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Role of Ecdysteroids and Methyl Farnesoate in Morphogenesis and Terminal Moult in Polymorphic Males of the Spider Crab Libinia Emarginata

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Role of Ecdysteroids and Methyl Farnesoate in Morphogenesis and Terminal Moult in Polymorphic Males of the Spider Crab Libinia Emarginata Aquaculture 190Ž. 2000 103±118 www.elsevier.nlrlocateraqua-online Role of ecdysteroids and methyl farnesoate in morphogenesis and terminal moult in polymorphic males of the spider crab Libinia emarginata Guiomar Rotllant ), Peter Takac 1, Lei Liu 2, Grant L. Scott, Hans Laufer Department of Molecular and Cell Biology, UniÕersity of Connecticut, Storrs, CT 06269, USA Received 10 January 2000; received in revised form 23 March 2000; accepted 30 March 2000 Abstract Here we examine morphogenesis and terminal anecdysis in male morphotypes of the spider crab Libinia emarginata through eyestalk removalŽ. ablation . Methyl farnesoate Ž. MF , an unepoxidated form of juvenile hormoneŽ. JH III and hydroxyecdysone, a moulting hormone, were measured in attempt to understand these processes and to determine the physiological character- istics of each morphotype, to be able to induce maturation by hormonal treatment and improve crustacean culture. Following arrival at the laboratory, ablated small-claw unabraded small-cara- pace malesŽ. SUM moulted within 30 days to a juvenile and control SUM moulted within 75 days to a mature morphotype with large claws. Following eyestalk removal small-carapace abraded malesŽ. SAM , large-carapace unabraded large-claw Ž. LUL and large-carapace abraded large-claw Ž.LAL males never moulted even after 60 days, while the other ablated morphs moulted in 25±35 days. Significant increase of MF levels was observed in SUM, SAM and LUL de-stalked animals compared to intact control group, while no differences were observed in LAL individuals. In fact, LAL crabs presented the highest level of MF up to 2.23 ngrml. Ten days prior to moulting MF increased 4-fold, and the ecdysteroids increased 15-fold in the haemolymph of ablated SUM and 25% in their testes. Ecdysteroid levels in the haemolymph of the SAM, LUL and LAL ) Corresponding author. Present address: Institut de CienciesÁÂ del Mar, C.S.I.C. Passeig Joan de Borbo, srn, E-08039 Barcelona, Spain. E-mail addresses: [email protected]Ž. G. Rotllant , [email protected] Ž. P. Takac , [email protected] Ž.L. Liu , [email protected] Ž H. Laufer . 1 Present address: Institute of Zoology, Slovak Academy of Sciences, Dubravska cesta, 9, SK-842 06 Bratislava, Slovak Republic. 2 Present address: W.M. Keck Center for Comparative and Functional Genomics, University of Illinois at Urbana-Champaign, 330 Edward R. Madigan Laboratory, 1201 W. Gregory Drive, Urbana, IL 61801, USA. 0044-8486r00r$ - see front matter q2000 Elsevier Science B.V. All rights reserved. PII: S0044-8486Ž. 00 00388-4 104 G. Rotllant et al.rAquaculture 190() 2000 103±118 morphotypes remained lowŽ. around 5 ngrml , and none of these animals moulted. The results strongly suggest that:Ž. 1 SUM are able to moult, and represent the juvenile stage, Ž. 2 SAM, LUL and LAL are terminally moulted and may represent the reproductive population,Ž. 3 circulating ecdysteroids induce moulting in juveniles,Ž. 4 high levels of ecdysteroids in the testes of SAM, LUL and LAL suggest a gonadal function, andŽ. 5 circulating MF controls morphogenesis of juvenilesŽ. SUM and seems to stimulate gonads in adults. q 2000 Elsevier Science B.V. All rights reserved. Keywords: Spider crab; Morphogenesis; Terminal moult; Ecdysteroids; Methyl farnesoate 1. Introduction While many species of decapod crustaceans continue to moult and grow throughout their lives, others, like spider crabsŽ. Majidae undergo an allometric differentiation of the chelae when they moult to maturity and become anecdysicŽ Teissier, 1933, 1935; Hartnoll, 1963; Conan and Comeau, 1986; Conan et al., 1988; Comeau et al., 1991. However, some authors propose that the large species of spider crabs such as Chionoe- cetes, continue to moult after reaching the large claw form. This is based on the finding of morphometrically mature males that had well developed second carapaces, indicating imminent moultingŽ. Somerton, 1981; Dawe et al., 1991 , and from long-term captivity experiments that allow morphometrically mature male Chionoecetes bairdi to moult after 26±27 months of captivityŽ. Paul and Paul, 1995 . The terminal moult is not necessarily a maturational moult, because spermatophores may be present in the sperm duct of male spider crabs prior to this moult. In Libinia emarginata, HinschŽ. 1972 reported that males with a carapace length Ž. CL of 19 mm had sperm that is morphologically indistinguishable from that of mature males. The different male morphotypes of the spider crab present differences in the size and weight of the reproductive system, morphological features of the carapace and reproductive behaviourŽ. Homola et al., 1991; Sagi et al., 1994 . Crabs are anecdysic after they have undergone a terminal moult, and are therefore incapable of additional moulting. It has been proposed that the Y-organs may degenerate or become permanently inhibited following this moult. CarlisleŽ. 1957 noted a reduction in the size of the Y-organs after the moult to puberty in Maia squinado, and this gland is not present after the onset of sexual maturity in Pisa tetradon ŽVernet-Cornubert, 1958, 1960. In Acanthonyx lunulatus, histology of the Y-organs revealed that these degenerate completely after the terminal moultŽ. Chaix et al., 1976 . In the isopod Sphaeroma serratum the concentration of 20-hydroxyecdysone and the size of the Y-organs also decrease after the onset of sexual maturityŽ Charmantier et al., 1977; Charmantier and Trilles, 1979.Ž. Furthermore, eyestalk removal ablation initiates ecdysis in juvenile P. tetradon and L. emarginata but not in the adultsŽ Vernet-Cornu- bert, 1960; Hinsch, 1972. Generally, haemolymph ecdysteroid content is higher in young crabs than in mature malesŽ. Cormier et al., 1992; Laufer et al., 1993 . In addition, ecdysteroids have been identified in the ovaries and eggs of Parapenaeus fissurus ŽJeng et al., 1978.Ž.Ž , Penaeus monodon Young et al., 1993 , Palaemon serratus Spindler et al., 1987.Ž , Macrobrachium rosenbergii Wilder et al., 1991; Young et al., 1991 . , G. Rotllant et al.rAquaculture 190() 2000 103±118 105 Homarus americanus Ž.ŽLisk, 1961; Couch et al., 1987 , H. gammarus Goudeau et al., 1990.Ž.Ž , Nephrops norÕegicus Fairs et al., 1989 and A. lunulatus Chaix and De Reggi, 1982.Ž. , and in the testes of H. americanus Burns et al., 1984 and L. emarginata Ž.Laufer et al., 1993 . Bilateral extirpation of the stalked eyes not only resulted in an accelerated moult but has been shown to delay metamorphosis in larvae by the production of extra larval stages in shrimp, Palaemon macrodactylus Ž.Little, 1969 and Palaemonetes Õarians ŽLe Roux, 1984.Ž. ; the lobster H. americanus Charmantier et al., 1988 ; and intermediate stages in crabs, Rhithropanopeus harisii Ž.Costlow, 1968 , and Sesarma reticulatum Ž.Costlow, 1966; Freeman and Costlow, 1980 . The endocrine control of morphogenesis in crustaceans is not well understood, but evidence suggests that inhibitory factors from the sinus glands in the eyestalks are involved. Morphogenesis and reproduction in crustaceans seem to be regulated by a juvenile hormoneŽ. JH , as in insects. The JH-like compound, methyl farnesoate Ž MF . , synthe- sized and secreted by the mandibular organŽ. MO functions in adult crustaceans in a manner similar to its function in adult insects, that is JHs seem to stimulate reproduction in both males and femalesŽ. Laufer et al., 1987; Laufer et al., 1988; Homola et al., 1991 . Synthesis of MF in MOs is negatively regulated by factors from sinus glandsŽ. SG Ž.Laufer et al., 1987, 1989 . These factors are called mandibular organ inhibiting hormonesŽ. MOIHs , and they have recently been isolated from the sinus gland, sequenced and cloned in L. emarginata Ž.Liu and Laufer, 1996; Liu et al., 1997a,b and in Cancer pagurus Ž.Wainwright et al., 1996 . The present study uses eyestalk ablation to induce moulting. Ecdysteroids and MF levels were measured to determine which male morphotypes in L. emarginata are anecdysic and sexually mature. 2. Material and methods 2.1. Animals L. emarginata were collected in two locations, off the coast 2 km south of Woods Hole, MA and 1 km north of Vineyard Haven harbour, Martha's Vineyard, during the summers of 1993 and 1994; and 2±4 km off shore from New London, CT during the summer of 1995. Male morphotypes were identified and selected according to the length of their carapaceŽ. CL , small Ž CL-60 mm . or large Ž CL)60 mm . ; the condition of their exoskeleton, abradedŽ. old shell or unabraded Ž new shell . ; and claw Ž. propodus lengthsŽ.Ž.Ž. PL , small PL-CL or large PL)CL . Hence, the following nomenclature was used: SUMssmall-claw, unabraded, small-carapace male, with flexible exoskele- ton covered with a scaly epicuticle; LULslarge-carapace, unabraded, large-claw male; LALslarge-carapace, abraded, large-claw male; and SAMssmall-carapace, abraded, males, with heavily calcified exoskeleton. A total of 1402 animals were measured Ž.carapace and propodus length , weighed and tagged, then held in tanks in the facilities of the Marine Biological LaboratoryŽ. Woods Hole, MA , or in the Marine Biological Laboratory of the University of ConnecticutŽ. Noank, CT . They were maintained separately in individual plastic cages on a shallow sea-table supplied with fresh running 106 G. Rotllant et al.rAquaculture 190() 2000 103±118 seawater at ambient temperatureŽ. 18"28C and salinity Ž 33.0"1 ppt . The crabs were fed with fresh or frozen squid every other day ad libitum. The animals were divided into two groups: intact eyestalk controlsŽ. 742 , and eyestalk-ablatedŽ. 660 . Eyestalks were removed with forceps after the crabs had been chilled on ice for 30 min; then the wounds were cauterized immediately to reduce mortality due to possible infection and bleeding. Eyestalk removal caused around 20% of mortality. Haemolymph samples and testes were taken from animals that were sacrificed on day 1 of the experiment and at various intervals up to day 73.
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