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Mating behavior and methyl farnesoate levels in male morphotypes of the spider crab, Libinia emarginata (Leach)
Journal
ELSEVIER
of Experimental Marine Biology 193 (1995) 15-20
and Ecology
JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY
Mating behavior and methyl farnesoate levels in male morphotypes of the spider crab, Libinia emarginata (Leach) Hans
Laufer*,
Jonna
S.B. Ah1
Department of Molecular and Cell Biology, University of Connecticut, Box U-125, 75 North Eagleville Rd., Storrs, CT 06269-3125, USA Marine Biological Laboratory. Woods Hole, MA 02543, USA
Abstract
We presently recognize at least six male morphotypes in Libinia emarginata which differ with respect to their appearance and reproductive behavior. The primary reproductives have a large carapace, large claws and their exoskeletal epicuticle is worn away, giving them an “abraded” appearance. These animals also have large reproductive system indices (RI), and high methyl farnesoate (MF) blood levels. Smaller abraded males with short claws do not compete with the larger aggressive ones, but employ alternative tactics such as “sneak mating” and female mimicry. They also have large RIs and high levels of MF in their blood. Unabraded morphs of any size do not attempt to mate. Their MF levels are lower (usually one half that of the abraded males) as are their RIs, suggesting that they are in a state of reproductive diapause. Incompletely abraded males have intermediate levels of MF and will attempt mating in the absence of the large-claw abraded ones. This relationship between behavior and hormone level suggests that MF may be involved in determining the type of mating behavior displayed by the different male morphotypes. Keywords:
Libinia
emarginata;
Male morphotypes;
Methyl farnesoate;
Mating strategies
In Crustacea, the existence of different types of males within a species that exhibit different patterns of mating behavior have been described for several decapods, such as, the amphipod Jassa fulcutu (Borowsky, 1983, the freshwater prawn Mucrobruchium rosenbergii (Ra’anan and Sagi, 1985), the isopod Paracerceis sculpta (Shuster, 1987), the snow crab Chionoecetes opilio (Conan and Comeau, 1986), the Tanner crab Chionoecetes bairdi (Donaldson and Adams, 1989), and the spider crab Libinia emurginutu (Laufer et al., 1992). These mating
* Corresponding
author.
0022-0981/95/$09.50 0 1995 Elsevier SSDI 0022-0981(95)00107-7
Science
B.V. All rights
reserved
16
H. Laufer. J.S.B.
Ahl I J. Exp. Mar. Bid.
Ecol. 193 (1995) 15-20
patterns have been explained mostly from an ethological perspective based upon the physical differences of the morphotypes, and less from the standpoint of their physiology. It has been well established that hormones play an important role in the regulation of behavior in vertebrates. In particular, sex hormone levels are closely related to variations in reproductive system size and mating behavior. For invertebrates, the trend is similar, having been described most commonly in insects. Differences in mating behavior have been attributed to varying levels of juvenile hormone (JH) in the hemolymph (DeWilde, 1983; Denlinger, 1985). Moreover, JH controls development and the onset of reproduction, and is associated with polymorphisms in aphids, bees and termites (Nijhout and Wheeler, 1982) but very little is known about the relationship of hormones and behavior in crustaceans. In this paper, we review our work on methyl farnesoate (MF) and its possible relationship to mating strategies among male morphotypes of the spider crab Libinia emarginatu (Leach). Methyl farnesoate is an unepoxidated form of JH III in insects (Laufer et al., 1987), that has been found in the hemolymph of both sexes in more than 20 crustacean species (Laufer et al., 1987; Sagi et al., 1991). Similar to JH, MF may play a role in reproduction, being found in Libiniu emarginata males that have the largest reproductive systems (Homola et al., 1991; Laufer et al., 1992) and in females that are undergoing vitellogenesis (Laufer et al., 1986, 1987). Male spider crabs are markedly polymorphic regarding the length of their claws (CL) (Hartnoll, 1963; (propodus) (PL) re 1a t ive to the length of their carapace Aldrich, 1974; Homola et al., 1991), and the condition of the epicuticle covering their exoskeleton (Homola et al., 1991; Sagi et al., 1993). There are large bodied males (60-80 mm CL) with claws longer than their carapace (70-100 mm PL) that are covered with a pubescent epicuticle (unabraded), which indicates that the animal has recently molted, or the epicuticle has been partially or completely worn off (abraded). There are large bodied unabraded males with claws shorter than the carapace length, as well as, small bodied (<60 mm CL) males, with either abraded or unabraded exoskeletons, that have short claws. Sexual maturation in male spider crabs takes place when the animals are still quite small (219 mm CL) (Homola et al., 1991) as evidenced by the presence of sperm in their vas deferens (Hinsch, 1972). However, the display of mating behavior and attempts at copulation with a receptive female is quite variable among the different morphotypes. The primary reproductives are the large-bodied abraded males with long claws (Homola et al., 1991). These males actively compete with each other for the opportunity to mate with a receptive female. The winner of such a competition, after mating, will use his last pair of walking legs to carry the female behind him and will continue to guard her from take-over by another male until she releases the next clutch of fertilized eggs. Males with large claws which are incompletely abraded attempt copulation if isolated with a receptive female, but do not compete with abraded males. The presence of a partially worn epicuticle indicates that this type of male has
H. Laufer,
J.S.B. Ah1 I J. Exp. Mar. Biol. Ecol. 193 (1995) 15-20
17
undergone the final molt fairly recently, and probably is participating in the mating season for the first time. In contrast, the primary reproductives are most likely experiencing their second mating season, suggests that perhaps prior experience, and/or higher MF levels, contribute to their mating success. Small abraded males, approximately the same size as a mature female (30-55 mm CL), exhibit the female-like behavior of being passive in the presence of the large-claw abraded males. We have also observed small abraded males being carried by primary reproductives. These small males, which appear to “mimic” females, avoid aggressive behavior from the primary reproductives, and may be able to increase their mating opportunities by “sneak” mating. Indeed, on one occasion, we observed a small male, that was being carried, grasp a receptive female, with which he then commenced to copulate (Sagi et al., 1994). Unabraded males of any size do not exhibit any mating behavior, even when isolated with a receptive female. The differences in mating activity among the male morphotypes of Libinia emarginatu can be explained partly in terms of reproductive readiness with respect to the size of the reproductive system. The males that mate, either in competition or in isolation, all have relatively large reproductive system indices (RI) (Fig. 1). The abraded males, both large and small, have the largest RIs, 2.32 ? 0.03 and 2.86 + 0.35, respectively. The large-claw incompletely abraded males have intermediate sized RIs (1.73 t 0.06). The unabraded males of any size have considerably smaller RIs, (0.20-0.72). The levels of MF in the hemolymph of male morphotypes vary in a manner
RI in male morphs
3’5w 3.0 2s
-
201.5 1.0 0.6 -
Fig. 1. Reproductive indices in male morphotypes of the spider crab Libinia emarginata. SUS, small carapace unabraded small-claw; SAS, small carapace abraded small-claw; LUS, large carapace unabraded small-claw; LUL, large carapace unabraded large-claw; LIL, large carapace incompletely abraded large-claw; LAL, large carapace abraded large-claw.
18
H. Laufer, J.S.B.
Ah1 I J. Exp. Mar. Biol. Ecol. 193 (1995) 15-20
MF levels in male morphs
SJS Fig. 2. Hemolymph emarginafa. Labels
549
LUS
levels of methyl farnesoate on abscissa are as in Fig. 1.
LUL in male
LIL
morphotypes
LAL of the
spider
crab
Libinia
similar to the RIs (Fig. 2). Both of the completely abraded types have the highest MF levels, 39.7 f 2.09 ng ml -’ in the large-claw males and 40.3 t 9.3 ng . ml- ’ in the small males. The incompletely abraded males have intermediate MF levels, 24.2 + 0.82 ng* mll’, and all of the unabraded males have low levels, 15.8-16.0 ng.mll’. The apparent absence of mating behavior in the unabraded males, which also have small RIs and low MF levels, probably reflects a state of reproductive diapause. In insects, reproductive diapause occurs in pre-reproductives and in adults during the non-breeding season and is characterized by low JH levels in the blood and small RIs (DeWilde, 1983; Denlinger, 1985). Small-claw unabraded males have not yet undergone their terminal molt and are still growing. If mating is delayed so that energy can be invested in growth, then the result is a larger body and claw size that ultimately enhances mating success (Sagi et al., 1988). This then may explain why small unabraded males do not attempt to mate, even though sperm have been produced. The large unabraded males, on the other hand, have undergone their final molt and reached their maximal external size. However, their internal organs are approximately the same size as prior to the molt. Again, energy is used for growth and to build up the reproductive system prior to the commencement of the energetically expensive processes of competing for females and mating. The data and observations we have presented suggest that in Crustacea, as in insects, differences in mating behavior and activity vary with the relative size of the reproductive system and with hormone level. Crustaceans differ from insects, however, in that maturation of the reproductive tract is interspersed with periods
H. Laufer, J.S.B.
Ah1 I J. Exp. Mar. Biol. Ecol. 193 (1995)
15-20
19
of growth, sperm sometimes being present even in relatively very small males. We conclude that MF may be a reproductive hormone, although the exact mechanism by which MF works remains to be elucidated.
Acknowledgements
We would like to thank David Dodge and the staff of the New England Utilities Environmental Laboratory at Millstone Power Plant in Niantic, CT, for the collection of Libinia emarginatu, Dr. Maury of the University of Connecticut Biotechnology Center for technical advice, and for use of the center’s HPLC facilities. This work was supported in part by the Connecticut Sea Grant College Program, NOAA, U.S. Dept. of Commerce, an economic development grant from the Office of the Provost, The University of Connecticut, and a Fellowship of the Lady Davis Trust to H.L.
References Aldrich, J.C., 1974. Allometric studies on energy relationships in the spider crab Libinia emarginata (Leach). Biol. Bull. Woods Hole Mass., Vol. 147, pp. 257-273. Borowsky, B., 1985. Differences in reproductive behavior between two male morphs of the amphipod crustacean Jassa falcata Montagu. Physiol. Zool., Vol. 58, pp. 497-502. Conan, G.Y. and M. Comeau, 1986. Functional maturity and terminal molt of the male snow crab, Chionoecetes opilio. Can. J. Aquat. Sci., Vol. 43, pp. 1710-1719. Denlinger, D.L., 1985. Hormonal control of diapause. In, Comparative insect physiology, biochemistry, and pharmacology, Vol. & Endocrinology II, edited by G.A. Kerkut & L.I. Gilbert, Pergamon Press, New York, pp. 353-412. DeWilde, J., 1983. Endocrine aspects of diapause in the adult stage. In, Invertebrate endocrinology, Vol. 1: Endocrinology of insects, edited by R.G.H. Downer & H. Laufer, A.R. Liss, Inc., New York, pp. 357-368. Donaldson, W.E. and A.E. Adams, 1989. Ethogram of behavior with emphasis on mating for the Tanner crab Chionoecetes bairdi Rathbun. J. Crust. Biol., Vol. 9, pp. 37-53. Hartnoll, R.G., 1963. The biology of the Manx spider crabs. Proc. 2001. Sot. London, Vol. 141, pp. 432-496. Hinsch, G.W. 1972. Microtubules in the sperm of the spider crab, Libinia emarginata. J. Ultrastruct. Res., Vol. 29, pp. 525-534. Homola, E., A. Sagi and H. Laufer, 1991. Relationship of claw form and exoskeleton condition to reproductive system size and methyl farnesoate in the male spider crab, Libinia emarginata. Invert. Reprod. Dev., Vol. 20, pp. 219-225. Laufer, H., D. Borst, F.C. Baker, C. Carrasco, M. Sinkus, C.C. Reuter, L.W. Tsai and D.S. Schooley, 1987. Identification of a juvenile hormone-like compound in a crustacean. Science, Vol. 235, pp. 202-205. Laufer, H., M. Landau, D. Borst and E. Homola, 1986. The synthesis and regulation of methyl farnesoate, a new juvenile hormone for crustacean reproduction. Advances in invertebrate reproduction.Vol. 4, edited by M. Porchet, J.C. Andries and A. Dhainaut, Elsevier Science Pub]., Amsterdam, pp. 135-143. Laufer, H., A. Sagi and J.S.B. Ahl, 1992. Juvenile hormone-like compounds in Crustacea and their implications for reproductive behavior. Advances in regulation of insect reproduction, edited by B. Bennettova, I. Gelbic and T. Soldan, Institute of Entomology, Czech Acad. Sci., pp. 153-155.
20
H. Laufer, J.S.B.
Ah1 I J. Exp. Mar. Biol. Ecol. 193 (1995) 15-20
Nijhout, H.F. and D.E. Wheeler, 1982. Juvenile hormone and the physiological basis of insect polymorphisms. Quart. Rev. Biol., Vol. 57, pp. 109-133. Ra’anan, Z. and A. Sagi, 1985. Alternative mating strategies in male morphotypes of the freshwater prawn Macrobrachium rosenbergii (deMan). Biol. Bull., Vol. 196, pp. 592-601. Sagi, A., J. Ahl, H. Danaee and H. Laufer, 1991. Methyl farnesoate and reproductive behavior in male morphotypes of the spider crab Libinia emarginata. Am. Zool.,Vol. 31, p. 87A. Sagi, A., J.S.B. Ahl, H. Danaee and H. Laufer, 1994. Methyl farnesoate levels in male spider crabs exhibiting active reproductive behavior. Horm. Behav., Vol. 28, pp. 261-272. Sagi, A., E. Homola and H. Laufer, 1993. Distinctive reproductive types of male spider crabs Libinia emarginatu differ in circulating and resynthesizing methyl farnesoate. Biol. Bull., Vol. 185, pp. 168-173. Sagi, A., Y. Milner and D. Cohen, 1988. Spermatogenesis and sperm storage in the testes of the behaviorally distinctive male morphotypes of Macrobrachium rosenbergii (Decapoda, Palaemonidae). Biol. Bull., Vol. 174, pp. 330-336. Shuster, S.M., 1987. Alternative reproductive behaviors: three discrete male morphs in Paracerceis sculpta, an intertidal isopod from the northern Gulf of California. J. Crust, Biol.,Vol. 7, pp. 318-327.
ELSEVIER
of Experimental Marine Biology 193 (1995) 15-20
and Ecology
JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY
Mating behavior and methyl farnesoate levels in male morphotypes of the spider crab, Libinia emarginata (Leach) Hans
Laufer*,
Jonna
S.B. Ah1
Department of Molecular and Cell Biology, University of Connecticut, Box U-125, 75 North Eagleville Rd., Storrs, CT 06269-3125, USA Marine Biological Laboratory. Woods Hole, MA 02543, USA
Abstract
We presently recognize at least six male morphotypes in Libinia emarginata which differ with respect to their appearance and reproductive behavior. The primary reproductives have a large carapace, large claws and their exoskeletal epicuticle is worn away, giving them an “abraded” appearance. These animals also have large reproductive system indices (RI), and high methyl farnesoate (MF) blood levels. Smaller abraded males with short claws do not compete with the larger aggressive ones, but employ alternative tactics such as “sneak mating” and female mimicry. They also have large RIs and high levels of MF in their blood. Unabraded morphs of any size do not attempt to mate. Their MF levels are lower (usually one half that of the abraded males) as are their RIs, suggesting that they are in a state of reproductive diapause. Incompletely abraded males have intermediate levels of MF and will attempt mating in the absence of the large-claw abraded ones. This relationship between behavior and hormone level suggests that MF may be involved in determining the type of mating behavior displayed by the different male morphotypes. Keywords:
Libinia
emarginata;
Male morphotypes;
Methyl farnesoate;
Mating strategies
In Crustacea, the existence of different types of males within a species that exhibit different patterns of mating behavior have been described for several decapods, such as, the amphipod Jassa fulcutu (Borowsky, 1983, the freshwater prawn Mucrobruchium rosenbergii (Ra’anan and Sagi, 1985), the isopod Paracerceis sculpta (Shuster, 1987), the snow crab Chionoecetes opilio (Conan and Comeau, 1986), the Tanner crab Chionoecetes bairdi (Donaldson and Adams, 1989), and the spider crab Libinia emurginutu (Laufer et al., 1992). These mating
* Corresponding
author.
0022-0981/95/$09.50 0 1995 Elsevier SSDI 0022-0981(95)00107-7
Science
B.V. All rights
reserved
16
H. Laufer. J.S.B.
Ahl I J. Exp. Mar. Bid.
Ecol. 193 (1995) 15-20
patterns have been explained mostly from an ethological perspective based upon the physical differences of the morphotypes, and less from the standpoint of their physiology. It has been well established that hormones play an important role in the regulation of behavior in vertebrates. In particular, sex hormone levels are closely related to variations in reproductive system size and mating behavior. For invertebrates, the trend is similar, having been described most commonly in insects. Differences in mating behavior have been attributed to varying levels of juvenile hormone (JH) in the hemolymph (DeWilde, 1983; Denlinger, 1985). Moreover, JH controls development and the onset of reproduction, and is associated with polymorphisms in aphids, bees and termites (Nijhout and Wheeler, 1982) but very little is known about the relationship of hormones and behavior in crustaceans. In this paper, we review our work on methyl farnesoate (MF) and its possible relationship to mating strategies among male morphotypes of the spider crab Libinia emarginatu (Leach). Methyl farnesoate is an unepoxidated form of JH III in insects (Laufer et al., 1987), that has been found in the hemolymph of both sexes in more than 20 crustacean species (Laufer et al., 1987; Sagi et al., 1991). Similar to JH, MF may play a role in reproduction, being found in Libiniu emarginata males that have the largest reproductive systems (Homola et al., 1991; Laufer et al., 1992) and in females that are undergoing vitellogenesis (Laufer et al., 1986, 1987). Male spider crabs are markedly polymorphic regarding the length of their claws (CL) (Hartnoll, 1963; (propodus) (PL) re 1a t ive to the length of their carapace Aldrich, 1974; Homola et al., 1991), and the condition of the epicuticle covering their exoskeleton (Homola et al., 1991; Sagi et al., 1993). There are large bodied males (60-80 mm CL) with claws longer than their carapace (70-100 mm PL) that are covered with a pubescent epicuticle (unabraded), which indicates that the animal has recently molted, or the epicuticle has been partially or completely worn off (abraded). There are large bodied unabraded males with claws shorter than the carapace length, as well as, small bodied (<60 mm CL) males, with either abraded or unabraded exoskeletons, that have short claws. Sexual maturation in male spider crabs takes place when the animals are still quite small (219 mm CL) (Homola et al., 1991) as evidenced by the presence of sperm in their vas deferens (Hinsch, 1972). However, the display of mating behavior and attempts at copulation with a receptive female is quite variable among the different morphotypes. The primary reproductives are the large-bodied abraded males with long claws (Homola et al., 1991). These males actively compete with each other for the opportunity to mate with a receptive female. The winner of such a competition, after mating, will use his last pair of walking legs to carry the female behind him and will continue to guard her from take-over by another male until she releases the next clutch of fertilized eggs. Males with large claws which are incompletely abraded attempt copulation if isolated with a receptive female, but do not compete with abraded males. The presence of a partially worn epicuticle indicates that this type of male has
H. Laufer,
J.S.B. Ah1 I J. Exp. Mar. Biol. Ecol. 193 (1995) 15-20
17
undergone the final molt fairly recently, and probably is participating in the mating season for the first time. In contrast, the primary reproductives are most likely experiencing their second mating season, suggests that perhaps prior experience, and/or higher MF levels, contribute to their mating success. Small abraded males, approximately the same size as a mature female (30-55 mm CL), exhibit the female-like behavior of being passive in the presence of the large-claw abraded males. We have also observed small abraded males being carried by primary reproductives. These small males, which appear to “mimic” females, avoid aggressive behavior from the primary reproductives, and may be able to increase their mating opportunities by “sneak” mating. Indeed, on one occasion, we observed a small male, that was being carried, grasp a receptive female, with which he then commenced to copulate (Sagi et al., 1994). Unabraded males of any size do not exhibit any mating behavior, even when isolated with a receptive female. The differences in mating activity among the male morphotypes of Libinia emarginatu can be explained partly in terms of reproductive readiness with respect to the size of the reproductive system. The males that mate, either in competition or in isolation, all have relatively large reproductive system indices (RI) (Fig. 1). The abraded males, both large and small, have the largest RIs, 2.32 ? 0.03 and 2.86 + 0.35, respectively. The large-claw incompletely abraded males have intermediate sized RIs (1.73 t 0.06). The unabraded males of any size have considerably smaller RIs, (0.20-0.72). The levels of MF in the hemolymph of male morphotypes vary in a manner
RI in male morphs
3’5w 3.0 2s
-
201.5 1.0 0.6 -
Fig. 1. Reproductive indices in male morphotypes of the spider crab Libinia emarginata. SUS, small carapace unabraded small-claw; SAS, small carapace abraded small-claw; LUS, large carapace unabraded small-claw; LUL, large carapace unabraded large-claw; LIL, large carapace incompletely abraded large-claw; LAL, large carapace abraded large-claw.
18
H. Laufer, J.S.B.
Ah1 I J. Exp. Mar. Biol. Ecol. 193 (1995) 15-20
MF levels in male morphs
SJS Fig. 2. Hemolymph emarginafa. Labels
549
LUS
levels of methyl farnesoate on abscissa are as in Fig. 1.
LUL in male
LIL
morphotypes
LAL of the
spider
crab
Libinia
similar to the RIs (Fig. 2). Both of the completely abraded types have the highest MF levels, 39.7 f 2.09 ng ml -’ in the large-claw males and 40.3 t 9.3 ng . ml- ’ in the small males. The incompletely abraded males have intermediate MF levels, 24.2 + 0.82 ng* mll’, and all of the unabraded males have low levels, 15.8-16.0 ng.mll’. The apparent absence of mating behavior in the unabraded males, which also have small RIs and low MF levels, probably reflects a state of reproductive diapause. In insects, reproductive diapause occurs in pre-reproductives and in adults during the non-breeding season and is characterized by low JH levels in the blood and small RIs (DeWilde, 1983; Denlinger, 1985). Small-claw unabraded males have not yet undergone their terminal molt and are still growing. If mating is delayed so that energy can be invested in growth, then the result is a larger body and claw size that ultimately enhances mating success (Sagi et al., 1988). This then may explain why small unabraded males do not attempt to mate, even though sperm have been produced. The large unabraded males, on the other hand, have undergone their final molt and reached their maximal external size. However, their internal organs are approximately the same size as prior to the molt. Again, energy is used for growth and to build up the reproductive system prior to the commencement of the energetically expensive processes of competing for females and mating. The data and observations we have presented suggest that in Crustacea, as in insects, differences in mating behavior and activity vary with the relative size of the reproductive system and with hormone level. Crustaceans differ from insects, however, in that maturation of the reproductive tract is interspersed with periods
H. Laufer, J.S.B.
Ah1 I J. Exp. Mar. Biol. Ecol. 193 (1995)
15-20
19
of growth, sperm sometimes being present even in relatively very small males. We conclude that MF may be a reproductive hormone, although the exact mechanism by which MF works remains to be elucidated.
Acknowledgements
We would like to thank David Dodge and the staff of the New England Utilities Environmental Laboratory at Millstone Power Plant in Niantic, CT, for the collection of Libinia emarginatu, Dr. Maury of the University of Connecticut Biotechnology Center for technical advice, and for use of the center’s HPLC facilities. This work was supported in part by the Connecticut Sea Grant College Program, NOAA, U.S. Dept. of Commerce, an economic development grant from the Office of the Provost, The University of Connecticut, and a Fellowship of the Lady Davis Trust to H.L.
References Aldrich, J.C., 1974. Allometric studies on energy relationships in the spider crab Libinia emarginata (Leach). Biol. Bull. Woods Hole Mass., Vol. 147, pp. 257-273. Borowsky, B., 1985. Differences in reproductive behavior between two male morphs of the amphipod crustacean Jassa falcata Montagu. Physiol. Zool., Vol. 58, pp. 497-502. Conan, G.Y. and M. Comeau, 1986. Functional maturity and terminal molt of the male snow crab, Chionoecetes opilio. Can. J. Aquat. Sci., Vol. 43, pp. 1710-1719. Denlinger, D.L., 1985. Hormonal control of diapause. In, Comparative insect physiology, biochemistry, and pharmacology, Vol. & Endocrinology II, edited by G.A. Kerkut & L.I. Gilbert, Pergamon Press, New York, pp. 353-412. DeWilde, J., 1983. Endocrine aspects of diapause in the adult stage. In, Invertebrate endocrinology, Vol. 1: Endocrinology of insects, edited by R.G.H. Downer & H. Laufer, A.R. Liss, Inc., New York, pp. 357-368. Donaldson, W.E. and A.E. Adams, 1989. Ethogram of behavior with emphasis on mating for the Tanner crab Chionoecetes bairdi Rathbun. J. Crust. Biol., Vol. 9, pp. 37-53. Hartnoll, R.G., 1963. The biology of the Manx spider crabs. Proc. 2001. Sot. London, Vol. 141, pp. 432-496. Hinsch, G.W. 1972. Microtubules in the sperm of the spider crab, Libinia emarginata. J. Ultrastruct. Res., Vol. 29, pp. 525-534. Homola, E., A. Sagi and H. Laufer, 1991. Relationship of claw form and exoskeleton condition to reproductive system size and methyl farnesoate in the male spider crab, Libinia emarginata. Invert. Reprod. Dev., Vol. 20, pp. 219-225. Laufer, H., D. Borst, F.C. Baker, C. Carrasco, M. Sinkus, C.C. Reuter, L.W. Tsai and D.S. Schooley, 1987. Identification of a juvenile hormone-like compound in a crustacean. Science, Vol. 235, pp. 202-205. Laufer, H., M. Landau, D. Borst and E. Homola, 1986. The synthesis and regulation of methyl farnesoate, a new juvenile hormone for crustacean reproduction. Advances in invertebrate reproduction.Vol. 4, edited by M. Porchet, J.C. Andries and A. Dhainaut, Elsevier Science Pub]., Amsterdam, pp. 135-143. Laufer, H., A. Sagi and J.S.B. Ahl, 1992. Juvenile hormone-like compounds in Crustacea and their implications for reproductive behavior. Advances in regulation of insect reproduction, edited by B. Bennettova, I. Gelbic and T. Soldan, Institute of Entomology, Czech Acad. Sci., pp. 153-155.
20
H. Laufer, J.S.B.
Ah1 I J. Exp. Mar. Biol. Ecol. 193 (1995) 15-20
Nijhout, H.F. and D.E. Wheeler, 1982. Juvenile hormone and the physiological basis of insect polymorphisms. Quart. Rev. Biol., Vol. 57, pp. 109-133. Ra’anan, Z. and A. Sagi, 1985. Alternative mating strategies in male morphotypes of the freshwater prawn Macrobrachium rosenbergii (deMan). Biol. Bull., Vol. 196, pp. 592-601. Sagi, A., J. Ahl, H. Danaee and H. Laufer, 1991. Methyl farnesoate and reproductive behavior in male morphotypes of the spider crab Libinia emarginata. Am. Zool.,Vol. 31, p. 87A. Sagi, A., J.S.B. Ahl, H. Danaee and H. Laufer, 1994. Methyl farnesoate levels in male spider crabs exhibiting active reproductive behavior. Horm. Behav., Vol. 28, pp. 261-272. Sagi, A., E. Homola and H. Laufer, 1993. Distinctive reproductive types of male spider crabs Libinia emarginatu differ in circulating and resynthesizing methyl farnesoate. Biol. Bull., Vol. 185, pp. 168-173. Sagi, A., Y. Milner and D. Cohen, 1988. Spermatogenesis and sperm storage in the testes of the behaviorally distinctive male morphotypes of Macrobrachium rosenbergii (Decapoda, Palaemonidae). Biol. Bull., Vol. 174, pp. 330-336. Shuster, S.M., 1987. Alternative reproductive behaviors: three discrete male morphs in Paracerceis sculpta, an intertidal isopod from the northern Gulf of California. J. Crust, Biol.,Vol. 7, pp. 318-327.