Coordination of Reproduction and Molt in Decapods
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9 Coordination of Reproduction and Molt in Decapods S. Raviv1, S. Parnes1 and A. Sagi1,2 1Department of Life Sciences and 2National Institute for Biotechnology in the Negev, Ben-Gurion University of the Negev, P.O. Box 653, Beer-Sheva 84105, Israel INTRODUCTION Factors Affecting the Reproductive Cycle The molt cycle is a constitutive phenomenon in crustaceans, with molting being a complex and energy-demanding process. Therefore, most aspects of the life history of crustaceans are, at least to some extent, synchronized with the molt cycle (Chang, 1995). Reproduction and metabolism in crustaceans depend on the molt stage, and all three phenomenamolt, reproduction and metabolismare correlated with the seasons (Aiken, 1969a; Conan, 1985; Bouchon et al., 1992). Breeding cycles are correlated with seasonal changes in such a way that the offspring are produced at a time most favorable to their survival. The relative importance of particular environmental factors may vary among different species and indeed among different environments (Sastry, 1983; Dall et al., 1990; Bauer, 1992; Bouchon et al., 1992). Generally, the frequency and amplitude of changes in temperature and day length are the proximate factors controlling the temporal patterns of reproduction, especially in species inhabiting the subtropical and temperate latitudes, i.e., in areas 366 Reproductive Biology of Crustaceans with clear differences between seasons (Stephens, 1952; Aiken, 1969b; Rice and Armitage, 1974; Penn, 1980; Lipcius and Herrnkind, 1987; Nelson et al., 1988; Justo et al., 1991; Ituarte et al., 2004). In some species, the reproduction cycle is synchronized with the circatidal and circalunar cycles (Nascimento et al., 1991; Morgan and Christy, 1994; Morgan, 1996; Yamahira, 2004; Skov et al., 2005). The interrelationships between reproductive and molt cycles during the reproductive season are discussed in this chapter. Environmental factors are dealt with only as they pertain to reproduction. Aspects of energy allocation for growth versus reproduction and the apparent competition between these two processes are addressed in brief. A large number of studies describe reproduction in decapod crustaceans (Meusy and Payen, 1988; Wilder et al., 2002), but only a few studies relate reproduction to the molt cycle (reviewed previously by Adiyodi and Adiyodi, 1970; Hartnoll, 1985; Nelson, 1991). The reproductive cycle comprises gonad development and copulation plus spawning and, in Pleocyemata, also brooding (this latter feature is common to this suborder and distinguishes it from the other decapod suborder, Dendrobranchiata). A variety of strategies for coordinating the reproductive and molt cycles are found in the different decapod species; in some, each of the above-mentioned reproductive stages is synchronized with the molt cycle, while in others there is no apparent synchronization between molt and reproduction. Integumental Machinery Essential for Mating and Brooding As a rule, in organisms with exoskeletons, any morphological change necessary for reproductive activity must involve a molting event. Successful brooding may depend on overt integumental modifications (e.g., abdominal broadening and changes in setal length and in the morphology of the seminal receptacle). The changes may be abrupt, occurring in a single puberty molt, or they may develop gradually with age and size or disappear and reappear according to the breeding season (common in non-continuously reproductive species). In crab species, for example, an abdominosternal chamber is formed only at the terminal molt in Ebalia tuberosa and Chionoecetes opilio (Brachyura) (Schembri, 1982; Alunno-Bruscia and Sainte-Marie, 1998), and in Maja squinado (Brachyura) the spermathecae (an enlarged portion of the genital duct in which sperm is stored and, in species with indeterminate growth, retained over molting) develop only after the terminal molt (Gonzalez- Gurriaran et al., 1998). In the lobster Homarus americanus (Astacidea), the development of ovigerous setae in the female parallels the gradual Coordination of Reproduction and Molt in Decapods 367 broadening of the second abdominal segment, rather than occurring suddenly at a maturity molt (Aiken and Waddy, 1980). In the spiny lobster Panulirus argus (Palinura), in addition to a gradual change, ovigerous setae lengthen and shorten in pre- and post-reproductive molt cycles, respectively (Lipcius and Herrnkind, 1987). Loss of ovigerous setae during the non-reproductive season has been observed in Crangon crangon (Caridea: Bomirski and Klek, 1974), Pandalus borealis (Caridea: Bergstrom, 2000) and Jasus edwardsii (Palinura: MacDiarmid, 1989), whereas ovigerous setae, once formed, remain permanent structures that are retained throughout molt in Panulirus homarus and Palinurus delagoae (Palinura: Berry, 1971a; Berry, 1971b). In Jasus lalandii the nature of ovigerous setae has not been established unequivocally (Palinura: Fielder, 1964; Berry, 1971b; Lipcius, 1985). Palaemonidae species (Caridea) have extra setae for egg bearing during the breeding season, and in these species the periodic appearance of chromatophores is believed to play a camouflage role in otherwise transparent animals (Antheunisse et al., 1968). In the female Penaeus latisulcatus, the thelycum (external organ into which the female receives and stores spermatophores from the male during copulation) develops gradually, with development being completed by the time the carapace length is about 25 mm, but mated females have rarely been observed with a carapace length of less than 28 mm (Penn, 1980). An exception to the general requirement for molting to precede reproductive activity is the decalcification of the opercula (lids covering the female vulvae) prior to mating in brachyuran species (Hartnoll, 1969; Fukui, 1993; Brockerhoff and McLay, 2005). Strategies for Coordination of Molt and Reproductive Cycles in Decapods In decapods, molt and reproduction are coordinated in a wide variety of ways. Some reproductive strategies can be related to a particular taxon, and others may be found in a number of taxa. Alternatively, various species within the same taxon might exhibit different strategies. Moreover, a single species might use more than one reproductive strategy. The reproductive cycle is regulated by internal cues that are related to the physiological nature of a species (e.g., molt cycle interval, integumental reproductive-related machinery, energy allocation, maternal care, and embryonic development of the offspring) and by external cues related to the environment (e.g., habitat and season). Different reproductive events, i.e., mating and oviposition, may be coupled to different molt stages (i.e., A-E). Since mating may indicate the 368 Reproductive Biology of Crustaceans Fig. 1 Five strategies describing the different ways in which the reproductive cycle is coordinated with the molt cycle. To cover an entire reproductive cycle, two consecutive molt cycles are drawn for which the first cycle does not include spawning. a. Species that cease to grow in a pubertal molt, and mating/s followed by oviposition/s occur when the female exoskeleton is hard. b. Species in which the ovary develops in a parturial molt and that mate and oviposit immediately after ecdysis. c. Species in which mating is coupled to ecdysis; mating occurs when the female is soft-shelled. Oviposition/s take/s place during intermolt and in some species also in premolt. d. Species that oviposit in concert with mating during intermolt or premolt, while the female is hard-shelled. e. Species in which ecdysis, mating, and oviposition are not coupled and are relatively independent events. Two possible alternatives for the vitellogenic periods are marked by gradient shading I and II. I relates to species whose ovaries begin to develop during the previous molt cycle, and II applies to those species that do not carry developing ovaries through ecdysis. Black arrows indicate how timing may vary according to the vitellogenesis rate. onset, acceleration (Fig. 1c), or completion (Fig. 1a, b and d) of vitellogenesis and since oviposition indicates the start of egg incubation (in Pleocyemata), the sequence of mating and oviposition combined with the occurrence of ecdysis comprise different reproductive strategies, which we have classified into the five categories shown in Fig. 1. The patterns shown in Fig. 1 have been generalized and are not scaled to time: A particular strategy can thus describe the reproductive cycle found in species belonging to different taxa, even though the time scale may vary considerably among the different species. Specific examples of the five categories of reproductive strategy are given in Table 1. Coordination of Reproduction and Molt in Decapods 369 Table 1. Examples for the five categories described in Fig. 1 in which the reproductive cycle is coordinated with the molt cycle. Strategy Species Infraorder or Reference Superfamily a Ebalia tuberosa Brachyura Schembri, 1982 a Inachus dorsettensis Brachyura Jones and Hartnoll, 1997 a Libinia emarginata Brachyura Hinsch, 1972 a Maja brachydactyla Brachyura Gonzalez-Gurriaran et al., 1998 a Maja squinado Brachyura Corgos et al., 2006 b Alpheus normanni Caridea Bauer, 1989 b Callianassa japonica Thalassinidea Tamaki et al., 1996 b Crangon crangon Caridea Oh and Hartnoll, 2004 b Emerita asiatica Anomura Gunamalai and Subramoniam, 2002 b Hippolyte curacaoensis Caridea Bauer, 1989 b Jasus edwardsii Palinura MacDiarmid, 1989 b Latreutes fucorum Caridea Bauer, 1989