Living with a crab: effect of Austinotheres angelicus (Brachyura, Pinnotheridae) infestation on the condition of Saccostrea palmula (Ostreoida, Ostreidae)

Mena, Sebastián; Salas-Moya, Carolina; Wehrtmann, Ingo S.

Abstract

Some members of the Pinnotheridae family exhibit close symbiotic relationships with bivalves, which may cause severe damage to the mollusk. The condition index (CI) is a tool that serves to evaluate the effect of biotic and abiotic factors on the morphology and physiology of mollusks, including those caused by symbiotic organisms. In the present study, we evaluated the effects of the infestation of the pinnotherid crab Austinotheres angelicus on the oyster Saccostrea palmula through monthly sampling (April to November 2012) in Punta Morales, Pacific coast of Costa Rica. A total of 245 oysters were analyzed, of which 38% were infested by the pinnotherid crab. Most of the oysters analyzed (92%) varied in depth between 1.5 and 15.0 mm; 89% of the infested oysters were in this depth range. The prevalence was positively correlated with the depth of the oyster. Our results revealed that crab infestation could reduce the CI by 11 to 33%. The obtained findings suggest that the infestation by A. angelicus provokes alterations of the flesh production of the oyster, especially when the association is with a pair of crabs including an ovigerous female. The association of A. angelicus with S. palmula is best described as facultative parasitism for male crabs and obligatory parasitism for females.

Fitness; interaction; parasitism; pea crab; symbiosis

Austin, H.; Haven, D.S. and Moustafa, M.S. 1993. The relationship between trends in a condition index of the American oyster, Crassostrea virginica, and enviromental parameters in three Virginia estuaries. Estuaries, 16(2): 362-374.
Baeza, J.A. 1999. Indicadores de monogamia en el cangrejo comensal Pinnixa transversalis (Milne Edwards & Lucas) (Decapoda: Brachyura: Pinnotheridae): distribución poblacional, asociación macho-hembra y dimorfismo sexual. Revista de Biología Marina y Oceanografía, 34(2): 303-313.
Bierbaum, R.M. and Ferson, S. 1986. Do symbiotic pea crabs decrease growth rate in mussels? Biological Bulletin, 170: 51-61.
Bierbaum, R.M. and Shumway, S.E. 1988. Filtration and oxygen consumption in mussels, Mytilus edulis, with and without pea crabs, Pinnotheres maculatus Estuaries, 11(4): 264-271.
Brugnoli Olivera, E. and Morales Ramírez, A. 1999. Parámetros físico-químicos de la columna de agua, en la zona de Punta Morales, Golfo de Nicoya, durante un evento "El Niño". Tópicos Meteorológicos y Oceanográficos, 6(2): 52-57.
Cabrera Peña, J.H.; Protti Quesada, M.; Urriola Hernández, M. and Saénz Vargas, O. 2001a. Crecimiento y madurez sexual de una población de Saccostrea palmula (Mollusca: Bivalvia), Costa Rica. Revista Biología Tropical, 49(3-4): 877-882.
Cabrera Peña, J.H.; Protti Quesada, M.; Urriola Hernández, M.; Saénz Vargas, O. and Alfaro Hidalgo, R. 2001b. Tallas y fecundidad de Juxtafabia muliniarum (Brachyura: Pinnotheridae) asociado con Saccostrea palmula (Mollusca: Bivalvia), Costa Rica. Revista de Biología Tropical, 49(3-4): 889-894.
Campos, E. 1990. Calypotraeotheres, a new genus for the limpet crab Fabia granti Glassell, 1933 (Crustacea, Brachyura). Proceedings of the Biological Society of Washington, 103(2): 364-371.
Campos, E. 1996. Partial revision of pinnotherid crab genera with a two-segmented palp on the third maxilliped (Decapoda: Brachyura). Journal of Crustacean Biology, 16(3): 556-563.
Campos, E. 2002. Two new genera of pinnotherid crabs from the tropical Easter pacific (Decapoda: Brachyura: Pinnotheridae). Journal of Crustacean Biology, 22(2): 328-336.
Campos, E. and Vargas-Castillo, R. 2014. Austinotheres angelicus (Lockington, 1877): the correct name for the symbiotic crab Juxtafabia muliniarum sensu Cabrera-Peña et al. (2001) (Crustacea, Brachyura, Pinnotheridae). Latin American Journal of Aquatic Research, 42(3): 598-603.
Derby, C.D. and Atema, J. 1980. Induced host odor attraction in the pea crab Pinnotheres maculates Biological Bulletin, 158: 26-33
Feldmann, R.M.; Mackinnon, D.I.; Endo, K. and Chirino-Galvez, L. 1996. Pinnotheres laquei Sakai (Decapoda: Pinnotheridae), a tiny crab commensal within the Brachiopod Laqueus rubellus (Sowerby) (Terebratulida: Laqueidae). Journal of Paleontology, 70(2): 303-311.
Filgueira, R.; Comeau, L.A.; Landry, T.; Grant, J.; Guyondet, T. and Mallet, A. 2013. Bivalve condition index as an indicator of aquaculture intensity: A meta-analysis. Ecological Indicators, 25: 215-229.
Froese, R. 2006. Cube law, condition factor and weight-length relationships: history, meta-analysis and recommendations. Journal of Applied Ichthyology, 22: 241-253.
Geiger, D.L. and Martin, J.W. 1999. The pea crab Orthotheres haliotidis new species (Decapoda: Brachyura: Pinnotheridae) in the Australian abalone Haliotis asinina Linnaeus, 1758 and Haliotis squamata Reeve, 1846 (Gastropoda: Vetigastropoda: Haliotidae). Bulletin of Marine Science, 64(2): 269-280.
Grove, M.W. and Woodin, S.A. 1996. Conspecific recognition and host choice in a pea crab, Pinnixa chaetopterana (Brachyura: Pinnotheridae). Biological Bulletin, 190: 359-366.
Haines, C.M.C.; Edmunds, M. and Pewsey, A.R. 1994. The pea crab, Pinnotheres pisum (Linnaeus, 1967), and its association with the common mussel, Mytilus edulis (Linnaeus, 1758), in the Solent (UK). Journal of Shellfish Research, 13(1): 5-10.
Harry, H.W. 1985. Synopsis of the supraspecific classification of living oysters (Bivalvia: Gryphaeidae and Ostreidae). The Veliger, 28(1): 121-158.
Iyengar, E.V. 2008. Kleptoparasitic interactions throughout the animal kingdom and a re-evaluation, based on participant mobility, of the conditions promoting the evolution of kleptoparasitism. Biological Journal of the Linnean Society, 93: 745-762.
Kruczynski, W.L. 1972. Effect of the pea crab, Pinnotheres maculatus Say, on growth of the Bay Scallop, Argopecten irradians concentricus (Say). Chesapeake Science, 13(3): 218-220.
Kruczynski, W.L. 1975. A radioactive tracer study of food uptake by Pinnotheres maculatus in molluscan hosts. Biological Bulletin, 148: 60-67.
Lemaitre, R. and Álvarez León, R. 1992. Crustáceos decápodos del Pacífico colombiano: Lista de especies y consideraciones zoogeográficas. Anales del Instituto de Investigaciones Marinas de Punta Betín, 21: 33-76.
Loosanoff, V.L. and Nomejko, C.A. 1949. Growth of oysters, O. virginica, during different months. The Biological Bulletin, 97(1): 82-94.
Mantelatto, F.L. and Cuesta, J.A. 2010. Morphology of the first zoeal stage of the commensal southwestern Atlantic crab Austinixa aidae (Righi 1967) (Brachyura: Pinnotheridae), hatched in the laboratory. Helgoland Marine Research, 64(4): 343-348.
Mercado-Silva, N. 2005. Condition index of the eastern oyster, Cassostrea virginica (Gmelin, 1791) in Sapelo Island Georgia-Efects of site, position on bed and pea crab parasitism. Journal of Shellfish Research, 24(1): 121-126.
Miller, M.R.; White, A. and Boots, M. 2006. The evolution of parasites in response to tolerance in their host: The good, the bad, and apparent commensalism. Evolution, 60(5): 945-956
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 Pacific, with notes on allied genera. Proceedings of the Biological Society of Washington, 116(4): 901-919.
Ocampo, E.H.; Nuñez, J.D.; Cledón, M. and Baeza, J.A. 2012. Host-specific reproductive benefits, host selection behavior and host use pattern of pinnotherid crab Calyptraeotheres garthi Journal of Experimental Marine Biology and Ecology, 429: 36-46.
Peiró, D.F. and Mantelatto, F.L. 2011. Population dynamics of the pea crab Austinixa aidae (Brachyura, Pinnotheridae): a symbiotic of the ghost shrimp Callichirus major (Thalassinidea, Callianassidae) from the southwestern Atlantic. Iheringia, Série Zoologia, 101(1-2): 5-14.
Rathbun, M.J. 1900. Synopses of North-American invertebrates. XI. The catometopous or grapsoid crabs of North America. The American Naturalist, 34(403): 583-592.
Salas-Moya, C.; Mena, S. and Wehrtmann, I.S. 2014. Reproductive traits of the pea crab Austinotheres angelicus (Crustacea, Pinnotheridae) living in Saccostra palmula (Bivalvia, Ostreidae), Pacific coast of Costa Rica. Zookeys, 457: 239-252.
Silas, E.G. and Alagarswami, K. 1967. On an instance of parasitisation by the pea-crab (Pinnotheres sp.) on the backwater clam (Meretrix casta (Chemnitz)) from India with a review of the work on the systematics, ecology, biology and ethology of the pea crabs of the genus Pinnotheres Latreille. Proceedings of the Symposium on Crustacea, 3: 1161-1227.
Sun, W.; Sun, S.; Yuqi, W.; Baowen, Y. and Weibo, S. 2006. The prevalence of the pea crab, Pinnotheres sinenis, and its impact of the condition of the cultured mussel, Mytilus galloprovincialis, in Jiaonan waters (Shandong Province, China). Aquaculture, 253: 57-63.
Trottier, O.; Walker, D. and Jeff, A.G. 2012. Impact of the parasitic crab Pinnotheres novaezelandiae on aquacultured New Zeland green-lipped mussels, Perna canaliculus Aquaculture, 344-346: 23-28.
Zapalski, M.K. 2011. In absence of proof a proof of absence? Comments on commensalism. Palaeogeography, Palaeoclimatology, Palaeoecology, 302: 484-488.

Publication Dates

Publication in this collection
28 Jan 2015
Date of issue
Dec 2014

History

Received
20 Nov 2014
Accepted
29 Dec 2014

This work is licensed under a Creative Commons Attribution 4.0 International License.

[1] Austin, H.; Haven, D.S. and Moustafa, M.S. 1993. The relationship between trends in a condition index of the American oyster, Crassostrea virginica, and enviromental parameters in three Virginia estuaries. Estuaries, 16(2): 362-374.

[2] Baeza, J.A. 1999. Indicadores de monogamia en el cangrejo comensal Pinnixa transversalis (Milne Edwards & Lucas) (Decapoda: Brachyura: Pinnotheridae): distribución poblacional, asociación macho-hembra y dimorfismo sexual. Revista de Biología Marina y Oceanografía, 34(2): 303-313.

[3] Bierbaum, R.M. and Ferson, S. 1986. Do symbiotic pea crabs decrease growth rate in mussels? Biological Bulletin, 170: 51-61.

[4] Bierbaum, R.M. and Shumway, S.E. 1988. Filtration and oxygen consumption in mussels, Mytilus edulis, with and without pea crabs, Pinnotheres maculatus Estuaries, 11(4): 264-271.

[5] Brugnoli Olivera, E. and Morales Ramírez, A. 1999. Parámetros físico-químicos de la columna de agua, en la zona de Punta Morales, Golfo de Nicoya, durante un evento "El Niño". Tópicos Meteorológicos y Oceanográficos, 6(2): 52-57.

[6] Cabrera Peña, J.H.; Protti Quesada, M.; Urriola Hernández, M. and Saénz Vargas, O. 2001a. Crecimiento y madurez sexual de una población de Saccostrea palmula (Mollusca: Bivalvia), Costa Rica. Revista Biología Tropical, 49(3-4): 877-882.

[7] Cabrera Peña, J.H.; Protti Quesada, M.; Urriola Hernández, M.; Saénz Vargas, O. and Alfaro Hidalgo, R. 2001b. Tallas y fecundidad de Juxtafabia muliniarum (Brachyura: Pinnotheridae) asociado con Saccostrea palmula (Mollusca: Bivalvia), Costa Rica. Revista de Biología Tropical, 49(3-4): 889-894.

[8] Campos, E. 1990. Calypotraeotheres, a new genus for the limpet crab Fabia granti Glassell, 1933 (Crustacea, Brachyura). Proceedings of the Biological Society of Washington, 103(2): 364-371.

[9] Campos, E. 1996. Partial revision of pinnotherid crab genera with a two-segmented palp on the third maxilliped (Decapoda: Brachyura). Journal of Crustacean Biology, 16(3): 556-563.

[10] Campos, E. 2002. Two new genera of pinnotherid crabs from the tropical Easter pacific (Decapoda: Brachyura: Pinnotheridae). Journal of Crustacean Biology, 22(2): 328-336.

[11] Campos, E. and Vargas-Castillo, R. 2014. Austinotheres angelicus (Lockington, 1877): the correct name for the symbiotic crab Juxtafabia muliniarum sensu Cabrera-Peña et al. (2001) (Crustacea, Brachyura, Pinnotheridae). Latin American Journal of Aquatic Research, 42(3): 598-603.

[12] Derby, C.D. and Atema, J. 1980. Induced host odor attraction in the pea crab Pinnotheres maculates Biological Bulletin, 158: 26-33

[13] Feldmann, R.M.; Mackinnon, D.I.; Endo, K. and Chirino-Galvez, L. 1996. Pinnotheres laquei Sakai (Decapoda: Pinnotheridae), a tiny crab commensal within the Brachiopod Laqueus rubellus (Sowerby) (Terebratulida: Laqueidae). Journal of Paleontology, 70(2): 303-311.

[14] Filgueira, R.; Comeau, L.A.; Landry, T.; Grant, J.; Guyondet, T. and Mallet, A. 2013. Bivalve condition index as an indicator of aquaculture intensity: A meta-analysis. Ecological Indicators, 25: 215-229.

[15] Froese, R. 2006. Cube law, condition factor and weight-length relationships: history, meta-analysis and recommendations. Journal of Applied Ichthyology, 22: 241-253.

[16] Geiger, D.L. and Martin, J.W. 1999. The pea crab Orthotheres haliotidis new species (Decapoda: Brachyura: Pinnotheridae) in the Australian abalone Haliotis asinina Linnaeus, 1758 and Haliotis squamata Reeve, 1846 (Gastropoda: Vetigastropoda: Haliotidae). Bulletin of Marine Science, 64(2): 269-280.

[17] Grove, M.W. and Woodin, S.A. 1996. Conspecific recognition and host choice in a pea crab, Pinnixa chaetopterana (Brachyura: Pinnotheridae). Biological Bulletin, 190: 359-366.

[18] Haines, C.M.C.; Edmunds, M. and Pewsey, A.R. 1994. The pea crab, Pinnotheres pisum (Linnaeus, 1967), and its association with the common mussel, Mytilus edulis (Linnaeus, 1758), in the Solent (UK). Journal of Shellfish Research, 13(1): 5-10.

[19] Harry, H.W. 1985. Synopsis of the supraspecific classification of living oysters (Bivalvia: Gryphaeidae and Ostreidae). The Veliger, 28(1): 121-158.

[20] Iyengar, E.V. 2008. Kleptoparasitic interactions throughout the animal kingdom and a re-evaluation, based on participant mobility, of the conditions promoting the evolution of kleptoparasitism. Biological Journal of the Linnean Society, 93: 745-762.

[21] Kruczynski, W.L. 1972. Effect of the pea crab, Pinnotheres maculatus Say, on growth of the Bay Scallop, Argopecten irradians concentricus (Say). Chesapeake Science, 13(3): 218-220.

[22] Kruczynski, W.L. 1975. A radioactive tracer study of food uptake by Pinnotheres maculatus in molluscan hosts. Biological Bulletin, 148: 60-67.

[23] Lemaitre, R. and Álvarez León, R. 1992. Crustáceos decápodos del Pacífico colombiano: Lista de especies y consideraciones zoogeográficas. Anales del Instituto de Investigaciones Marinas de Punta Betín, 21: 33-76.

[24] Loosanoff, V.L. and Nomejko, C.A. 1949. Growth of oysters, O. virginica, during different months. The Biological Bulletin, 97(1): 82-94.

[25] Mantelatto, F.L. and Cuesta, J.A. 2010. Morphology of the first zoeal stage of the commensal southwestern Atlantic crab Austinixa aidae (Righi 1967) (Brachyura: Pinnotheridae), hatched in the laboratory. Helgoland Marine Research, 64(4): 343-348.

[26] Mercado-Silva, N. 2005. Condition index of the eastern oyster, Cassostrea virginica (Gmelin, 1791) in Sapelo Island Georgia-Efects of site, position on bed and pea crab parasitism. Journal of Shellfish Research, 24(1): 121-126.

[27] Miller, M.R.; White, A. and Boots, M. 2006. The evolution of parasites in response to tolerance in their host: The good, the bad, and apparent commensalism. Evolution, 60(5): 945-956

[28] 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 Pacific, with notes on allied genera. Proceedings of the Biological Society of Washington, 116(4): 901-919.

[29] Ocampo, E.H.; Nuñez, J.D.; Cledón, M. and Baeza, J.A. 2012. Host-specific reproductive benefits, host selection behavior and host use pattern of pinnotherid crab Calyptraeotheres garthi Journal of Experimental Marine Biology and Ecology, 429: 36-46.

[30] Peiró, D.F. and Mantelatto, F.L. 2011. Population dynamics of the pea crab Austinixa aidae (Brachyura, Pinnotheridae): a symbiotic of the ghost shrimp Callichirus major (Thalassinidea, Callianassidae) from the southwestern Atlantic. Iheringia, Série Zoologia, 101(1-2): 5-14.

[31] Rathbun, M.J. 1900. Synopses of North-American invertebrates. XI. The catometopous or grapsoid crabs of North America. The American Naturalist, 34(403): 583-592.

[32] Salas-Moya, C.; Mena, S. and Wehrtmann, I.S. 2014. Reproductive traits of the pea crab Austinotheres angelicus (Crustacea, Pinnotheridae) living in Saccostra palmula (Bivalvia, Ostreidae), Pacific coast of Costa Rica. Zookeys, 457: 239-252.

[33] Silas, E.G. and Alagarswami, K. 1967. On an instance of parasitisation by the pea-crab (Pinnotheres sp.) on the backwater clam (Meretrix casta (Chemnitz)) from India with a review of the work on the systematics, ecology, biology and ethology of the pea crabs of the genus Pinnotheres Latreille. Proceedings of the Symposium on Crustacea, 3: 1161-1227.

[34] Sun, W.; Sun, S.; Yuqi, W.; Baowen, Y. and Weibo, S. 2006. The prevalence of the pea crab, Pinnotheres sinenis, and its impact of the condition of the cultured mussel, Mytilus galloprovincialis, in Jiaonan waters (Shandong Province, China). Aquaculture, 253: 57-63.

[35] Trottier, O.; Walker, D. and Jeff, A.G. 2012. Impact of the parasitic crab Pinnotheres novaezelandiae on aquacultured New Zeland green-lipped mussels, Perna canaliculus Aquaculture, 344-346: 23-28.

[36] Zapalski, M.K. 2011. In absence of proof a proof of absence? Comments on commensalism. Palaeogeography, Palaeoclimatology, Palaeoecology, 302: 484-488.

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Living with a crab: effect of Austinotheres angelicus (Brachyura, Pinnotheridae) infestation on the condition of Saccostrea palmula (Ostreoida, Ostreidae)

Abstract

Publication Dates

History