ZOOGEOGRAPHY OF HERMIT CRABS (DECAPODA: DIOGENIDAE, PAGURIDAE) FROM FOUR COASTAL LAGOONS IN THE GULF OF MEXICO

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1 JOURNAL OF CRUSTACEAN BIOLOGY, 24(4): , 2004 ZOOGEOGRAPHY OF HERMIT CRABS (DECAPODA: DIOGENIDAE, PAGURIDAE) FROM FOUR COASTAL LAGOONS IN THE GULF OF MEXICO A. Raz-Guzman, A. J. Sánchez, P. Peralta, and R. Florido (AR-G, correspondence; PP) Facultad de Ciencias, Circuito Exterior, Ciudad Universitaria, Universidad Nacional Autónoma de México, 04510, D.F., México (AJS, RF) División Académica de Ciencias Biológicas, Universidad Juárez Autónoma de Tabasco, México ABSTRACT Hermit crabs were collected over 13 years from different habitats in the coastal lagoons of Términos, Alvarado, Tamiahua, and Madre in the southwestern Gulf of Mexico. The distribution, habitat, relative abundance, shield-length data, and zoogeographical affinities of each of the ten species are presented. A zoogeographical analysis assigned the species to four distribution patterns: Eurytopic (Clibanarius vittatus, Petrochirus diogenes, Paguristes tortugae, Pagurus criniticornis); Endemic to the Gulf of Mexico (Paguristes hernancortezi); Warm-Temperate Caribbean (P. hummi, Pagurus maclaughlinae); and Warm-Temperate (P. annulipes, P. longicarpus, P. pollicaris). Five species extend their previously recorded distribution southward, and eight species are now recorded further south within the Gulf of Mexico. The coast along the southwestern Gulf of Mexico includes 15 estuarine systems among which the largest are Laguna de Términos (170,000 ha) in the state of Campeche, Laguna de Alvarado (11,833 ha) and Laguna de Tamiahua (88,000 ha) in Veracruz, and Laguna Madre (200,000 ha) in Tamaulipas. These coastal lagoons are important in the western Atlantic for their biological diversity and abundant fauna, as well as for their value as nurseries for commercial species (García Cubas, 1981; Reséndez and Kobelkowski, 1991; Alvarez et al., 1996; Raz-Guzman and Sánchez, 1996a; Sánchez et al., 1996). Furthermore, the contrast in the environmental characteristics in these four lagoons results in a variety of communities with different structures and trophic complexities (Sánchez et al., 1996; Sánchez, 1997; Sánchez and Raz-Guzman, 1997). Several species of caridean and penaeid shrimp and of anomuran and brachyuran crabs are dominant among the decapod crustaceans of these lagoons (Raz-Guzman and Sánchez, 1996a; Sánchez et al., 1996). The brachyurans have been well studied, and several catalogues for these and one for hermit crabs have been published (Raz-Guzman et al., 1986, 1992b; Raz-Guzman and Sánchez, 1992a, 1992b, 1996b, 1998). The anomurans include members of the families Diogenidae, Paguridae and Porcellanidae. These are important components of benthic communities considering their role in trophic chains and their contribution to the biodiversity of the estuarine systems of Mexico. The porcelain crabs are represented by two species, Petrolisthes armatus (Gibbes, 1850) and P. galathinus (Bosc, [1802]) (Raz-Guzman et al., 1986), and the hermit crabs are represented by the ten species recorded here. The hermit crabs of the lagoons and inner continental shelf of the Mexican section of the Gulf of Mexico are poorly known, whereas those from the coasts of the United States and Central and South America have been better studied. For the latter, there are ecological studies that deal with predation, selection of shells, sharing of resources, and interspecific competition (Kellogg, 1977; Abrams, 1980; Borjesson and Szelistowski, 1989; Lively, 1989; Mantelatto and Garcia, 2000; Garcia and Mantelatto, 2001a; Mantelatto and Dominciano, 2002), distribution (Hebling et al., 1994; Fransozo et al., 1998; Strasser and Price, 1999; Mantelatto et al., 2001; Nizinski, 2003), population structure (Fransozo and Mantelatto, 1998; Mantelatto and Sousa, 2000; Garcia and Mantelatto, 2001b; Martinelli et al., 2002), and reproduction (Negreiros-Fransozo et al., 1992; 625

2 626 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 24, NO. 4, 2004 Mantelatto et al., 2002; Fransozo et al., 2003), as well as taxonomic studies (Provenzano, 1959; McLaughlin and Provenzano, 1974; García-Gómez, 1982; Lemaitre, 1982; Lemaitre et al., 1982; Williams, 1984; McLaughlin, 2003). Lemaitre (1982) and Lemaitre et al. (1982) dealt with the taxonomic aspects of the species of the Provenzanoi group from the northern Gulf of Mexico and neighbouring western Atlantic, with the purpose of clearing up the problematic systematics of a group characterised by a high degree of both intraspecific variation and interspecific similarities. Inventories of living resources are necessary as they provide data bases that aid in the design of research projects and management strategies that include the rational use and preservation of natural systems and their species. Among these, estuaries are particularly rich as they play the part of bridges between watersheds and the sea. The environmental characteristics and water dynamics of estuaries favour the presence of both freshwater and marine species that share the area throughout the year. The present study fills a gap in the distributional and zoogeographical information on the estuarine hermit crab fauna of the Gulf of Mexico. MATERIALS AND METHODS Study Area Laguna de Términos is characterised by the inlets of Puerto Real and El Carmen, and the rivers Candelaria, Chumpán, and Palizada, as a result of which a well-marked and seasonally variable salinity gradient is established from the southwest (0) to the northeast (35) within the lagoon (Raz- Guzman and de la Lanza, 1991). Laguna de Alvarado is an oligo-mesohaline estuarine system where the salinity conditions are determined by an artificial canal to the northwest, the inlet of Alvarado further south, and the rivers Papaloapan, Acula, Camarón, and Blanco (Raz-Guzman et al., 1992a). Laguna de Tamiahua is located in a transition area where Carolinean-temperate and Caribbean-tropical species meet (Galtsoff, 1954). The inlets of Tampachichi and Corazones and the creeks La Laja, Cucharas, San Jerónimo, Tancochín, Tampache, and Milpas result in a salinity range of 16 to 37. Laguna Madre is the largest lagoon in Mexico with a length of 200 km. The inlets of Mezquital, Catán, Caballo, and Soto La Marina are permanent, and a variable number of inlets are temporary. As a result of its location in a semi-arid area, its restricted communication with the sea, and a minimum river runoff from the San Fernando river, the lagoon is hypersaline with marine conditions restricted to the areas of tidal influence near the inlets (Fig. 1). The shoalgrass Halodule wrightii Aschers forms extensive seagrass beds in Tamiahua and Madre. This species and turtlegrass, Thalassia testudinum Banks ex König, form seagrass beds in Términos that cover extensive areas along the northern, eastern, and southern margins, together with less dense manatee grass, Syringodium filiforme Kütz, to the northeast of the lagoon. Widgeon grass, Ruppia maritima L., is the only species in Alvarado, where it forms dense meadows along the inner margin of the sand barrier. Red macroalgae are widely distributed in the first three lagoons. The surrounding vegetation in all but Laguna Madre includes palm trees and the mangrove species Rhizophora mangle L., Avicennia germinans (L.) L., Laguncularia racemosa (L.) C. F. Gaertner, and Conocarpus erectus L. Species Collection and Data This paper is part of a series of species catalogues of anomuran and brachyuran crabs of the four largest coastal lagoons of the southwestern Gulf of Mexico (citations in Introduction). The information on hermit crabs presented in this paper was gathered by sampling throughout 13 years at localities that represent the environmental heterogeneity in each of the four lagoons, including the inlets, river mouths, islands, bare substrates, submerged aquatic vegetation, and the intertidal fringe. The number of localities in each lagoon was 45 in Términos, 17 in Alvarado, 59 in Tamiahua, and 76 in Madre. Sampling in each lagoon covered the dry (March June), rainy (July October), and northers (November February) seasons characteristic of this geographical area. The northers are strong cold winds that originate in the Gulf of Mexico anticyclone and travel southwards (Stumpf, 1975). Hermit crabs were collected with a Renfro beam net (Renfro, 1962), a Colman-Segrove sled net (Eleftheriou and Holme, 1985), an otter trawl net, and by hand. Identification of specimens was based on the taxonomic characters used by Wass (1955), Provenzano (1959), McLaughlin and Provenzano (1974), García-Gómez (1982), Lemaitre (1982), Lemaitre et al. (1982), and Williams (1984). Shield length data were recorded as mm SL. The specimens are located in the Laboratorio de Ecología del Bentos, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México. The data for each species includes the scientific name, the geographical and bathymetric distribution, the habitat, the number of specimens collected in each lagoon, and shield length measurements, as well as remarks where necessary. A zoogeographical analysis assigned the species to two distribution patterns and two zoogeographical provinces. The geographical distribution of the provinces along the Tropical Western Atlantic has been described by Briggs (1974), updated by Barnwell and Thurman (1984), and discussed by Raz-Guzman et al. (1986). The northern transition between the Temperate Transatlantic and the Tropical Caribbean regions is located at a line joining Cape Canaveral and Tampa Bay, U.S.A., with Cabo Rojo, Mexico, and the southern transition between the Tropical Caribbean and the Southern Temperate regions is located at Cabo Frio, Brazil. RESULTS The 1007 specimens collected in the four lagoons represent four genera and ten species of the families Diogenidae and Paguridae. The former family includes Clibanarius vittatus (Bosc, [1802]), Petrochirus diogenes (Linnaeus, 1758), Paguristes hummi Wass, 1955, P. tortugae Schmitt, 1933, and P. hernancortezi McLaughlin and Provenzano, 1974, and the latter family includes Pagurus annulipes (Stim-

3 RAZ-GUZMAN ET AL.: ZOOGEOGRAPHY OF HERMIT CRABS FROM THE GULF OF MEXICO 627 Fig. 1. Location and place names of Laguna Madre, Laguna de Tamiahua, Laguna de Alvarado, and Laguna de Términos, Mexico. pson, 1860), P. criniticornis (Dana, 1852), P. maclaughlinae García-Gómez, 1982, P. longicarpus Say, 1817, and P. pollicaris Say, The species P. annulipes deserves special mention. Lemaitre (1982) revised specimens that had been collected in the northern Gulf of Mexico and had been assigned a variety of names, and he proposed that all those that had been named P. annulipes were in actual fact P. gymnodactylus Lemaitre, His studies did not include material collected in the southern Gulf of Mexico. Considering the uncertainty as to the identification of specimens thought to be P. annulipes in the northern Gulf of Mexico, spe-

4 628 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 24, NO. 4, 2004 Table 1. Principal characters that distinguish the closely related species Pagurus maclaughlinae, P. gymnodactylus, P. annulipes, and P. criniticornis of the Provenzanoi group. Characteristics/species Pagurus maclaughlinae Pagurus gymnodactylus Pagurus criniticornis Pagurus annulipes A1 A2 B1 B2 C1 C2 Antennal flagella with irregularly short and long, or with short, not uniformly paired setae, over entire length Antennal flagella with long, uniformly paired setae, every second article proximally Dactyls of 2nd and 3rd pereopods unarmed Dactyls of 2nd and 3rd pereopods with a row of small spinules nearly parallel to the ventral margin Antennal flagella long, carpus of 2nd right pereopod without dorsal row of spines Antennal flagella short, carpus of 2nd right pereopod with dorsal row of spines cial attention was given here in the identification of the Mexican specimens to the characters that distinguish the taxonomically closely related species that may be present in this geographical area. These species are P. annulipes, P. criniticornis, P. maclaughlinae, and P. gymnodactylus of the Provenzanoi group. The characters concerned are included in the taxonomic key of Lemaitre et al. (1982) and are presented here in Table 1. Other characters that distinguish Pagurus annulipes from P. gymnodactylus include: (1) the setae in P. annulipes are symmetrical and diminish in length gradually along the antennal flagella, whereas in P. gymnodactylus these setae are unequal in length, and (2) the dorsal margin of the carpus of the second right pereopod always has a row of strong spines in P. annulipes, whereas there are only a few weak spines in P. gymnodactylus. The specimens collected in the Mexican lagoons were examined in detail considering all these characters, and the species was confirmed to be P. annulipes. Another species that merits discussion is Paguristes hernancortezi, considering that only one specimen was collected and the scarcity of distribution records. This species is one of seven closely related species that constitute the Paguristes tortugae complex where, similarly to the Provenzanoi group, the identification of species has been complicated by marked interspecific similarities as well as intraspecific variations particularly related to ontogenetic development (McLaughlin and Provenzano, 1974). The main characters that separate this species from others in the complex are included in the taxonomic key of McLaughlin and Provenzano (1974). Within this group, P. hernancortezi appears to be closest to P. hewatti Wass, 1963, from which it differs in the following characters: (1) the absence of a prominent ridge on the dorsal surface of the carpi, (2) a flattened dorsal surface of the palms of the chelipeds, (3) the absence of banding on the ocular peduncles, (4) the females can be ovigerous at 1.5 mm SL, and (5) the male gonopods are well developed at 1.7 mm SL (McLaughlin and Provenzano, 1974). The specimen studied here agreed with these characters. Other characters that are present in P. hernancortezi are those of the armature of the chelipeds, the carpi and meri of the third pereiopods, the ocular peduncles and acicles, the shape and armature of the shield, and the shape of the rostrum. Diogenidae Clibanarius vittatus (Bosc, [1802]) Geographic Distribution. From Potomac River, Gunston, Virginia, to Florianópolis, Santa Catarina, Brazil (Forest and de Saint Laurent, 1967); from North Carolina to Brazil (Rodríguez, 1980); east coast of the United States, Gulf of Mexico, Antilles, Venezuela, Surinam to Santa Catarina, Brazil (Melo, 1999); 3 3

5 RAZ-GUZMAN ET AL.: ZOOGEOGRAPHY OF HERMIT CRABS FROM THE GULF OF MEXICO 629 from North Carolina to the upper Florida Keys (Provenzano, 1959); west coast of Florida (Wass, 1955; Strasser and Price, 1999); northwestern Gulf of Mexico (Felder, 1973); mouth of the Rio Bravo (Stimpson, 1862); Soto la Marina, Tamaulipas (Cordero, 1984); Laguna de Alvarado, Veracruz (Raz-Guzman et al., 1992b); Laguna de Términos, Campeche (Raz- Guzman et al., 1986). New records in Mexico: Laguna Madre, Tamaulipas; Laguna de Tamiahua, Veracruz. Bathymetric Distribution. Water line to 22 m (Williams, 1984). Habitat. In estuaries, harbour beaches, muddy banks, rocky jetties, and shallow margins of bay shores (Rodríguez, 1980; Williams, 1984); in estuaries, coral reefs, sand, Halodule beds (Melo, 1999). Petrochirus diogenes (Linnaeus, 1758) Geographic Distribution. North Carolina, Gulf of Mexico, Antilles, Venezuela, Surinam, Brazil to Uruguay (Melo, 1999); from North Carolina to Brazil (Rodríguez, 1980); from Cape Lookout, North Carolina, Gulf of Mexico and Antilles, to Ilha de Sao Sebastiao, Brazil (Forest and de Saint Laurent, 1967); west coast of Florida (Strasser and Price, 1999); Ubatuba, Sao Paulo, Brazil (Hebling et al., 1994; Fransozo et al., 1998); Uruguay (Rieger, 1998). New records in Mexico: Laguna Madre, Tamaulipas; Laguna de Términos, Campeche. Bathymetric Distribution. From 18 to 128 m (Wenner and Read, 1982). Habitat. On coastal jetties, muddy, sandy, shelly bottoms, and shrimping grounds, in Thalassia testudinum beds (Williams, 1984); on shells, sand, Thalassia beds (Melo, 1999). Paguristes hummi Wass, 1955 Geographic Distribution. From Newport River, North Carolina, to Sapelo Island, Georgia; from Marco Island and southwest Florida to Isles Dernieres, Louisiana (Williams, 1984); west coast of Florida (Provenzano, 1959; Strasser and Price, 1999); Colombia (Campos and Sánchez, 1995). New records in Mexico: Laguna Madre, Tamaulipas. Bathymetric Distribution. Intertidal to 22 m (Williams, 1984). Habitat. In intertidal pools, small sponges, bryozoans, and gastropod shells; on reefs and sandy and shelly substrates (Williams, 1984). Paguristes tortugae Schmitt, 1933 Geographic Distribution. North Carolina, Florida, (?) Gulf of Mexico, Central America, Antilles, Surinam to Rio de Janeiro, Brazil (Melo, 1999); from Beaufort reefs, North Carolina, to Miami, Florida; Antilles to northern Brazil (Williams, 1984); from Florida, Lesser Antilles, Honduras to northern Brazil (McLaughlin and Provenzano, 1974); from Miami to Florida keys; Dry Tortugas; west coast of Florida; Puerto Rico (Provenzano, 1959); west coast of Florida (Strasser and Price, 1999);? northern Gulf of Mexico (Wass, 1955); Surinam (Holthuis, 1959); Ubatuba, São Paulo, Brazil (Negreiros-Fransozo et al., 1992; Hebling et al., 1994; Fransozo et al., 1998; Mantelatto and Sousa, 2000; Mantelatto et al., 2002); Santa Catarina, Brazil (Rieger and Giraldi, 1997). New records in Mexico: Laguna de Términos, Campeche. Bathymetric Distribution. Intertidal to 91 m (McLaughlin and Provenzano, 1974). Habitat. In interstices of Porites and shells, on hard shelly bottoms (Williams, 1984); on gravel, sand, calcareous algae (Melo, 1999). Paguristes hernancortezi McLaughlin and Provenzano, 1974 Geographic Distribution. Off Sanibel Island, Florida (McLaughlin and Provenzano, 1974). New records in Mexico: Laguna de Términos, Campeche. Bathymetric Distribution. From 55 to 73 m (McLaughlin and Provenzano, 1974). Habitat. Continental shelf off Sanibel Island (McLaughlin and Provenzano, 1974). Remark. Range of geographical distribution extended south from Florida to Laguna de Términos, Campeche. Paguridae Pagurus annulipes (Stimpson, 1860) Geographic Distribution. From Massachusetts to south central Florida (Lemaitre et al., 1982). New records in Mexico: Laguna Madre,

6 630 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 24, NO. 4, 2004 Tamaulipas; Laguna de Tamiahua, Veracruz; Laguna de Términos, Campeche. Bathymetric Distribution. Subtidal to 90 m (Lemaitre et al., 1982). Habitat. On sandy and shelly bottoms, in marine shallow water and Thalassia testudinum beds (Provenzano, 1959; Williams, 1984). Remark. Range of geographical distribution extended south from Florida to Laguna de Términos, Campeche. Pagurus criniticornis (Dana, 1852) Geographic Distribution. Northern Gulf of Mexico, Bahía de Cartagena in Colombia; from Brazil to Argentina (Lemaitre et al., 1982); Gulf of Mexico, Antilles, north coast of South America, Brazil, Uruguay to Argentina (Melo, 1999); Ubatuba, Sao Paulo, Brazil (Hebling et al., 1994; Fransozo et al., 1998). New records in Mexico: Laguna de Términos, Campeche. Bathymetric Distribution. From 2 to 50 m (Lemaitre et al., 1982). Habitat. Inner continental shelf, bays (Lemaitre et al., 1982); on sand (Melo, 1999). Pagurus maclaughlinae García-Gómez, 1982 Geographic Distribution. From Wassaw Sound, Georgia to Biscayne Bay, Florida; Gulf of Mexico; Caribbean; Curaçao (Lemaitre et al., 1982); west coast of Florida (Strasser and Price, 1999); from central eastern Florida to Puerto Rico; from the Florida keys to Chandeleur Island, Louisiana (García-Gómez, 1982). New records in Mexico: Laguna Madre, Tamaulipas; Laguna de Tamiahua, Veracruz; Laguna de Términos, Campeche. Bathymetric Distribution. Subtidal to 5 m (García-Gómez, 1982; Lemaitre et al., 1982). Habitat. Estuaries, bays, sounds (García- Gómez, 1982). Pagurus longicarpus Say, 1817 Geographic Distribution. From Minas Basin and Chignecto Bay, Nova Scotia, Canada (Bousfield and Leim, 1960) to Hutchinson Island, Florida (Camp et al., 1977); from Massachusetts to northern Florida; west coast of Florida from Sanibel Island to Alligator Harbor and to Texas (Provenzano, 1959); from southwest Florida to Texas (Whitten et al., 1950; Rouse, 1970); west coast of Florida (Strasser and Price, 1999). New records in Mexico: Laguna de Tamiahua, Veracruz; Laguna de Términos, Campeche. Bathymetric Distribution. Subtidal to 200 m (Wenner and Boesch, 1979). Habitat. On harbour beaches, bay shores, soft substrates and detritus, in harbour channels and seagrass beds (Wenner and Boesch, 1979). Remark. Range of geographical distribution extended south from Texas to Laguna de Términos, Campeche. Pagurus pollicaris Say, 1817 Geographic Distribution. From Grand Manan Island, New Brunswick, Canada, to northeast Florida (Williams, 1984); from Massachusetts to northeastern Florida; west coast of Florida from Key West to Alligator Harbor and to Texas (Provenzano, 1959); west coast of Florida (Strasser and Price, 1999). New records in Mexico: Laguna Madre, Tamaulipas. Bathymetric Distribution. Subtidal to 112 m (Wenner and Boesch, 1979). Habitat. Along sandy coasts, in shallow estuaries and deep harbour channels (Wenner and Boesch, 1979). Remark. Range of geographical distribution extended south from Texas to Laguna Madre, Tamaulipas. The number of specimens of each of the ten species collected in each of the four lagoons is presented in Table 2, together with shield-length data. DISCUSSION Zoogeography Although the geographical distribution of a species is easily established through records of observations, the task of assigning a species to a zoogeographical province is not as readily done, particularly as species and localities that are not well studied continue to provide new information to distribution data bases. With respect to the abundance of the hermit crabs collected in the four lagoons, Pagurus

7 RAZ-GUZMAN ET AL.: ZOOGEOGRAPHY OF HERMIT CRABS FROM THE GULF OF MEXICO 631 Table 2. Numbers of male (M), female (F), ovigerous female (OF), and total specimens of the ten hermit crab species collected in the four lagoons, together with minimum (min), maximum (max) and average (av) shield-length data (mm). Términos Alvarado Tamiahua Madre Percentage of total Shield length (mm) Species/lagoon M F OF total M F OF total M F OF total M F OF total abundance min max av Diogenidae Clibanarius vittatus Petrochirus diogenes Paguristes hummi Paguristes tortugae Paguristes hernancortezi Paguridae Pagurus annulipes Pagurus criniticornis Pagurus maclaughlinae Pagurus longicarpus Pagurus pollicaris maclaughlinae occupies first place (66.9%) and is followed by Clibanarius vittatus (19.3%), with markedly lower values for P. criniticornis (5.4%), P. annulipes (4.4%), P. pollicaris (2.3%), P. longicarpus (0.7%), Paguristes tortugae (0.5%), Petrochirus diogenes (0.4%), Paguristes hummi (0.1%), and P. hernancortezi (0.1%) (Table 2). These ten species of hermit crabs, together with another 50 species of anomuran and brachyuran crabs recorded for these four lagoons (Raz-Guzman et al., 1986, 1992b; Raz-Guzman and Sánchez, 1992a, 1992b, 1996b, 1998), form part of a highly diversified fauna that is distributed throughout a vast zoogeographical area known as the Tropical Western Atlantic (Ekman, 1953). In the case of the Gulf of Mexico, water temperature defines two provinces: a Temperate Province from Cabo Rojo, Veracruz, to Tampa Bay, Florida, and a Caribbean Province south of the line formed between these two points. The geographical distribution of the ten hermit crab species shows that they can be assigned to four groups. These are two distribution patterns: Eurytopic (with Clibanarius vittatus, Petrochirus diogenes, Paguristes tortugae, and Pagurus criniticornis) and Endemic (with Paguristes hernancortezi), and two zoogeographical provinces: Warm-Temperate Caribbean (with P. hummi and Pagurus maclaughlinae) and Warm-Temperate (with P. annulipes, P. longicarpus, and P. pollicaris) (Figs. 2, 3). The collection of these ten hermit crab species in the Mexican lagoons of the Gulf of Mexico has now extended the previously recorded distribution of five species southward. These are Paguristes hummi, P. hernancortezi, Pagurus annulipes, P. longicarpus, and P. pollicaris. Within the Gulf of Mexico, seven species are now recorded further south, with Paguristes tortugae and P. hernancortezi extended from Florida to Laguna de Términos, Pagurus maclaughlinae from Louisiana to Laguna de Términos, P. criniticornis and P. longicarpus from Texas to Laguna de Términos, Paguristes hummi from Louisiana to Laguna Madre, and Pagurus pollicaris from Texas to Laguna Madre. Pagurus annulipes had been previously recorded with a temperate distribution along the eastern coast of the United States, and has now had its distribution extended from south central Florida (Lemaitre et al., 1982) to the west and south within the Gulf of Mexico to Laguna Madre, Laguna de Tamiahua, and Laguna de Términos. Furthermore, the records of these ten species in these four Mexican lagoons are new to Mexico, except for two lagoons where Clibanarius vittatus had been previously recorded. Eurytopic Species. The species of the Eurytopic distribution pattern are widely distributed from the Temperate Transatlantic region in the north to the Tropical Brazilian and Southern Temperate regions in the south. These include Clibanarius vittatus, Petrochirus diogenes, Paguristes tortugae, and Pagurus criniticornis (Fig. 2). The presence of Clibanarius vittatus in the four lagoons of this study can be attributed to the fact that it is physiologically tolerant of an

8 632 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 24, NO. 4, 2004 Fig. 2. Distribution of Eurytopic and Endemic species along the western Atlantic (n) including the Mexican lagoons ( ). ample gradient of salinity and temperature, and it is found in a variety of environments that include the shallow intertidal fringe of estuarine systems where it is resistant to desiccation (Williams, 1984; Lowery and Nelson, 1988). Petrochirus diogenes has a strong affinity for the marine environment, and only sexually immature specimens have been occasionally collected in estuarine systems (Grizzle, 1974; Kellogg, 1977). However, one adult specimen (27 mm SL) was collected in Laguna de Términos and three in Laguna Madre, all in high salinity areas. It is also a dominant species among the hermit crabs of the continental shelf off the southwestern Gulf of Mexico. The specimens of Paguristes tortugae from Laguna de Términos were collected from a seagrass bed along the inner margin of El Carmen island where salinity is marine throughout the year. Pagurus criniticornis was the third most abundant species in Laguna de Términos. The geographical distribution of these four species includes no records for Central America, except for one mention of Honduras for Paguristes tortugae. This discontinuity in the eurytopic distribution pattern could be the result of a lack of studies in this geographical area. Endemic Species. The Endemic distribution pattern refers here to the ecosystem of the Gulf of Mexico. The single species in this group is represented by one male specimen of Paguristes hernancortezi from Laguna de Términos that was found in a shallow seagrass bed dominated by Thalassia testudinum at 30& (Fig. 2). Notwithstanding that only one specimen was collected, it is significant that this species was found in a different habitat from that reported previously (McLaughlin and Provenzano, 1974). The collection of seemingly rare outlying specimens is one of several mechanisms that extend the range of distribution of marine species. This and the dynamics of the water currents in the area between Yucatan, Cuba, and Florida (Fernández et al., 1998) help explain the presence of this species in this lagoon.

9 RAZ-GUZMAN ET AL.: ZOOGEOGRAPHY OF HERMIT CRABS FROM THE GULF OF MEXICO 633 Fig. 3. Distribution of Warm-Temperate Caribbean and Warm-Temperate species along the western Atlantic (n) including the Mexican lagoons ( ). Warm-Temperate Caribbean Species. The Warm-Temperate Caribbean province is here defined as the geographical area that includes the continental and island coasts of the Caribbean Sea, the Gulf of Mexico, and the temperate coast of the United States. The species assigned to this province are Paguristes hummi and P. maclaughlinae (Fig. 3). Paguristes hummi is represented by a single specimen collected in Laguna Madre. However, the fact that this specimen is an ovigerous female validates the presence of this species further west and south within the Gulf of Mexico and indicates that the species might be in a process of recruitment in the area. The scarcity of specimens might also respond to the fact that this species is considered occasional in estuaries and is more abundant in marine environments (Kellogg, 1977). Pagurus maclaughlinae is a dominant faunistic component of communities associated with seagrasses (Tunberg et al., 1994; Sánchez et al., 1996). It was collected throughout the year in markedly high numbers in the lagoons of Términos, Tamiahua, and Madre where it was found associated with seagrasses, macroalgae, and detritus. The geographical distribution of these two species includes no records for Central America, similarly to the four Eurytopic species mentioned above, and thus present the same discontinuity in distribution and probable lack of studies in this geographical area. Warm-Temperate Species. The Warm-Temperate province is here defined as the geographical area that includes the Gulf of Mexico and the temperate coasts of the United States and Canada. The species assigned to this province are Pagurus annulipes, Pagurus longicarpus, and P. pollicaris (Fig. 3). Pagurus annulipes was collected from seagrass beds and macroalgae in Laguna Madre, from seagrass beds in Laguna de Tamiahua, and from detritus in the western area of Laguna de Términos. The presence of this species well inside the Gulf of Mexico can be explained by the temporal changes in the direction of the ocean currents in the Gulf of Mexico that allow colder water to flow westward into the Gulf (Fernández et al., 1998) and favour the dispersion and establishment of species from the northwestern Atlantic. The presence of 44 specimens of this species in these three lagoons, including seven ovigerous females that confirm the establishment of P. annulipes in this geographical area, extends the species range of distribution west and south within the Gulf of Mexico. The collection of ovigerous females of P. longicarpus in Laguna de Términos and of P. pollicaris in Laguna Madre validates the extension of the geographic range of these two species to the south, and establishes these localities as the southern limits of their geographical distribution. The northern geographical distribution of P. pollicaris indicates that this species is adapted to low water temperatures, and our data agree with this as most of the 23 specimens were collected in February in 118C. This species, including ovigerous females, has also been collected from the continental shelf off Tamaulipas at a depth of 15 m during the cold northers season (unpublished data). No records for Central America were found for these three species, as

10 634 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 24, NO. 4, 2004 is the case for the Eurytopic and Warm- Temperate Caribbean species stated above. ACKNOWLEDGEMENTS The authors thank A. de la Torre and P. Rangel (UNAM), E. Barba (Ecosur-Villahermosa), A. Reda (UNAM), and E. Gamboa (SEMARNAT, Alvarado) for assistance in the field; J. L. Villalobos, L. Cárdenas, and C. Rosas (UNAM) for providing access to collections; the personnel at the field station of El Carmen (UNAM); P. Schmidtsdorf (UNAM) for help with the identification of specimens; R. Rodríguez (UNAM) for making the basic maps; and R. Lemaitre (Smithsonian Institution), L. A. Soto and M. Hendrickx (UNAM) for valuable advice. Funding was provided by ICMyL-UNAM (No. 603), PAPIIT-DGAPA-UNAM (IN211795), PADEP-UNAM (DCCH9003, DCCH9248), CONABIO (H258) and CONACyT (PCECBNA ). LITERATURE CITED Abrams, P. A Resource partitioning and interspecific competition in a tropical hermit crab community. Oecologia 46: Alvarez, F., A. J. 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