Differences in δ13C and δ15N values between feathers and blood of seabird chicks: implications for non-invasive isotopic investigations

Blood and feathers are the most targeted tissues for isotopic investigations in avian ecology, primarily because they can be easily and non-destructively sampled on live individuals. Comparing blood and feather isotopic ratios can provide valuable information on dietary shifts, trophic specialization and migration patterns, but it requires a good knowledge of the isotopic differences between the two tissues. Here, δ¹³C and δ¹⁵N values of whole blood (in blood cells of a few species) and simultaneously grown body feathers were measured in seabird chicks to quantify the tissue-related isotopic differences. Seabirds include 27 populations of 22 wild species that were sampled in 2000–2008, and a review of the literature added 8 groups (including adult birds) to the analysis. The use of a large data set that overall encompasses wide δ¹³C and δ¹⁵N ranges allowed us to depict for the first time accurate relationships between blood and feather isotopic ratios across avian taxa. Blood was impoverished in ¹³C and generally in ¹⁵N compared with feathers. Both mean δ¹³C and δ¹⁵N values of feathers and blood were highly positively and linearly related [feather δ¹³C = 0.972 (±0.020) blood δ¹³C + 0.962 (±0.414), and feather δ¹⁵N = 1.014 (±0.056) blood + 0.447 (±0.665), respectively; both P < 0.0001]. The regressions should be applied to mathematically correct feather or whole blood δ¹³C and δ¹⁵N values when comparing isotopic ratios within and between ecological studies on birds.     

δ15N and δ13C values in dental collagen as a proxy for age- and sex-related variation in foraging strategies of California sea lions

We assessed the foraging habits of California sea lions, Zalophus californianus, from Isla Santa Margarita, BCS, Mexico, by analyzing δ¹³C and δ¹⁵N values of dentin collagen. Since dentin is deposited annually in growth layer groups (GLGs), it can be subsampled to construct ontogenetic isotopic profiles at the individual level. We drilled 20 canine teeth and obtained 141 samples for isotopic analysis that were assigned to age-specific categories from GLG-based estimated ages. Pups’ GLGs had the highest mean δ¹⁵N values and the lowest mean δ¹³C values, a pattern likely driven by the consumption of milk. Juveniles had δ¹⁵N values between those of pups and adult females, which may reflect continued nursing into the second year or preferential consumption of coastal benthic versus pelagic prey. Significant differences were observed between the sexes of adults; adult females had lower mean δ¹³C and δ¹⁵N values than adult males. Higher isotope values in adult males relative to females may reflect a higher trophic position, but differences in foraging grounds cannot be excluded as a potential explanation because tracking data are not available at this time. Evidence of intra-specific foraging diversification may be related to a strategy to reduce competition within and among age and sex categories.     

Spatial and seasonal variation in δ15N and δ13C values in a mesopredator shark, Squalus suckleyi, revealed through multitissue analyses

We used variance decomposition to explore the importance of body size, sex, location, and sampling period as predictors of intrapopulation variation in δ¹⁵N and δ¹³C values in spiny dogfish Squalus suckleyi from the Puget Sound–Strait of Georgia basin. Isotopes in two tissues with long (dorsal white muscle) and short (liver) isotopic turnover rates (~1 year and ~3–4 months, respectively) were sampled to evaluate whether the relative importance of each variable differed depending on the time span over which diet information was integrated. Significant spatial variation was observed in both muscle and liver isotopic composition, whereby location uniquely explained 25 and 17 % of the total variance, respectively. The remaining variables explained considerably less variation in both tissue types. Furthermore, evidence of seasonal isotopic shifts in δ¹⁵N and δ¹³C values was apparent, but differed widely in direction and magnitude among groups. These findings suggest that members of spiny dogfish schools may share a common feeding history, possibly by spending extended time periods (weeks to months) foraging in a spatially fixed region. Another explanation is that individuals may move and feed in aggregations that exist for extended periods. These complex group-level patterns suggest that even for large-bodied, motile predators such as sharks, population-level diet estimates derived from averaging isotope ratios of individuals collected from only a few locations may poorly reflect the true population mean.     

Stable isotopes (δ13C, δ15N) and modelling as tools to estimate the trophic ecology of cultivated oysters in two contrasting environments

Food sources for cultivated marine bivalves generally are not well identified, although they are essential for a better understanding of coastal ecosystems and for the sustainability of shellfish farming activities. In addition to phytoplankton, other organic matter sources (OMS), such as microphytobenthos and detritus (of terrestrial or marine origins), can contribute significantly to the growth of marine bivalves. The aim of this study was to identify the potential food sources and to estimate their contributions to the growth of the Pacific oyster (Crassostrea gigas) in two contrasting trophic environments of Normandy (France): the Baie des Veys (BDV) and the Lingreville area (LIN). Two sites were studied in the BDV area (BDV-S and BDV-N) and one in the LIN area. To estimate the contribution of each type of OMS, we used a combination of stable natural isotope composition (δ¹³C, δ¹⁵N) analysis of OMS and oyster tissue together with a modelling exercise. Field sampling was conducted every 2 months over 1 year. The sampled sources were suspended particulate organic matter from marine (PhyOM) and terrestrial (TOM) origins, microphytobenthos (MPB), detrital organic matter from the superficial sediment (SOM), and macroalgae (Ulva sp., ULV). A statistical mixing model coupled to a bioenergetic model was used to calculate the contributions of each different source at different seasons. Results showed that isotopic composition of the animal flesh varied with respect to the potential OMS over the year within each ecosystem. Significant differences were also observed among the three locations. For instance, the δ¹³C and δ¹⁵N values of the oysters ranged from −20.0 to −19.1‰ and from 6.9 to 10.8‰ at BDV-S, from −19.4 to −18.1‰ and from 6.4 to 10.0‰ at BDV-N, and from −21.8 to −19.4‰ and from 6.3 to 8.3‰ at LIN. The contributions of the different sources to oyster growth differed depending on the ecosystem and on the period of the year. Phytoplankton (PhyOM) predominated as the principal food source for oysters (particularly in the LIN location). MPB, TOM, and ULV detritus also possibly contributed to oysters’ diet during summer and autumn at the BDV-S and BDV-N sites. SOM was not considered an OMS because it was already a mix of the other four OMS, but rather a trophic reservoir that potentially mirrored the trophic functioning of marine ecosystems.     

Temporal and spatial variation in the δ<Superscript>15</Superscript>N and δ<Superscript>13</Superscript>C values of fish and squid from Alaskan waters

To test the hypothesis that stable isotope ratios from marine organisms vary, the δ¹⁵N and δ¹³C values from fish and squid collected in Alaskan waters were measured across years (1997, 2000, and 2005), seasons, geographic locations, and different size/age classes, and between muscle tissue and whole animals. Temporal, geographic, and ontogenetic differences in stable isotope ratios ranged from 0.5–2.5‰ (δ¹⁵N) to 0.5–2.0‰ (δ¹³C). Twenty-one comparisons of stable isotope values between whole organisms and muscle tissue revealed only four small differences each for δ¹⁵N and δ¹³C, making costly and space prohibitive collection of whole animals unnecessary. The data from this study indicate that significant variations of stable isotope values from animals in marine systems necessitates collection of prey and predator tissues from the same time and place for best interpretation of stable isotope analysis in foraging ecology studies.     

δ<Superscript>13</Superscript>C and δ<Superscript>15</Superscript>N values in reef corals <Emphasis Type="Italic">Porites lutea</Emphasis> and <Emphasis Type="Italic">P. cylindrica</Emphasis> and in their epilithic and endolithic algae

In summer 1998, shallow water corals at Sesoko Island, Japan (26°38′N, 127°52′E) were damaged by bleaching. In August 2003, partially damaged colonies of the massive Porites lutea and the branching P. cylindrica were collected at depths of 1.0–2.5 m. The species composition of epilithic algal communities on dead skeletal surfaces of the colonies (‘red turfs’, ‘green turfs’, ‘red crusts’) and the endolithic algae (living in coral skeletons) growing close to and away from living coral polyps was determined. Carbon and nitrogen stable isotope values of organic matter (δ¹³C and δ¹⁵N) from all six of these biological entities were determined. There were no significant differences in the isotope composition of coral tissues of the two corals, with P. lutea having δ¹³C of −15.3 to −9.6‰ and δ¹⁵N of 4.7–6.1‰ and P. cylindrica having similar values. Polyps in both species living close to an interface with epilithic algae had similar isotope values to polyps distant from such an interface. Despite differences in the relative abundance of the algal species in red turfs and crusts, their δ¹³C and δ¹⁵N values were not significantly different from each other (−18.2 to −13.9, −20.6 to −16.2, 1.1–4.3, and 3.3 to 4.9‰, respectively). The green algal turf had significantly higher δ¹³C values (−14.9 to −9.3‰) than that of red turfs and crusts but similar δ¹⁵N (1.2–4.1‰) to the red algae. The data do not suggest that adjoining associations of epilithic algae and coral polyps exchange carbon- and nitrogen-containing metabolites to a significant extent. The endolithic algae in the coral skeletons had δ¹³C values of −14.8 to −12.3‰ and δ¹⁵N of 4.0–5.4‰. Thus they did not differ significantly from the coral polyps in their carbon and nitrogen isotope values. The similarity in carbon isotope values between the coral polyps and endolithic algae may be attributed to a common source of CO₂ for zooxanthellae and endolithic algae, namely, from respiration by the coral host. While it is difficult to fully interpret similarity in the nitrogen isotope composition of coral tissue and of green endolithic algae and the difference in δ¹⁵N between green epilithic and endolithic algae, the data are consistent with nitrogen-containing metabolites from the scleractinian coral serving as a significant source of nitrogen for the endolithic algae.     

Tissue,ontogenic and sex-related differences in δ<Superscript>13</Superscript>C and δ<Superscript>15</Superscript>N values of the oceanic squid <Emphasis Type="Italic">Todarodes filippovae</Emphasis> (Cephalopoda: Ommastrephidae)

Stable isotopes are increasingly used in the study of trophic interactions of many aquatic animals and most recently cephalopods. To evaluate the application of the method to squids, it is important to assess isotopic differences among and within consumer tissues that may confound the resolution of ecological relationships. Inter- and intra-tissue isotopic variation was examined in 55 individuals of the oceanic squid Todarodes filippovae that were collected at the beginning of April 2000 in the southwestern Indian Ocean (between 44°S, 76°E, and Saint Paul and Amsterdam islands, 38°S, 78°E). Delipidated soft tissues (mantle, arm, buccal mass, gill and reproductive organs) showed small δ¹³C and δ¹⁵N differences, which were probably tissue-specific. A lower carbon value was observed in the digestive gland as a consequence of incomplete lipid removal. Hard tissues, such as beaks and gladii, had lower ¹⁵N values than soft tissues, which can be explained by the presence of chitin, a ¹⁵N-depleted molecule. Females (n = 38) and males (n = 17) had identical δ¹³C values, but females showed higher δ¹⁵N values than males. The difference was size-related rather than sex-related, however, as females were generally larger than males. A comparison of similar-sized females and males produced identical nitrogen values. These data suggest dietary shifts from lower to higher trophic levels during growth, because δ¹⁵N values of large T. filippovae were much higher than that of small specimens. As expected, nitrogen values of lower beaks and gladii of large squids increased from the oldest to the most recently formed region, reflecting the progressive growth of chitinized tissues in parallel with dietary changes. Sequential sampling along the growth increments of squid beaks and gladii can likely be used to produce a chronological record of dietary information throughout an individual’s history.