© 2001 by The Society for Integrative and Comparative Biology
Hormones in the Lives of Crustaceans: An Overview1
1 Bodega Marine Laboratory, University of California, P.O. Box 247, Bodega Bay, California 94923
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We present an overview of the isolation and characterization of three hormones (or hormone families) important for the growth and development of decapod crustaceans. These hormones include the ecdysteroids (steroid molting hormones), the hyperglycemic hormone neuropeptide family, and the terpenoid methyl farnesoate. Using examples primarily from our laboratory, we describe work on these hormones using various life stages of the lobster (Homarus americanus) as the principal model.
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INTRODUCTION |
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The crustaceans have a particularly complex physiology due to the multiple processes that may overlap and influence each other. These processes may include dramatically different life stages (from embryo to larva to juvenile to adult), a cyclical molt cycle that can occur many times during the life of the crustacean, and a reproductive cycle that may alter much of the adult physiology.
We selectively describe some of the research concerning three of the hormones that have been examined at various life stages using the lobster (Homarus americanus) as the primary experimental animal. We describe the characterization and quantification of these hormones at various life stages. Functions of these hormones at some life stages are still lacking. Most of this discussion concerns work from our laboratory or work with collaborators. Some other examples, however, are also presented. This is not meant to be an exhaustive review of the topic. A number of reviews have been published that more extensively cover various aspects of crustacean endocrinology that are touched upon in our paper (Skinner, 1985
; Keller, 1992; Chang, 1993, 1997; Landau et al., 1997; Van Herp, 1998; Webster, 1998).
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MATERIALS AND METHODS |
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The materials and methods described in this section are pertinent for the previously unpublished experiments described below and are applicable to the data shown in Figures 1–4.
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Hemolymph ecdysteroids
This study consisted of 42 full sibling adult lobsters (H. americanus) that were raised in our culture facility (Chang and Conklin, 1993
; Conklin and Chang, 1993). They were fed shrimp three times a week but starved for one day prior to the experiments. Experiments were initiated at approximately the same time of day (0900). Water temperature was 11.1 ± 0.9°C (mean ± SD). Lobsters were chosen for this study based upon similarities in weight and their previous molt interval. Molt stages were defined by the monitoring of previous and current molt histories and by examination of the exoskeleton and pleopods for premolt stages (Aiken, 1973). Stress effects were minimized by returning examined lobsters to ambient seawater for at least 2 hr prior to the start of the dissections. The wet weight of the lobsters used was 422.0 ± 83.0 g (mean ± SD) and the carapace length was 82.8 ± 5.9 mm (mean ± SD).
Hemolymph (100 µl) was withdrawn from the base of the last pair of legs with a 1-ml syringe (26 gauge needle) and mixed with 300 µl of methanol. Following centrifugation, the supernatant was reduced to dryness under a vacuum and the residue assayed for ecdysteroids using radioimmunoassay (Chang and O'Connor, 1979).
Crustacean hyperglycemic hormone (CHH) in embryos
Two wild-caught female lobsters were maintained in our culture facility. Two weeks after the eggs were extruded, the sampling of the whole embryos began. The sampling continued every week for the first two months and the remaining four months the embryos were sampled every three weeks until hatching. Water temperature for the duration of embryogenesis was 12.2 ± 3.1°C (mean ± SD).
Approximately 75 embryos per sample (the actual number was counted) were removed from each female lobster, placed on a petri dish and kept on ice during the counting process. The embryos were blotted and weighed and the average eyespot index was determined using the Perkins (1972) method. The index is one-half of the sum of the length plus width of the eyespot (in micrometers). The whole embryos were then frozen in liquid nitrogen and stored at –70°C.
After all of the samples were collected, the thawed embryos were homogenized in 10 µl of phosphate-buffered saline (PBS; 136.89 mM NaCl, 10.14 mM Na2HPO4, 2.68 mM KCl, 1.76 mM KH2PO4, pH 7.3) per embryo, vortexed, and centrifuged. The samples were assayed for CHH by an enzyme-linked immunosorbent assay (ELISA) (Chang et al., 1998).
CHH in larvae
Lobster larvae were hatched in our culture facility and fed live brine shrimp. Larval Stages I-III were divided into three substages (early, middle, and late). Only larvae in the early substage were used for Stage IV. Beginning with newly hatched Stage I larvae, individuals were removed from the rearing container and placed on a tared glass slide, blotted, and weighed. Larvae were homogenized in 300 µl of PBS and stored at –70°C. Water temperature for the duration of the experiment was 15.3 ± 1.3°C (mean ± SD; n = 8 for each substage).
The larval stages were determined by observing the external morphological features through a dissecting microscope, using published guidelines (Factor, 1995). For Stage I, the early, middle, and late substages were sampled 0, 2, and 5 days after hatching, respectively. For Stage II, the sampling periods were 5, 8, and 9 days after hatching. For Stage III, the sampling periods were 10, 15, and 19 days after hatching. For Stage IV, only larvae in the early substage were used; they were taken 19 days after hatching. The approximate mean durations of Stages I, II, and III were 4.5, 5.5, and 8 days, respectively. After all the samples were obtained, they were thawed and individually assayed for CHH by ELISA.
CHH content of sinus glands and subesophageal ganglion
The same lobsters described above for the hemolymph ecdysteroid study were used for this experiment. Both eyestalks were removed and put on ice prior to further dissection. We observed that there was no significant difference in CHH content if we removed the left or right eyestalk first. The sinus gland was dissected free from the rest of the neural tissue and homogenized in 100 µl of 0.1 N HCl. The homogenate was heated in a boiling water bath for 1 min (Chang et al., 1990) and then stored at –70°C until assayed by ELISA.
The subesophageal ganglion was removed from these same lobsters and homogenized in 300 µl of PBS. After centrifugation, the supernatant was frozen at –70°C until assayed by ELISA.
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ECDYSTEROIDS |
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The steroid arthropod molting hormone was first isolated from insects and it was called ecdysone (Butenandt and Karlson, 1954
). The structure of the more active and most predominant form of the hormone was subsequently determined to be 20-hydroxyecdysone (20E). The first isolation of 20E from a crustacean was from the spiny lobster (Hampshire and Horn, 1966; Horn et al., 1966). It is now apparent that ecdysone and 20E are the two most predominant members of a family of steroids that possess molting hormone activity (Lafont, 1997). Members of this hormone family are collectively called the ecdysteroids. Our laboratory has examined changing concentrations and the possible roles of ecdysteroids during various crustacean life stages.
In embryos, from extrusion (fertilization) to hatch, several different patterns of ecdysteroid concentrations have been observed. In the crab Cancer magister, embryos displayed a biphasic pattern with decreasing titers from extrusion to the middle of embryonic life followed by increasing concentrations until hatching. In the congener Cancer anthonyi, ecdysteroids declined continuously from a very high initial concentration at extrusion until hatching (Okazaki and Chang, 1991). This is in contrast to the shrimp Sicyonia ingentis that displayed a rise in the concentration of ecdysteroids from non-detectable levels at spawning to high amounts at hatching (Chang et al., 1992).
Several different mechanisms could be involved in the regulation of embryonic ecdysteroids. Maternal investment into eggs is likely the source of ecdysteroids in those species where high concentrations are observed just after egg extrusion. After fertilization, alterations in embryonic ecdysteroid concentrations are probably due to the development of the embryonic y-organ (molting gland) and x-organ/sinus gland neurosecretory system. Although studies have demonstrated the appearance of several neurotransmitters and neuromodulators in the lobster central nervous system prior to mid-embryonic life (Beltz and Kravitz, 1987; Beltz et al., 1990, 1992; Schneider et al., 1996), little work has been conducted on embryonic development of the x-organ/sinus gland. There is also a paucity of information about the embryonic y-organ. Therefore, no definitive correlations can be made between hormone titers and endocrine structures.
Similarly, little research has been conducted on the role of embryonic ecdysteroids. Lachaise and Hoffmann (1982) and Goudeau et al. (1990) hypothesized that ecdysteroids mediate the formation of the various embryonic envelopes that surround the embryo during development. These embryonic ecdysteroids may also be involved in early morphogenesis as described for insects (Lanot et al., 1989).
Since larval crustaceans must also shed their confining exoskeletons as a prerequisite to molting, growth, and development, it is not surprising that ecdysteroid levels rise and fall during each larval lobster stage (Chang and Bruce, 1981). Manipulation of the appearance of the ecdysteroid peaks in larval lobsters can be achieved through either eyestalk ablation (which shortens the larval molt interval via removal of the x-organ/sinus glands containing the molt-inhibiting hormone, MIH) or through injection of sinus gland extracts (which lengthens the larval molt interval by increasing the amount of MIH) (Snyder and Chang, 1986a, b).
Both juvenile (Chang and Bruce, 1980) and adult (Fig. 1) lobsters display a characteristic pattern of low concentrations of ecdysteroids during postmolt and intermolt and a dramatic rise in concentration starting at stage 
(early premolt) that declines prior to ecdysis.
Ecdysteroids may also play a gonadotropic role in crustaceans. A peak of hemolymph ecdysteroids is correlated with a peak of sequestered ecdysteroids in ovaries of the crab Carcinus maenas (Lachaise et al., 1981) and several other species (for review see Subramoniam, 2000). Whether high levels of ecdysteroids in the hemolymph mediate ovarian development or are concomitant with the sequestration of embryonic ecdysteroids remains to be determined.
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CRUSTACEAN HYPERGLYCEMIC HORMONE NEUROPEPTIDE FAMILY |
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Over half a century ago, Abramowitz et al. (1944)
observed that a factor from the crustacean eyestalk was able to elevate the concentration of hemolymph glucose. The hormone responsible for this diabetogenic effect is called crustacean hyperglycemic hormone (CHH; for reviews see De Kleijn and Van Herp, 1995; Chang, 2001).
As described above for the ecdysteroids, we wanted to determine if CHH was present at all crustacean life stages. For these experiments, we used an ELISA for detection of CHH immunoactivity in the lobster (Chang et al., 1998). Lobster embryos were removed from two different females and assayed. Figure 2 shows that early embryos have no detectable CHH for approximately the first 50 days of embryonic life. The level of CHH rises rapidly after this time and parallels the development of the eyespot. We do not know how embryos younger than 50 days are able to regulate their glucose levels.
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Since the assays were conducted with whole embryos, we do not know if the CHH activity was localized in the embryonic x-organ/sinus gland neurosecretory complex in the eyestalk. However, this increase in embryonic CHH is most likely due to synthesis/storage by the developing x-organ/sinus gland complex since the majority of assayable CHH is found in the x-organ/sinus gland of juvenile and adult lobsters (see below).
We then examined whole body content of CHH in lobster larvae. In the first larval stage, it appears that CHH is low initially (early and middle substages) with a peak at the end of the stage (Fig. 3). There is another peak at the end of the Stage II. Most of the whole-body CHH (>90%) in larvae is located in the eyestalks (unpublished observations). The remainder is found in circulation in the hemolymph or intracellularly in other body locations.
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Adult lobsters were next assayed for hemolymph CHH during the molt cycle. For postmolt and intermolt, lobsters were monitored for molt cycle progress and grouped into representatives that had progressed through the molt cycle in 10% subintervals. For the final 10% of premolt, molt-staging criteria were used to determine the precise stage of premolt (Aiken, 1973
). We did not observe any significant differences in the circulating levels of CHH during the molt cycle (data not shown). However, when we used a finer time scale, we observed a dramatic increase in CHH during the hour just prior to the completion of ecdysis (Keller and Chang, unpublished). Our observations in the lobster are consistent with those of Chung et al. (1999) for the crab C. maenas. They demonstrated that this brief peak of CHH at ecdysis is responsible for the rapid influx of water necessary for expansion of the new exoskeleton.
Several lines of evidence indicate that there is a source of CHH immunoactivity in addition to the x-organ/sinus gland (Chang et al., 1999; Chang, 2001). We have previously observed that the subesophageal ganglion is one of these extra-eyestalk sources of CHH. We dissected this ganglion from lobsters that were in various molt stages. The whole ganglion had a CHH content of 266 ± 432 fmol. There were no significant differences in the amounts of CHH contained in the ganglion from one molt stage to the next (data not shown).
From these same lobsters, we had initially removed the eyestalks and then quickly dissected the sinus glands from both eyestalks. The glands were individually homogenized and assayed for CHH. We did not find a difference between the left and right glands regardless of which eyestalk was removed first. There were, however, significant differences in the CHH content of the combined sinus glands from lobsters depending upon the molt stage. A peak of stored CHH was found in glands from mid-premolt (stages D1–D2; Fig. 4). We do not know the significance of this increased content nor do we know if this immunoactivity is represented by CHH-A (which has both hyperglycemic and molt-inhibiting hormone activity; Chang et al., 1990) or by CHH-B (which has hyperglycemic activity only) since our assay does not distinguish between the two peptides.
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It is puzzling that there is an apparent lack of correlation between sinus gland content and hemolymph concentrations of CHH. Since the hemolymph data indicate a general steady-state situation for CHH, an increase in the sinus gland content implies either an increase in synthesis and storage or a decreased release by the x-organ/sinus gland complex (with a concomitant decrease in CHH metabolism and/or elimination). We are unable to distinguish between these possibilities at this time.
As in the larvae, the majority (>90%) of the whole-body CHH content in adult lobsters is contained in the sinus gland. We suspect that this large amount of CHH is held in reserve for times of stress when rapid increases in hemolymph glucose are required (Chang et al., 1998; Stentiford et al., 2001).
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METHYL FARNESOATE |
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Methyl farnesoate (MF) is a sesquiterpene that is related to the insect juvenile hormone. In insects, juvenile hormone has profound developmental and reproductive effects. Elucidation of the role of MF in development and reproduction is currently an active field of investigation. MF is secreted by the mandibular organ (Laufer et al., 1987
). There is some evidence that MF may have a role in larval development by acting as a hormone that retards development (a juvenilizing factor). Relatively low amounts (0.1 ng/g) of MF were identified in lobster larvae (Stages II and III; Borst et al., 1987). When added to the water in which lobster larvae were developing, MF caused a significant increase in the time from hatching to Stage IV. Control larvae (at 19°C) took 20.8 ± 1.5 days while larvae incubated with 10–6 M MF took 22.0 ± 1.3 days (P < 0.01; Borst et al., 1987).
In adults, MF may function in a reproductive capacity. In lobsters, the relative size of the mandibular organ increases much more in adult males than females, suggesting that the mandibular organ may function differentially in reproduction (Aiken, unpublished; cited in Waddy et al., 1995). MF titers in females may be lower than in males because the mandibular organs are smaller and less active or because MF is sequestered by the gonads. MF is present in the lobster ovary at 2.7 ng/g (Borst et al., 1987); however, the ovary is unable to synthesize MF. It is not certain whether these differences in MF titers mediate sex-specific physiology and morphology or whether these differences are the result of sexual differentiation.
The specific role of MF in lobster reproduction is ambiguous. In H. americanus, mandibular organ ablation had no apparent effect on the later phases of female reproduction, including secondary vitellogenesis and oviposition (Byard, 1975). MF injection had no effect upon vitellogenin titer in female lobsters. However, it is possible that MF has a role in the early stages of ovarian development; these early stages of ovarian maturation coincide with elevated MF titers of approximately 2 ng/ml of hemolymph (unpublished data of Tsukimura, Waddy, and Borst; cited in Waddy et al., 1995). As spawning approaches, the hemolymph concentration of MF falls below 0.4 ng/ml. Our laboratory has observed that MF may act as an ecdysiotropin in C. magister (Tamone and Chang, 1993). However, the elevated MF concentration in vitellogenic females cited above do not correlate with observable alterations in circulating ecdysteroids (Chang, 1984).
In other species, there is evidence that supports a role for MF in various reproductive functions (for review see Landau et al., 1997). It remains to be determined if those reproductive functions of MF are mediated without the involvement of ecdysteroids.
We have described the multifunctional nature of three crustacean hormones (or hormone families). Ecdysteroids may serve as morphogens or promote protective membranes during embryonic development. They then function as molting hormones from larval to adult life. In adults, they may act as gonadotropins. Members of the CHH family of neuropeptides appear to be present from embryos to adults and a single peptide can have multiple functions (acting as a molt-inhibiting hormone and as a hyperglycemic hormone). MF may also function as a developmental hormone in larvae and as a gonadotropin in adults. These examples illustrate the amazing economy of nature—a single hormone that can mediate different functions at different life stages.
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ACKNOWLEDGMENTS |
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We thank the many collaborators who have contributed to our understanding of the topics presented in this review and W. A. Hertz for his technical assistance. We also thank the editors and anonymous reviewers who improved this manuscript. Some of the work described in this paper was funded in part by a grant from the National Sea Grant College Program, National Oceanic and Atmospheric Administration, U.S. Department of Commerce, under grant number NA66RG0477, project number R/A-111A through the California Sea Grant College System, and in part by the California State Resources Agency. The views expressed herein are those of the authors and do not necessarily reflect the views of NOAA or any of its sub-agencies. Contribution Number 2149 from the Bodega Marine Laboratory, University of California at Davis.
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FOOTNOTES |
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1 From the Symposium Ontogenetic Strategies of Invertebrates in Aquatic Environments presented at the Annual Meeting of The Society for Integrative and Comparative Biology, 3–7 January 2001, at Chicago, Illinois.
2 To whom all correspondence should be sent; E-mail: eschang{at}ucdavis.edu
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References |
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Abramowitz, A., F. Hisaw, and D. Papandrea. 1944. The occurrence of a diabetogenic factor in the eyestalks of crustaceans. Biol. Bull, 86:1-4.
Aiken, D. E. 1973. Proecdysis, setal development, and molt prediction in the lobster. J. Fish. Res. Board Can, 30:1334-1337.
Beltz, B. S., S. M. Helluy, M. L. Ruchhoeft, and L. S. Gammill. 1992. Aspects of the embryology and neural development of the American lobster. J. Exp. Zool, 261:288-297.[CrossRef][Web of Science][Medline]
Beltz, B. S., and E. A. Kravitz. 1987. Physiological identification, morphological analysis, and development of identified serotonin-proctolin containing neurons in the lobster ventral nerve cord. J. Neurosci, 7:533-546.[Abstract]
Beltz, B. S., M. S. Pontes, S. M. Helluy, and E. A. Kravitz. 1990. Patterns of appearance of serotonin and proctolin immunoreactivities in the developing nervous system of the American lobster. J. Neurobiol, 21:521-542.[CrossRef][Web of Science][Medline]
Borst, D. W., H. Laufer, M. Landau, E. S. Chang, W. A. Hertz, F. C. Baker, and D. A. Schooley. 1987. Methyl farnesoate (MF) and its role in crustacean reproduction and development. Insect Biochem, 17:1123-1127.[CrossRef]
Butenandt, A., and P. Karlson. 1954. Uber die Isolierung eines Metamorphose-Hormons der Insekten in Kristallisierter Form. Z. Naturforsch, 9B:389-391.
Byard, E. H. 1975. The female specific protein and reproduction in the lobster, Homarus americanus. Ph.D. Thesis, Univ. of Western Ontario, London, Ontario.
Chang, E. S. 1984. Ecdysteroids in Crustacea: Role in reproduction, molting, and larval development. In W. Engels, W. H. Clark, A. Fischer, and D. F. Went (eds.), Advances in invertebrate reproduction, Vol. 3, pp. 223–230. Elsevier Science Publishers, Amsterdam.
Chang, E. S. 1993. Comparative endocrinology of molting and reproduction: Insects and crustaceans. Ann. Rev. Entomol, 38:161-180.[Web of Science][Medline]
Chang, E. S. 1997. Chemistry of crustacean hormones that regulate growth and reproduction. In M. Fingerman, R. Nagabhushanam, and M.-F. Thompson (eds.), Recent advances in marine biotechnology, pp. 163–178. Oxford & IBH Publishing, New Delhi.
Chang, E. S. 2001. Crustacean hyperglycemic hormone family: Old paradigms and new perspectives. Amer. Zool, 41:380-388.[CrossRef]
Chang, E. S., and M. J. Bruce. 1980. Ecdysteroid titers of juvenile lobsters following molt induction. J. Exp. Zool, 214:157-160.[CrossRef]
Chang, E. S., and M. J. Bruce. 1981. Ecdysteroid titers of larval lobsters. Comp. Biochem. Physiol, 70A:239-241.[CrossRef]
Chang, E. S., S. A. Chang, B. S. Beltz, and E. A. Kravitz. 1999. Crustacean hyperglycemic hormone in the lobster central nervous system: Localization and release from cells in the subesophageal ganglion and thoracic second roots. J. Comp. Neurol, 414:50-56.[CrossRef][Web of Science][Medline]
Chang, E. S., and D. E. Conklin. 1993. Larval culture of the American lobster (Homarus americanus). In J. P. McVey (ed.), CRC handbook of mariculture, 2nd ed., Vol. 1, pp. 489–495. CRC Press, Boca Raton.
Chang, E. S., W. A. Hertz, and G. D. Prestwich. 1992. Reproductive endocrinology of the shrimp Sicyonia ingentis: Steroid, peptide, and terpenoid hormones. NOAA Tech Rep NMFS, 106:1-6.
Chang, E. S., R. Keller, and S. A. Chang. 1998. Quantification of crustacean hyperglycemic hormone by ELISA in hemolymph of the lobster, Homarus americanus, following various stresses. Gen. Comp. Endocrinol, 111:359-366.[CrossRef][Web of Science][Medline]
Chang, E. S., and J. D. O'Connor. 1979. Arthropod molting hormones. In B. M. Jaffe and H. R. Behrman (eds.), Methods of hormone radioimmunoassay, 2nd ed., pp. 797–814. Academic Press, New York.
Chang, E. S., G. D. Prestwich, and M. J. Bruce. 1990. Amino acid sequence of a peptide with both molt-inhibiting and hyperglycemic activities in the lobster, Homarus americanus. Biochem. Biophys. Res. Commun, 171:818-826.[CrossRef][Web of Science][Medline]
Chung, J. S., H. Dircksen, and S. G. Webster. 1999. A remarkable, precisely timed release of hyperglycemic hormone from endocrine cells in the gut is associated with ecdysis in the crab Carcinus maenas. Proc. Natl. Acad. Sci. U.S.A, 96:13103-13107.
Conklin, D. E., and E. S. Chang. 1993. Culture of juvenile lobsters (Homarus americanus). In J. P. McVey (ed.), CRC handbook of mariculture, 2nd ed., Vol. 1, pp. 497–510. CRC Press, Boca Raton.
De Kleijn, D. P. V., and F. Van Herp. 1995. Molecular biology of neurohormone precursors in the eyestalk of Crustacea. Comp. Biochem. Physiol, 112B:573-579.[CrossRef][Medline]
Factor, J. R. 1995. Introduction, anatomy, and life history. In J. R. Factor (ed.), Biology of the lobster Homarus americanus, pp. 1–11. Academic Press, San Diego.
Goudeau, M., F. Lachaise, G. Carpentier, and B. Goxe. 1990. High titers of ecdysteroids are associated with the secretory process of embryonic envelopes in the European lobster. Tiss. Cell, 22:269-281.[CrossRef]
Hampshire, F., and D. H. S. Horn. 1966. Structure of crustecdysone, a crustacean moulting hormone. Chem. Commun, 1966:37-38.
Horn, D. H. S., E. J. Middleton, J. A. Wunderlich, and F. Hampshire. 1966. Identity of the moulting hormones of insects and crustaceans. Chem. Commun, 1966:339-340.
Keller, R. 1992. Crustacean neuropeptides: Structures, functions and comparative aspects. Experientia, 48:439-448.[CrossRef][Web of Science][Medline]
Lachaise, F., M. Goudeau, C. Hetru, C. Kappler, and J. A. Hoffmann. 1981. Ecdysteroids and ovarian development in the shore crab, Carcinus maenas Hoppe-Seyler's Z. Physiol. Chem, 362:521-529.
Lachaise, F., and J. A. Hoffmann. 1982. Ecdysteroids and embryonic development in the shore crab, Carcinus maenas. Hoppe-Seyler's Z. Physiol. Chem, 363:1059-1067.[Web of Science][Medline]
Lafont, R. 1997. Ecdysteroids and related molecules in animals and plants. Arch. Insect Biochem. Physiol, 35:3-20.[Medline]
Landau, M., W. J. Biggers, and H. Laufer. 1997. Invertebrate endocrinology. In W. H. Dantzler (ed.), Handbook of physiology, Section 13, Comparative physiology, pp. 1291–1389. Oxford Univ. Press, New York.
Lanot, R., A. Dorn, B. Günster, J. Thiebold, M. Lagueux, and J. A. Hoffmann. 1989. Functions of ecdysteroids in oocyte maturation and embryonic development of insects. In J. Koolman (ed.), Ecdysone: From chemistry to mode of action, pp. 262–270. Georg Thieme Verlag, Stuttgart.
Laufer, H., D. Borst, F. C. Baker, C. Carrasco, M. Sinkus, C. C. Reuter, L. W. Tsai, and D. A. Schooley. 1987. Identification of a juvenile hormone-like compound in a crustacean. Science, 235:202-205.
Okazaki, R. K., and E. S. Chang. 1991. Ecdysteroids in the embryos and sera of the crab, Cancer magister and C. anthonyi. Gen. Comp. Endocrinol, 81:174-186.[CrossRef][Web of Science][Medline]
Perkins, H. C. 1972. Developmental rates at various temperatures of embryos of the northern lobster (Homarus americanus Milne-Edwards). Fish. Bull, 70:95-99.
Schneider, H., P. Budhiraja, I. Walter, B. S. Beltz, E. Peckol, and E. A. Kravitz. 1996. Developmental expression of the octopamine phenotype in lobsters, Homarus americanus. J. Comp. Neurol, 371:3-14.[CrossRef][Web of Science][Medline]
Skinner, D. M. 1985. Molting and regeneration. In D. E. Bliss and L. H. Mantel (eds.), The biology of Crustacea, Vol. 9, pp. 43–146. Academic Press, New York.
Snyder, M. J., and E. S. Chang. 1986a.. Effects of eyestalk ablation on larval molting rates and morphological development of the American lobster Homarus americanus. Biol. Bull, 170:232-243.
Snyder, M. J., and E. S. Chang. 1986b.. Effects of sinus gland extracts on larval molting and ecdysteroid titers of the American lobster Homarus americanus. Biol. Bull, 170:244-254.
Stentiford, G. D., E. S. Chang, S. A. Chang, and D. M. Neil. 2001. Carbohydrate dynamics and the crustacean hyperglycemic hormone (CHH): Effects of parasitic infection in Norway lobsters (Nephrops norvegicus). Gen. Comp. Endocrinol, 121:13-22.[CrossRef][Web of Science][Medline]
Subramoniam, T. 2000. Crustacean ecdysteroids in reproduction and embryogenesis. Comp. Biochem. Physiol. C, 125:135-156.
Tamone, S. L., and E. S. Chang. 1993. Methyl farnesoate stimulates ecdysteroid secretion from crab Y-organs in vitro. Gen. Comp. Endocrinol, 89:425-432.[CrossRef][Web of Science][Medline]
Van Herp, F. 1998. Molecular, cytological and physiological aspects of the crustacean hyperglycemic hormone family. In G. M. Coast and S. G. Webster (eds.), Recent advances in anthropod endocrinology, pp. 53–70. Cambridge Univ. Press, Cambridge.
Waddy, S. L., D. E. Aiken, and D. P. V. De Klein. 1995. Control of growth and reproduction. In J. R. Factor (ed.), Biology of the lobster Homarus americanus, pp. 217–266. Academic Press, San Diego.
Webster, S. G. 1998. Neuropeptides inhibiting growth and reproduction in crustaceans. In G. M. Coast and S. G. Webster (eds.), Recent advances in anthropod endocrinology, pp. 33–52. Cambridge Univ. Press, Cambridge.
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