Heat shock induced metamorphosis of the queen conch, Strombus gigas: comparison with induction by algal associated cues.ABSTRACT Recent research indicates that abiotic a·bi·ot·ic adj. Nonliving: The abiotic factors of the environment include light, temperature, and atmospheric gases. a environmental factors, including temperature, may be as important as chemical cues in controlling the induction of metamorphosis metamorphosis (mĕt'əmôr`fəsĭs) [Gr.,=transformation], in zoology, term used to describe a form of development from egg to adult in which there is a series of distinct stages. of marine invertebrate invertebrate (ĭn'vûr`təbrət, –brāt'), any animal lacking a backbone. The invertebrates include the tunicates and lancelets of phylum Chordata, as well as all animal phyla other than Chordata. larvae Larvae, in Roman religion Larvae: see lemures. . In this study, the effects of elevated temperature or heat shock on the induction of metamorphosis in the tropical marine gastropod gastropod, member of the class Gastropoda, the largest and most successful class of mollusks (phylum Mollusca), containing over 35,000 living species and 15,000 fossil forms. , Strombus gigas, are examined. Elevations in temperature above culture temperatures (28[degrees]C to 29[degrees]C) to 37[degrees]C to 38[degrees]C induced high levels of metamorphosis (77% to 100%), equivalent to those induced by a known algal algal pertaining to or caused by algae. algal infection is very rare but systemic and udder infections are recorded. See protothecosis. algal mastitis the algae Prototheca trispora and P. associated inducer inducer /in·duc·er/ (in-dldbomacs´er) a molecule that causes a cell or organism to accelerate synthesis of an enzyme or sequence of enzymes in response to a developmental signal. in·duc·er n. , an extract of Laurencia poitei. The age for competency to metamorphosis and the exposure time needed to induce this process were similar for heat shock and for the algal-associated cue. Understanding the interaction between abiotic and biotic factors during metamorphosis may help to better predict recruitment patterns for this commercially important species. KEY WORDS: heat shock, larvae, metamorphosis, Strombus gigas, queen conch (Zool.) a very large West Indian cameo conch (Cassis cameo). It is much used for making cameos. See also: Queen INTRODUCTION The survival, growth and development of marine invertebrate larvae are affected by abiotic environmental factors such as salinity and temperature (see Pechenik 1987, Pechenik et al. 1998 for reviews). Recent work indicates that these factors can also directly affect larval larval 1. pertaining to larvae. 2. larvate. larval migrans see cutaneous and visceral larva migrans. metamorphosis. Low salinity decreased induction of metamorphosis of the Rhizocephalan rhi·zo·ceph·a·lan n. Any of various small aquatic crustaceans of the order Rhizocephala that are parasitic on other crustaceans. [From New Latin Rhizocephala, order name : rhizo- barnacle barnacle, common name of the sedentary crustacean animals constituting the subclass Cirripedia. Barnacles are exclusively marine and are quite unlike any other crustacean because of the permanently attached, or sessile, mode of existence for which they are highly Loxothylacus texanus (Tindle et al. 2004) and increased the time it took to metamorphose for the ascidian ascidian: see Chordata; tunicate. Styela plicata (Thiyagarajan & Qian 2003). Elevated temperatures (heat shock) induced metamorphosis in several temperate marine invertebrates (Lutz et al. 1970, Pechenik 1984, Kroiher et al. 1992, Pennington et al. 1999, Gaudette et al. 2001). In some cases, as with the brachiopod Laqueus californianus, abnormal metamorphosis or incomplete metamorphosis incomplete metamorphosis n. A life cycle of certain insects, such as crickets and grasshoppers, characterized by the absence of a pupal stage between the immature and adult stages. was induced by heat shock (Pennington et al. 1999). However, in other species, the induction was similar to that seen with known chemical inducers (Kroiher et al. 1992, Gaudette et al. 2001). Understanding how environmental factors affect larval development and metamorphosis will help to explain variability in recruitment and how changes in environmental conditions may impact this process (see Pechenik 1987 for review). Salinity and temperature have a significant effect on growth and survival of the queen conch, Strombus gigas, a tropical marine gastropod. High growth rates Growth Rates The compounded annualized rate of growth of a company's revenues, earnings, dividends, or other figures. Notes: Remember, historically high growth rates don't always mean a high rate of growth looking into the future. and survival were seen at temperatures from 24[degrees]C to 32[degrees]C and 30-40 practical salinity units (psu) with high mortality at temperatures <24[degrees]C and salinities >40 psu (Davis 2000). The effects of salinity and temperature on metamorphosis of queen conch have not been examined. In this study, the effects of heat shock on metamorphosis in S. gigas were examined. Exposure temperature and duration of exposure to increased temperature were considered, as was the onset of metamorphic met·a·mor·phic adj. 1. also met·a·mor·phous Of, relating to, or characterized by metamorphosis. 2. Geology Changed in structure or composition as a result of metamorphism. Used of rock. competence. Responses to heat shock were compared with those seen with a known inducer of metamorphosis, an extract of the red macroalga Laurencia poitei (Davis 1994a, Davis & Stoner ston·er n. 1. One that stones. 2. Slang a. One who is habitually intoxicated by alcohol or drugs. b. One who is a delinquent or failure. 1994, Boettcher & Targett 1996, Boettcher & Targett 1998). MATERIAL AND METHODS Metamorphosis Assays All metamorphosis assays were carried out at the Caicos Conch conch (kŏngk, kŏnch, kôngk), common name for certain marine gastropod mollusks having a heavy, spiral shell, the whorls of which overlap each other. Farm (CCF CCF abbr. Cooperative Commonwealth Federation of Canada ), Providenciales, Turks and Caicos, BWI BWI abbr. British West Indies , using S. gigas larvae provided by CCF. Techniques for the culture of conch larvae were as described in Davis (1994a). Assays were run using a variation of the methods described in Boettcher and Targett (1996). The assays were conducted as static no-choice experiments with 5 replicates per treatment and 10 larvae per replicate. Larvae within an experiment were all from a single hatch of a single egg mass. Assays were run in 118 mL plastic containers with 50-70 mL (based on experiment) of UV sterilized ster·il·ize tr.v. ster·il·ized, ster·il·iz·ing, ster·il·iz·es 1. To make free from live bacteria or other microorganisms. 2. 10-[micro]m filtered seawater seawater Water that makes up the oceans and seas. Seawater is a complex mixture of 96.5% water, 2.5% salts, and small amounts of other substances. Much of the world's magnesium is recovered from seawater, as are large quantities of bromine. . Each assay included a negative control (seawater only at culture temperatures, 28[degrees]C to 29[degrees]C) as a test for spontaneous metamorphosis and a positive control (an extract of Laurencia poitei [0.01 g wet weight/mL seawater = 20 [micro]l extract/mL seawater], 28[degrees]C to 29[degrees]C) as a measure of metamorphic competence (Davis 1994a, Boettcher & Targett 1996). Except as noted in the exposure time experiment, exposure times for all treatments were 4 h, after which the larvae were transferred to a fresh volume of sterilized seawater. Percent metamorphosis was determined after 24 h and was calculated as the total number of larvae metamorphosed/total number recovered (Pearce & Scheibling 1990). In all experiments the majority of larvae (>95%) were recovered. Experiments were run at ambient salinity (ca 39 practical salinity units), pH (8.3-8.4) and light conditions (ca 12 h light:12 h dark). Differences in metamorphosis between or among treatments in each experiment were compared using Student t-tests or Model 1 ANOVAs and Tukey multiple comparison tests ([alpha] = 0.05) (Zar 1984). Treatments in which percent metamorphosis was equal to zero for all replicates were not included in the statistical analyses. Given that percentages follow a binomial distribution binomial distribution n. The frequency distribution of the probability of a specified number of successes in an arbitrary number of repeated independent Bernoulli trials. Also called Bernoulli distribution. ; all data were arcsine transformed before analyses were performed (Zar 1984). For ease of comparison, results for all treatments are included in figures and are presented as percentages. Exposure Temperature All heat shock treatments were run in water baths raised to the appropriate temperature. Four experiments were run examining the effects of exposure to temperatures from 4[degrees]C to 15[degrees]C above culture temperatures (28[degrees]C to 29[degrees]C) on larval metamorphosis. In all cases, acute response to heat shock was tested. In the first experiment, the exposure temperatures were 33[degrees] to 34[degrees], 35[degrees] to 36[degrees]and 37[degrees] to 38[degrees]C. Temperatures of 37[degrees] to 38[degrees], 42[degrees] to 43[degrees] and 45[degrees]C to 46[degrees]C were tested in the second experiment; 32[degrees] to 33[degrees], 37[degrees] to 38[degrees] and 42[degrees]C to 43[degrees]C in the third; and 32[degrees] to 33[degrees], 37[degrees] to 38[degrees] and 39[degrees]C to 40[degrees]C in the fourth. Exposure Time The effect of exposure time to heat shock on induction of metamorphosis was examined in a single experiment using the following exposure times: 1, 2 and 4 h. Based on the results of the exposure temperature experiments, an exposure temperature of 37[degrees]C to 38[degrees]C was chosen. The responses of larvae to heat shock at the three exposure times were compared with their response to the L. poitei-associated cue (28[degrees]C to 29[degrees]C) and to seawater at normal culture temperatures (28[degrees]C to 29[degrees]C). Larval Competence The competence of larvae to metamorphose in response to heat shock was examined by testing the responses of larvae to an exposure temperature of 37[degrees]C to 38[degrees]C as a function of age. The response of larvae to heat shock was compared with their response to the L. poitei-associated cue (28[degrees]C to 29[degrees]C) and to seawater at normal culture temperatures (28[degrees]C to 29[degrees]C) as a function of age. Larvae from a single hatch of a single egg mass were used for all treatments and ages in a single experiment. The experiment was repeated with two hatches of larvae from two separate egg masses. Larvae from the first hatch were tested on alternate days from day 5-17 posthatch, and larvae from the second hatch were tested on alternate days from day 3-15 posthatch. RESULTS Exposure Temperature Exposure to temperatures <37[degrees]C had no significant effect on larval metamorphosis or behavior. At these temperatures, most larvae continued to swim and <30% were induced to metamorphose (Fig. 1a, b, c). Induction at these temperatures was significantly lower than that seen for the L. poitei-associated inducer, although, in one experiment spontaneous metamorphosis at culture temperature was not statistically different from that induced by the L-poitei associated cue (Fig. 1b). High levels of metamorphosis were seen when larvae were exposed to temperatures of 37[degrees]C to 38[degrees]C (Fig. 1a, b, c). Percent metamorphosis induced by this temperature range was not significantly different than that induced by the L. poitei extract (Fig. 1a, b, c). Exposure to temperatures >38[degrees]C induced metamorphosis, however, there was high mortality post metamorphosis (Fig. 1b, c). One hundred percent mortality was seen at temperatures of >41[degrees]C (Fig. 1b and Experiment 2 data not shown). At these temperatures, larval tissue began to break apart, therefore, it was unclear if metamorphosis occurred prior to mortality. [FIGURE 1 OMITTED] Exposure Time There was no significant effect of 1 h heat shock (37[degrees]C to 38[degrees]C) on larval metamorphosis (Fig. 2). However, exposure to heat shock for 2 h and 4 h induced as many larvae to metamorphose as the 4 h L. poitei treatment (Fig. 2). [FIGURE 2 OMITTED] Larval Competence Larvae became competent to metamorphose at the same stage for the L. poitei-associated cue and heat shock. Low percent metamorphosis (<5%) was seen in larvae <11 days posthatch (Fig. 3a, b). These larvae were morphologically precompetent using the following characteristics: presence of shell beak beak or bill Stiff, projecting oral structure of birds and turtles (both of which lack teeth) and certain other animals (e.g., cephalopods and some insects, fishes, and mammals). structure projecting over shell aperture, primarily orange pigment on the foot, and rounding of the left posterior lobe lobe (lob) 1. a more or less well-defined portion of an organ or gland. 2. one of the main divisions of a tooth crown. of the foot (Davis 1994a, 1994b). On day 11 posthatch, low percent metamorphosis (range of means: 16% to 38%) was seen in response to both inducers with no significant difference in metamorphosis between inducers (Fig. 3a, b). By this age larvae had lost the prominent beak, increased green pigmentation pigmentation, name for the coloring matter found in certain plant and animal cells and for the color produced thereby. Pigmentation occurs in nearly all living organisms. on their foot, and the claw of the adult foot had begun to extend from the left posterior lobe of the foot. High percent metamorphosis (range of means: 77% to 100%) was seen for both treatments on days 13 and 15 posthatch (Fig. 3a, b). For both days, percent metamorphosis induced by heat shock was significantly lower than that induced by the L. poitei-associated cue for one of the experiments, however, there was no significant difference between inducers for the other experiment (Fig. 3a vs. b). The larvae at these ages were considered morphologically competent (Davis, 1994a, 1994b). They had completely lost the beak projection, pigment on the foot was dominantly green, and the adult claw was fully extended. On day 17 posthatch high levels of metamorphosis were induced by the L. poitei-associated cue (98%), but there was a drop in percent metamorphosis in response to heat shock (55%) with a significant difference between treatments (Fig. 3 a). [FIGURE 3 OMITTED] DISCUSSION The responses of S. gigas larvae to heat shock parallel those of several temperate marine invertebrates that were tested with this inducer of metamorphosis. As was seen for the hydroid Hydractinia echinata and the tunicate tunicate (t  `nəkĭt), marine animal of the phylum Chordata, which also includes the vertebrates. Ciona intestinales (Kroiher et al. 1992),
exposure of S. gigas to temperatures of 10[degrees]C above culture
temperatures led to high levels of metamorphosis. Because tests were run
with S. gigas, H. echinata, and C. intestinales cultured at only one
temperature; it is unclear if the induction temperature for these
species is based on absolute increases in temperature as with the
gastropod Crepidula fornicata or with relative increases (Kroiher et al.
1992, Gaudette et al. 2001). However, for all four species, there was a
narrow range of temperatures that induced metamorphosis, and at
temperatures 12[degrees]C to 15[degrees]C above culture temperatures
high larval mortality associated with the disintegration of larval
tissue occurred (Kroiher et al. 1992, Gaudette et al. 2001). Heat shock
induced high levels of metamorphosis in S. gigas and C. fornicata in as
little as 2 h (Gaudette et al. 2001). The optimal exposure times for H.
echinata and C. intestinales were slightly longer, ranging from 3-5 h
(Kroiher et al. 1992). For S. gigas, the timing required for a response
to heat shock was similar to the timing required for a response to the
algal inducer, L. poit i (Boettcher & Targett 1998).
There were differences in the responses of the two gastropods, C. fornicata and S. gigas, in terms of the age at which they could be induced to metamorphose by heat shock. Competence to metamorphose in S. gigas occurred at similar developmental stages for both heat shock and L. poitei extract, however, there was a delay in competence to metamorphose seen for C. fornicata in response to heat shock relative to induction by elevated potassium levels (Gaudette et al. 2001). This delay is similar to that seen for S. gigas in response to hydrogen peroxide hydrogen peroxide, chemical compound, H2O2, a colorless, syrupy liquid that is a strong oxidizing agent and, in water solution, a weak acid. It is miscible with cold water and is soluble in alcohol and ether. (pers. obs.). Differences in duration of competency for S. gigas between the algal-associated inducer and heat shock are suggested by the results of the first competency experiment. On day 17 posthatch, the mean percent metamorphosis induced by heat shock was significantly less than that induced by the L. poitei extract and only ca 60% of that induced by heat shock on day 15 posthatch. Algal associated chemical cues are known to be key factors in the induction of metamorphosis of S. gigas and it is believed that these cues allow conch to identify appropriate habitat for subsequent juvenile development (Davis & Stoner 1994, Boettcher & Targett 1996, Boettcher & Targett 1998). However, as this study suggests, abiotic environmental factors may interact with these chemical cues and potentially lead to metamorphosis of larvae in areas not predicted to support juveniles. Few studies have identified sites with newly metamorphosed (<30 mm) juvenile queen conch and thus there is not a clear understanding of their distribution in the wild (Wickland et al. 1991, Sandt & Stoner 1993, Stoner & Ray 1993, Ray & Stoner 1994, Stoner et al. 1994, Stoner et al. 1996, De Jesus-Navarrete & Valencia-Beltran 2003). Interactions between physical and biological factors are believed to be important in explaining the distribution of juveniles >30 mm (Stoner et al. 1996, De Jesus-Navarrete & Valencia-Beltran, 2003). Future studies focused on the interactive effects of biotic biotic /bi·ot·ic/ (bi-ot´ik) 1. pertaining to life or living matter. 2. pertaining to the biota. bi·ot·ic adj. 1. Relating to life or living organisms. and abiotic environmental factors on the metamorphosis process and post-metamorphic survival and growth, like those that have examined these factors on larval development and survival (see Pechenik 1987, Pechenik et al. 1998 for reviews; Davis 2000), will provide a better understanding of the control of metamorphosis in the wild and subsequent recruitment success. ACKNOWLEDGMENTS The author thanks the Caicos Conch Farm for use of both larvae and laboratory space; C. Dyer and D. Martin for laboratory assistance; K. Major, D. Martin, and anonymous reviewers for comments on the text. Research was supported by grants from the University of South Alabama The University of South Alabama is a public, doctoral-level university in Mobile, Alabama, USA. It was created by the Alabama Legislature in 1963, and replaced existing extension programs operated in Mobile by the University of Alabama. Research Council and the Department of Biological Sciences. LITERATURE CITED Boettcher, A. A. & N. M. Targett. 1996. Induction of metamorphosis in queen conch, Strombus gigas Linnaeus, larvae by cues associated with red algae red algae: see seaweed; Rhodophyta. from their nursery grounds. J. Exp. Mar. Biol. Ecol. 196:29-52. Boettcher, A. A. & N. M. Targett. 1998. Role of chemical inducers in larval metamorphosis of queen conch, Strombus gigas Linnaeus: relationship to other marine invertebrate systems. Biol. Bull. 194:132-142. Davis, M. 1994a. Mariculture mariculture marine aquaculture. techniques for queen conch (Strombus gigas Linne) eggmass to juvenile stage. In: R. S. Appeldoorn & B. Rodriguez, editors. The biology, fisheries, mariculture and management of the queen conch. Fundacion Cientifica Los Roques Roques is the name or part of the name of several communes in France:
Davis, M. 1994b. Short-term competence in larvae of queen conch, Strombus gigas: shifts in behavior, morphology, and metamorphic response. Mar. Ecol. Prog. Ser. 104:101-108. Davis, M. 2000. The combined effects of temperature and salinity on growth, development, and survival for tropical gastropod veligers of Strombus gigas. J. Shell Res. 19:883-889. Davis, M. & A. W. Stoner. 1994. Trophic trophic /tro·phic/ (tro´fik) (trof´ik) pertaining to nutrition. troph·ic adj. Of, relating to, or characterized by nutrition. cues induce metamorphosis of queen conch larvae (Strombus gigas Linnaeus). J. Exp. Mar. Biol. Ecol. 180:83-102. De Jesus-Navarrete, A. & V. Valencia-Beltran. 2003. Abundance of Strombus gigas zero year class juveniles at Banco Chinchorro Banco Chinchorro is an atoll reef near Belize that is one of the world's premiere shipwreck diving spots. The reef, which lies in Mexican waters in the Caribbean Sea, is home to at least nine shipwrecks, including two Spanish Galleons. Biosphere biosphere, irregularly shaped envelope of the earth's air, water, and land encompassing the heights and depths at which living things exist. The biosphere is a closed and self-regulating system (see ecology), sustained by grand-scale cycles of energy and of Reserve, Quintana Roo Quintana Roo (kēntä`nä rō`ō), state (1990 pop. 493,277), 19,630 sq mi (50,842 sq km), SE Mexico, on the Caribbean. Chetumal is the capital. , Mexico. Bull Mar. Sci. 73:231-240. Gaudette, M. F., J. L. Lowther & J. A. Pechenik. 2001. Heat shock induces metamorphosis in the larvae of the prosobranch gastropod Crepidula fornicata. J. Exp. Mar. Biol. Ecol. 266:151-164. Kroiher, M., M. Walther & S. Berking. 1992. Heat shock as an inducer of metamorphosis in marine invertebrates. Rouxs Arch. Dev. Biol. 201: 169-172. Lutz, R. A., H. Hidu & K. G. Drobeck. 1970. Acute temperature increase as a stimulus to setting in the American oyster, Crassostrea virginica (Gmelin). Proc. Natl. Shellfish shellfish, popular name for certain edible mollusks (see Mollusca), e.g., oysters, clams, and scallops, and for certain edible crustaceans, e.g., crabs, lobsters, and shrimps. All are aquatic invertebrates with shells; they are not fish. . Assoc. 60:68-71. Pearce, C. M. & R. E. Scheibling. 1990. Induction of metamorphosis of larvae of the green sea urchin sea urchin, spherical-shaped echinoderm with movable spines covering the body. The body wall is a firm, globose shell, or test, made of fused skeletal plates and marked by regularly arranged tubercles to which the movable spines are attached. Strongylocentrotus droebachiensis by coralline cor·al·line adj. 1. Of, consisting of, or producing coral. 2. Resembling coral, especially in color. n. 1. red algae. Biol. Bull 179:304-311. Pechenik, J. A. 1984. Influence of temperature and temperature shifts on the development of chiton chiton (kī`tən), common name for rock-clinging marine mollusks of the class Polyplacophora. Chitons are abundant on rocky coasts throughout most of the world, from the intertidal zone to a depth of about 1,200 ft (400 m). larvae, Mopalia muscosa. Int. J. Invertebr. Reprod. Dev. 7:3-12. Pechenik, J. A. 1987. Environmental influences on larval survival and development. In: A. C. Geise, J. S. Pearce & V. B. Pearce, editors. Reproduction of marine invertebrates, vol. 9. Palo Alto Palo Alto, city, California Palo Alto (păl`ō ăl`tō), city (1990 pop. 55,900), Santa Clara co., W Calif.; inc. 1894. Although primarily residential, Palo Alto has aerospace, electronics, and advanced research industries. : Blackwell Scientific Publications. pp. 551-608. Pechenik, J. A., D. E. Wendt & J. N. Jarrett. 1998. Metamorphosis is not a new beginning. Bioscience 48:901-910. Pennington, J. T., M. N. Tamburri & J. P. Barry. 1999. Development, temperature tolerance, and settlement preference of embryos and larvae of the articulate brachiopod Laqueus californianus. Biol. Bull 196:245-256. Ray, M. & A. W. Stoner. 1994. Experimental analysis of growth and survivorship survivorship n. the right to receive full title or ownership due to having survived another person. Survivorship is particularly applied to persons owning real property or other assets, such as bank accounts or stocks, in "joint tenancy. at a juvenile queen conch aggregation: balancing growth with safety in numbers in numbered parts; as, a book published in numbers. See also: Number . Mar. Ecol. Prog. Ser. 105:47-59. Sandt, V. J. & A. W. Stoner. 1993. Ontogenetic on·to·ge·net·ic adj. Of or relating to ontogeny. shift in habitat by early juvenile queen conch, Strombus gigas: patterns and potential mechanisms. Fish. Bull U.S. 91:516-525. Stoner, A. W. & M. Ray. 1993. Aggregation dynamics in juvenile queen conch: population structure, growth, mortality, and migration. Mar. Biol. 116:571-582. Stoner, A. W., M. D. Hanisak, N. P. Smith & R. A. Armstrong. 1994. Large scale distribution of queen conch nursery habitats In marine environments, a nursery habitat is a subset of all habitats where juveniles of a species occur, having a greater level of productivity per unit area than other juvenile habitats (Beck et al. 2001). : implications for stock enhancement. In: R. S. Appeldoorn & B. Rodriguez, editors. The biology, fisheries, mariculture and management of the queen conch. Fundacion Cientifica Los Roques, Caracas. pp. 169-189. Stoner, A. W., P. A. Pitts & R. A. Armstrong. 1996. Interaction of physical and biological factors in the large-scale distribution of juvenile queen conch in seagrass meadows. Bull, Mar. Sci. 58:217-233. Thiyagarajan, V. & P.-Y. Qian. 2003. Effect of temperature, salinity and delayed attachment on development of the solitary ascidian Styela plicata (Lesueur). J. Exp. Mar. Biol. Ecol. 290:133-146. Tindle, S., E. Boone, J. O'Brien & A. Boettcher. 2004. Effects of salinity on larval stages of the rhizocephalan barnacle Loxothylacus texanus: survival and metamorphosis in response to the host, Callinectes sapidus. J. Exp. Mar. Biol. Ecol. 302:165-176. Wickland, R. I., L. J. Hepp & G. A. Wenz. 1991. Preliminary studies on the early life history of the queen conch, Strombus gigas, in the Exuma Cays, Bahamas. Proc. Gulf Car. Fish. Inst. 40:283-298. Zar, J. H. 1984, Biostatistical analysis, 2nd ed. Englewood Cliffs: Prentice-Hall, Inc. ANNE A. BOETTCHER Department of Biological Sciences, Life Sciences Building 124, University of South Alabama, Mobile, Alabama 36688 E-mail: aboettch@jaguar1.usouthal.edu Note: Parts of this work were previously published in abstract form in the Proceedings of the Gulf and Caribbean Fisheries Institute. |
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