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Jeopardy: Host and Parasite Lessepsian Migrants from The JounNar op Narunal Hrsronv, 1998, 32, 1549-1551 Jeopardy: host and parasite lessepsianmigrants from the Mediterranean coast of Israel B. S. GALTLf and J. LUTZEN+ f Isruel Oceanographicand Limnological Research, Jt.iationalInstitute oJ' Oceanography,P.O.B. 8030, Haifa 31080, Israel f Department oJ'Cell Biology and Anatomy, Zoological Institute, Universitetsparken 15, DK-2 100 Copenhagen,Denmark (Accepted:8 May 1998) Knvwonos: Crustacea,population dynamics, Lessepsian migration, Charybdis longicollisLeene, Heterosaccus dollfusi Boschma. The defining feature of the fauna off the Mediterranean coast of Israel has been the mass establishment of migrant speciesfrom the Red Sea that entered through the SuezCanal. Of approximately 300 speciesthat have been identified as Lessepsian migrants, 40 are decapod crustaceans (Galil , 1992). Churybdis longicollis Leene, found in the Red Sea (Leene, 1938), the Persian Gulf (Stephensen, 1946) and Madagascar (Guinot, 1966), was first recorded in the Mediterranean in 1954 from the Bay of Mersin, Turkey (Holthuis, L961). Since then, it has been recorded all along the Levant coast, from Egypt to the southern coast of Turkey (Lewinsohn and Holthuis, 1986). Off the Israeli coast, C. longicollis is common on sandy-mud bottoms at25 60m and occasionallydeeper, to a record of l35m (Galil, 1992).Of the thousands of specimens of C. longicollis collected off the Israeli coast in over three decades,none was parasitized until 1992. Among the C. longicollis collected off Palmahim in October of 1992, a few had bulging yellow protuberancescarried beneath the abdomen. Those protrusions were identified as the externaeof a sacculi- nid rhizocephalan, Heterosaccusdollfu,ri, Boschma, previously known only from a few specimensfrom the Gulf of Suez (Galil and LliJ.tzen,1995). This is the first reported instanceof Lessepsianmigration by a rhizocephalan.Subsequent collections at the same site in October 1993 and May and November 1994, conflrmed its presence(Galil and L;jtzen, 1995). In March 1995,H. dollfusi was found infesting C. longicollis on the easternmostpart of the Anatolian coast (Enzenross, personal communication). lt seems that although the host crab had immigrated to the Mediterranean over forty years ago, the parasite has appeared only recently and is spreading rapidly. C. longicollis specimenswere collected in October 1993 and in May and November 1994by the RiV Shikmona with a 1.15m wide beam trawl at depths of 31 36m in the course of a monitoring programme of a marine sewage outlet at Palmahim (Galil andLiJtzen, 1995). Each samplewas made up of l6 trawls of identical duration, taken within a limited area. The material from all trawls was pooled. A total of 1l 15 Charybdlsspecimens was examined.Among these,345 were 0022-2933198$12.00 O 1998 Taylor & Francis Ltd. I 550 B. S. Galil and J. Lirzen externae-bearingcrabs and 81 were morphologically modified pre-externalinfections. The incidence of infection varied among the samples from an overall infection of 23.9% in October 1993 and 31.6o/nin November 1994, to 62.4% in May 1994.The infection rate recorded from Palmahim is very high compared with levels reported for other infected portunid hosts. Pillai and Thomas ( 1972) found that I2.2'h of l\,leptunuspelagicus (Linnaeus, l75B) from the Gulf of Mannar, India, were infected by Heterosaccusindicus Boschma, l95l.In Lake Pulicat, 17.5%of Portunussanguin- olentus(Herbst) were infectedby H.ruginosus Boschma,l93l (Srinivasagam,1982; fide Galil and L:d;tzen,1995). H. dollfusi forms a vegetative interna consisting of numerous microscopic roots. The late stageof the interna forms a bud of the externa, that breaks through the host's skin and forms a flattened, semicircular disc. The immature externa, at first flat and milky-white, becomesdistended and turns cream- coloured. After producing its first batch of eggs, the externa is mature, its cuticle coarsensand its colour darkens to burnt orange. When the externa dies, it withers and drops off, leaving a circular, dark scar behind, marking the base of the lost externa stalk. Charting the distribution of H. dollfusi developmental stagesagainst the phasesof the host's ecdysial cycle, it was apparent that buds and most virginal and immature externaeoccur in the stagefollowing the moult, whereasold externae are always associatedwith the last phase of the crab's moulting cycle. The relative number of buds, virginal and immature externae in May is twice that in October, whereas old externae and scars are proportionally more numerous in lall samples. This indicates that emergence occurs mostly in spring, presumably continues throughout the summer and decreasesin fall. Eighty-six per cent of mature externae were found to be ovigerous. Since one or two days pass betweenemission of nauplii and the next oviposition, this means that practically all externaewere reproducing in both the spring and fall. The abdomen of both sexesof infected Charybdis is modified to such an extent that the sexual apertures remain the only reliable sex criterion. Infection of the females causesthe loss of the swimmerets.Males acquire mobility of the normally fused abdominal segments,lose the copulatory appendages, and the entire abdomen broadens and closely resemblesthat of a mature female. The shape of the crab's modified abdomen perfectly matches the shapeand the size of a singlemature externa,offering it optimal protection. When two or more externae are present on the same crab, their individual size decreasesconsiderably, but their cumulative weight increasescompared to singleparasites. There is a positive correla- tion between the size of the host and the total weight of externae,whether single or multiple. Multiple infections occur most frequently among the younger crabs, pre- sumably becauseby placing a high nutritional demand on the host, they weaken it, and in many cases,cause its untimely death. Multiple infections are much more common in spring than in fall, and rise with increasedincidence of infestation. Thus, in the samplecollected in May 1994,incidence of infestation is 62.6% and percentage of multiple infestation is 52oh,whereas in November 1994 the corresponding values are 37.6"h and23.5u/u.Sloan ( 19S4)noted that multiple infestation was more frequent in crowded populations and attributed it to simultaneous infection. Our results suggest that multiple infestation may be related to incidence of infestation, and occurs more frequently when the host population is heavily infested. Contagious distributions were noted in Callinectespopulations in the Gulf of Mexico (Lazaro' Chavez et al., 1996; Alvarez and Calderon, 1996) and may be due to the aggregated pattern of distribution of the crabs. The rapid spread and the high prevalence of H. dollJusi infestation can be ascribed to the dense population of the host and the Jeopardy: host and parasitelessepsian migrants from Israel 1551 year-round reproduction of the parasite, causing recurrent infection. As heavily- infested populations are presumably maintained by immigration (Kuris, 1974, Yamaguchr et al., 1994), it is possible that the Levantine population of C. longicollis, effectively isolated from its Indian Ocean source, will suffer drastic perturba- tions, as it is doubtful that immigration of non-infested crabs through the Suez Canal suffices for population renewal. Lessepsian migration affords us the unique opportunity of testing nature in nature. In this case, a game of Jeopardy is played out between host and parasite. References ALVAREz, F. and CatonRoN, J., 1996, Distribution of Loxothylacus texanzzs(Cirripedia: Rhizocephala) parasitrzing crabs of the genus Callinectes in the Southwestern Gulf of Mexico, Gulf Research,Reporrs, 9 (3), 205-210. GALIL, B. S., 1992, Eritrean decapods in the Levant. Biogeography in motion, Bulletin de I'Institut de Oceanographie,Monaco,9, ll5 I23. GaLn, B. S. and LurzEN, J.,1995, Biological observationson HeterosaccusdollJusi Boschma (Cirripedia: Rhizocephala), a parasite of Charybdis longicollis Leene (Decapoda: Brachyura), a lessepsianmigrant to the Mediterranean, Journal oJ'Crustacean Biology, ls (4), 6s9 670. GutNor, D., 1966, La faune carcinologique (Crustacea Brachyura) de I'Ocean Indien occi- dental et de la Mer Rouge. Catalogue, remarques biogeographiqueset bibliographie, Memoires de I'Institut Frangaisde I'Afrique Noire,77,235 352. Hot-tuuts, L. 8., 1961, Report on a collection of Crustacea Decapoda and Stomatopoda from Turkey and the Balkans, Zoologische Verhandelingen,4T,| 61. KuRIs, A. M., 1974, Trophic interactions: similarity of parasite castrators to parasitoids, Quarterly Review of Biology, 49, I29 148. Llznno-Cr.AvEZ, E., Ar-vnREZ,F. and RosrrS,C., 1996, Records of Loxothylucus texanus (Cirripedia:Rhizocephala), parasitizing the blue crab Callinectes sapidus, in Tamiahua Lagoon, Mexico, Journal of CrustaceanBiology, 16 (1), 105 110. LunNn,J. E., 1938, The Decapoda Brachyura of the Siboga Expedition. VII. Brachygnatha: Portunidae, Siboga Expedition, 31 (C3), I 156. LnwtNsouN, C. and HoLtuuts, L. B. 1986,The CrustaceaDecapoda of Cyprus, Zoologische Verhandelingen,230, | 64. PILLat, G. C. S. and Tuouns, P. A., 1972, Frequency of occurrenceof Heterosaccusindicus (Rhizocephala) on the edible crab Neptunuspelagicus in the Gulf of Mannar, Journal oJ Marine Biological Association,India, 14 (2),867 869. SLoAN, N. A., 1984, Incidence and effects of parasitism by the rhizocephalan barnacle, Briarosac'cuscallosus Boschma, in the golden king crab, Lithodes aequispina Benedict, from deepfiords in northern British Columbia, Canada, Journal of ExperimentalMarine Bblogy and Ecology,84, I I 1-131. SRtNtvrrs'rcAM,S., 1982,An instanceof large scaleparasitism of Heterosaccusdollfusi Boschma on the edible crab, Portunus sanguinolentus(Herbst) in Pulicat Lake, Journal of Inland Fishery Society, India, 14, 88 90. SrrpusNspN,K., 1946,The Brachyura of the lranian Gulf, Dan. Sci.Invest. Iran,4,57-237. YnnncucHl, T., ToruNaca, S. and ARRrarn, H., 1994,Contagious infection by the rhizoce- phalan parasite Sacculina sp. in the grapsid crab Hemigrapsu.;sanguineu,s (De Haan), Cru,staceanResearch- 23- 89 101..
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