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First published online December 1, 2006
Journal of Experimental Biology 209, 4974-4983 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02586
Males also have their time of the month! Cyclic disposal of old spermatophores, timed by the molt cycle, in a marine shrimp
Department of Life Sciences and National Institute for Biotechnology in the Negev, Ben-Gurion University of the Negev, PO Box 653, Beer-Sheva 84105, Israel
Author for correspondence (e-mail:
sagia{at}bgu.ac.il)
Accepted 5 October 2006
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Key words: Litopenaeus vannamei, shrimp, male, female, sperm, spermatophore, melanization, mating system, impotency, sterility, molt cycle, reproductive cycle
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).
Spermatophores or seminal fluids - the end-product of the male reproductive
process - are held inside the reproductive tract, but topologically outside
the body: they are therefore not protected by the animal's defense system and
may be subject to environmental (e.g. oxidative) stress and/or the action of
contaminants. Despite the potential time-related loss of sperm viability
during storage in the male reproductive tract, the notion that sperm might
have an inherent `expiry date' has never been given any serious consideration.
It is similarly not known whether sperm are recycled periodically in
non-mating males.
In crustaceans, numerous physiological processes, including female
reproduction, have been shown to be closely linked to the molt cycle
(Skinner, 1985). In many
decapod crustacean species, such as shrimps, lobsters and crabs, female
reproduction is synchronized with the molt cycle and is thus cyclic by
definition (Adiyodi, 1985;
Nelson, 1991). The nature of
the association between molt cycles and reproduction in decapod males is,
however, not known, although a few clues do exist, all of them from penaeid
shrimp: manually ejaculated Litopenaeus vannamei exhibited new pairs
of spermatophores in their ejaculatory ducts (ampoules) only after molting
(Heitzmann and Diter, 1993); a
decline in spermatophore quality as the molt cycle progressed was observed in
Fenneropenaeus indicus
(Muthuraman, 1997); and
naturally mating L. vannamei and L. setiferus were shown to
be carrying new pairs of spermatophores a few days after mating within the
same molt cycle that the mating had occurred
(Leung-Trujillo and Lawrence,
1991). Whereas these are the only reported indications of an
underlying periodic reproductive mechanism in shrimp males, another
reproduction-related phenomenon, spermatophore melanization, is well
documented in these animals. In captive penaeid shrimps, such as L.
vannamei, the brown pigment, melanin, accumulates in the spermatophores,
and males with heavily melanized spermatophores are sexually impotent, since
they cannot ejaculate (Leung-Trujillo and
Lawrence, 1987; Talbot et al.,
1989; Wyban and Sweeney,
1991; Alfaro and Lozano,
1993; Alfaro et al.,
1993; Perez-Velazquez et al.,
2001). Melanin specks may appear in the ampoule of sub-adult males
even before the appearance of a spermatophore
(Parnes et al., 2004).
In an investigation of melanin deposition and spermatophore viability in relation to the presence of females in L. vannamei shrimps held in captivity, we observed that old spermatophores were replaced with new ones in a regular cyclic manner that was closely coupled to the molt cycle. In this manuscript, we describe, first, the progressive melanization of the spermatophores observed in our captive shrimp populations, a process that can permanently render the shrimps impotent. Then, we show, by using the melanin specks as a color marker, that melanization can be delayed and even reversed as long as the males are engaged in sexual activity. Last and most important, we show that male shrimp go through reproductive cycles that are strictly associated with their molt cycles, which are, in turn, hormonally regulated.
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Materials and methods |
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Experimental system: adult male/adult female and all-male populations
Adult shrimp were sampled from the farm populations described above and
transferred to an experimentally controlled seawater system situated in a
greenhouse at Ben-Gurion University of the Negev, Beer-Sheva, Israel. Water
quality was monitored for ammonia, nitrite, nitrate, alkalinity, oxygen, total
dissolved solids and pH. Temperature was kept at 29±1°C.
Photoperiod was 14 h:10 h light:dark. The shrimp were fed with an enriched
diet of fresh-frozen sandworms and squid, chopped and mixed with paprika and
shrimp maturation pellets. These items were fed to the shrimps in an amount of
about 25% of the wet body mass (
25%=9-10% sandworms, 15-16% squid and
1-2% pellets). For individual identification, each shrimp was eye tagged with
a numbered, colored plastic ring, and a white patch with the same number was
attached to the cuticle with fast-drying glue. For males, the patch was
attached to the carapace, and for females, to the first segment of the abdomen
so that it would not obscure the developing anterior lobes of the ovary. Each
day, molt exuviae were scooped out of the tank and identified, and the
respective shrimps were weighed and re-tagged with a new patch on the cuticle.
Male exuviae were examined for the presence of spermatophores, as was the
bottom of the shrimp pool and the biofilters.
The reproduction experiment (Fig. 1B) was conducted in the first 23 weeks of the study in an experimental system that housed 36 male and 30 female adult shrimp, with average weights per shrimp of 25.4±3.5 g and 31.4±3.3 g, respectively. After ovarian maturation had been endocrinologically induced, all females were monitored daily for signs of ovarian development. Females with fully developed ovaries were captured, identified and examined for the presence of spermatophores/sperm-mass. Twice a week, all males were examined for the appearance of spermatophores. This examination was performed in direct sunlight, since the internal features of the spermatophores and terminal ampoules were not fully visible upon examination in the dark room with the aid of artificial light, especially in the last 36 h before exuviation.
At the end of the reproduction experiment, an all-male experiment (Fig. 1C) was started with nine males from the previous phase plus 45 additional males (30.4±4.0 g per shrimp). For a period of 9 weeks, the molt cycles of these males were monitored as follows. A male that had molted was retagged and not examined again until 8-10 days had passed after the molt event, since it was already known from the reproduction experiment that the average molt cycle is about 14 days. From then on, the animal was examined every day until it molted again. This schedule was followed so as to minimize stress but nevertheless to obtain the maximum number of observations and minimize the chance of missing an observation of the ampoules before a molt event. The results from the statistical analysis appear as mean ± s.d.
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Our field observations on large maturing populations showed that the ovaries of pre-pubertal females did not mature spontaneously and that the animals did not become receptive to the males. Nevertheless, the males did mature, with the spermatophores containing mature spermatozoa. In each type of population of the current study, some of the males were found to be `empty', i.e. without spermatophores in the ampoules. The percentage of empty males decreased with time, from 100% in juveniles to an average of 9.7±8.6% in sub-adults (Fig. 1A). In the maturing male/pre-pubertal female population, neither males nor females were found with attached spermatophores at any time.
In the experimental adult male/adult female population (Fig. 1B), melanin specks appeared on the spermatophores of some of the males about a month after the beginning of the experiment. Nevertheless, in several males the specks apparently disappeared, only to reappear after some time. This melanization phenomenon and temporary recovery from it are addressed below.
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A better understanding of the relationship between reproductive activity and disappearance of melanization can be reached from examining the effects of artificial in vitro ejaculation (Fig. 4), when it can be seen that the accumulated melanin is evacuated from the ampoule together with the spermatophores.
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Cases of males found to be `empty' about 12 h before they molted (number of observations = 105, green bars in Fig. 5) were observed throughout the 32-week period of the experiment, irrespective of the presence or absence of females; these cases are referred to as molt-related spermatophore disappearance (note the double-headed arrows in Fig. 5 and Fig. 1Bi,C). It was possible to record some of these cases in consecutive molt cycles, i.e. in two (N=11), three (N=2), four (N=4) and even five (N=4) molt cycles. Since the molt cycle in adult L. vannamei shrimp follows a very regular pattern, it was to be expected that the average percentage of males molting each night would also follow a steady pattern (black circles in Fig. 5). The percentage of `empty' males also followed the same general pattern (green bars in Fig. 5), except for the peaks when the females were receptive (sum of red and green bars, inside the pink rectangle, Fig. 5). This percentage was similar in the mixed and all-male populations (5.6% and 5%, respectively, in Fig. 1Bi,C), but was slightly smaller than the average percentage of molting males per night (7.3±5.7% and 7.0±4.8% in the mixed and all-male populations, respectively). This discrepancy is due to the fact that we were able to record all molting events but not all spermatophore disappearance events.
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In 45 males with slightly melanized spermatophores, the melanin specks were clearly visible when the spermatophores filled the stretched ampoule. In these cases, unlike the sexually related recovery from melanization, melanized fragments of the spermatophore probably remained inside the ampoules, even as the spermatophores were degraded. When the emptying ampoules shrank and retracted from the cuticle, those fragments remained visible, but only faintly. Then, after the male had molted and new spermatophores had appeared, the ampoule became stretched and the melanized fragments were again clearly visible through the cuticle.
The last line of evidence comes from five males examined in late premolt apolysis (according to their pleopods and uropods) that did not have spermatophores visible through the cuticle at the time they were due to molt (according to the observation logbook). On dissection, the ampoules of these animals were found to be empty and flaccid, as expected and described above (Fig. 4).
Thus, in this study it was found that spermatophores periodically disappeared from the terminal ampoules of males during the 24 h premolt and that new spermatophores appeared after the exuviations. Fig. 6A shows the white spermatophores of a representative intermolt male shrimp observed through the cuticle. Fig. 6B shows the same shrimp about 12 h premolt. The muscular ampoules, which are visible as two lumps underneath the cuticle, do not contain spermatophores. The animal was apparently about to molt, according to the loss of rigidity of the cuticle and the state of the pleopods. Following the molt, a new pair of white spermatophores that had reached the ampoules on the night of ecdysis could be seen through the cuticle (Fig. 6C). The lower part of Fig. 6 shows three representative male time tracks, each describing four consecutive molt cycles in which the spermatophore disappearance phenomenon was observed.
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). The disappearance of melanin in some of the
shrimp in this study is most probably the result of spermatophore evacuation
from the ampoules during mating. This can efficiently remove melanin debris
from the ampoules, and indeed in this study recovery of males from
melanization was observed exclusively during the period that there were
vitellogenic, receptive females in the population. The fact that
spermatophores of sexually active males remain white is probably considered
common knowledge and has been referred to only by two studies other than the
current study (Leung-Trujillo and
Lawrence, 1991; Browdy et al.,
1996). Manually or electrically ejaculating the spermatophores can
also remove melanin debris from the ampoules, and many studies use these
methods to keep males in good condition in the absence of females. Indeed,
most of these studies reported that, over extended time periods,
spermatophores did not show deterioration
(Leung-Trujillo and Lawrence,
1991; Alfaro, 1993;
Alfaro and Lozano, 1993;
Heitzmann and Diter, 1993;
Pratoomchat et al., 1993;
Alfaro, 1996;
Pascual et al., 1998;
Diaz et al., 2001;
Ceballos-Vazquez et al.,
2004). If the spermatophores are not evacuated (manually,
electrically or through mating), they may become melanized in some individuals
even within few days (as in Fig.
2) and subsequently hardened enough to prevent their ejaculation
(Leung-Trujillo and Lawrence,
1987; Talbot et al.,
1989; Alfaro et al.,
1993; Perez-Velazquez et al.,
2001). All these studies thus suggest that penaeid male readiness
for the next copulation might actually be increased through the previous
copulation. We now need to ask whether male shrimp can maintain their readiness for copulation when there is a shortage of receptive females. Generally, the percentage of `empty' males found in this study at any given time clearly depended on the maturational status of the males, decreasing from 100% in juveniles to about 5% in adults (see Fig. 1). Ceballos-Vasquez et al. (Ceballos-Vasquez et al., 2003) similarly reported that the percentage of `empty' males decreased from juvenility to adulthood, but they did not explain the fact that 2.1% of their adult males were found to be `empty' although the population under observation was a non-breeding population. In the current study, the only time that this seemingly basal level of `empty' adult males was found to be higher was during the `vitellogenic window' of the females, i.e. when adult males were able to mate with receptive females. At no time, were males found carrying attached spermatophores, ruling out homosexual activity, and females were never found with attached spermatophores outside the `vitellogenic window'. In addition, there was no evidence that intact spermatophores were ejaculated through means other than sexual activity. The possibility that ejaculated spermatophores could have been eaten by the shrimp, and thus not found on the tank bottom or water filters, was not ruled out completely in this study. However, this explanation also required us to assume that the shrimp engage in a kind of regular ejaculation and such a phenomenon was never reported from shrimp studies. All the evidence suggested that when a male was found `empty' in the absence of receptive females in the population, exuviation was imminent and would occur in less than 12 h. Thus, it was hypothesized that in such cases the spermatophores underwent `programmed degradation', which was strictly molt related (see Fig. 1, right). Unlike ejaculation-related spermatophore disappearance, which depends on the presence of receptive females, molt-related spermatophore disappearance is an endogenous, cyclic phenomenon that occurs in all mature L. vannamei males at all times. This phenomenon involves the disappearance of the spermatophores during the 12 h before molt and their reappearance immediately after the molt. It probably accounts for the fact that males were observed with white spermatophores (some of them for quite a long time), even in the absence of females. We therefore propose that spermatophores have an `expiry date' and that their average life time in L. vannamei matches the duration of the molt cycle.
Some clues to the timed regulation of spermatophore behavior during storage
within the male have indeed appeared in the literature. In Melicertus
(formerly Penaeus) kerathurus, a complete spermatophore is
accommodated in the terminal ampoule while another is simultaneously forming
in the medial vas deferens (Malek and
Bawab, 1974a; Malek and Bawab,
1974b). Judging from the small variability in the dimensions of
the medial vas deferens, Ro et al. (Ro et
al., 1990) concluded that the migration of a new spermatophore
along the sperm duct does not occur at random but is under precise regulation.
In other animals, almost all the current knowledge on sperm viability,
longevity and storage duration, relates to the time after ejaculation while
the sperm cells are inside the female reproductive tract
(Birkhead and Moller, 1993;
Parker, 1970;
Saunders, 2002). However, in
some seasonal animal species, in which the males are known to store sperm for
long periods of time, it has never been shown that the sperm is recycled
during storage, and in these cases the fertilizing sperm can be several months
old (Mann, 1984).
Flushing out seminal fluid or evacuating spermatophores from the
reproductive tract on a regular basis could serve as a mechanism that ensures
sperm viability. Whether masturbation in primates
(Baker and Bellis, 1993;
Starin, 2004) or sperm leakage
(Cooper, 1999) represents such
examples is still open to question. An isolated male cricket was seen to push
out the spermatophore after grooming his abdominal tip onto the substrate, and
it was suggested that in the absence of a partner, such an action might be
profitable in that spermatozoa could be perpetually renewed before they became
obsolescent (Sakai et al.,
1991). In the many species of the Myriapoda, Arachnida and some of
the more primitive groups in the Insecta (e.g. Collembola), spermatophores are
extruded onto a substrate, from where they are collected by the female
(Mann, 1984). However, these
cases represent specific reproductive strategies, and in all of them sperm is
evacuated from the body in contrast to the mechanism reported here in which
the sperm is replaced while inside the body of the male shrimp.
The regular replacement of `old' sperm probably involves acellular-matrix
degradation processes and phagocytosis of the spermatozoa. In echinoderms,
phagocytosis of spermatozoa remaining in the testicular lumen after the
completion of the spawning season has indeed been observed
(Chia and Bickell, 1983). In
the Myriapoda, it is possible that the cells of the vasa deferentia may be
either secretory or phagocytic in function, depending upon the time of the
year and/or the animal's reproductive cycle
(Reger and Fitzgerald, 1983).
In celibate human males, aging spermatozoa undergo intraluminal degeneration
in the distal epididymal lumen, but the rare reports of spermiophagy by
epithelial cells along the posttesticular tract do not provide evidence for
wholesale removal of sperm by this mechanism
(Cooper, 1999). Cyclic
reproductive readiness is usually associated with female life histories
(Campbell et al., 1999):
females have been shown to go through reproductive cycles in many animal
species ranging from chelicerates (Taylor
and Chinzei, 2002) through crustaceans
(Adiyodi, 1985;
Nelson, 1991;
Wilder et al., 2002) and
insects (Attardo et al., 2005)
to fish, amphibians (Polzonetti-Magni,
1999), reptiles, birds
(Williams, 1999) and mammals.
There are, however, also cyclic reproductive processes in males, most of them
in species with a circannual cycle that includes a particular reproductive
period during the course of the year. Although these cycles are hormonally
regulated, they are also strictly environmentally mediated through temperature
and day length changes, as has been observed in some cnidarians
(Fautin, 1999), most
echinoderms (Byrne, 1999),
fish (Koob, 1999), most
reptiles (Gist, 1999), birds
(Williams, 1999), and some
long-lived mammals (Zucker and
Prendergust, 1999). Male insects do not produce gametes
cyclically, but appear to be ready to mate at any time
(Nijhout, 1994). However, in
some lepidopteran insects release of sperm from the testes and secretion of a
carbohydrate-rich material from cells of the upper vas deferens exhibits a
circadian rhythm (Gillott,
1999). Despite of the above data regarding cyclic reproductive
phenomena in males, Saunders (Saunders,
2002) concluded that: "Rhythmicity in spermatogenesis
appears not to have been examined. The absence of studies may well be related
to the enduring fascination of biologists with the female system, which is
usually regarded as more important to reproductive success as well as being
morphologically more impressive. Indeed, much less is known of the physiology
of the male reproductive system than of the female." This statement
is also true for crustaceans, but if strictly hormonally regulated
reproductive processes are to be characterized, it is from this group of
animals. A unique feature of crustaceans, at least in species with
indeterminate growth, is that to grow they have to molt on a regular basis
throughout their lifespan. Reproduction and molting are hormonally coupled in
a variety of ways (Adiyodi,
1985; Meusy and Payen,
1988; Nelson,
1991). A close link between the molt and vitellogenic cycles has
been demonstrated in the female of the caridean species Macrobrachium
rosenbergii (Meusy and Payen,
1988; Wickins and Beard,
1974). In some brachyuran
(Cheung, 1969;
Kurup and Adiyodi, 1981) and
astacidean (Nelson, 1991)
species, reproductive cycles are completed within a single intermolt period
with marked seasonality. In some astacidean
(Aiken and Waddy, 1980;
Barki et al., 1997), brachyuran
(Cheung, 1969) and caridean
(Wickins and Beard, 1974)
species, reproductive cycle or egg incubation may delay ecdysis and lengthen
the molt cycle. In penaeids, resources are more or less simultaneously
utilized for weight gain and reproduction throughout the molt cycle
(Adiyodi, 1985). Penaeid
females may spawn several times during a single molt cycle, but if they do not
spawn, the oocytes are resorbed before molting takes place
(Emmerson, 1980;
Emmerson, 1983;
Quinitio et al., 1993;
Raviv et al., 2006).
Males, as opposed to females, are currently viewed as continuous breeders. To the best of our knowledge, this is the first study to describe males that go through periodic sperm replacement episodes when not sexually active. This degradation process could be induced by the premolt peak in ecdysteroids, but it seems that it is not as efficient as ejaculation in removing melanized debris from the ampoules.
Ejaculation-related spermatophore disappearance apparently offers active
males a chance to recover from melanization while in captivity, whereas the
process responsible for `programmed degradation' does not remove melanin
debris, resulting in the progressive melanization patterns observed in this
study. The adaptive value of this mechanism seems to be clear, since there are
no reports of melanization of the sperm duct in animals in the wild
(King, 1948;
Lindner and Anderson, 1956;
DeLancey et al., 2005), although melanization of the cuticle and gills in wild
shrimp has been observed (?. DeLancey, personal communication). Moreover,
there is only one report of a single wild-caught Litopenaeus sp.
specimen with melanized spermatophores
(Chamberlain et al., 1983). In
addition, this mechanism grants the male a periodic opportunity to replace old
spermatophores with new ones if mating has not taken place. In L.
vannamei, molt-coupled spermatophore disappearance is not merely the
result of the reproductive system being `switched off', like that of seasonal
organisms, but the active degradation of old spermatophores before new ones
occupy the ampoules. Based on our recent study of moltrelated cyclic
vitellogenic activity and Vg gene expression in L. vannamei
females (Raviv et al., 2006)
and the current study on molt-related cyclic spermatophore degradation in
L. vannamei males, it is clear that in these organisms no phenomenon
can be separated from the molt cycle and examined in isolation. Because the
reproductive organs of males and females develop from essentially the same
embryonic tissue, one cannot escape the similarity in the cyclic nature of
these systems in L. vannamei. Generally, a male animal with a
relatively long life span would benefit from a maintenance mechanism that
keeps its reproductive tract in good condition, but whether the mechanism
suggested by the present study is unique to litopenaeid shrimp or can be found
in other animals is an open question.
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Acknowledgments |
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Footnotes |
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References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Adiyodi, R. G. (1985). Reproduction and its control. In The Biology of Crustacea: Integument, Pigments, and Hormonal Processes. Vol. 9 (ed. D. E. Bliss), pp. 147-215. New York: Academic Press.
Aiken, D. E. and Waddy, S. L. (1980). Reproductive biology. In The Biology and Management of Lobsters: Physiology and Behavior. Vol. 1 (ed. J. S. Cobb and B. F. Philips), pp. 215-276. New York: Academic Press.
Alfaro, J. (1993). Reproductive quality evaluation of male Penaeus stylirostris from a grow-out pond. J. World Aquacult. Soc. 24, 6-11.
Alfaro, J. (1996). Effect of 17 alpha-methyltestosterone and 17 alphahydroxyprogesterone on the quality of white shrimp Panaeus vannamei spermatophores. J. World Aquacult. Soc. 27,487 -492.
Alfaro, J. and Lozano, X. (1993). Development and deterioration of spermatophores in pond-reared Penaeus vannamei.J. World Aquacult. Soc. 24,522 -529.
Alfaro, J., Lawrence, A. L. and Lewis, D. (1993). Interaction of bacteria and male reproductive-system blackening disease of captive Penaeus setiferus.Aquaculture 117,1 -8.[CrossRef]
Attardo, G. M., Hansen, I. A. and Raikhel, A. S. (2005). Nutritional regulation of vitellogenesis in mosquitoes: Implications for anautogeny. Insect Biochem. Mol. Biol. 35,661 -675.[CrossRef][Medline]
Baker, R. R. and Bellis, M. A. (1993). Human sperm competition - ejaculate adjustment by males and the function of masturbation. Anim. Behav. 46,861 -885.[CrossRef]
Barki, A., Levi, T., Hulata, G. and Karplus, I. (1997). Annual cycle of spawning and molting in the red-claw crayfish Cherax quadricarinatus, under laboratory conditions. Aquaculture 157,239 -249.[CrossRef]
Birkhead, T. R. and Moller, A. P. (1993). Sexual selection and the temporal separation of reproductive events - sperm storage data from reptiles, birds and mammals. Biol. J. Linn. Soc. Lond. 50,295 -311.[CrossRef]
Browdy, C. L., McGovern-Hopkins, K., Stokes, A. D., Hopkins, J. S. and Sandifer, P. A. (1996). Factors affecting the reproductive performance of the Atlantic white shrimp, Penaeus setiferus, in conventional and unisex tank systems. J. Appl. Aquacult. 6,11 -25.
Byrne, M. (1999). Echinodermata. In Encyclopedia of Reproduction. Vol.1 (ed. E. Knobil and J. D. Neill), pp.940 -954. San Diego: Academic Press.
Campbell, N. A., Reece, J. B. and Mitchell, L. G. (1999). Biology. Menlow Park: Benjamin/Cummings, Addison Wesley Longman, Inc.
Ceballos-Vazquez, B. P., Rosas, C. and Racotta, I. S. (2003). Sperm quality in relation to age and weight of white shrimp Litopenaeus vannamei. Aquaculture 228,141 -151.[CrossRef]
Ceballos-Vazquez, B. P., Aparicio-Simon, B., Palacios, E. and Racotta, I. S. (2004). Sperm quality over consecutive spermatophore regenerations in the Pacific white shrimp Litopenaeus vannamei. J. World Aquacult. Soc. 35,178 -188.
Chamberlain, G. W., Johnson, S. K. and Lewis, D. H. (1983). Swelling and melanization of the male reproductive system of captive adult penaeid shrimp. J. World Maricult. Soc. 14,135 -136.
Cheung, T. S. (1969). The enviromental and
hormonal control of growth and reproduction in the adult female stone crab,
Menippe mercenaria (Say). Biol. Bull.
136,327
-346.
Chia, F.-S. and Bickell, L. R. (1983). Echinodermata. In Reproductive Biology of Invertebrates: Spermatogenesis and Sperm Function. Vol. 2 (ed. K. G. Adiyodi and R. G. Adiyodi), pp. 545-620. Chichester: John Wiley and Sons.
Cooper, T. G. (1999). Epididymis. In Encyclopedia of Reproduction. Vol.2 (ed. E. Knobil and J. D. Neill), pp.1 -17. San Diego: Academic Press.
DeLancy, L. B., Jenkins, J. E., Maddox, M. B., Whitaker, J. D. and Wenner, E. L. (2005). Field observations on white shrimp, Litopenaeus cetiferus, during spring spawning season in South Carolina, USA, 1980-2003. J. Crust. Biol. 25,212 -218.[CrossRef]
Diaz, A. C., Fernandez Gimenez, A. V., Haran, N. S. and Fenucci, J. L. (2001). Reproductive performance of male Argentine red shrimp Pleoticus muelleri Bate (Decapoda, Penaeoidea) in culture conditions. J. World Aquacult. Soc. 32,236 -242.
Emmerson, W. D. (1980). Induced maturation of prawn Penaeus indicus. Mar. Ecol. Prog. Ser. 2, 121-131.
Emmerson, W. D. (1983). Maturation and growth of ablated and unablated Penaeus monodon Fabricius. Aquaculture 32,235 -241.[CrossRef]
Fautin, D. G. (1999). Cnidaria. In Encyclopedia of Reproduction. Vol.1 (ed. E. Knobil and J. D. Neill), pp.645 -652. San Diego: Academic Press.
Gillott, C. (1999). Male reproductive system, insects. In Encyclopedia of Reproduction. Vol.3 (ed. E. Knobil and J. D. Neill), pp.41 -48. San Diego: Academic Press.
Gist, D. H. (1999). Male reproductive system, reptiles. In Encyclopedia of Reproduction. Vol.3 (ed. E. Knobil and J. D. Neill), pp.60 -70. San Diego: Academic Press.
Hamamah, S. and Gatti, J. L. (1998). Role of the ionic environment and internal pH on sperm activity. Human Reprod. 13,20 -30.
Heitzmann, J. C. and Diter, A. (1993). Spermatophore formation in the white shrimp, Penaeus vannamei Boone 1931 - Dependence on the intermolt cycle. Aquaculture 116, 91-98.[CrossRef]
King, J. E. (1948). A study of the reproductive
organs of the common marine shrimp, Penaeus setiferus (Linnaeus).
Biol. Bull. 94,244
-262.
Koob, T. J. (1999). Elasmobranch reproduction. In Encyclopedia of Reproduction. Vol.1 (ed. E. Knobil and J. D. Neill), pp.1009 -1018. San Diego: Academic Press.
Kurup, K. N. P. and Adiyodi, R. G. (1981). The programming of somatic growth and reproduction in the crab, Paratelphusa hydrodromous (Herbest). Int. J. Invertebr. Repr. 3, 27-39.
Leung-Trujillo, J. R. and Lawrence, A. L. (1987). Observations on the decline in sperm quality of Penaeus setiferus under laboratory conditions. Aquaculture 65,363 -370.[CrossRef]
Leung-Trujillo, J. R. and Lawrence, A. L. (1991). Spermatophore generation times in Penaeus setiferus, P. vannamei, and P. stylirostris. J. World Aquacult. Soc. 22,244 -251.
Lindner, M. J. and Anderson, W. W. (1956). Growth, migrations, spawning and size distribution of shrimp Peneaus setiferus. Bull. Bur. Fish. 56,555 -645.
Malek, S. R. A. and Bawab, F. M. (1974a). The formation of the spermatophore in Penaeus kerathurus (Forskal, 1775) (Decapoda, Penaeidae). I. The initial formation of a sperm mass. Crustaceana 26,273 -285.
Malek, S. R. A. and Bawab, F. M. (1974b). The formation of the spermatophore in Penaeus kerathurus (Forskal, 1775) (Decapoda, Penaeidae). II. The deposition of the main layers of the body and of the wing. Crustaceana 27, 73-83.
Mann, T. (1984). Spermatophores. Berlin: Springer-Verlag.
Meusy, J. J. and Payen, G. G. (1988). Female reproduction in malacostracan crustacea. Zool. Sci. 5, 217-265.
Muthuraman, A. L. (1997). Effect of ecdysial cycle on the semen and spermatophore production of the Indian white prawn (Penaeus indicus H. M. Edwards). Fish. Technol. 34,11 -14.
Nelson, K. (1991). Scheduling of reproduction in relation to molting and growth in malacostracan crustaceans. In Crustacean Issues: Crustacean Egg Production. Vol.7 (ed. A. Wenner and A. Kuris), pp.77 -113. Rotterdam: Balkema Press.
Nijhout, H. F. (1994). Insect Hormones. Princeton, NJ: Princeton University Press.
Parker, G. A. (1970). Sperm competition and its evolutionary consequences in the insects. Biol. Rev. 45,525 -567.
Parnes, S., Mills, E., Segall, C., Raviv, S., Davis, C. and Sagi, A. (2004). Reproductive readiness of the shrimp Litopenaeus vannamei grown in a brackish water system. Aquaculture 236,593 -606.[CrossRef]
Pascual, C., Valera, E., Re-Regis, C., Gaxiola, G., Sanchez, A., Ramos, L., Soto, L. A. and Rosas, C. (1998). Effect of water temperature on reproductive tract condition of Penaeus setiferus adult males. J. World Aquacult. Soc. 29,477 -484.
Perez-Velazquez, M., Bray, W. A., Lawrence, A. L., Gatlin, D. M., III and Gonzalez-Felix, M. L. (2001). Effect of temperature on sperm quality of captive Litopenaeus vannamei broodstock. Aquaculture 198,209 -218.[CrossRef]
Polzonetti-Magni, A. M. (1999). Amphibian ovarian cycles. In Encyclopedia of Reproduction. Vol.1 (ed. E. Knobil and J. D. Neill), pp.154 -160. San Diego: Academic Press.
Pratoomchat, B., Piyatiratitivorakul, S., Menasveta, P. and Fast, A. W. (1993). Sperm quality of pond-reared and wild-caught Penaeus monodon in Thailand. J. World Aquacult. Soc. 24,530 -540.
Quinitio, E. T., Caballero, R. M. and Gustilo, L. (1993). Ovarian development in relation to changes in the external genitalia in captive Penaeus monodon.Aquaculture 114,71 -81.[CrossRef]
Raviv, S., Parnes, S., Segall, C., Davis, C. and Sagi, A. (2006). The complete Litopenaeus vannamei (Crustacea: Decapoda) vitellogenin cDNA and its expression in endocrinologically induced sub-adult females. Gen. Comp. Endocrinol. 145, 39-50.[CrossRef][Medline]
Reger, J. F. and Fitzgerald, M. E. C. (1983). Arthropoda-Myriapoda. In Reproductive Biology of Invertebrates: Spermatogenesis and Sperm Function. Vol. 2 (ed. K. G. Adiyodi and R. G. Adiyodi), pp. 451-476. Chichester: John Wiley and Sons.
Ro, S., Talbot, P., Leung-trujillo, J. and Lawrence, A. L. (1990). Structure and function of the vas-deferens in the shrimp Penaeus-setiferus - segments 1-3. J. Crust. Biol. 10,455 -468.[CrossRef]
Sakai, M., Taoda, Y., Mori, K., Fujino, M. and Ohta, C. (1991). Copulation sequence and mating termination in the male cricket Gryllus bimaculatus Degeer. J. Insect Physiol. 37,599 -615.[CrossRef]
Saunders, D. S. (2002). Insect Clocks. Amsterdam: Elsevier Science.
Skinner, D. M. (1985). Molting and regeneration. In The Biology of Crustacea: Integument, Pigments, and Hormonal Processes. Vol. 9 (ed. D. E. Bliss), pp. 43-146. New York: Academic Press.
Starin, E. D. (2004). Masturbation observations in Temmnick's red colobus. Folia Primatol. 75,114 -117.
Talbot, P., Howard, D., Leung-trujillo, J., Lee, T. W., Li, W. Y., Ro, H. and Lawrence, A. L. (1989). Characterization of male reproductive-tract degenerative syndrome in captive penaeid shrimp (Penaeus-setiferus). Aquaculture 78,365 -377.[CrossRef]
Taylor, D. and Chinzei, Y. (2002). Vitellogenesis in ticks. In Reproductive Biology of Invertebrates: Progress in Vitellogenesis. Vol. 12 (ed. A. S. Raikhel and T. W. Sappington), pp. 175-199. Enfield, USA: Science Publishers.
Wickins, J. F. and Beard, T. W. (1974). Observations on breeding and growth of the giant freshwater prawn Macrobrachium rosenbergii (de Man) in the laboratory. Aquaculture 3,159 -174.
Wilder, M. N., Subramoniam, T. and Aida, K. (2002). Yolk proteins of crustacea. In Reproductive Biology of Invertebrates: Progress in Vitellogenesis. Vol.12 (ed. A. S. Raikhel and T. W. Sappington), pp.131 -174. Enfield, USA: Science Publishers.
Williams, T. D. (1999). Avian reproduction, overview. In Encyclopedia of Reproduction. Vol.1 (ed. E. Knobil and J. D. Neill), pp.325 -336. San Diego: Academic Press.
Wyban, J. A. and Sweeney, J. N. (1991). Intensive Shrimp Production Technology. Redmond, WA: Argent Chemical Laboratories.
Zucker, I. and Prendergust, B. J. (1999). Circannual rhythms. In Encyclopedia of Reproduction. Vol. 1 (ed. E. Knobil and J. D. Neill), pp.620 -627. San Diego: Academic Press.
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