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The Journal of Experimental Biology 212, 2349-2355 Published by The Company of Biologists 2009 doi:10.1242/jeb.027565 Carbon and nitrogen stable isotope turnover rates and diet–tissue discrimination in Florida manatees (Trichechus manatus latirostris) Christy D. Alves-Stanley1 and Graham A. J. Worthy1,2, * 1Physiological Ecology and Bioenergetics Lab, Department of Biology, University of Central Florida, 4000 Central Florida Boulevard, Orlando, FL 32816, USA and 2Hubbs-SeaWorld Research Institute, 6295 Sea Harbor Drive, Orlando, FL 32821, USA INTRODUCTION The isotopic composition of consumer tissues reflects that of local food webs and can be used to predict diet composition, the trophic level at which the consumer is feeding, and even habitat use and migratory patterns (e.g. Deniro and Epstein, 1978; Deniro and Epstein, 1981; Fry, 1981; Peterson and Fry, 1987) (reviewed by Hobson, 1999). Two stable isotope ratios commonly analyzed in feeding ecology studies are those of carbon ( 13 C/ 12 C) and nitrogen ( 15 N/ 14 N). Carbon isotope ratios indicate the likely source of primary production and have been used to differentiate between C3 and C4 plants, terrestrial and marine ecosystems, deep forest and open habitat consumers, and benthic and pelagic aquatic systems (e.g. Cloern et al., 2002; Cerling et al., 2004; Hall-Aspland et al., 2005). Nitrogen isotope ratios exhibit a predictable, step-wise enrichment between trophic levels and also have been shown to differ between terrestrial and marine ecosystems (e.g. Hobson and Welch, 1992). Stable isotope analysis is especially advantageous when investigating the feeding ecology and habitat use of marine mammals where it is often impossible to directly observe feeding or migratory behavior. Tissue samples, such as skin or blubber, may be analyzed for stable isotope ratios without sacrificing the animal and this approach has been successfully applied to a variety of marine mammal species including mysticetes (e.g. Lee et al., 2005), odontocetes (e.g. Walker et al., 1999), pinnipeds (e.g. Hobson and Welch, 1992; Kurle and Worthy, 2002; Newsome et al., 2006), sirenians (e.g. Ames et al., 1996; MacFadden et al., 2004; Yamamuro et al., 2004; Reich and Worthy, 2006), sea otters (Clementz and Koch, 2001) and polar bears (e.g. Ramsay and Hobson, 1991). In order to accurately interpret isotopic results, it is imperative to determine both isotopic discrimination (the difference in isotopic *Author for correspondence (e-mail: gworthy@mail.ucf.edu) Accepted 3 May 2009 SUMMARY The Florida manatee (Trichechus manatus latirostris) is a herbivorous marine mammal that occupies freshwater, estuarine and marine habitats. Despite being considered endangered, relatively little is known about its feeding ecology. The present study expands on previous work on manatee feeding ecology by providing critical baseline parameters for accurate isotopic data interpretation. Stable carbon and nitrogen isotope ratios were examined over a period of more than 1 year in the epidermis of rescued Florida manatees that were transitioning from a diet of aquatic forage to terrestrial forage (lettuce). The mean half-life for 13 C turnover was 53 and 59 days for skin from manatees rescued from coastal and riverine regions, respectively. The mean halflife for 15 N turnover was 27 and 58 days, respectively. Because of these slow turnover rates, carbon and nitrogen stable isotope analysis in manatee epidermis is useful in summarizing average dietary intake over a long period of time rather than assessing recent diet. In addition to turnover rate, a diet–tissue discrimination value of 2.8‰ for 13 C was calculated for long-term captive manatees on a lettuce diet. Determining both turnover rate and diet–tissue discrimination is essential in order to accurately interpret stable isotope data. Key words: turnover, stable isotope, Florida manatee, diet–tissue discrimination, 13 C, 15 N, Trichechus manatus, feeding ecology. THE JOURNAL OF EXPERIMENTAL BIOLOGY 2349 ratios between consumer tissue and diet) and turnover rate (the time it takes for the isotope to be assimilated into the consumer’s tissue) of the sampled tissue. Diet–tissue discrimination may be difficult to determine for animals feeding on multiple, isotopically distinct prey items for which the proportions contributing to the diet are unknown. However, controlled captive studies on a variety of taxa have allowed for more precise measurements (e.g. Roth and Hobson, 2000; Cherel et al., 2005; Logan et al., 2006; Seminoff et al., 2006). In addition to diet–tissue discrimination, turnover rates in tissues must be determined in order to assess whether the isotope signature of the tissue represents the most recent diet or the long-term diet. An effective method to determine turnover rate is to experimentally switch an animal from one known diet to another isotopically distinct diet. Turnover rates of stable isotopes have been calculated using this method for mammals (e.g. Tieszen et al., 1983), birds (e.g. Hobson and Clark, 1992a), fish (e.g. Bosley et al., 2002) and invertebrates (e.g. Olive et al., 2003). These studies have shown that tissues with higher metabolic activity (e.g. blood, liver) have faster turnover rates than less active tissue (e.g. bone). The endangered Florida manatee (Trichechus manatus latirostris L.) is known to feed on a variety of aquatic plants in fresh, estuarine and marine habitats (e.g. Campbell and Irvine, 1977; Hartman, 1979; Best, 1981), each of which has a distinct isotopic signature (e.g. Fry and Sherr, 1984; Reich and Worthy, 2006) (C.D.A.-S. and G.A.J.W., in preparation). Little is known about fine-scale manatee feeding ecology and habitat use because manatees often occupy shallow, turbid water. In addition, manatee population counts and trends remain unclear (Lefebvre et al., 1995; US Fish and Wildlife Service, 2001). Consequently, it has become increasingly important to understand manatee feeding ecology and its relation to habitat use in order to improve conservation efforts.
2350 C. D. Alves-Stanley and G. A. J. Worthy The present study used skin samples from Florida manatees transitioning between two isotopically distinct diets (aquatic to terrestrial) to determine turnover rates and diet–tissue discrimination in epidermis tissue. Manatees were part of the rehabilitation program at SeaWorld of Florida, and were in need of captive care for reasons including physical trauma, nutritional stress and/or cold stress. The overall objectives of the present study were to determine 13 C and 15 N turnover rates in epidermis tissue and to calculate diet–tissue discrimination values for carbon and nitrogen stable isotopes in manatee skin. MATERIALS AND METHODS Sample collection Manatees held long-term at SeaWorld of Florida (Orlando, FL, USA) were fed a diet consisting primarily of romaine lettuce (>90% by mass) with minimal amounts of other terrestrial vegetation (176 Subadult–adult 512 Charlotte F 1136 330 Adult >365 Primo F 494 277 Adult >365 Rita F >900 >275 Adult >365 Sarah F 1136 325 Adult >365 Stubby F 823 252* Subadult–adult >365 SWF Tm 0110 F 367 255 Subadult 1231 SWF Tm 0302 F Unknown >176 Subadult–adult 512 SWF Tm 0338 F Unknown >176 Subadult–adult 429 *Missing large portion of paddle. THE JOURNAL OF EXPERIMENTAL BIOLOGY at various time intervals as they transitioned from wild forage to a captive diet. Carbon and nitrogen stable isotope turnover rates in skin were calculated for manatees rescued from two habitats in Florida: ‘coastal’ (Naples on the Gulf coast and Cape Canaveral on the central east coast) and ‘riverine’ or fresh water (St Johns River near Jacksonville; Fig.1). The terms ‘coastal’ and ‘riverine’ represent rescue locations only, and are not intended to describe overall habitat use. Biopsies of epidermal tissue were collected from the trailing edge of the paddle using either a scalpel or ronguers (samples were approximately 10mm5mm, full depth of the paddle). Partially sloughed epidermis was collected directly off individual manatees (approximately 2cm2cm) if biopsies were not available. Body mass and sex were determined, and length measurements taken, where body length was measured as the straight distance from snout to paddle (O’Shea et al., 1985). Manatees were categorized into three age classes based on body length measurements (adults >275cm, subadults/late juveniles 176–275cm, and calves
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during the summer months while othe
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Florida manatee. National Biologica
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direction, and (e) when ‘travelli
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172 NOTES Caribbean Journal of Scie
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174 FIG. 1. Drowned Cayes study are
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194 C.M. Duarte well as more recent
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206 C.M. Duarte Ramos-Esplá, A., M
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$1.2 million (Moore et al. 2009a).
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animals may adopt microhabitat choi
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manatus in Costa Rica. Biological C
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574 D. J. Semeyn et al. and natural
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582 D. J. Semeyn et al. biologists
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III. RESULTS Manatees in Florida an
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Genetica (2011) 139:833-842 DOI 10.
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