Abstract
The Levantine populations of the invasive swimming crab Charybdis longicollis have been parasitized by the rhizocephalan Heterosaccus dollfusi, itself an alien, since 1992. The parasite affects the host morphology, moulting, behaviour, causes its sterilization, and induces mortality. The high prevalence of H. dollfusi can be ascribed to the dense population of the host, the year-round reproduction of the parasite that promotes recurrent re-infection, and the recruitment dynamics that likely permit the synchronous development of both host and parasite. After 17 years, despite the high prevalence of the parasite and its injurious impact on the host reproduction, the invasive host-parasite pair has reached an apparent modus vivendi, with no evident reduction in the host population and with recurrent seasonal high rates of parasitization and multiple externae.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abello P, Macpherson E (1992) Epibiosis and rhizocephalan infestation patterns in relation to the reproductive biology of Lithodes ferox (Filhol, 1885) (Anomura: Lithodidae). J Crust Biol 12:561–570
Abello P, Villanueva R, Gili JM (1990) Epibiosis in deep-sea crab populations as indicator of biological and behavioural characteristics of the host. J Mar Biol Ass UK 70:687–695
Alvarez F, Calderon J (1996) Distribution of Loxothylacus texanus (Cirripedia: Rhizocephala) parasitizing crabs of the genus Callinectes in the Southwestern Gulf of Mexico. Gulf Res Rep 9:205–210
Alvarez F, Hines AH, Reaka-Kudla ML (1995) The effects of parasitism by the barnacle Loxothylacus panopaei (Gissler) (Cirripedia: Rhizocephala) on growth and survival of the host crab Rhithropanopaeus harrisii (Gould) (Brachyura: Xanthidae). J Exp Mar Biol Ecol 192:221–232
Alvarez F, Gracia A, Robles R, Calderon J (1999) Parasitization of Callinectes rathbunae and Callinectes sapidus by the rhizocephalan barnacle Loxothylacus texanus in Alvarado Lagoon, Veracruz, Mexico. Gulf Res Rep 11:15–21
Alvarez F, Campos E, Høeg J, O’Brien J (2001) Distribution and prevalence records of two parasitic barnacles (Crustacea: Cirripedia: Rhizocephala) from the west coast of North America. Bull Mar Sci 68:233–241
Bishop RK, Cannon LRG (1979) Morbid behaviour of the commercial sand crab, Portunus pelagicus (L.), parasitized by Sacculina granifera Boschma, 1973 (Cirripedia: Rhizocephala). J Fish Dis 2:131–144
Bocquet-Védrine J (1959) Sur un Cancer pagurus L. porteur de cinq sacs de Sacculina triangular Leuckart. Arch Zool Exp Gen 98:57–61
Boschma H (1960) A rhizocephalan parasite of the crab Charybdis hoplites (Wood-Mason). Crustaceana 1:58–67
Boschma H (1972) On the occurrence of Carcinus maenas (Linnaeus) and its parasite Sacculina carcini Thompson in Burma, with notes on the transport of crabs to new localities. Zool Meded 47:145–155
Day JH (1935) The life cycle of Sacculina. Q J Microsc Sci 77:549–583
Delage Y (1884) Evolution de la Sacculine (Sacculina carcini Thomps.) crustace endoparasite de I’ordre nouveau des kentrogonides. Archs Zool Exp Gén 2:417–736
Gaddes SW, Sumpton WD (2004) Distribution of barnacle epizoites of the crab Portunus pelagicus in the Moreton Bay region, eastern Australia. Mar Freshw Res 55:241–248
Galil BS (1986) Red Sea decapods along the Mediterranean coast of Israel: ecology and distribution. In: Dubinsky Z, Steinberger Y (eds) Environmental quality and ecosystem stability. Bar Ilan University Press, Ramat Gan, pp 179–183
Galil BS, Innocenti G (1999) Notes on the population structure of the portunid crab Charybdis longicollis Leene, parasitized by the rhizocephalan Heterosaccus dollfusi Boschma, off the Mediterranean coast of Israel. Bull Mar Sci 64:451–463
Galil BS, Kevrekidis K (2002) Exotic decapods and stomatopods off Rhodes Island (Greece) and the eastern Mediterranean transient. Crustaceana 75:925–930
Galil BS, Lützen J (1995) Biological observations on Heterosaccus dollfusi Boschma (Cirripedia: Rhizocephala), a parasite of Charybdis longicollis Leene (Decapoda: Brachyura), a lessepsian migrant to the Mediterranean. J Crust Biol 15:659–670
George AI (1959) Heterosaccus ruginosus (Boschma), a rhizocephalan parasite of the crab Neptunus sanguinolentus (Herbst). J Zool Soc India 11:171–204
Gherardi F, Cassidy PM (1995) Life history patterns of Discorsopagurus schmitti, a hermit crab inhabiting polychaete tubes. Biol Bull 188:68–77
Gili JM, Abello P, Villanueva R (1993) Epibionts and intermoult duration in the crab Bathynectes piperitis. Mar Ecol Prog Ser 98:107–113
Guinot D (1966) La faune carcinologique (Crustacea Brachyura) de I’Ocean Indien occidental et de la Mer Rouge. Catalogue, remarques biogeographiques et bibliographie. Mém Inst Fond Afr Noire 77:235–352
Hartnoll RG (1967) The effects of sacculinid parasites on two Jamaican crabs. Zool J Linn Soc 46:275–295
Hawkes CR, Meyers TR, Shirley TC, Koeneman TM (1986) Prevalence of the parasitic barnacle Briarosaccus callosus on king crabs of Southeastern Alaska. Trans Am Fish Soc 115:252–257
Hawkes CR, Meyers TR, Shirley TC (1987) Growth of Alaskan blue king crabs, Paralithodes platypus (Brandt), parasitized by the rhizocephalan Briarosaccus callosus Boschma. Crustaceana 52:78–84
Heath JR (1971) Seasonal changes in a population of Sacculina carcini Thompson (Crustacea: Rhizocephala) in Scotland. J Exp Mar Biol Ecol 6:15–22
Hines AH, Alvarez F, Reed SA (1997) Introduced and native populations of a marine parasitic castrator: variation in prevalence of the rhizocephalan Loxothylacus panopaei in xanthid crabs. Bull Mar Sci 61:197–214
Hochberg RT, Bert TM, Steele P, Brown SD (1992) Parasitization of Loxothylacus texanus on Callinectes sapidus: aspects of population biology and effects on host morphology. Bull Mar Sci 50:117–132
Hoddle MS (2004) Restoring balance: using exotic species to control invasive exotic species. Conserv Biol 18:38–49
Høeg JT (1995) The biology and life cycle of the Rhizocephala (Cirripedia). J Mar Biol Ass UK 75:517–550
Høeg JT, Lützen J (1985) Crustacea Rhizocephala. Marine invertebrates of Scandinavia 6. Norwegian University Press, Oslo, pp 1–92
Høeg JT, Lützen J (1995) Life cycle and reproduction of the Cirripedia Rhizocephala. Oceanogr Mar Biol Ann Rev 33:427–485
Høeg JT, Glenner H, Shields J (2005) Cirripedia Thoracica and Rhizocephala (barnacles). In: Rohde K (ed) Marine parasites. CABI Publishing, Wallingford UK and CSIRO Publishing, Collingwood, pp 154–165
Holthuis LB (1961) Report on a collection of Crustacea Decapoda and Stomatopoda from Turkey and the Balkans. Zool Verh 47:1–67
Innocenti G, Galil BS (2007) Modus vivendi: invasive host/parasite relations – Charybdis longicollis Leene, 1938 (Brachyura: Portunidae) and Heterosaccus dollfusi Boschma, 1960 (Rhizocephala: Sacculinidae). Hydrobiologia 590:95–101
Innocenti G, Galil BS (2010) Observations on parasite and epibiont prevalence in the Levantine population of the Erythrean alien portunid Charybdis longicollis Leene. Monog Mus Reg Sc Nat Torino 40:379–388
Innocenti G, Vannini M, Galil BS (1998) Notes on the behaviour of the portunid crab Charybdis longicollis Leene parasitized by the rhizocephalan Heterosaccus dollfusi Boschma. J Nat Hist 32:1577–1585
Innocenti G, Pinter N, Galil BS (2003) Observations on the agonistic behavior of the swimming crab Charybdis longicollis Leene infected by the rhizocephalan barnacle Heterosaccus dollfusi Boschma. Can J Zool 81:173–176
Kruse I, Hare MP (2007) Genetic diversity and expanding nonindigenous range of the rhizocephalan Loxothylaxus panopaei parasitizing mud crabs in the western north Atlantic. J Parasitol 93:575–582
Kuris AM (1974) Trophic interactions: similarity of parasitic castrators to parasitoids. Q Rev Biol 49:129–148
Kuris AM (1997) Conceptual framework for biocontrol of introduced marine pests. In: Proceedings of the first international workshop on the demography, impacts and management of introduced populations of the European crab, Carcinus maenas. Center for Research on Introduced Marine Pests. Tech Rep 11:66–68
Lazaro-Chavez E, Alvarez F, Rosas C (1996) Records of Loxothylacus texanus (Cirripedia: Rhizocephala), parasitizing the blue crab Callinectes sapidus, in Tarniahua Lagoon, Mexico. J Crust Biol 16:105–110
Leene JE (1938) The Decapoda Brachyura of the Siboga expedition VII. Brachygnatha: Portunidae. Siboga Expeditie 39:1–156
Lewinsohn C, Holthuis LB (1964) New records of decapod Crustacea from the Mediterranean coast of Israel and the eastern Mediterranean. Zool Meded Leiden 40:45–63
Lützen J (1984) Growth, reproduction, and life span in Sacculina carcini Thompson (Cirripedia: Rhizocephala) in the Isefjord, Denmark. Sarsia 69:91–106
Matsumoto K (1952) On the sacculinization of Charybdis japonica (A. Milne-Edwards). Biol J Okayama Univ 1:84–89
Miller A, Inglis GJ, Poulin R (2006) Comparison of the ectosymbionts and parasites of an introduced crab, Charybdis japonica, with sympatric and allopatric populations of a native New Zealand crab, Ovalipes catharus (Brachyura: Portunidae). NZ J Mar Freshw Res 40:369–378
Monod T (1938) Decapoda Brachyura Mission Robert Ph. Dollfus en Egypte. Mém Inst Egypte 37:91–162
Mouritsen KN, Jensen T (2006) The effect of Sacculina carcini infections on the fouling, burying behaviour and condition of the shore crab, Carcinus maenas. Mar Biol Res 2:270–275
Nair NB, Gurumani ON (1956) On the occurrence of three Sacculina parasitising the edible crab Neptunus sanguinolentus. J Bombay Nat Hist Soc 53:730–732
O’Brien J, van Wyk P (1985) Effects of crustacean parasitic castrators (epicaridean isopods and rhizocephalan barnacles) on the growth of their crustacean hosts. In: Wenner AM (ed) Crustacean growth: factors in adult growth, vol 3. Balkema Press, Rotterdam, pp 191–218
Øksnebjerg B (2000) The Rhizocephala (Crustacea: Cirripedia) of the Mediterranean and Black seas: taxonomy, biogeography and ecology. Isr J Zool 46:1–102
Øksnebjerg B, Enzenross R, Enzenross L (1997) First record of Rhizocephala (Crustacea: Cirripedia) from Turkish waters, with notes on Lessepsian migration. Stutt Beitr Naturk A 557:1–7
Overstreet RM (1983) Metazoan symbionts of crustaceans. In: Provenzano AJ Jr (ed) Pathobiology, the biology of Crustacea, vol 6. Academic, New York, pp 155–250
Özcan T, Katagan T, Kocatas A (2005) Brachyuran crabs from Iskenderun Bay (southeastern Turkey). Crustaceana 78:237–243
Pearse AS (1953) Parasitic crustaceans from Alligator Harbor, Florida. Q J Fla Acad Sci 15(4):187–243
Perez C, Basse E (1928) Sur un monstre double de Sacculine. Bull Soc Zool Fr 53:139–145
Phillips WJ, Cannon LRG (1978) Ecological observations on the commercial sand crab Portunus pelagicus (L.), and its parasite, Sacculina granifera Boschma, 1973 (Cirripedia: Rhizocephala). J Fish Dis 1:137–149
Pillai GCS, Thomas PA (1972) Frequency of occurrence of Heterosaccus indicus (Rhizocephala) on the edible crab Neptunus pelagicus in the Gulf of Mannar. J Mar Biol Ass India 14:867–869
Rainbow PS, Ford MP, Hepplewhite I (1979) Absence of gregarious settling behaviour by female cypris larvae of British parasitic rhizocephalan barnacles. J Mar Biol Ass UK 59:591–596
Rasmussen E (1959) Behaviour of sacculinized shore crabs (Carcinus maenas Pennant). Nature 183:479–480
Reinhard EG (1950) An analysis of the effects of a sacculinid parasite on the external morphology of Callinectes sapidus Rathbun. Biol Bull 98:277–288
Reinhard EG (1954) A case of conjoined twins in Loxothylacus (Crustacea, Rhizocephala). Proc Helminth Soc Wash 21:67–71
Ritchie LE, Høeg JT (1981) The life history of Lernaeodiscus porcellanae (Crustacea, Rhizocephala) and co-evolution with its porcellanid host. J Crust Biol 1:334–347
Shields JD (1992) Parasites and symbionts of the crab Portunus pelagicus from Moreton Bay, Eastern Australia. J Crust Biol 12:94–100
Sloan NA (1984) Incidence and effects of parasitism by the rhizocephalan barnacle, Briarosaccus callosus Boschma, in the golden king crab, Lithodes aequispina Benedict, from deep fjords in northern British Columbia, Canada. J Exp Mar Biol Ecol 84:111–131
Smith G (1906) Rhizocephala. Fauna Flora Golf Neapel Monogr 29:1–123
Srinivasagam S (1982) An instance of large scale parasitism of Heterosaccus dollfusi Boschma on the edible crab, Portunus sanguinolentus (Herbst) in Pulicat Lake. J Inland Fish Soc India 14:88–90
Stephensen K (1946) The Brachyura of the Iranian Gulf with an appendix: the male pleopoda of the Brachyura. In: Jessen K, Sparck R (eds) Danish scientific investigations in Iran, Part 4. Ejnar Munksgaard, Copenhagen, pp 57–237
Tattersall WM (1920) Sacculina and its effects on the host species. Rep Trans Manch Microsc Soc 1920:29–41
Thomson JM (1951) Catch composition of the sand crab fishery in Moreton Bay. Aust J Mar Freshw Res 2:37–244
Thresher RE, Werner M, Høeg JT, Svane L, Glenner H, Murphy NE, Wittwer C (2000) Developing the options for managing marine pests: specificity trials on the parasitic castrator, Sacculina carcini, against the European crab, Carcinus maenas, and related species. J Exp Mar Biol Ecol 254:37–51
Torchin ME, Lafferty KD, Dobson AP, McKenzie J, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630
Van Engel W, Dillon WA, Zwerner D, Eldridge D (1966) Loxothylacus panopaei (Cirripedia, Sacculinidae) an introduced parasite on a xanthid crab in Chesapeake Bay, U.S.A. Crustaceana 10:110–112
Veillet A (1945) Recherches sur le parasitisme des crabes et des galathées par les rhizocephales et les epicarides. Ann Inst Océanogr Monaco 22:193–341
Wardle WJ, Tirpak AJ (1991) Occurrence and distribution of an outbreak of infection of Loxothylacus texanus (Rhizocephala) in blue crabs in Galveston Bay, Texas, with special reference to size and coloration of the parasites’ external reproductive structures. J Crust Biol 11:553–560
Weng HT (1987) The parasitic barnacle, Sacculina granifera Boschma, affecting the commercial sand crab, Portunus pelagicus (L.), in populations from two different environments in Queensland. J Fish Dis 10:221–227
Wolfe LM (2002) Why alien invaders succeed: support for the Escape-from-Enemy Hypothesis. Am Nat 160:705–711
Yamaguchi T, Tokunaga S, Aratake H (1994) Contagious infection by the rhizocephalan parasite Sacculina sp. in the grapsid crab Hemigrapsus sanguineus (De Haan). Crustacean Res 23:89–101
Acknowledgements
The authors are deeply grateful to Jørgen Lützen for awakening their interest in this fascinating rhizocephalan barnacle, and to Marco Vannini for helpful suggestions throughout the years. The authors thank Daniela Friedmann, Mel Cooper, Limor Shoval, Eva Mizrahi and Kinneret Gal, IOLR, for their assistance in assembling the material.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2011 Springer Science+Business Media B.V.
About this chapter
Cite this chapter
Innocenti, G., Galil, B.S. (2011). Live and Let Live: Invasive Host, Charybdis longicollis (Decapoda: Brachyura: Portunidae), and Invasive Parasite, Heterosaccus dollfusi (Cirripedia: Rhizocephala: Sacculinidae). In: Galil, B., Clark, P., Carlton, J. (eds) In the Wrong Place - Alien Marine Crustaceans: Distribution, Biology and Impacts. Invading Nature - Springer Series in Invasion Ecology, vol 6. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-0591-3_20
Download citation
DOI: https://doi.org/10.1007/978-94-007-0591-3_20
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-007-0590-6
Online ISBN: 978-94-007-0591-3
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)