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Isotopic Turnover in Aquatic Predators: Quantifying the Exploitation of Migratory Prey

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Isotopic Turnover in Aquatic Predators: Quantifying the Exploitation of Migratory Prey 1 Isotopic turnover in aquatic predators: quantifying the exploitation of migratory prey Stephen E. MacAvoy, Stephen A. Macko, and Greg C. Garman Abstract : In the tidal freshwaters of Virginia, U.S.A., the blue catfish ( Ictalurus furcatus ), an introduced piscivore, derives a significant proportion of its nutrition from spawning anadromous fish (genus Alosa , including blueback her - ring ( A. aestivalis ), American shad ( A. sapidissima ), and alewife ( A. pseudoharengus )). Because the Alosa are not con - tinually available to I. furcatus , there is an isotopic turnover, defined as change in isotope composition due to growth and metabolic tissue replacement, in I. furcatus tissues associated with the diet switch from freshwater to anadromous fishes. However, isotopic turnover rates for ictalurid fish are unknown. This study determined the maximum isotopic turnover rate of channel catfish ( Ictalurus punctatus ) tissues and compared this maximum rate with that of I. furcatus captured in the field over the 3-month Alosa spawning run. Maximum turnover rates for 13 C were 0.014 and 0.017‰ per day in muscle and blood. For 34 S, rates were 0.017 and 0.020‰ per day in muscle and blood, respectively. Isotopic turnover of muscle carbon reflected growth rate, but sulfur did not match growth as well. Ictalurus furcatus captured in the field showed no enrichment during the Alosa spawning run owing to slow turnover and variable diet. In aquatic ecosystems that have migrating prey, exploitation by predators may be underestimated using isotopes because of slow tissue turnover. Résumé : Dans les eaux douces intertidales de la Virginie, aux États-Unis, Ictalurus furcatus , un poisson piscivore in- troduit, retire une proportion significative de son alimentation des poissons anadromes du genre Alosa , dont le l’Alose d’été ( A. aestivalis ), l’Alose savoureuse ( A. sapidissima ) et le Gaspareau ( A. pseudoharengus ), qui viennent y frayer. Parce que les Alosa ne sont pas toujours disponibles à I. furcatus , il se produit un virement isotopique dans les tissus de la barbue, c’est à dire un changement dans la composition isotopique reliée à la croissance et au renouvellement métabolique des tissus consécutif à un remplacement dans le régime des poissons d’eau douce par des poissons anadromes. Cependant, les taux de renouvellements isotopiques chez les poissons ictaluridés sont inconnus. Noua avons déterminé le taux maximal de renouvellement isotopique dans les tissus de la Barbue de rivière ( Ictalurus punctatus ) et l’avons comparé avec le taux maximum observé chez les I. furcatus capturés en nature durant les 3 mois de la montai- son de reproduction des Alosa . Les taux maximaux de renouvellement du 13 C sont respectivement de 0,014 et de 0,017‰ par jour dans le muscle et dans le sang, alors que les taux maximaux de 34 S sont respectivement de 0,017 et de 0,020‰ par jour dans les mêmes tissus. Le taux de renouvellement isotopique du carbone musculaire reflète le taux de croissance, mais celui du soufre ne suit pas la croissance d’aussi près. Les I. furcatus capturés en nature ne font preuve d’aucun enrichissement durant la montaison des Alosa à cause du faible taux de renouvellement et du régime alimentaire variable. Dans les écosystèmes aquatiques où il y a des proies migratrices, l’utilisation des isotopes peut sous-estimer l’exploitation par les prédateurs à cause du faible taux de renouvellement des tissus. [Traduit par la Rédaction] MacAvoy et al. 10 Introduction be relatively constant over time. Therefore, the isotopic signa - ture of the consumer organisms is assumed to reflect the Stable isotopes are useful in the study of food webs be - available prey items at any given time. Often, this assumption cause they can often be used to differentiate among nutrient may be valid; however, it may be violated in ecosystems that sources contributing to consumers’ diets. The carbon, nitro - occasionally experience migrations of animals, such as birds, gen, and sulfur isotope ratios of prey animals are assumed to mammals, and fish. The migratory animals may have unique carbon, nitrogen, or sulfur isotopic signatures relative to prey Received August 14, 2000. Accepted January 26, 2001. items in the system they enter. In such a system, the predators Published on the NRC Research Press Web site on XXX XX, that consume the migrating prey should have their own isoto - 2001. pic signatures shift toward that of the prey species (Kline et J15917 al. 1998; Persson and Hansson 1999). However, the isotopic S.E. MacAvoy 1,2 and S.A. Macko. Department of turnover rate of most animals, especially large vertebrates, is Environmental Sciences, University of Virginia, unknown (Gannes et al. 1997). Charlottesville, VA 22903, U.S.A. Isotopic turnover is defined in this paper as the isotopic G.C. Garman. Center for Environmental Studies, Virginia change due to growth and metabolic tissue replacement as - Commonwealth University, Richmond, VA 23284, U.S.A. sociated with a change in diet. Isotopic turnover studies on 1Corresponding author (e-mail: [email protected]). brine shrimp (Fry and Arnold 1982) and krill (Frazer et al. 2Present address: Department of Marine Sciences, University 1997) have shown high rates of isotopic turnover owing to of Georgia, Athens, GA 30601, U.S.A. the quick growth of these invertebrates. Herzka and Holt Can. J. Fish. Aquat. Sci. 58 : 1–10 (2001) © 2001 NRC Canada PROOF/ÉPREUVE 2 Can. J. Fish. Aquat. Sci. Vol. 58, 2001 (2000) also found quick turnover rates in larval red drum bolic tissue replacement components in order to address the (Sciaenops ocellatus ) owing to growth. Hesslein et al. relative importance of these two components (Hesslein et al. (1993) found slow turnover rates in broad whitefish 1993). Ideally, documenting isotopic turnover allows tempo - (Coregonus nasus ). In their study, Hesslein et al. (1993) de - ral interpretation of the percentage of marine carbon, sulfur, termined that more than a year was required for C. nasus and nitrogen consumed by I. furcatus during the course of muscle tissue 13 C and 34 S to completely reflect consumed the Alosa spawning run and would augment estimates of food, and they hypothesized that in slow-growing wild pop - I. furcatus exploitation of marine material derived from iso - ulations, it could take longer. Because of the uncertainties tope mixing equations (MacAvoy et al. 2000). about tissue turnover rates, it becomes difficult to determine isotopically the extent to which a migrating population is Materials and methods being preyed upon by local predators. Additionally, if the predator is migratory, then its role in the ecosystem it moves Turnover determination through would be difficult to determine isotopically. Deter - Channel catfish ( Ictalurus punctatus ) were used in this experi - mination of isotopic turnover rate is also important for un - ment as a surrogate for I. furcatus because they could be obtained derstanding the temporal relationship between the isotopic locally with minimal transport and handling stress and the growth signature of a predator and that of its prey. Some period of rates of the two ictalurids are similar (Conder and Hoffarth 1962; time may be required for a predator to reflect the isotope Webster et al. 1992, 1995). On 7 April 1999, 36 I. punctatus were signature of a new prey item. obtained from Hale Farm, Oilville, Va. Seven fish were sacrificed Many coastal river systems worldwide experience a sea - to determine initial isotopic values. All fish were transported to the University of Virginia and, once there, were measured (total length sonal influx of spawning anadromous fish. The large influx in inches), tagged, and placed in a Living Stream model LSW-900 may be an important nutrient source to freshwater ecosys - (190 gal; Frigid Units, Inc., Toledo, Ohio). The catfish were fed a tems, particularly if the species are semelparous (Kline et al. marine fish diet (100% tuna meat) of known isotopic composition 1993; Ben-David et al. 1998; MacAvoy et al. 1998). The beginning on 8 April 1999 and ending on 17 June 1999; over the anadromous fish are enriched in 13 C, 15 N, and 34 S relative to 90 days of the study, food was added so that it was always visible freshwater animals and plants because they have spent the (Fry and Arnold 1982). Ninety days is the approximate length of majority of their lives in the marine environment and have the Alosa spawning run in Virginia and was chosen as the optimal acquired its relatively enriched isotopic signal. Therefore, length for the turnover experiment because it would encompass the the nutrients (in the form of their biomass) that they deliver time that Alosa adults and I. furcatus share the tidal freshwater. to freshwater are detectable using stable isotope techniques Fish were placed on ice prior to sampling. For all fish, muscle and skin were sampled. Most fish had blood samples taken (in some as shown in Alaska and the Pacific Northwest by Kline et al. cases, blood could not be obtained), and catfish with barbels had (1990, 1993) and Ben-David et al. (1998). those sampled as well. In the coastal rivers of the eastern United States, the dom- As a control group, 19 I. punctatus obtained from Hale Farm inant anadromous fishes are Alosa (including blueback her- were kept in the Living Stream for 60 days and were fed the com- ring ( A. aestivalis ), American shad ( A. sapidissima ), and mercial fish food (Big Strike floating fish food, SSC-338220) they alewife ( A. pseudoharengus )), and they have been found to had been raised on. This food had 32.0% crude protein and 4.0% be substantially enriched in 34 S and 13 C relative to freshwa - fat (Southern States Cooperative Inc., Richmond, Va.). The fish ter species (Garman and Macko 1998; MacAvoy et al.
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