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Using Stable Isotopes of Nitrogen and Carbon to Study Seabird Ecology: Applications in the Mediterranean Seabird Community*

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Using Stable Isotopes of Nitrogen and Carbon to Study Seabird Ecology: Applications in the Mediterranean Seabird Community* SCI. MAR., 67 (Suppl. 2): 23-32 SCIENTIA MARINA 2003 MEDITERRANEAN SEABIRDS AND THEIR CONSERVATION. E. MÍNGUEZ, D. ORO, E. DE JUANA and A. MARTÍNEZ-ABRAÍN (eds.) Using stable isotopes of nitrogen and carbon to study seabird ecology: applications in the Mediterranean seabird community* MANUELA G. FORERO1 and KEITH A. HOBSON2 1 Instituto Mediterráneo de Estudios Avanzados (CSIC-UIB), C/Miquel Marqués, 21, 07190 Esporles, Mallorca, Spain. E-mail: [email protected] 2 Canadian Wildlife Service, 115 Perimeter Road, Saskatoon, SK, Canada, S7N0X4 SUMMARY: The application of the stable isotope technique to ecological studies is becoming increasingly widespread. In the case of seabirds, stable isotopes of nitrogen and carbon have been mainly used as dietary tracers. This approach relies on the fact that foodweb isotopic signatures are reflected in the tissues of the consumer. In addition to the study of trophic ecology, stable isotopes have been used to track the movement of seabirds across isotopic gradients, as individuals moving between isotopically distinct foodwebs can carry with them information on the location of previous feeding areas. Studies applying the stable isotope methodology to the study of seabird ecology show a clear evolution from broad and descriptive approaches to detailed and individual-based analyses. The purpose of this article is to show the different fields of applica- tion of stable isotopes to the study of the seabird ecology. Finally, we illustrate the utility of this technique by considering the particularities of the Mediterranean seabird community, suggesting different ecological questions and conservation prob- lems that could be addressed by using the stable isotope approach in this community. Key words: stable isotopes, Mediterranean Sea, seabirds, trophic ecology, conservation, nitrogen, carbon. RESUMEN: EL EMPLEO DE ISÓTOPOS ESTABLES DE NITRÓGENO Y CARBONO PARA ESTUDIAR LA ECOLOGÍA DE LAS AVES MARI- NAS: APLICACIONES A LA COMUNIDAD DE AVES MARINAS DEL MEDITERRÁNEO. – La aplicación de la medición de isótopos esta- bles a los estudios ecológicos es cada vez más frecuente. En el caso de las aves marinas, los isótopos estables de nitrógeno y carbono han sido empleados principalmente como indicadores del régimen alimenticio. Este enfoque se basa en el hecho de que las concentraciones isotópicas de las cadenas tróficas se reflejan en los tejidos del consumidor. Además de para el estudio de la ecología trófica, los isótopos estables se han utilizado para estudiar el movimiento de las aves marinas a tra- vés de gradientes isotópicos, ya que los individuos que se mueven entre cadenas tróficas isotópicamente distintas pueden llevar con ellos información sobre la ubicación de áreas de alimentación anteriores. Los estudios que aplican la metodolo- gía de los isótopos estables al conocimiento de la ecología de las aves marinas muestran una clara evolución, desde los enfo- ques amplios y descriptivos, a los análisis detallados y basados en los individuos. El objetivo de este trabajo es mostrar los diferentes campos de aplicación de los isótopos estables en el estudio de la ecología de las aves marinas. Finalmente, ilus- tramos la utilidad de esta técnica considerando las particularidades de la comunidad de aves marinas del mar mediterráneo, sugiriendo diferentes cuestiones ecológicas y problemas de conservación que se podrían abordar empleando la técnica de los isótopos estables en esta comunidad. Palabras clave: isótopos estables, Mediterráneo, aves marinas, ecología trófica, conservación, nitrógeno, carbono. *Received October 1, 2001. Accepted September 8, 2002. STABLE ISOTOPES AND MEDITERRANEAN SEABIRDS 23 BACKGROUND 1995). Studies that have determined the diet-tissue fractionation factor of nitrogen and carbon isotopes For some time the measurement and use of natu- for marine consumers show that most tissues are rally occurring stable isotopes has been restricted enriched over the diet by about 3-5‰ and 1-3‰ largely to investigations in the earth sciences. How- respectively, although important variations may exist ever, during the last two decades the application of among tissues (DeNiro and Epstein, 1981; Mizutani this methodology to ecological studies has become et al., 1992; Hobson and Clark, 1992a, 1992b; Mich- widespread (Lajtha and Michener, 1994; Hobson, ener and Schell, 1994; Bearhop et al., 1999). 1999; Kelly, 1999). In addition to a growing interest The advantages of the isotope methodology for by ecologists and physiologists, the increase has studying seabird trophic ecology are numerous. Pre- also resulted from substantial technical advances vious conventional studies of seabird diet relied that allow minimal sample preparation and the auto- upon examination of stomach contents of birds. mated processing of a large number of samples. Sta- However, this methodology has several sources of ble isotope ratios are measured using an isotope bias, including the rapid digestion of soft-bodied ratio mass spectrometer (IRMS) with values report- prey (see review in Duffy and Jackson, 1986 and ed as the ratio between the heavy and light isotopes González-Solís et al., 1997a). In addition, there are compared to standards which vary depending on the some ecological problems in which the stable iso- stable isotope used. In the case of nitrogen and car- tope technique provides solutions and conventional bon, the most commonly used in marine systems, studies of diet perform poorly (e.g. quantifying the standards are AIR (N2) and Pee Dee Belemnite trophic level). Combined approaches in which con- (PDB) respectively. The deviation (δ) of the ratio ventional studies and the stable isotope technique (R) is expressed per thousand (‰): are complementary could avoid these biases and limitations. Feeding experiments have shown that δ ]× X= [ (Rsample/Rstandard) - 1 1,000 the turnover rate of elements in a particular tissue varies with that tissue’s metabolic activity (Tieszen where X is the heavier isotope and R is the corre- et al., 1983; Hobson and Clark, 1992a). Therefore, sponding ratio between the heavier and the lighter different tissues sampled from the same individual isotope. can provide dietary information reflecting different Stable isotope measurements of carbon and nitro- periods of time, allowing the evaluation of diet over gen have been used mainly as dietary tracers in various temporal scales and reducing the need for seabirds, but recent investigations also show that expensive sampling efforts. Recent investigations these have the potential for locating moulting areas have also indicated that a great deal of dietary infor- of migratory seabird species (Hobson, 1993; Cherel mation can be obtained from the isotopic analysis of et al., 2000). The utility of δ15N measurements in blood and feathers, thereby reducing the need to sac- studies of seabirds and feeding ecology relies on rifice birds just for analysis of diet (Hobson and trophic enrichment of the heavier isotope (15N) in Clark, 1992a, 1993; Thompson and Furness, 1995; foodwebs. During the production of urea and uric Hobson et al., 1997; Hodum and Hobson, 2000; acid, molecules of compounds containing the lighter Cherel et al., 2000). In the case of feathers, since atom 14N are preferentially excreted over those con- keratin is a metabolically inert tissue it conserves taining the heavier isotope (Peterson & Fry, 1987). dietary signals integrated over the period in which Tissues of consumers tend to be enriched in 15N com- they have grown. This quality, together with differ- pared to their diet (Minagawa and Wada, 1984; ences in isotope signatures between geographically Michener and Schell, 1994). Studies using δ13C val- separated foodwebs, offers an additional application ues have been valuable because the rate at which 13C of stable isotope analysis to the study of spatial and and 12C isotopes are fixed by plants differ among long-term changes in diet. photosynthetic pathways. In marine systems, phyto- Evaluation of animal movement is an important plankton have lighter δ13C values than many inshore component in understanding population dynamics plants, suggesting that information about the sources and ecology. Conventional approaches used to track of feeding, including inshore vs. offshore sources in animal movements, such as external markers or tags, marine habitats are available through stable isotope necessarily involve the subsequent recovery or measurements (Fry and Sherr, 1989; Boutton, 1991; sighting of individuals. In the case of seabirds, they Hobson et al., 1994; France, 1995; Hobson et al., are accessible for investigation only during a short 24 M.G. FORERO and K.A. HOBSON period of the year because they spend most of their Hobson and Welch (1992) studied δ15N and δ13C time offshore. Stable isotope analyses of feathers in an Arctic food-web from primary producers to sampled on the breeding grounds offers an alterna- higher-level carnivores including seabirds. They tive means of studying diet and foraging areas dur- found that although Arctic cod (Boreogadus saida), ing the non-breeding period. Because some ocean previously thought to be critical in the transfer of areas differ in the isotopic signature of foodwebs energy from primary producers to higher level ver- (e.g. Wada et al., 1987), isotopic analyses may pro- tebrates, was an important component, lower troph- vide inference on location of moulting areas of ic level invertebrates also play a critical role in this seabirds (Schell et al., 1999; Cherel et al., 2000). process of energy
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