Austinotheres angelicus (Lockington, 1877): nombre correcto para el cangrejo simbiotico Juxtafabia muliniarum sensu Cabrera-Pena et al.
Ongoing studies on the pinnotherid crabs of Costa Rica continue to yield new information on the species recorded for this country. The present study deals with Juxtafabia muliniarum sensu Cabrera-Pena et al. (2001), a symbiont of the oyster Saccostrea palmula Carpenter, 1857. Juxtafabia Campos, 1993 is a monotypic genus, closely related to Fabia Dana, 1851 (Campos, 1993, 1996). Females of both genera share an asymmetrical pair of pereopods 3 (walking legs 2), longer than the others, and males possess two or more abdominal somites fused (Campos, 1993, 1996). In addition, both males and females in both genera lack a tubercle on the basal article of the antennae (Campos, 2009). Recently, Dr. Maurizio Protti-Quesada (Escuela de Ciencias Biologicas, Universidad Nacional, Heredia, Costa Rica) allowed us to examine some of the specimens formerly studied by Cabrera-Pena et al. (2001) in order to revise their taxonomic identification. Specimens studied by these authors were compared with all the known genera and species of the American Pinnotheridae, including the type species of the genus Juxtafabia (Campos, 1993), J. muliniarum (Rathbun, 1918). The morphology of males and females of the symbiotic crab of the oyster S. palmula did not match with that of Juxtafabia. In the present study, the taxonomic identity of J. muliniarum sensu CabreraPena et al. (2001) is emended, providing a diagnostic description for this species and a morphological comparison with all pinnotherid crabs of America.
MATERIALS AND METHODS
Both, specimens studied by Cabrera-Pena et al. (2001) and new material collected in the intertidal zone of the estuary of Punta Morales, Puntarenas, Pacific coast of Costa Rica, in the oyster Sacosstrea palmula (see details in the next section) were analyzed. In addition, 26 species of different pinnotherid genera were studied for a comparative purpose. Material obtained from the following institutions were analyzed: Laboratorio de Sistematica de Invertebrados, Universidad Autonoma de Baja California, Mexico (UABC); Coleccion Nacional de Crustaceos, Instituto de Biologia, Universidad Nacional Autonoma de Mexico, Distrito Federal, Mexico (CNCR); Coleccion Nacional de Equinodermos, Instituto de Ciencias del Mar y Limnologia, Universidad Nacional Autonoma de Mexico, Distrito Federal, Mexico (CNE); Coleccion de Macroinvertebrados, Instituto de Ciencias del Mar y Limnologia (Estacion Mazatlan), Universidad Nacional Autonoma de Mexico, Sinaloa, Mexico (EMU); Crustacean Collection, Department of Biology, University of Louisiana, Lafayette, USA (ULLZ); Museum national d'Histoire naturelle, Paris, France (MNHN); National Museum of Natural History, Smithsonian Institution, Washington D.C., USA (USNM); Natural History Museum of Los Angeles County, California, USA (formerly at the Allan Hancock Foundation) (AHF), and Naturalis, Nationaal Naturhistorisch Museum (formerly Rijksmuseum van Natuurlijke Historie), Leiden, The Netherlands (RMNH). The species studied include: Austinotheres angelicus (Lockington, 1877), USNM 71334, 67723, UABC, EMU; Austinotheres sp., ULLZ 5547; Calyptraeotheres granti (Glassell, 1933), UABC, CNCR 1425; Epulotheres sp., UABC; Fabia subquadrata Dana, 1851, UABC, USNM, AHF 1467-42; Fabia sp., ULLZ 8563, 8564, 8565; Gemmotheres chamae (Roberts, 1975), USNM 139098; Glassella costaricana (Wicksten, 1982), UABC; Holothuriophilus pacificus (Poeppig, 1836), ULLZ 5569; Holothuriophilus trapeziformis Nauck, 1880, UABC; Juxtafabia muliniarum (Rathbun, 1918), UABC, USNM 23443, 18217, 229724; Limotheres nasutus Holthuis, 1975, USNM 151039; Opisthopus transversus Rathbun, 1893, USNM 50997, UABC; Orthotheres ungifalcula Glassell, 1936, USNM; Ostracotheres tridacnae (Ruppell, 1830) MNHN B.10578, RMNH-D 1542; Parapinnixa nitida (Lockington, 1877), EMU 3753; Pinnaxodes floridensis H.W. Wells & Wells, 1961, ULLZ, USNM 186366; P. chilensis (Milne-Edwards, 1837), USNM 22112, 49238; P. gigas Green, 1992, UABC; Pinnixa spp, UABC; Pinnotheres pisum (Linnaeus, 1758), UABC; Pinnotherelia laevigata H. Milne Edwards & Lucas, 1843, UABC, USNM 125585; Raytheres clavapedatus Glassell, 1935, UABC; Scleroplax granulata Rathbun, 1893, UABC, ULLZ, USNM 17497; Tetrias scabripes Rathbun, 1898, EMU 3744, 4026; Tumidotheres margarita (Smith, 1969), UABC, USNM 229723, EMU; Tunicotheres moseri (Rathbun, 1918), USNM 74954; Zaops geddesi (Miers, 1880), USNM 23767, 51000; Z. ostreum Rathbun, 1900, UABC, USNM, CNCR 2252, 2571.
Other abbreviations used include: MZUCR: Museo de Zoologia, Universidad de Costa Rica; SDNH: San Diego Natural History, California, USA; CL: carapace length; CW: carapace wide; MXP3: third maxilliped; P1: pereopod 1 (cheliped), P2-P5: pereopods 2-5 (walking legs 1-4).
Order Decapoda Latreille (1802)
Suborder Pleocyemata Burkenroad (1963) Infraorder Brachyura Linnaeus (1758) Section Eubrachyura de Saint Laurent (1980) Family Pinnotheridae de Haan (1833) Genus Austinotheres Campos (2002) Austinotheres angelicus (Lockington, (1877) (Figs. 1a-1f, 2a)
Synonymy: For previous synonymy, see Schmitt et al. (1973): 10, 38.
Pinnotheres angelicus: Lemaitre & Alvarez-Leon (1992): 36-76; Hendrickx (1995): 142.
Austinotheres angelicus: Campos (2002): 328-335; 2009: 30, 40; Ng et al. (2008): 248; Palacios-Theil et al. (2009): 459, 464, 466; Campos & Hernandez-Avila (2010): 42. Juxtafabia muliniarum [not J. muliniarum (Rathbun, 1918)]: Cabrera-Pena et al. (2001): 889-894.
Pinnotheres angelicus Lockington 1877, by the original designation and monotypy.
Geographic distribution and host
San Felipe, Baja California, upper Gulf of California, Mexico to Colombia (Lemaitre & Alvarez-Leon, 1992; Campos, 2002). In Myrakeena angelica (Rochebrune, 1895) and Saccostrea palmula Carpenter, 1857.
1 [male], 4 [female], San Felipe, Baja California, Mexico, USNM 71334, 67723; 30 [female], 30 [male], Campo E1 Pescador, 4 km north of San Felipe, Baja California, Mexico, 18 September 1986, in the oyster Mayrakeena angelica (Rochebrune, 1895), UABC, USNM 205688; 5 [female], San Jose Island, Baja California Sur, Mexico, Albatross, 16 May 1889, USNM 17467; 3 [female], Bahia de los Angeles, BC, Mexico, May 1982, in Mayrakeena angelica, USNM210921; 2 [female], Punta Morales Beach, Puntarenas, Costa Rica, 7 June 1992, USNM 256984; 2 [male], 8 [female] (4 ovigerous) Punta Morales, Playa Blanca (Golfo de Nicoya) in Saccostrea palmula, M. Protti & A. Baeza, coll, MZUCR 2617-01; 34 [male], 107 [female], 15 juveniles, same locality, habitat and host, 18-19 April 2009, MZUCR-2782-01; same locality, habitat and host, 7 November 2009, MZUCR 2782-01; 4 [male], 12 [female] (1 juvenile), same locality, habitat and host, 30 October 2010, MZUCR 2832-01; 4 [male], 9 [female] (2 ovigerous), same locality, habitat and host, 30 October 2010, mZuCR2831-01; 11 [male], 61 [female] (6 juveniles, 28 ovigerous), same locality, habitat and host, 30 October 2010, mZuCR2833-01, Rita Vargas coll.
Female (after Campos, 2002). Carapace suborbicular, regions ill-defined, smooth, shiny, thin, easily wrinkled; anterior margin strongly arcuate and not protruding anteriorly; posterior margin wide, slightly sinuous, sides rounded. Front advanced, laterally rounded. Orbits and eyes oval, hidden from dorsal view. Antenna with a prominent tubercle at posterior end of basal joint of antenna. MXP3 obliquely placed on buccal cavity, ischium and merus indistinguishably fused, palp of three articles, joined end to end; carpus larger than propodus and dactylus combined, propodus extending distally, small dactylus distally inserted on ventral margin of propodus. Exopod of MXP3 with a 2segmented flagellum. Pereopod 1 (chelipeds) elongate, manus slightly compressed and increasing in width distally; pollex slightly deflexed, swollen in basal half, with small teeth on cutting edge; dactylus slightly curved, with small proximal tooth on cutting edge; curved tips cross each other and leave a small gape when fingers are closed. P2-P5 slender, relative length P3 > P4 > P2 > P5; P3 asymmetrical, right from 1.10 to 1.22 longer than left. Dactyli of P2-P5 slightly curved at tip, relative length 3 > 4 > 2 > 5, those of P3 subequal to or longer than respective propodi. Abdomen extremely large, with six somites, and telson free articulated; margin with tomentum, laterally covering ischia and distally buccal cavity and eyes.
(After Campos, 2002). Much smaller than female. Carapace flat, suborbicular; front projecting, triangular, tip bent ventrally to a blunt point, not visible in dorsal view; surface hard, lightly pubescent, punctuate; cardiac region faintly defined. Eyestalk large and stout, diminishing from base to tip; pubescent on upper frontal surface; cornea large. A small tubercle at posterior end of basal joint of antenna. MXP3 similar to that of female. Pereopod 1 (chelipeds) stout, similar, slightly pubescent, palm smooth, swollen on basal half, tapering distally; exterior of manus crossed longitudinally by granulated ridge. Pollex short, stout, hooked at tip; a large ridge-like tooth occupying entire central portion; a deep notch at gape. Dactyli long and curved at tip; armed with two well-developed teeth at proximal end, the distal one the larger; fingers fitting together when closed, curved tips crossing each other; a row of setae on ventral margin of hand. P2-P5 slender, relative length P3 = P4 > P2 > P5. Dactyli long and straight, with tips hooked, acuminate. Propodus of P3-P5 crested with setae. Lower distal edges of carpus of P3-P4 with setae. Abdomen of six somites, and telson free articulated, widest at third segment, which represents almost 3A of entire length; gradually narrowing from third somite to telson, which is obtusely rounded. Abdomen and sternum pubescent.
Color in life
Carapace and chelipeds of male a deep chocolate brown; finger of chelipeds and ambulatory legs much lighter. Carapace and chelipeds of female a deep chocolate brown; ambulatory legs from light cream color to white (modified from Glassell, 1935).
Austinotheres angelicus is a holosymbiont of oysters (Ostreidae) including Myrakeena angelica (Rochebrune, 1895) and Saccostrea palmula (Carpenter, 1857). The only other two American pinnotherid crabs, which are symbionts of oysters of the genus Crassostrea in the Atlantic Ocean include Zoaps ostreum and Z. geddesi (see Rathbun, 1918; Schmitt et al., 1973; Campos & Manning, 2000). In addition, several hundreds of Modiolus capax (Conrad, 1837) from the Gulf of California were collected in the intertidal zone of San Felipe, and Los Angeles Bay, Baja California, and La Paz Bay, Baja California Sur, Mexico. Like Glassell (1935) we were unable to verify Rathbun's (1918) record of A. angelicus in M. capax. Only Fabia concharum (Rathbun, 1893) and Opisthopus transversus Rathbun, 1893 have been confirmed as symbionts of M. capax but from the west coast of Baja California Sur, Mexico (Campos et al., 1992; Campos, 1996).
The morphological analyses of the specimens collected in Punta Morales, Pacific coast of Costa Rica, in Saccostrea palmula and their comparison with topotypes of Austinotheres angelicus collected in Los Angeles Bay and another in San Felipe, Baja California, in Mayrakeena angelica, has led to the conclusion that the Costa Rican specimens belong to A. angelicus (Fig. 1). The genus Austinotheres Campos, 2002 along with other 17 genera worldwide has been included in the subfamily Pinnotherinae sensu stricto by Campos (2009). The consistent and distinct characters of this group include a soft and thin carapace, and a conspicuous protuberance at the basal antennal article, which is conspicuous in A. angelicus (Fig. 2a). Although Juxtafabia muliniarum has a carapace soft and thin, it is lacking such a protuberance at the basal antennal article (Fig. 2b). In addition, adult females of J. muliniarum have the dactyl of P5 longer than the other pereopods (Fig. 3a); males of this genus, and those of Fabia share long swimming setae on external face of carpus and propodus of P3 and P4, and two or more abdominal somites fused (Figs. 3b, 3d; Campos, 1993, 1996; Campos & Manning, 1998). Females of A. angelicus have the dactylus of P3 longer than the others pereopods, and males have all abdominal somites and telson well separated (Fig. 1d). The oyster crab, A. angelicus, as well as Enigmatheres canfieldi (Rathbun, 1918) (type species of Enigmatheres Campos, 2009) and Bonita mexicana Campos, 2009 (type species of Bonita Campos, 2009) comprise a subgroup within the Pinnotherinae sensu Campos (2009) that share a third maxilliped with a palp of three segments, being the carpus longer than the propodus (Figs. 1e, 1f). These shared and exclusive features of these species allow their taxonomic separation
from other members of this subfamily. The presence of an even and smooth carapace, and the P3 longer than the others (Fig. 1a) permit to separate A. angelicus from B. mexicana, which has the carapace tumid with two longitudinal sulci arising from the orbits and extending to the middle the of carapace, and the P4 longer than the others. On the other hand, E. canfieldi and A. angelicus can be distinguished from other pinnotherines by the asymmetrical P3 and because the propodus of the third maxilliped is shorter than the carpus (Figs. 1e, 1f).
Others species in the Pinnotherinae sensu Campos, 2009, except B. mexicana, have symmetrical walking legs, and the propodus of the third maxilliped is always larger than the carpus (Figs. 2b, 3c). A. angelicus differs from E. canfieldi in the obtuse angle of the outer margin of the ischium-merus of the third maxilliped (Fig. 1f) and by the insertion of the dactylus of this appendage on the distal third of the ventral margin of the propodus (Figs. 1e, 1f). E. canfieldi has a gently curved outer margin of the MXP3, and the insertion of the dactylus is on the middle third of the ventral margin of the propodus. The oyster crab, A. angelicus, can be also distinguished from E. canfieldi by its slender and long walking legs with long, blade-shaped and slightly curved dactyli. The walking legs of E. canfieldi are relatively stouter, and the dactyli are shorter, conical and slightly curved up to hooked and hard tip.
In summary, the following diagnostic characteristics as well as its symbiotic relationship with oysters (Ostreidae) permit to distinguish A. angelicus from other pinnotherid crabs from the entire Pacific Ocean: 1) the presence of a soft and thin carapace colored deep chocolate brown with dark purple tones, 2) a conspicuous protuberance in the basal antennal article (Fig. 2a), 3) a third maxilliped with a ischiummerus fused with its inner margin angled, 4) a carpus longer than the propodus, and 5) a digitiform dactylus insert subdistally (Figs. 1e, 1f).
Received: 24 October 2013; Accepted: 17 June 2014
Our great appreciation to Odalisca Breedy, Jorge Cortes and Ingo Wehrtmann, Escuela de Biologia and CIMAR (Centro de Investigaciones en Ciencias del Mar y Limnologia), Universidad de Costa Rica, for their careful revision of the manuscript; to Ingo Wehrtmann (Escuela de Biologia, Universidad de Costa Rica) for supporting our pinnotherid crab studies, and to Alma Rosa de Campos for her artwork. This research was partially co-funded by the following grants: Consejo Nacional de Ciencia y Tecnologia (CONACyT), Project S52903-Q, "Sistematica, relaciones filogeneticas y evolucion de los generos americanos de la subfamilia Pinnotherinae (Crustacea, Brachyura, Pinnotheridae)", UABC-204 and UABC213 and Red Tematica sobre Especies Exoticas de Mexico UABC-UANL-UdelMar (SEP-PROMEP); Academic Mobility Programs (2008 and 2011) of the UABC, and Office of International Affairs of Universidad de Costa Rica funded three research stays of EC at the Museo de Zoologia of the Universidad de Costa Rica. This is a contribution of the Museo de Zoologia, Escuela de Biologia, Universidad de Costa Rica.
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Received: 24 October 2013; Accepted: 17 June 2014
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Ernesto Campos (1) & Rita Vargas-Castillo (2)
(1) Facultad de Ciencias, Universidad Autonoma de Baja California Apartado Postal 296, Ensenada, 22800 Baja California, Mexico
(2) Museo de Zoologia, Escuela de Biologia, Universidad de Costa Rica San Pedro, 11501-2060 San Jose, Costa Rica
Corresponding author: Ernesto Campos (email@example.com)
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|Title Annotation:||articulo en ingles|
|Author:||Campos, Ernesto; Vargas-Castillo, Rita|
|Publication:||Latin American Journal of Aquatic Research|
|Date:||Jul 1, 2014|
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