THE NAUTILUS 131 (2):107-126, 2017 Page 107 First inventory of the introduced and invasive mollusks in Mexico Edna Naranjo-Garcfa Zoila G. Castillo-Rodriguez Instituto de Biologfa Instituto de Ciencias del Mar y Limnologia Universidad Nacional Autonoma de Mexico Depto. de Biodiversidad y Ecologfa Acuatica Apartado Postal 70-153 Universidad Nacional Autonoma de Mexico Mexico City, C.P. 04510, MEXICO Apartado Postal 70-153 [email protected] Mexico City, C.P. 04510, MEXICO zgcr@cm arl. u nam. mx ABSTRACT organisms are poorly understood; however, we face loss of diversity (Reyna et ah, 2013) of formerly diverse Early historical records are included in this first national in¬ ecosystems (Cowie, 1998, 2001; Cowie and Robinson, ventory of species of mollusks introduced, whether intentionally 2003; Lopez-Lopez et ah, 2009). It may be possible that or not, into Mexico hv humans. Of the 56 exotic-invasive mol¬ endemic species are the most vulnerable, although un¬ lusks listed, 15 inhabit brackish and marine environments, 10 fortunately, knowledge of the diversity and abundance of freshwater, and 31 are terrestrials. Thirty-six per cent of the introduced species come from Europe and the Mediterranean, much of the world’s fauna remains unsatisfactory. In 18% from Asia-Australia-New Zealand, 46 % are cryptogenic, M exieo, where it is estimated that 75 % of brackish and coming from different regions of the planet, and the origin of marine species are known, it is suggested that 17 % of the several others is uncertain. The best-represented families are Pacific species, and 15% of those in the Gulf of Mexico Mvtilidae, Teredinidae (brackish and marine), Ampullariidae, and the Caribbean Mexican coast are endemic (Castillo- Thiaridae, and Planorbidae (freshwater), and Helieidae, Agrioli- Rodriguez, 2014). On the other hand, fewer than 35 % maeidae, Limacidae, Subulinidae, and Vallonidae (terrestrial). of the native non-marine mollusks are known and 85% They involve Mytilus galloprovincialis Lamarck, 1819, Pomacea of the Mexican territory is in need of exploration canaliculata, Lamarck, 1819, and Dreissena polynwrpha (Pallas, (Thompson, 2011). 1771), species included among the world's worst invasive species. In the case of the introduction pathways at global Some have become naturalized: three brackish and marine species, six freshwater, and twelve terrestrial. The increase in level, marine vectors are well documented. Mexico has exchange of goods, services, and transport litis assisted in the a navigation infrastructure that facilitates the in¬ transfer of species from distant places, as has intentional or troduction of alien species; human activities on the unintentional introduction of species of economic importance continental margins, and in the bays and estuaries of the (M. galloprovincialis, Crassostrea gigas (Thunberg, 1793), coastal zone, have evolved since the 16th century and are C. sikanxea (Amemiya, 1928)), without consideration of the now part of an impressive network of global marine epibionts, endobionts, and endoparasites that may also be traffic. Currently there is the threat of climate change, introduced. Effective strategies must be developed to minimize which will undoubtedly alter the structure and compo¬ the potential impact of biological invasions and raise public sition of native communities. This will also alter the awareness of the problem; this must include the rigorous ap¬ plication of more stringent regulations. functioning of ecosystems and become a stressor that will further increase the risk of biological invasions in marine Additional Keywords: exotic, freshwater, terrestrial mollusks, and non-marine systems. The effects of climate change marine, mollusks, economic and biological risks on the environment will include substantial impact on native species. Given the increase in threats to the native fauna, inventories of exotic species become the foun¬ dation for future actions, including the control and eradication of invasives (Mendoza et ah, 2014). This article offers a review of the brackish-marine and non¬ INTRODUCTION marine introduced mollusks in Mexico, constituting the Biological contamination in the world has increased first national inventory of this type elaborated in Mexico; markedly since 2000 (Crocetta et ah, 2013), Pimentel it also determines the naturalized species at the national et al. (2001) estimated that some 480000 species have level. We examine potential vectors and recommend been introduced around the world throughout the his¬ measures that may help prevent the entry of additional tory of humankind, and this is of great concern. The alien organisms and that could help control and serve as effects that alien species may have in ecosystems essential protective measures for the fauna and the (Carlton, 1999) and in their interaction with native environment at the national level in Mexico. Page 108 THE NAUTILUS, Vol. 131, No. 2 Early Records of Introduced Mollusks in Mexico Tamaulipas (Correa-Sandoval, 1993, 1998; Correa-Sandoval and Rodriguez, 2002), and soon afterward in Nuevo Leon In relation to introduced non-marine mollusks. Cornu (Correa-Sandoval 1999b; Correa-Sandoval and Rodriguez, aspersum (Muller, 1774) (as Helix aspersa Muller, 1774) 2005; Correa-Sandoval et al., 2007). Huttonella bicolor was detected in Mexico by Alexander Humboldt between (Hutton, 1834) (as Gulella bicolor (Hutton, 1834)) was 1803 and 1804 (Martens 1890-1901); and it was recorded collected at the archaeological site El Tajin, Veracruz by Pilsbry (1891) in Mexico City. It was also located in (Correa-Sandoval, 1999a, 2000). Jaral, Guanajuato, and other unspecified sites (Martens In relation to marine mollusks introduced into Mexican 1890-1901). The species became a pest in gardens waters, Hendrickx (1980) and Salgado-Barragan and throughout Mexico City (Ancona, 1947) and was later Toledano (2006) provided data from specimens ob¬ recorded at Chapultepec, and in mountains between served in situ and preserved in the Invertebrate Collec¬ Mexico City and the city of Cuernavaca (Jacobson, 1952). tion (EMU) of Unidad Aeademica of Mazatlan, Instituto Baker (1925) mentioned the presence of Phyllocaulis gatji de Ciencias del Mar y Limnologfa, Universidad Nacional (Fischer, 1871) in Mazatlan, Sinaloa. Andrews and Autonoma de Mexico. There are also other published Dundee (1987) stated for the first time the problems records: for example, Okolodkov et al. (2007) and Ortiz- caused by the slug Sarasinula plebeia (Fischer, 1868) in Arellano and Salgado-Barragan (2012). According to Chiapas (1980) and Veracruz (1981), and Naranjo-Garcfa Carlton (1999), the diversity and abundance of exotic and et al. (2007) reviewed the distribution of the family invasive marine species at worldwide level are still poorly Veronicellidae nationwide, with particular reference known; this is certainly true for Mexico, where lack to Sarasinula plebeia (= Sarasinula dubia (Semper, of awareness of the presence of exotic species is 1885)). As for other introduced slugs, Cockerell (1923) compounded bv unfamiliarity of their effects on the recorded Limacus flavus (Linnaeus, 1758) (as Limax ecosystems. flavus Linnaeus, 1758) with numerous individuals or populations in Mexico City. After that. Baker (1930) Found various European slugs (Limax nuiximus Linnaeus, MATERIALS AND METHODS 1758 in Desierto de Los Leones to Cuajimalpa; L. flavus in Huachinango, Puebla; Deroceras laeve (Muller, 1774) The present compilation was assembled based on records (apballic) in Desierto de Los Leones and Neeaxa; D. laeve of mollusks deposited in: Coleccion Nacional de Moluscos (phallic) (Muller, 1774) in Cuajimalpa and San Juan (National Collection of Mollusks), Instituto de Biologfa, Teotihuacan; and Milax gagates (Drapamaud, 1801) in Universidad Nacional Autonoma de Mexico); database of Desierto de Los Leones. The Cuban species Zachnjsia the Invertebrate Zoology division of the Florida Museum auricomya havanensis Pilsbry, 1894 was recorded in of Natural History, FLMNH; the Unidad Aeademica of Yucatan (Bequaert and Clench, 1936) and Vallonia Mazatlan of the Instituto de Ciencias del Mar y excentrica Sterld, 1893 was found by Joshua L. Baily Jr. in Limnologfa (ICMyL-MAZ, UNAM); the literature; field Cuernavaca (Pilsbry, 1948). observations by the authors and/or other specialists; a list The freshwater clam Corbictda fluminea (Nlidler, 1774) of organisms coming from Mexico and intercepted at (as Corbictda nianilensis (Philippi, 1844)) was recorded in customs upon arrival in the USA; and additional in¬ Baja California, northwestern Mexico (Fox, 1970) and formation provided by David Robinson (letter to E. Hillis and Mayden (1985) summarized its distribution Naranjo-Garcfa, 4 September 2014). In certain cases, along the coastal areas of Pacific and in the State of where the literature is very extensive, the first and the Tamaulipas; it was later recorded in Lake Catemaco, most recent articles or references were selected. Acro¬ southern Veracruz (Torres-Orozco and Revueltas-Valle, nyms used are: CNMO, Coleccion Nacional de Moluscos, 1996). The freshwater snail Melanoides tuberculata Universidad Nacional Autonoma de Mexico; CM, Car¬ (Muller, 1774) was found in the vicinity of Veracruz in negie Museum of Natural History, Pittsburgh; FLMNH, 1973 (Abliott, 1973), and its presence in Mexico was database of the Florida Museum of Natural History, confirmed in 1975 by Pointier and McCullough (1989). Gainesville; EMU, Coleccion de Invertebrados, Unidad More details of its distribution in Mexico have subsequently Aeademica de Mazatlan del Instituto de Ciencias del Mar emerged (Contreras-Arquieta, 1998; Contreras-Arquieta y Limnologfa. and Contreras-Balderas, 2000; Contreras-Arquieta, et al. 1995). The first record of Tarebia granifera (Lamarck, 1822) was at Lake Catemaco, Veracruz (Naranjo-Garcfa RESULTS et al., 2005), and other foci were later found in northern Veracruz State (Dipez-Lopez et al., 2009), in southern In total, 56 species of exotic-invasive mollusks from the Oaxaca State, and in the Lacandona Forest, Chiapas classes Bivalvia and Gastropoda have been so far in¬ (Naranjo-Garcfa non-published data); it was later recorded troduced into Mexico, whether intentionally or not: 15 from 11 lakes of three municipalities in the State of Tabasco brackish-marine, 10 freshwater, and 31 terrestrial mol¬ (Rangel-Ruiz et al., 2011). lusks (Tables 1, 2, and 3). Of these, 36 % came from The terrestrial species Rumina decollate (Linnaeus, 1758) Europe and the Mediterranean (the majority are terres¬ was recorded in 1993 in the States of San Luis Potosf and trial mollusks), 18 % from Asia- Australia-New Caledonia E. Naranjo-Garcfa and Z.G. 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(cid:9632)pp (cid:9632)cp H H 5 s Q H Page 110 THE NAUTILUS, Vol. 131, No. 2 (several estuarine/brackish- marine and some freshwater and Lozano, 1901; Mariscal, 1902) regarding re¬ species), 46 % from different regions of the planet quirements of the asphalt composition in Submarine (Table 4), with the place of origin of several being Telegraph cables between the port of Veracruz and uncertain. Campeche in order to avoid damage caused by the Most of the brackish and marine species (Table 1) “marine worm”, T. navalis. More recently, there are belong to the families Mytilidae and Teredinidae checklists, reports and theses records of its presence in (Bivalvia). Among the freshwater mollusks (Table 2), estuaries on the Mexican coast of the Gulf of Mexico, such gastropods are the dominant group, in particularly as the Tampamachoco Lagoon, Veracruz (without ref¬ species in the families Ampullariidae, Thiaridae, and erence code), where it has been an element of the epi- Planorbidae. Most of the terrestrial mollusks (Gastro¬ biosis on the mangrove Rhizophora mangle Linnaeus, poda) (Table 3) belong to the family Helieidae, followed 1753 since 1980. by the Agriolimacidae, the Limacidae, the Subulinidae, Oysters of Asian origin, Crassostrea gigas (Thunberg, and the Vallonidae. The species that have been 1793) and, more recently, C. sikamea (Amemiya, 1928), recorded only once are: Theora lubrica Gould, 1861 are cultivated in Baja California Norte and Sur in Mexico. (marine), Helisoma duriji (Wetherby, 1879) (as Pla- Sessile oysters adhering by cementing to any hard sub¬ norbella duriji (Wetherby, 1879)) (freshwater), and stratum, together with the large accompanying fauna on Phyllocaulis gayi, Cecilioides acicula (Mtiller, 1774), the surface of their shells, represent a potential risk to Arion circumscriptum Johnston, 1828, Vallonia costata wildlife; hence, a study of their ecological impact would be (Miiller, 1774), Zachrysia auricomya havanensis, and most important. Crassostrea gigas exists as an exotic Cantareus apertus (Born, 1778) (as Helix aperta Born, species on the southern Pacific coast and, since un¬ 1778) (terrestrial). controlled introduction is possible through ballast water and aquaculture practices, it might also be expected to eventually be introduced along the southern Gulf of DISCUSSION Mexico, in locations as Veracruz State. Anadara transversa (Say, 1822), a clam from the Marine Mollusks northwestern Atlantic, is considered a non-invasive exotic The ecosystems that now are home to exotic mollusks are species. It was recorded in Tamiahua lagoon, Veracruz by vulnerable to changes in their composition, regardless of Garcia-Cubas (1969) and Abbott (1974). Although there whether those mollusks were introduced inadvertently or are no recent records of substantial living populations, for commercial purposes. Especially threatening are those abundant disjointed valves have been reported. species that have been restricted to environments dis¬ Theora lubrica Gould, 186L originally from Asia, is turbed either naturally or by human intervention, as is the considered as one of the most important invasive species case of brackish and marine mollusks such as Mytilus in Europe (Balena et ill., 2002). According to Steneck and galloprovindolis Lamarck, 1819 (Mytilidae). Mytilus Carlton (2001), it is one of the 15000 species that have galloprovincialis, originally from the Mediterranean, been transported across the world in ballast water. It is Black Sea and Adriatic Sea, has been categorized as one of recorded from Baja California Norte, where it possibly the 100 worst invasive alien species of the world. Despite arrived secondarily introduced from San Francisco Bay, this, the species is cultivated for food in the states of Baja USA; it can be considered a potentially invasive species for California Norte and Sur, and this is without any the Pacific States of Mexico. knowledge of its ecological impact on the native species. There are fewer records of exotic marine gastropods Populations of the mussel Pema perna (Linnaeus, 1758) species in Mexico than of exotic bivalve species. Among are distributed from Texas to southern Veracruz State, these gastropods is the pyramidellid Boonea bisuturalis Mexico (Hicks and Tunnell, 1993, 1995; McGrath et al., (Say, 1822), a native of the northern coast of the Atlantic 1998), and Hicks et al. (2001) consider that its occurrence (Canada and USA) that feeds on the body fluids of in¬ on Mexican coasts should be carefully monitored. vertebrates (Fretter and Graham, 1949; 1962; Fretter, Mussels and shipworms can survive tough conditions in 1951), including polychaetes, gastropods, and bivalves, variable estuarine and marine environments, as well as in and minor groups such as polyplacophorans and some sheltered sites that may be favorable to their development eehinoderms (Robertson and Orr, 1961). The Mexican and dispersal: they are adapted to this survival by their coast of the Gulf of Mexico houses marine resources that sessile habit, their filter feeding, and their modes of include the Eastern Oyster C. virginica (Gmelin, 1791), reproduction, growth, and morphological protection which represents 90% of the catch produced along that ((McDonald and Koehn, 1988; Turner, 1966; Tuente coast (Caeeres-Martinez and Vasquez-Yeomans, 2013). et al., 2002; Petes et al., 2007; Didziulis, 2007). Despite studies on diseases and ectoparasites of C. Tl re shipworms, such as Teredo navalis Linnaeus, 1758, virginica in Mexico (Aguirre-Macedo et al., 2007; bore into submerged wood substrata all over the world, Caeeres-Martinez and Vasquez-Yeomans, 2013), a study and there are few records of the species in Mexico. Lopez- of non-native endo- and ecto-parasites of mollusks in the Garrido (2008) recorded the species from sunken boats in coastal lagoons and coral reefs of the southern gulf is still the state of Campeche, in the southern Gulf of Mexico. lacking. However, B. bisuturalis (Say, 1822) has been There are also references from the early 1900s (Dublan registered by De la Cruz and Gcnzalez-Gandara (2006) E. Naranjo-Garefa and Z.G. Castillo-Rodriguez, 2017 Page 111 d d) r e a u g n with re pact (Conti act Im p m d i n a at abit c c r C CC/D3 o LO on (vector), h Habitat CCcCci—r/DD3. Cc£3D b *cCCc>xDd: '13^CcC/D3' £ o£ci (cid:9632)3*CS_C-D>o ’G-0CoS5D CO "CCc„6/ D3, O(VcD CqbD;£ GGc 0007 cCvCC/DD3s _-oCtJDi ^^2 oI2d < 07 cti 5 u d o r nt f i .c t; .c o . C ns CC/3 c (D CC/3 5— urce, mea Vectors (cid:9632)c £« G 'C %C—>cD *'£-"CCP§D 2*c £2 Z so i cm r cr o < < D s e c n e wn: place of origin, refer David G. Robinson. 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