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Fecal Corticosterone Assessment in the Epaulette Shark, Hemiscyllium Ocellatum AMANDA H

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Fecal Corticosterone Assessment in the Epaulette Shark, Hemiscyllium Ocellatum AMANDA H JOURNAL OF EXPERIMENTAL ZOOLOGY 299A:188–196 (2003) Fecal Corticosterone Assessment in the Epaulette Shark, Hemiscyllium ocellatum AMANDA H. KARSTEN* and JOHN W. TURNER, JR.n Medical College of Ohio, Department of Physiology and Molecular Medicine, Toledo, Ohio 43614–5804 ABSTRACT The present study examined the feasibility of measuring the steroid hormone corticosterone in fecal extracts of epaulette sharks, Hemiscyllium ocellatum. Six immature, captive- raised epaulette sharks (four females and two males) were obtained from two different zoos and were maintained in a closed-system, 530–liter aquarium. After a one-month adaptation, fecal samples were collected daily from each animal for 33 days. Five-day sets of samples were pooled within animals to insure sufficient material for analysis. Fecal hormone extraction was achieved using repeated cycles of dichloromethane and aqueous washes. The levels of corticosterone were measured by reverse-phase high-performance liquid chromatography (HPLC). Corticosterone presence in HPLC eluent peaks from fecal extracts was determined by comparison of the elution pattern of corticosterone standard with the elution patterns of fecal extracts with and without the addition of tritiated corticosterone or exogenous, unlabeled corticosterone. Exclusive presence of corticosterone in HPLC eluent peaks presumed to be corticosterone was determined by nuclear magnetic resonance mass spectrometry. Corticosterone levels, calculated from a 10–point standard curve, ranged from 1.2 to 20.9 ng/g feces across all sharks, with 92.3% of values being r13.5 ng/g. Within individuals, the lowest average for corticosterone levels across 33 days was 2.670.4 ng/g feces, and the highest average was 8.472.2 ng/g feces. This study demonstrated that corticosterone was extractable from and reliably measurable in fecal extracts of epaulette sharks. This is the first evidence of this hormone in epaulette sharks and the first report of fecal corticosterone in elasmobranchs. J. Exp. Zool. 299A:188–196, 2003. r 2003 Wiley-Liss, Inc. INTRODUCTION glucocorticoids have also been measured in a variety of other mammals (Whitten, ’97; Jurke In the face of ecological compromises associated et al., ’97; Goymann et al., ’99; Wasser et al., 2000; with marine environments in recent years (Rogers Turner et al., 2002) and in birds (Wasser and et al., ’94; Carpenter et al., ’98; Abelson et al., ’99) Starling, ’88). Glucocorticoids are only sparingly assessment of stress in marine vertebrates may be soluble in water, therefore, their measurement in useful. Glucocorticoids have been employed as fecal casts of marine animals may be feasible, if indicators of stress (Asterita, ’85) and have been these casts can be identified and collected. measured in fish (Barton and Iwama, ’91; Bonga The present study was undertaken to determine and Wendelaar, ’97; Grutter and Pankhurst, 2000) the feasibility and reliability of measuring the and elasmobranchs (Rasmussen and Crow, ’93; stress-related hormone, corticosterone, in extracts Rasmussen and Gruber, ’93; Snelson et al., ’97). of feces obtained in captivity from the reef- Studies to date have utilized plasma or serum for glucocorticoid assessment. However, invasive techniques of blood collection are in themselves Dr. Karsten’s current address is: Clemson University, Pendelton, stressful and have been found to increase the South Carolina, 29670–0709 Grant sponsor: MCO Research Incentive Program; Grant number levels of corticosteroids (Bassett and Hinks, ’69; 96850004 n Stephens, ’80). Correspondence to: Amanda H. Karsten, Clemson University, Department of Environmental Toxicology, 509 Westinghouse Road, An alternative means for obtaining information P.O. Box 709, Pendleton, SC 29670–0709. E-mail: hkamand@ regarding glucocorticoids is via analysis of fecal clemson.edu; or: John W. Turner, Medical College of Ohio, Depart- ment of Physiology and Molecular Medicine, Toledo, Ohio, 43614– extracts. Miller et al. (’91) used this noninvasive 5804. E-mail: [email protected] approach to measure stress in Rocky Mountain Received 11 February 2003; Accepted 27 June 2003 Published online in Wiley InterScience (www.interscience.wiley. bighorn sheep (Ovis canadensis canadensis). Fecal com) DOI: 10.1002/jez.a.10300 r 2003 WILEY-LISS, INC. FECAL CORTICOSTERONE IN SHARK 189 dependent epaulette shark (Hemiscyllium removed, passed through a 0.45 mm syringe filter, ocellatum). vacuum dried and stored in a À401C freezer. Samples were thawed and reconstituted in 50 ml of 100% acetonitrile (ACN) for 10 min. Water (18 MATERIALS AND METHODS megaohm) was added in three portions totaling 450 ml (with 2 min. of mixing per portion). One- This study was performed under auspices of half of the final 500 ml reconstituted sample was animal-use protocol (IACUC #100679) at the injected into a reverse-phase high-performance Medical College of Ohio. The epaulette shark is a liquid chromatography (RP-HPLC model 300, carnivorous species found off the coast of Australia Dionex Corporation, Sunnyvale, CA) attached to and New Guinea (Dingerkus and DeFino, ’83; a C–18 column (Waters Corp., Milford, MA) and a Dingerkus, ’91; Last and Stevens, ’94; Heupel and variable-wavelength UV detector locked at a Bennett, ’98). Advantages of this shark species for wavelength of 240 m (Dionex Corporation, Sunny- the present study include its ready adaptation to vale, CA). The procedure utilized a water blank to captivity (i.e., opportunity to observe basal corti- establish stable baseline and a corticosterone costerone levels) and small size (o50 cm in this standard at the beginning, middle, and end of study), compared to other shark species. Six each fecal-extract set. epaulette sharks (four females and two males) Sample hormone concentration was based on were used. Four of these animals were born in UV absorbance of the area under the elution peak January, 1998, at the Florida Aquarium and two for corticosterone. Each corticosterone concentra- were born at the Columbus Zoo in January, 1998. tion was calculated from a 10–point standard All subjects were sexually immature, a circum- curve (range 1.0 to 100.0 ng). The correlation stance which minimized the possibility of con- coefficient for actual values vs. calculated loga- founding effects of sex steroids in corticosterone rithmic curve was 0.992. Hormone values are assessment (Heupel et al., ’99). reported as ng/g feces (wet weight), and the lower The animals were placed in a 530–liter, closed- limit of corticosterone detection was 1.0 ng per system, salt-water aquarium in conditions similar sample. Variation in the HPLC analysis was to their previous aquarium environments. Water determined by measuring elution-peak times and was tested every one to three days to monitor elution-peak concentrations of corticosterone in salinity (30–32 ppt), ammonia (o0.1 mg/l), tem- seven aliquots of the same pooled shark fecal perature (651–701F) and pH (8.1–8.4). The animals extract. experienced a 12–hr light/dark cycle and were fed Some fecal samples were in the water up to 12 a mixed diet of shrimp, scallops, krill, and smelt hours before collection. Therefore it was necessary five days per week. Food consumption approxi- to determine whether biodegradation of corticos- mated 1% of body weight. The aquarium was terone occurred. Four grams of pooled feces was divided into six equal sections by plastic mesh, slurried in 4 ml of aquarium water, and the slurry separating individuals and permitting separate was spiked with tritiated corticosterone (2.1 Â 105 collection of feces from each shark. Fecal casts counts per min). One-half of the slurry was were solid, well-formed spirals and were collected immediately extracted, and the other half was from each animal daily for 33 days and were incubated at 271C for 12 hrs and then extracted. frozen at À401C until extracted and assayed. Up Both aliquots were run on HPLC and the eluent to five days of fecal samples from each animal were peaks presumptive for corticosterone were mixed combined to ensure that there was sufficient with Sigma Fluor cocktail (Sigma, St. Louis, MO) hormone for analysis. for aqueous samples. Radioactivity was deter- All samples were extracted as described below. mined in a Beckman LS 6500 liquid scintillation Four ml of fecal slurry (2 ml of tank water and counter (Beckman Coulter, Inc., Fullerton, CA). 2 ml of fecal material) was homogenized and added To support the identity of corticosterone in to a plastic scintillation vial containing 12 ml of HPLC eluents, tritiated corticosterone (ICN Phar- dichloromethane (MeCl2). The mixture was mixed maceuticals, Inc. Costa Mesa, CA) was used in for 60 min, followed by 10 min centrifugation at initial HPLC elution experiments. A 0.1 ml aliquot 2000 g. The MeCl2 layer was removed and shaken of the tritiated corticosterone was added to with 1 ml of 0.10 N NaOH for 2 min. The MeCl2 scintillation fluid and measured for radioactivity layer was then removed and mixed with 1 ml of as above. Aliquots of this tritiated corticosterone 18 megaohm water for 2 min. This layer was were then added to non-radioactive corticosterone 190 A.H. KARSTEN AND J.W. TURNER TABLE 1 Comparison of HPLC elution pattern of corticosterone 19.41 and 19.60 min with an average of 19.52 min. standard and fecal extract using tritiated corticosterone as a spike Representative elution profiles for an unlabeled, b spiked fecal extract and an unspiked fecal extract PERCENT OF TOTAL TRITIUM SPIKE ELUTION are presented in Figure 1. TIMEa (min) STANDARD FECAL EXTRACT The fecal sample spiked with tritiated corticos- 16 1.8 2.0 terone and the tritiated corticosterone standard 17 0.8 3.1 alone showed HPLC retention times of 19.58 and 18 2.3 3.1 19.60 min, respectively, suggesting reliable mea- 19 88.1 87.3 surement of corticosterone by HPLC and non- 20 5.3 2.9 interference by fecal constituents in corticosterone 21 1.0 0.8 measurement (Table 1).
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