medium-sized species (Rios, 1994), exhibits a wider tropical distribution, ranging from Venezuela to Laje dos Santos and Trindade Island (Brazil; Rios, 1994). The temperate species O. puelchana, distributed from Southern Aquatic Conserv: Mar. Freshw. Ecosyst. (2008) DOI: 10.1002/aqc

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17 Despite their current and potential socio-economic and ecological importance, there has been an absence of long19 term demographic studies in oyster populations throughout the study region. In fact, there are no oysters included in the 21 IUCN red list of endangered species (IUCN, 2006), even though severe population declines have been documented 23 elsewhere (Kirby, 2004). Therefore, in this section we focus on identifying population trends, based on four main features: (1) 25 habitat loss and deterioration (that includes the present or threatened destruction, modification or curtailment of its 27 habitat or range, due, for example, to urbanization and/or pollution); (2) overfishing; (3) negative effects of exotic species; 29 and (4) impact of diseases in wild populations.

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CONSERVATION STATUS AND THREATS TO SOUTH AMERICAN OYSTERS

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during recent decades. For example, the current cover of mangroves around the perimeter of Lake Maracaibo is just 10% (Conde and Alarco´n, 1993) of that reported by Hueck (1960). This is not an isolated record, with depletion of mangroves reported for several localities in this country (Esteves, 1980). In French Guiana, mangroves found in fringing communities as a thin band along the coast have been affected by sedimentation and erosion along the coast. Guianan mangrove ecosystems have been significantly depleted, although large stands are still found in areas where human population density is lower. In Brazil, commercial fishing primarily for shrimp and gold mining that has led to mercury contamination (Kjerfve and Lacerda, 1993; RebeloMochel, 1997) are both important threats to the mangroves there. However, the Maranhao (36% of the total Brazilian mangrove area) and Para´ (28%) mangroves are largely intact due to low population density and poor accessibility (Kjerfve and Lacerda, 1993). This large region of mangrove has the potential to harbour important oyster populations, and should not be neglected as a conservation target. The close relationship between mangrove oysters and the extent of habitat cover provided by mangrove ecosystems supports the inference that large-scale reduction in habitat availability may lead to a concomitant population decline in mangrove-associated oysters. Further, there is evidence suggestive of a non-linear relationship between rates of decline of mangrove cover and oyster abundance: (1) extraction of Crassostrea spp. shells declined by nearly 75% in the Sundarbans of Bangladesh, whereas mangrove production declined only 0.04% (Manson et al., 2005; Ellison, 2008); (2) oyster production among the five major Caribbean producers (Colombia, Cuba, Dominican Republic, Jamaica, and Venezuela) fell in 2004 to 65% of their historic peak in 1990 (see Figure 5 in Ellison, 2008), associated with a decline of only 5% of the total mangrove area across these countries (Wilkie and Fortuna, 2003). The loss of macrobenthic diversity and declines in oyster abundance in Asian mangrove ecosystems have been related to negative changes in the status and functioning of these environments due to mangrove denudation and other anthropogenic interventions (Raut et al., 2005). However, to date, no continental-scale study links mangrove degradation and biodiversity loss in South America. Chemical pollution also affects oyster populations in the neighbourhood of urban centres (Lacerda et al., 1987; Carvalho et al., 1993; Meyer et al., 1998; Rebelo et al., 2003). Lacerda and Molisani (2006) provided long-term trends for the concentrations of Cd and Zn in mangrove oysters (Crassostrea spp.) at Sepetiba Bay, a semi-closed coastal lagoon about 60 km south of Rio de Janeiro city, SE Brazil. The results mainly show that average Zn concentrations in oysters increased continuously from 1978 to the present. Zinc

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1 Brazil (228 560 S) to Golfo San Matı´ as, Argentina (418300 S), is economically important (Pascual et al., 1989; Rios, 1994). 3 Since there has been some confusion regarding the names O. spreta, O. puelchana and O. equestris, we follow Harry (1985) 5 and considered O. spreta as a synonymy of O. equestris. Two further species, Lopha gibsonsmithi and Dendrostrea frons, 7 have been reported for the study area. Records for L. gibsonsmithi are restricted to the inner continental shelf of 9 Venezuela, while D. frons occurs also from the Caribbean to Rio de Janeiro, Brazil (Rios, 1994). 11

Habitat loss and deterioration

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33 Mangrove oysters face one of the most obvious threats: the loss of their habitat. Worldwide, original mangroves covered 35 approximately 75% of tropical coasts and inlets, but now only occupy about 25% (Farnsworth and Ellison, 1997). The fragile 37 mangrove ecosystem can be destroyed due to the impact of the resuspension of sediments (Orihuela et al., 1991) or a 39 combination of low temperatures and decreased salinity (Laboy-Nieves et al., 2001). In Colombia, the largest coastal 41 Caribbean lagoon (Cie´naga Grande de Santa Marta) has been affected by human-induced alterations in the exchange of 43 riverine and marine waters in this system. More than 58% of the mangrove area in the neighbouring Isla de Salamanca has 45 been lost and nearly 10% of total mangrove area has been severely degraded (Sa´nchez, 1988). In this coastal lagoon, 47 between 1960 and 1987, more than 30% of the mangrove habitat was lost (
16 460 ha). Cardona and Botero (1998) 49 estimated the rate of loss of mangrove habitat at 886 ha yr1 or 2.4 ha day1 in 1993. Venezuelan mangrove woodlands, although not 51 systematically monitored, have suffered dramatic losses Copyright # 2008 John Wiley & Sons, Ltd.

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Overfishing

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According to FAO (2005), most of the oysters currently marketed worldwide come from aquaculture, with the exploitation of wild populations currently being a very small fraction of worldwide oyster production. The increasing demand for shellfish has led to increasing attempts to enhance oyster production in South America, often by proposing and sometimes successfully introducing non-native species. The Pacific oyster C. gigas was introduced in Brazil before 1989 (Nascimento, 1991) and in 1982 in Argentina (Orensanz et al., 2002). Regarding the latter, there is evidence of negative ecological effects of the introduced oysters: Escapa et al. (2004) reported that C. gigas now occurs exclusively on rock outcrops in northern Patagonia, which produced a shift in the abundance patterns of epifaunal species and foraging behaviour of shorebirds. In addition, Orensanz et al. (2002) mentioned that C. gigas recruitment onto native mussels that normally dominate intertidal rocky shores, has affected the ecological structure of the native benthic community. The progressive increase in abundance of the exotic bivalve Isognomon bicolor (Domaneschi and Martins, 2002) reported for Southern Brazilian rocky outcrops, has been identified as a potential threat to Brazilian oyster populations due to probable competitive exclusion (Rocha et al., 2007). Congeneric species are not the only threat to native oyster populations: for example, in the 1990s the large predatory gastropod Rapana venosa was introduced through ballast water in the Rio de la Plata estuary (Scarabino et al., 1999; Pastorino et al., 2000; Carranza et al., 2008). Giberto et al. (2007) and Carranza and Rodrı´ guez (2007) reported R. venosa near O. puelchana banks, probably preying on this species. Results from the trophic food webs in the estuary, using stable dI5N and dI3C isotope signatures, supported this hypothesis (Giberto et al., 2007). This may further aggravate the apparent population decline of oyster beds in the Uruguayan portion of this estuary (Carranza and Rodrı´ guez, 2007), putatively caused by uncontrolled exploitation of local beds (Scarabino et al., 2006). Unfortunately estimates of oyster density or the area formerly covered by the oyster beds are lacking.

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The existence of prehistoric sambaquis (i.e. deposits of shells) 27 on the Brazilian coast near estuaries demonstrates the early use of oysters by human populations. Currently, excessive or 29 indiscriminate harvesting, incidental mortality of non-target species (‘bycatch’) and fishery-related disturbances to marine 31 habitats are the most obvious negative ecological effects of fishing and are, besides pollution, the principal cause of threat 33 to benthic invertebrates in South America, including oysters (Amaral and Jablonski, 2005). Oyster shellfisheries on the 35 Atlantic and Caribbean coasts of South America are mainly artisanal, largely unregulated, but with high socio-economic 37 importance, especially among lower income households (Pereira et al., 2001; Marques-Silva et al., 2006; Nishida 39 et al., 2006). In Venezuela, the mangrove oyster C. rhizophorae used to be 41 one of the most common and abundant species in the Rhizophora mangle roots (Ma´rquez and Jime´nez, 2002) and 43 an important resource for subsistence fishers, but it is now almost extinct due to overexploitation (Rodrı´ guez and Rojas45 Sua´rez, 1995). In Brazil, coastal shellfish are a major component of fishing activities concentrated at the periphery 47 of many towns close to estuaries (Nishida et al., 2006). In Mundau´ and Manguaba lagoons, the gatherers cut off the 49 intertidal roots of mangrove and thus damage the plants (Silva and Barros, 1987). Pereira et al. (2001) evaluated the stock and 51 growth patterns of Crassostrea brasiliana from the Canane´iaIguape estuarine complex (288S; 488W), showing that current

oyster extraction from natural beds is close to the maximum sustainable yield. According to these authors, exploitation during the 1990s was almost double the figures for 1970 (which was 25 tonnes month1). In 2000, total oyster production (including those from natural and cultured oyster beds) was near 18 tonnes month1. In San Matı´ as Gulf, clandestine fishing on the shallower O. puelchana beds, as well as the occurrence of the species as by-catch in mussel and scallop fisheries, is an increasing concern (M. Pascual personal communication), although the decline in scallop stocks has prompted a ban on the collection of this species (UNEP, 2004).

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1 concentrations are among the highest reported for oyster tissues worldwide. Chemical pollution affecting oyster 3 ecosystems is not an exclusive phenomenon of highly populated places: although the Mamanguape mangrove 5 forest is one of the best preserved in Paraı´ ba State (northeastern Brazil), local fishers reported that declining catch was 7 linked to the use of agrochemicals used in sugar-cane cultivation (Nishida et al., 2006). In Argentina, the main natural beds of the puelche oyster 9 occur exclusively in the NW of San Matı´ as Gulf, Argentina, 11 namely Banco las Grutas (408480 S; 658050 W) and Banco Reparo (408400 S; 638300 W) (Fernandez Castro and Le 13 Pennec, 1988; Pascual et al., 1989; Pascual and Zampatti, 1995). These two banks occupied an area of, respectively, 38 15 and 2 km2, with adult densities of 32 and 22 ind/10 m2 in 1987– 1988 (Pascual, 1997). Recently, one of the main oyster banks in 17 San Matı´ as Gulf has been eliminated during dredging operations prior to the construction of a shipping terminal 19 (M. Pascual personal communication). Since larvae of O. puelchana prefer to settle on conspecific live oysters (Pascual 21 and Zampatti, 1995), the loss of these substrata may lead to cascading population effects. 23

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ESTABLISHING CONSERVATION PRIORITIES

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31 There is no integrated large-scale assessment of the conservation status of oyster populations on the Atlantic and 33 Caribbean coasts of South America. The current approach was based on two components: one set of indicators specific to 35 oysters, and a second set of indicators to identify the general conservation status of the broad geographic ecoregions in 37 which particular shellfish occurred. 39

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The second step or set of indicators was used to develop a species condition index for each oyster species based on their bioecological features and socio-economic importance (Table 1). This process, which involved the selection of indicators as direct and indirect measures of bioecological and socio-economic value, allowed ranking of the conservation urgency for a given species in each ecoregion. To this end, a biological/ecological/socio-economic value was obtained for each species using data specific to each ecoregion, compiled from library research, scientists, local naturalists, and technical data sources. When quantitative data were not available, ranks were produced after a qualitative assessment based on existing knowledge. The overall ranking for biological/ecological/ socio-economic value was obtained by a simple sum of all ranked values for indicators related to abundance, potential impact on ecosystem functioning and species’ socio-economic importance, and weighing this sum by considering species size and evidence of population decline. Species with higher abundances were considered more important, as were epibenthic, reef-forming bivalves that provide significant vertical structure and are a dominant structural component of benthic ecosystems. The rationale here is that species with higher abundances are more likely to be overexploited and may have strong effects in ecosystem functioning, and that life habit is related to the species contribution to ecosystem functioning (Coen et al., 2007). This is not to say that rare species do not warrant conservation efforts but, in a trade-off between ecological rarity and a species impact on ecosystem functioning, we assigned high priority to the latter. Furthermore, effective conservation efforts devoted to these species should also benefit any associated rare species. The socio-economic value of the species was also included, taking into account the existence and modality of human exploitation. The weighting of species according to its size assumes that larger species are often preferentially collected,

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3 Introduced or endemic diseases threaten both natural and cultured oyster populations and can hinder restoration efforts. 5 These problems are similar to those in North America for C. virginica, whose remaining populations have been devastated 7 by diseases (primarily DERMO (caused by the pathogen Perkinsus marinus) and MSX (Multinucleated Sphere 9 Unknown); see Ewart and Ford, 1993). Information concerning this kind of episode is scant for the study area. 11 However, in cultures of the native flat oyster O. puelchana in San Antonio Bay, Argentina, cumulative mortality was 95% 13 when individuals reached marketable size and culture had to be discontinued. Histopathological analysis and evaluation of 15 parasitic prevalence determined that Bonamia spp. was the possible pathogen, suggesting that this parasite could be the 17 main cause of the recurrent mortalities observed in natural beds (Kroeck and Montes, 2005). This might also be the case 19 for the recent disappearance of O. equestris populations from the shallower areas of San Matı´ as Gulf, a problem even more 21 serious than the decline in O. puelchana abundance in the region (M. Pascual personal communication). Though not 23 found in Brazilian mangrove oyster cultures (Nascimento et al., 1986), the parasite Perkinsus marinus (the cause of the DERMO in C. virginica) has been detected in Jamaican 25 cultures of C. rhizophorae (Littlewood, 2000).

species. Scores were available for 11 coastal biogeographic ecoregions (hereafter ecoregion) identified within the study area: North Patagonian Gulfs (within the Cold-Temperate South-western Atlantic Province), Uruguay-Buenos Aires Shelf, Rı´ o de la Plata, Rio Grande and South-eastern Brazil (Warm-temperate South-western Atlantic Province), Eastern Brazil, North-eastern Brazil and Amazonian (Tropical Southwestern Atlantic Province) and Guianan and Central Caribbean (Tropical North-western Atlantic Province). These ecoregions were defined after consideration of a number of biological, physical and geographic characteristics, including the features of the continental shelf, sea surface temperature, ocean currents and the distribution of major faunal populations (Sullivan and Bustamante, 1999).

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41 The first step in developing an assessment of conservation need was to understand the regional need or context for 43 conservation. Sullivan and Bustamante (1999) identified a number of general (i.e. not specific to shellfish per se) measures 45 of conservation needs within South American ecoregions. The raw scores provided by Sullivan and Bustamante (1999), which 47 included 33 potential indicators that are applicable to entire provinces, ecoregions and coastal systems, and are measures of 49 general conservation needs were used. These 33 indicators can be divided into five main groups: (a) alteration of habitats, (b) 51 loss of species, (c) loss of breeding and nursery sites, (d) changes in abundance, and (e) potential threats for marine Copyright # 2008 John Wiley & Sons, Ltd.

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Abundance Very abundant (580%) Abundant (60–79%) Common (40–59%) Scarce (20–39%) Occasional (520%) Secondary structure Epibenthic reef-forming bivalves that provide significant vertical structure (50.5 m) and are the dominant structural component of the benthos Structurally complex epibenthic bivalves that occur at densities sufficient to form macro-relief (50.5 m) on the bottom Epibenthic bivalves that provide secondary structure on top of other underlying hard substrate such as rocks or mangrove roots Other infaunal or epifaunal bivalves that occur at lower densities and do not provide the majority of benthic structure, but may provide some important ecosystem services Individual size Largest species and maximum adult shell length Socio-economic importance No cultured, no harvested Experimental cultures and or/ artisanal harvesting Commercial cultures, industrial scale harvesting Evidences of stock decline No evidence of decline Evidence of decline

O

7

Ranking value

O

5

Bioecological socio-economic criteria

PR

3

Table 1. Bioecological and socio-economic criteria used to obtain a species condition index, including the associated ranking value

25

3 2 1 1 0 1 2 1 2

determine the scientific validity of establishing geographic priorities.

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27 thus being more prone to overexploitation (Roy et al., 2003 and references therein). Thus, all else being equal, the species 29 attaining maximum adult size will be the one with maximum need for immediate conservation actions (i.e. highest condition 31 index). However, since individual size usually varies along a species’ latitudinal range (Roy and Martien, 2001), a species 33 ranked with high priority in one ecoregion may have lower priority in another ecoregion where the size of individuals is 35 smaller. In addition, were there to be any historical evidence of population decline within an ecoregion, the score for that 37 species was doubled, thus stressing the need for conservation actions. An example of the construction of the condition index 39 calculation is shown in Table 2. The species condition indexes were then weighted by the 41 status scores of the ecoregions (see above) in which they occurred. Although ecoregions differed markedly, this 43 approach allowed identification and ranking of those combinations of species and ecoregions where both the need 45 for conservation actions and the ecological or biological value of a given species were suggestive of a conservation priority 47 (higher condition index). This ranking relied on the ecoregion conservation scores made by regional experts and project 49 personnel who previously reviewed the compiled information and decided which indicators should be used for ranking 51 within each province (Sullivan and Bustamante, 1999). The ranking process and criteria had previously been examined to

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5 4 3 2 1

Copyright # 2008 John Wiley & Sons, Ltd.

Aqc 993

Results C. gasar/brasiliana in Eastern Brazil, C. rhizophorae in the Caribbean region and O. puelchana in North Patagonian Gulfs were the species with the highest priorities for conservation actions (Table 3). This result is based on a combination of high values of the condition index and a large number of regional conservation problems (and is certainly strongly influenced by the evidence of population decline for these species in the ecoregions mentioned above). However, and particularly for C. rhizophorae, the scores are high all along the species’ range. It should be noted that the records for C. brasiliana and C. gasar were merged as they were considered to be the same species (C. gasar in tables and figures), according the specific epithet rhizophorae to those ecotypes that are associated with mangroves. This is supported by the empirical knowledge of Brazilian mollusc gatherers, who recognize two ecotypes of mangrove oysters, the ‘ostra-de-mangue’ or mangrove oyster sensu stricto (attached to the roots and stem of R. mangle) and the ‘ostra-de-mergulho’ or diving oyster (attached to stones, pebbles, and other hard substrates on the river bed and in river branches that penetrate the mangrove; Nishida et al., 2006). Aquatic Conserv: Mar. Freshw. Ecosyst. (2008) DOI: 10.1002/aqc

AQC : 993 8

49 51

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8.39 18.00

SUMMARY AND PROSPECTS FOR CONSERVATION, MANAGEMENT AND RESEARCH

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N/A

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N/A N/A N/A Guianan

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N/A

4 4 (Bonilla et al., 1969) 2 2 (Bonilla et al., 1969)

4 (Fernandes, 1981) 2

Ten species of native Ostreidae (plus three introduced) inhabit the coastal waters of the Atlantic and Caribbean coasts of South America, although there is some uncertainty on the taxonomic placement of certain populations. Only recently (2007), the scenario for South Atlantic and Caribbean Crassostrea taxonomy seemed to have been clarified, but earlier records are difficult to assign to species with high certainty. The proposed method for establishing conservation priorities may serve as a basis for practitioners and policymakers to develop conservation strategies aimed at reversing or mitigating the critical situation of the most threatened oyster populations. Although the methodology developed here did not consider uncertainty of information when prioritizing species, Knapp et al. (2003) found high concordance between conservation rankings generated by methods incorporating uncertainty and equivalent methods without uncertainty. Potential targets for conservation actions within a restricted geographic context were identified, a fact that may enhance the likelihood of successful short-term conservation measures. In order to improve management of the oyster populations and intertidal oyster reef habitats, it is suggested that it is necessary to: (1) identify overall management goals and possible options; (2) develop a standardized methodology to assess the status of oyster beds; and (3) design monitoring programmes to quantify the effect of each management option in the long term. This will be impossible without the establishment of an integrated research programme involving scientists from all South American countries. In addition, co-management of exploited oyster populations is considered one of the most promising ways to link sustainability and economic growth. This involves (1) incorporating local residents into land-use policy and management decisions, (2) giving people ownership of biological resources, and (3) returning economic benefits of conservation to local people (Castilla and Defeo, 2005; Defeo and Castilla, 2005). These approaches are relatively new to the region, but preliminary results are promising. For example, an oyster fishing cooperative (Cooperostra) was recently established in Cananeia (Sao Paulo, Brazil) and since its implementation, oyster stocks within the mangrove, and in particular the Mandira Extractive Reserve, have been relatively constant, and possibly might even have increased slightly (Medeiros, 2006). However, there needs to be better and more formal stock assessment to assess the success of this management approach (Medeiros, 2006). Additionally, to be successful in oyster conservation and management in South America, the loss of mangroves must be urgently addressed. The establishment of mangrove conservation and restoration programmes is strongly recommended. Taking

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1 9 2 (Rodrı´ guez and 18 Rojas-Sua´rez, 1995; Carpenter, 2005) N/A N/A

9.00 9 1

10.91 5 (Marques-Silva et al., 2006)

3 (Pie et al., 2006)

120

120 3 (Marques-Silva et al., 2006; Nishida et al., 2006) 3 (Fernandes, 1981; 120 Nishida et al., 2006; Cavalcanti et al., 2007) 3 120 3 (FAO, 2005) 120

1

2 (Marques-Silva 20 et al., 2006)

8

6.73

SpeciessCondition core index Evidence of population decline

Copyright # 2008 John Wiley & Sons, Ltd.

Tropical Northwestern Atlantic

47

0.93 1.00

45

Eastern Brazil Central Caribbean

43

1.00

41

O

39

Northeastern Brazil

37

2

35

0.55

33

C

31

Amazonian

29

3 (Tanaka and Magalha˜es, 2002)

27

2

25

0.84

23

N

21

Southeastern Brazil

19

U

17

Warm-temperate Southwestern Atlantic Tropical Southwestern Atlantic

15

Maximum adult size (mm)

13

Cultured / Harvested

11

Abundance

9

Weighed Secondary regional structure conservation score

7

Ecoregion

5

Province

3

Table 2. Example of a completed ranking process to assess a species condition index along different ecoregions: the mangrove oyster C. rhizophorae. See text for details on the ranking procedure

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Aquatic Conserv: Mar. Freshw. Ecosyst. (2008) DOI: 10.1002/aqc

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DIVERSITY, CONSERVATION STATUS AND THREATS TO NATIVE OYSTERS

1 Table 3. Condition index for all oyster species within each ecoregion. Due to the uncertainty in taxonomic identifications based solely on morphological traits, records for C. brasiliana and C. gasar were considered as a single taxonomic unit (see text for details)

3 Ecoregion

C. rhizophorae C. gasar O. cristata O. puelchana O. equestris O. lixula O. libela D. frons L. gibsonsmithi

5 North Patagonian gulfs

– Uruguay–Buenos Aires Shelf – Rio de la Plata – 7 Rı´ o Grande – Southeastern Brazil 5.77 9.35 9 Amazonian Northeastern Brazil 7.71 Eastern Brazil 7.18 11 Central Caribbean 15.42 Guianan N/A

– – – – 6.73 6.55 18.00 11.18 – N/A

– – – – 1.30 0.84 1.54 1.44 1.54 N/A

11.73 1.47 0.61 1.12 1.86 – – – – N/A

2.42 1.55 1.15 1.15 1.47 0.95 1.75 1.63 1.75 N/A

– – – – – – – – 1.00 N/A

– – – – – – – – 0.63 N/A

– – – – 1.05 0.68 1.25 1.16 1.25 N/A

– – – – – – – – 1.1 N/A

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Amaral ACZ, Jablonski S. 2005. Conservation of marine and coastal biodiversity in Brazil. Conservation Biology 19: 625– 631. Bonilla RJ, Benı´ tez J, Okuda T. 1969. Variacio´n estacional de la composicio´n quı´ mica del ostio´n, Crassostrea rhizophorae (Guilding) en Laguna Grande y la bahı´ a de Mochima. Boletı´n del Instituto Oceanogra´fico de la Universidad del Oriente (Venezuela) 8: 46–52. Cardona P, Botero L. 1998. Soil characteristics and vegetation structure in a heavily deteriorated mangrove forest in the Caribbean Coast of Colombia. Biotropica 30: 24–34. Carlton JT, Mann R. 1996. Transfers and world-wide introductions. In The Eastern Oyster Crassostrea virginica, Kennedy VS, Newell RIE, Eble AF (eds). Sea Grant Publications: College Park, MD; 691–706. Carpenter KE. 2005. The living marine resources of the Western Central Atlantic. Introduction, molluscs, crustaceans, hagfishes, sharks, batoid fishes and chimaeras. In FAO Species Identification Guide for Fishery Purposes and American Society of Ichthyologists and Herpetologists Special Publication No. 5. Food And Agriculture Organization of The United Nations (FAO): Rome. Carranza A, Rodrı´ guez M. 2007. On the benthic molluscs of Banco Ingle´s (Rı´ o de la Plata, Uruguay). Animal Biodiversity and Conservation 30: 161–168. Carranza A, Scarabino F, Ortega L. 2008. Distribution of large benthic gastropods in the Uruguayan continental shelf and Rı´ o de la Plata estuary. Journal of Coastal Research 24: 161–168. Carriker MR, Gaffney PM. 1996. A catalogue of selected species of living oysters (Ostreacea) of the World. In The Eastern Oyster: Crassostrea virginica, Kennedy VS, Newell RIE, Eble AF (eds). Maryland Sea Grant Publications: College Park, MD; 1–18. Carvalho CEV, Lacerda LD, Gomes MP. 1993. Metais pesados na biota bentica da Baia de Sepetiba e Angra dos Reis, RJ. Acta Limnologica Brasiliensia 6: 222–229. Castilla JC, Defeo O. 2001. Latin American benthic shellfisheries: emphasis on co-management and experimental practices. Reviews in Fish Biology and Fisheries 11: 1–30.

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15 into consideration the many ecosystem services (such as shellfisheries) that they provide, this strategy seems highly 17 profitable in the medium and long term if catalysed with a comanagement scenario. These concurrent practices should lead to 19 better fishery management and to reduced destructive fishing such as cutting mangroves (Castilla and Defeo, 2001; Pereira 21 et al., 2001; Kirby, 2004). The recognition of the socio-economic and ecological value of these shellfish habitats should also lead to 23 the establishment of MPAs explicitly designed to conserve these highly structured habitats. Finally, a region-wide policy for 25 exotic species should be implemented in view of the increasing risks associated with the introduction of non-native species 27 (Ruesink et al., 2005). The study region does not yet have a high occurrence of intensive non-native oyster culture (despite the 29 existence of localized examples documented here). Consequently, there is an opportunity to exercise a precautionary management 31 approach and exclude the introduction of exotic species for culture and, at the same time, look for marketing opportunities 33 for products derived from native oysters (Ruesink et al., 2005).

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ACKNOWLEDGEMENTS

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This work was partially supported by The Nature Conservancy 39 and the Kabcenell Family Foundation. Special thanks to F. Scarabino, G. Nishida, M. Pascual, O. Iribarne and M. Kroeck 41 for providing useful bibliography and/or invaluable information. AC acknowledges Marina and Estela for 43 encouragement and support .

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Aquatic Conserv: Mar. Freshw. Ecosyst. (2008) DOI: 10.1002/aqc

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Rebelo-Mochel F. 1997.