Marine Biodiversity Records, page 1 of 3. # Marine Biological Association of the United Kingdom, 2011 doi:10.1017/S1755267211000352; Vol.

4; e40; 2011 Published online

First record of the association of the crab Pinnaxodes gigas (Decapoda: Pinnotheridae) with the geoduck clam Panopea globosa (Bivalvia: Hiatellidae)
esteban j.m. emparanza1, raul ulloa2, araceli montiel-ramos2 and raul molina-ocampo2
Billund Aquaculture Chile SA, Bernardino 1057 Modulo 13, Parque Industrial San Andres, Puerto Montt, Chile, 2Instituto Nacional de Pesca, Direccion General de Investigacion Pesquera Pacico Norte, Miguel Aleman sur 605, CP 85400, Guaymas, Sonora, Mexico
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Specimens of the clam Panopea globosa were collected in the Gulf of California, Mexico in 2009. Tiny crabs were found living inside the clam, being Pinnaxodes gigas. Since both the description and the scarce subsequent reports of P. gigas were performed only from single free-living specimens, this is the rst record of P. gigas associated as a symbiont of any host. This is also the rst record of any geoduck clams as host of commensal crustaceans, and the second record of a pea crab of the genus Pinnaxodes encountered infesting bivalves in the Pacic.

Keywords: Panopea globosa, Pinnaxodes gigas, symbiosis, new host, Gulf of California
Submitted 8 November 2010; accepted 27 January 2011

INTRODUCTION

The geoduck clams belonging to the genus Panopea Menard de la Groye, 1807 are gigantic bivalves inhabiting soft mud sand bottoms from the intertidal to over 110 m depth, buried down to 1 m depending on its longitude (Valero et al., 2004; Siddon, 2007; Arambula-Pujol et al., 2008). The siphon of the clam is extended to catch food and to expel waste and gametes during the reproductive season (Arambula-Pujol et al., 2008). The geoduck clams have been commercially harvested from 1969 in the north-east Pacic geoduck shery (Vadopalas et al., 2010), its latitudinal distribution ranges from Alaska to Mexico (Anderson, 1971; Siddon, 2007). Arambula-Pujol et al. (2008) stated that the specimens collected inside the Gulf of California waters belong to Panopea globosa (Dall, 1898). Recent studies of P. globosa clams, with genetic and morphometric analyses carried out by Rocha-Olivares et al. (2010) and Calderon-Aguilera et al. (2010) respectively conrm the species is endemic from the Gulf of California. During a eld population study of Panopea globosa carried out in 2009 in Playa del Sol (27825 N 110835 W) on a beach located in the Municipio Empalme Sonora, off the eastern coast of the Gulf of California, the existence of a symbiont pea crab in the mantle cavity of P. globosa was noticed. A total number of ten individuals of the clam, four females and six males, were collected by divers at a depth ranging from 10 to 25 m, embracing a study area of 3500 ha (Figure 1). All individuals were sexed, measured and

conrmed that the species was P. globosa. The pea crab was identied later as being Pinnaxodes gigas Green, 1992, a species that was described by Green (1992) and subsequently reported by Campos et al. (1998) from single, free-living individuals. The specimens are deposited in the National Crustacean Collection (CNCR) from the Instituto de Biologa, Universidad Nacional Autonoma de Mexico (UNAM). SYSTEMATICS Order DECAPODA Latreille, 1802 Sub order PLEOCYEMATA Burkenroad, 1963 Infra order BRACHYURA Latreille, 1802 Family PINNOTHERIDAE de Haan, 1833 Sub Family PINNOTHERINAE de Haan, 1833 Genus Pinnaxodes Heller, 1865 Pinnaxodes gigas Green, 1992

material examined
Carapace measurements are carapace length maximum width respectively. Adult males: (17 20 mm), (19 23 mm), (29 31 mm), (16 18 mm), (15 17.5 mm), (23 25.5 mm). Ovigerous females: (25 30 mm), (28 32 mm), (27.5 32 mm), (23.5 26 mm). Adult females: (32 36 mm), (31.5 34 mm), (24 26.5 mm), (26 28.5 mm), (33 36.5 mm).

description
Corresponding author: E.J.M. Emparanza Email: akronos@yahoo.com

Characteristic features of the species have already been presented by Green (1992) and Campos et al. (1998). We emphasize some features. The carapace is heavy, subpentagonal, convex, front produced. The legs are strong, symmetrical.
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esteban j.m. emparanza et al.

Fig. 1. Study area in the eastern coast of the Gulf of California.

symbionts, either facultative or obligate, of many species of holothurians, mussels and echinoids (Rathbun, 1918; Konishi, 1977; Manning, 1993; Campos et al., 1998; Ng & Manning, 2003; Melo & Boehs, 2004). Green (1992) described P. gigas in the Gulf of California, subsequent reports indicated the species inhabiting only in the area (see Campos et al., 1998). The nding of P. gigas as a symbiont of Panopea globosa is the second record of a pea crab belonging to the genus Pinnaxodes infesting bivalves in the Pacic Ocean, the rst one being P. major Ortmann, 1849 from Japan, symbiont of the mussel Atrina pectinata (Linnaeus, 1767) (Takeda & Prince Masahito, 2000).

The chelae are strong with the propodus inated interiorly, the moveable nger presents large tooth at base, immovable nger presents two small teeth, one distal and one proximal. Abdomen is broad at base, narrowing towards sixth segment. The last third of sixth segment and base of telson are expanded, the telson narrowing to rounded tip. Third maxilliped is large with a suture present between merus and ischium, outer margin nearly straight and joining a broadly arched distal end, inner margin mostly concave. Dense pubescence surrounds the abdominal depression; the thoracic sternites are heavily calcied.

ACKNOWLEDGEMENTS

remarks
Pinnaxodes gigas and Pinnaxodes oridensis Wells & Wells (1961) are very similar in shape and coloration. The main characteristics used to identify the crabs collected in the present study were the shape of the abdomen and the size of the crabs, as suggested by Green (1992). Pinnaxodes gigas presents the abdomen narrow from its base to the sixth segment, the distal third of this segment and the base of the telson are expanded, and the telson narrows to form a rounded tip. In P. oridensis the abdomen presents an abruptly inated and rounded telson. In addition, the size (carapace width) of the crabs collected in the present study ranged from 17.5 to 31 mm for the males and from 26 to 36.5 mm for the females, much larger than the 11 mm of carapace width described by Wells & Wells (1961) for the largest specimen of P. oridensis collected in their study. Campos et al. (1998) held the hypothesis that P. gigas was a . . . symbiont of holothurids, capable of leaving its host temporarily . . . [sic], since the related species P. oridensis was described inhabiting holothurids in the West Atlantic (Wells & Wells, 1961; Miller & Pawson, 1984; Takeda & Prince Masahito, 2000). Wells & Wells (1961) have reported P. oridensis in the respiratory tree of the holothurian Holothuria (Theelothuria) princeps Selenka, 1867 in the Gulf of Mexico at an infestation rate of 45 61%, nding mostly a single specimen in each host, although male female pairs were also frequently encountered. In the present study one single specimen of P. gigas was mostly found in each host, however, male female pairs and even three crabs per host were also found in Panopea globosa, with an infestation rate of 100% and an average number of 1.4 crabs per host of the specimens studied. The association between Panopea generosa Gould, 1850 and an unspecied pinnotherid crab under the name cangrejo chcharo (pea crab) in Baja California was recently pointed out by Caceres-Martnez & Vasquez-Yeomans (2008). The members of the genus Pinnaxodes have been recognized as

The authors are grateful to Dr E. Campos for his kind help with literature and to Dr F. Alvarez for accepting the voucher material that will be deposited in the National Crustacean Collection (CNCR), Instituto de Biologa, Universidad Nacional Autonoma de Mexico (UNAM). A shing permit granted to R. Ulloa under the Programa de Investigacion para el seguimiento de la pesquera de almeja generosa (Panopea spp.) en la costa de Sonora, Mexico: pro speccion y evaluacion de nuevas areas de aprovechamiento research programme allowed the collection of the specimens and specically through the Permiso de pesca de fomento DGOPA.00980.130209.0467 permit to Mr Lorenzo Osuna, who collected the specimens. Thus, the study complies with the Mexican Federal regulations. Two anonymous referees helped us to improve this manuscript through insightful comments. E.J.M. Emparanza is grateful to Mr Vicente Hernandez, Mr Salvador Zamorano, Ms Rafaela Arce, Mr Benjamn Rivadeneira and Dr Madia Ferretti for additional logistic support and encouragement. E.J.M. Emparanza and R. Ulloa want to dedicate this work to the memory of the late Chilean marine biologist Sandra L. Cifuentes, a soulful friend and curious professional. This research received no specic grant from any funding agency, commercial or nonprot sectors.

REFERENCES
Anderson A.M. (1971) Spawning, growth and spatial distribution of the geoduck clam Panopea generosa (Gould) in Hood Canal, Washington. PhD thesis. University of Washington, USA. Arambula-Pujol E.M., Garca-Juarez A.R., Alcantara-Razo E. and Aragon-Noriega E.A. (2008) Aspectos de biologa reproductiva de la almeja de sifon Panopea globosa (Dall 1898) en el Golfo de California. Hidrobiologica 18, 8998. Caceres-Martnez J. and Vasquez-Yeomans R. (2008) La patologa en moluscos bivalvos: principales problemas y desafos para la produc cion de bivalvos en America Latina. In Lovatelli A., Faras A. and Uriarte I. (eds) Estado actual del cultivo y manejo de moluscos bivalvos y su proyeccion futura: factores que afectan su sustentabilidad en America Latina. Taller Tecnico Regional de la FAO, 2024 de agosto de 2007, Pto. Montt, Chile. FAO Actas de Pesca y Acuicultura, no. 12. Roma: FAO, pp. 327337. Calderon-Aguilera L.E., Aragon-Noriega E.A., Hand C.M. and Moreno-Rivera V.M. (2010) Morphometric relationships, age, growth, and mortality of the geoduck clam, Panopea generosa, along

panopea globosa, new host for pinnaxodes gigas

the Pacic coast of Baja California, Mexico. Journal of Shellsh Research 29, 319326. Campos E., Daz V. and Gamboa-Contreras J.A. (1998) Notes on distribution and taxonomy of ve poorly known species of pinnotherid crabs from the eastern Pacic (Crustacea: Brachyura: Pinnotheridae). Proceedings of the Biological Society of Washington 111, 372 381. Green T. (1992) Pinnaxodes gigas, a new species of Pinnotherid crab from the Gulf of California (Decapoda: Brachyura: Pinnotheridae). Proceedings of the Biological Society of Washington 105, 775779. Konishi K. (1977) On three species of the pinnotherid crabs from Hokkaido, Japan. Journal of the Faculty of Science Hokkaido University. Zoology, Series VI 20, 605610. Manning R.B. (1993) West African pinnotherid crabs, subfamily Pinnotherinae (Crustacea, Decapoda, Brachyura). Bulletin du Museum National dHistoire Naturelle, Paris, 4e Serie A 14, 125177. Melo G.A.S. and Boehs G. (2004) Rediscovery of Holothuriophilus tomentosus (Ortmann) comb. nov. (Crustacea, Brachyura, Pinnotheridae) in the Brazilian coast. Revista Brasileira de Zoologia 21, 229232. Miller J.E. and Pawson D.L. (1984) Holothurians (Echinodermata: Holothuroidea). Memoirs of the Hourglass Cruises 7, 179. Ng P.K.L. and Manning R.B. (2003) On two new genera of pea crabs parasitic in holothurians (Crustacea: Decapoda: Brachyura: Pinnotheridae) from the Indo-West Pacic, with notes on allied genera. Proceedings of the Biological Society of Washington 116, 901919. Rathbun M.J. (1918) The grapsoid crabs of America. Bulletin of the United States National Museum 97, 1 461. Rocha-Olivares A., Calderon-Aguilera L.E., Aragon-Noriega E.A., Saavedra-Sotelo N.C. and Moreno-Rivera V.M. (2010) Genetic and

morphological variation of northeast Pacic Panopea clams: evolutionary implications. Journal of Shellsh Research 29, 327335. Siddon C. (2007) Evaluation of the southeastern Alaska geoduck (Panopea abrupta): stock assessment methodologies. Alaska Department of Fish and Game, Special Publication no. 0702, 20 pp. Takeda M. and Prince Masahito (2000) Systematic notes on the Pinnotherid crabs from the genus Pinnaxodes (Crustacea: Decapoda: Brachyura). Bulletin of the National Science Museum, Series A (Zoology) 26, 99112. Vadopalas B., Pietsch T.W. and Friedman C.S. (2010) The proper name for the geoduck: resurrection of Panopea generosa Gould, 1850, from the synonymy of Panopea abrupta (Conrad, 1849) (Bivalvia: Myoida: Hiatellidae). Malacologia 52, 169173. Valero J.L., Hand C., Orensanz J.M., Parma A.M., Armstrong D. and Hilborn R. (2004) Geoduck (Panopea abrupta) recruitment in the Pacic north-west: long-term changes in relation to climate. CalCOFI Reports 45, 7 pp. and Wells H.W. and Wells M.J. (1961) Observations on Pinnaxodes oridensis, a new species of pinnotherid crustacean in holothurians. Bulletin of Marine Science of the Gulf and Caribbean 11, 267 279.

Correspondence should be addressed to: E.J.M. Emparanza Billund Aquaculture Chile SA Bernardino 1057 Modulo 13 Parque Industrial San Andres Puerto Montt Chile email: akronos@yahoo.com