Marine mollusks of Bahía Málaga , Colombia ( Tropical Eastern Pacific )

A checklist of mollusks reported in Bahía Málaga (Valle del Cauca, Colombia) was developed through recent samplings in the zone (2004–2012), together with bibliographic and museums’ collections reviews. Species’ distributions in Bahía Málaga were established through 18 different subregions, which included the inner, middle and outer zones of the bay. A revision of the western American distribution for the species was also carried out. A total of 426 species were found, of which 44 were new reports for the Colombian Pacific coast. Results supported the high marine biodiversity that has been reported for this region.


INTRODUCTION
Bahía Málaga (Malaga Bay) is one of the most biodiverse zones on the Pacific coast of Colombia.The high marine biodiversity of Bahía Málaga played a fundamental role in its declaration in 2010 as a marine protected area, becoming the 56 th unit of the National System of Colombian Protected Areas (Sistema Nacional de Áreas Marinas Protegidas).
Zoological studies on the Colombian Pacific coast have been focused mainly on crustaceans and fishes.Bahía Málaga is not an exception; most of the scientific research in the region has been focused on these taxonomic groups (INVEMAR et al. 2007).There have been some attempts to make checklists and to carry out other biological studies (at specific, population, and community levels) of Mollusca, some of them focused on species of economic interest (Rubio et al. 1988) and others relating species with their habitats (Escallón and Cantera 1989;Cantera 1991;Lozano-Cortés et al. 2012) but none of them is complete.Now, with more than 20 years of research, this checklist contains all species known in the bay.

Study site
Bahía Málaga is located in the central region of the Colombian Pacific coast (03°56'-04°05' N and 77°19'-77°21' W) (Figure 1).Due to the fact that it is a tectonic estuary, the bay is a hybrid between hard (tertiary cliffs) and soft (estuarine zones) substrates, presenting a high number of habitats and hence high biodiversity.Its littoral zone, with an area of 136 km 2 , is composed of different ecosystems, such as rocky and sandy shores, muddy flats, and mangrove forests (Cantera 1991).
Rocky shores in Bahía Málaga may consist of cliffs and/or boulders.The range in the size and texture of the particles present in the rocky shores allow for a variety of microhabitats, making it a very diverse ecosystem (INVEMAR et al. 2007).Sandy beaches consist of very fine particles that may be free or compacted, primary containing fragments of mollusk shells and decomposing vegetative matter, originating from the surrounding mangroves (Cantera et al. 1994).These zones have been found to be most affected by the tide action and are primary found near the bay's mouth.Mudflats consist of miry expanses resulting from erosion of coastal areas that are rich in detrital material.These zones are rich in nutrients; hence their energetic content is high (Prahl et al. 1990).Bahía Málaga's substrate variety leads to a fragmented distribution of mangroves.In zones where cliffs are common (north and south), dwarfed mangroves predominate, while in zones with greater influence of rivers (inner zone of the bay), mangrove forests are more developed, with tall mangrove trees and more extensive stands (INVEMAR et al. 2007).

Data collection
A detailed checklist for mollusks of Bahía Málaga was developed through the information gathered during three major research projects in the last nine years, both based on the projects' sampling results and on bibliographic and collection reviews.The projects were: Valuation of Marine and Coastal Diversity of Bahía Málaga, Valle del Cauca (2004-2007) (INVEMAR et al. 2007), Biodiversity of Vulnerable Life Cycle Stages of Marine Organisms in Bahía Málaga (Colombian Pacific) as a Conservation Criteria (2007)(2008)(2009)(2010) (UNIVALLE and INVEMAR 2010) and Environmental Vulnerability of Marine and Coastal Ecosystems of Bahía Málaga (Colombian Pacific): Natural and Anthropic Threats (2011)(2012)(2013) (UNIVALLE and INVEMAR. 2013).Sampling was carried out at 18 subregions in the bay (Figure 1) between 2004 and 2012, and was based on intense sampling, rapid ecological assessments for intertidal and shallow water habitats (using snorkeling and scuba diving), and on the use of different artificial habitats as collection

RESULTS
A total of 426 species of marine mollusks were reported in Bahía Málaga: Polyplacophora: 3 families, 7 species; Bivalvia: 34 families, 168 species; Gastropoda: 68 families, 249 species, Cephalopoda: 2 families, 2 species (Appendix 1).Between 2004 and 2012, there were 145 species newly reported in the bay (Figure 2).Forty-four of these species were new reports for the Colombian Pacific coast, hence extending their geographic distribution.Thirty-four species have been found only as empty shells in the bay.Unpublished literature, e.g., Master's theses, dissertations, undergraduate projects, etc., have reported 39 species in the bay that were neither found in the surveys of the previously mentioned research projects, reported in published papers, nor found in museum collections.These The taxonomic status of each species reported in Bahía Málaga was checked in the World Register of Marine Species online database (WoRMS 2014) (http://www.marinespecies.org).The geographic range of each species was also reviewed in Discover Life (2014) (http://www.discoverlife.org),Encyclopedia of Life (2014) (http://eol.org),Keen (1971), and Coan and Valentich-Scott (2012).CITES (2014) (http:// checklist.cites.org),IUCN (2014) (http://discover.iucnredlist.org), and local red lists (Ardila et al. 2002;Castellanos et al. 2011) and interviews with experts of the region were reviewed in order to identify species with some state of vulnerability.Species with economic importance were identified through a review of FAO (Food and Agriculture Organization of the United Nations) literature (Fischer et al. 1995) (Swainson, 1823).We identified 21 species with some degree of vulnerability, eleven of which local experts state that must be evaluated under UICN criteria.All but one of the vulnerable species are economically important.There are 75 economically important species in the bay.Information about the species' habitats in the bay was available in 94% of the species.

DISCUSSION
Bahía Malaga is the marine protected area of the Colombian Pacific coast with the second highest species richness of marine mollusks: Isla Gorgona: 661, Malpelo: 393, Utría: 316, Sanquianga: 356 (UNIVALLE and INVEMAR 2010).Gorgona Island is one of the few regions along the South American Pacific coast with coral reef formations (Barrios and López 2001), which are known to bear high diversities of mollusks (Cantera et al. 1979;Cosel 1984).The high diversity of marine mollusks in Bahía Málaga is the result of the different marine ecosystems and substrate heterogeneity that can be found in the bay.Previous studies have evidenced that mollusks' species richness gradually increases from the inner to the outer (closer to the ocean) zone of the bay, which coincides with an increase in substrate heterogeneity and spatial complexity (López de Mesa 2011).
The increase in species reported for the bay between 2007 and 2012 (Figure 2) is the result of the sampling carried out in subtidal habitats through the implementation of artificial habitats.Subtidal benthic organisms were scarcely studied because of the difficult accessibility of their habitats through traditional techniques (scuba diving, mud grabber, nets) due to the natural conditions of the bay (low visibility, the bottom composition is a mixture of mud and rocks) (UNIVALLE and INVEMAR 2010).Most of the new reports for the Colombian Pacific coast are micromollusks, mollusks with the greatest shell dimension <10 mm (Kay 1980), a group that currently has a scarce bibliography for the American Pacific coast.The results of this study show the lack of knowledge of the marine micromollusks of the Colombian Pacific.The study of micromollusks requires special techniques not only for sampling but also for sorting, preparing and identifying the samples.Presently, no studies focusing on micromollusks have been carried out in Colombian coasts.It is estimated that most of undescribed species of mollusks are micromollusks (Geiger et al. 2007), and it is expected that there are more new reports and probably new species of mollusks in the Colombian benthos.
The species in the bay that are currently identified as vulnerable are intensively harvested for local consumption (UNIVALLE and INVEMAR 2013).Castellanos-Galindo et al. (2011) stated that the decrease in number and size of individuals of Anadara spp.populations in the last years might be evidence of over-exploitation of this natural resource.The evidence of population decline of ark shells (A.similis and A. tuberculosa) along the tropical and subtropical American Pacific coast (MacKenzie, 2001) might be evidence of some vulnerability level for these species.We believe it would be appropriate to analyze the situation of A. similis and A. tuberculosa in future IUCN Red List assessment workshops.The species that local experts suspect might be in some sort of danger are also locally harvested for human consumption, but currently the Colombian environmental authorities are not concerned about the condition of their populations.Absence of information about molluscan populations inhabiting the Colombian Pacific coast is frequent.We consider that given the scarce population data of molluscan species in Bahía Málaga, population studies of harvested molluscan species in the Pacific coast of Colombia must be carried out, as well as ecosystem monitoring programs, in order to develop efficient conservation strategies.
species were: Anadara multicostata (G.B.Sowerby I, 1833); Anadara nux (G.B.Sowerby I, 1833); Anadara obesa (G.B.Sowerby I, 1833); Anadara perlabiata (Grant & Gale, sites for subtidal marine organisms in the bay.The artificial habitats consisted of plastic baskets filled with pieces of bricks, broken shells of Anadara sp.and/or coconut fiber.The baskets were tied to rocks on the sea bottom at a depth range of 2-5 m and collected three months later.The collected specimens were deposited in three different collections: Colección de Referencia Biología Marina Universidad del Valle, (Cali, Colombia), Museo Departamental de Ciencias Naturales INCIVA (Cali, Colombia) and Museo de Historia Natural Marina de Colombia, INVEMAR (Santa Marta, Colombia).
, as well as interviews with local people.Databases and collections from museums were reviewed in order to identify lots of marine mollusks collected in Bahía Málaga: Smithsonian National Museum of Natural History, Florida Museum of Natural History, Natural History Museum of Los Angeles County, Santa Barbara Museum of Natural History (SBMNH), Colección de Referencia Biología Marina Universidad del Valle (CRBMUV), Museo Departamental de Ciencias Naturales INCIVA (INCIVA) and Museo de Historia Natural Marina de Colombia, INVEMAR (MHNCI).Lots for Bahía Málaga were found in SBMNH, INCIVA, CRBMUV and MHNCI.

Distribution in Bahía Málaga (Bahía Málaga Sites): 1
, supported and conducted in cooperation with INVEMAR and Universidad del Valle.We want to thank Dr. Phillip Silverstone, M.Sc.Anne-Marie Gavlas and B.Sc. Patricia Cockett for assistance with English.Checklist of marine mollusks registered for Bahía Málaga, Colombian Pacific.Species marked with + indicates that only empty shells have been found in the zone.CO* indicates new reports for the Colombian Pacific coast (hence extension of the geographical distribution).CRBMUV: Colección de Referencia Biología Marina Universidad del Valle; IMCN: Museo Departamental de Ciencias Naturales INCIVA (B bivalvia, G: gastropoda); INV-MOL: Museo de Historia Natural Marina de Colombia, INVEMAR (Santa Marta, Colombia), SBMNH: Santa Barbara Museum Natural History.