Stable isotopes reveal individual variation in migration strategies and habitat preferences in a suite of seabirds during the nonbreeding period

Information on predator and prey distributions is integral to our understanding of migratory connectivity, food web dynamics and ecosystem structure. In marine systems, although large animals that return to land can be fitted with tracking devices, minimum instrument sizes preclude deployments on small seabirds that may nevertheless be highly abundant and hence major consumers. An increasingly popular approach is to use N and C stable isotope analysis of feathers sampled at colonies to provide information on distribution and trophic level for the preceding, and generally little-known, nonbreeding period. Despite the burgeoning of this research, there have been few attempts to verify such relationships. In this study, we demonstrate a clear correspondence between isotope ratios of feathers and nonbreeding distributions of seven species from South Georgia tracked using loggers. This generated a rudimentary isoscape that was used to infer the habitat preferences of eight other species ranging in size from storm petrels to albatrosses, and which could be applied, with caveats, in other studies. Differences in inferred distribution within and between species had major implications for relative exposure to anthropogenic threats, including climate change and fisheries. Although there were no differences in isotope values between sexes in any of the smaller petrels, mean stable C (δ¹³C), but not stable N isotope ratios (δ¹⁵N), tended to be greater in females than males of the larger, and more sexually size-dimorphic species. This indicates a difference in C source (distribution), rather than trophic level, and a correspondence between the degree of sexual size dimorphism in Procellariiformes and the level of between-sex niche segregation.     

Biochemical evidence for diverse strategies in the inner kinetochore

The kinetochore is a complex structure whose function is absolutely essential. Unlike the centromere, the kinetochore at first appeared remarkably well conserved from yeast to humans, especially the microtubule-binding outer kinetochore. However, recent efforts towards biochemical reconstitution of diverse kinetochores challenge the notion of a similarly conserved architecture for the constitutively centromere-associated network of the inner kinetochore. This review briefly summarizes the evidence from comparative genomics for interspecific variability in inner kinetochore composition and focuses on novel biochemical evidence indicating that even homologous inner kinetochore protein complexes are put to different uses in different organisms.     

Unexpected hydrogen isotope variation in oceanic pelagic seabirds

Hydrogen isotopes have significantly enhanced our understanding of the biogeography of migratory animals. The basis for this methodology lies in predictable, continental patterns of precipitation δD values that are often reflected in an organism’s tissues. δD variation is not expected for oceanic pelagic organisms whose dietary hydrogen (water and organic hydrogen in prey) is transferred up the food web from an isotopically homogeneous water source. We report a 142 ‰ range in the δD values of flight feathers from the Hawaiian petrel (Pterodroma sandwichensis), an oceanic pelagic North Pacific species, and inquire about the source of that variation. We show δD variation between and within four other oceanic pelagic species: Newell’s shearwater (Puffinus auricularis newellii), Black-footed albatross (Phoebastria nigripes), Laysan albatross (Phoebastria immutabilis) and Buller’s shearwater (Puffinus bulleri). The similarity between muscle δD values of hatch-year Hawaiian petrels and their prey suggests that trophic fractionation does not influence δD values of muscle. We hypothesize that isotopic discrimination is associated with water loss during salt excretion through salt glands. Salt load differs between seabirds that consume isosmotic squid and crustaceans and those that feed on hyposmotic teleost fish. In support of the salt gland hypothesis, we show an inverse relationship between δD and percent teleost fish in diet for three seabird species. Our results demonstrate the utility of δD in the study of oceanic consumers, while also contributing to a better understanding of δD systematics, the basis for one of the most commonly utilized isotope tools in avian ecology.     

Stable isotope evidence for the consumption of millet and other plants in Bronze Age Italy

Stable carbon and nitrogen isotope analysis was carried out on human and animal bones from four inland Early and Middle Bronze Age sites in Northern and Southern Italy. The main aims of the investigation were to explore the contribution of plant foods to the human diet and to examine any dietary differences between and within each of the sites. At two of the sites in Northern Italy, human and animal bones were significantly enriched in ¹³C. This finding was attributed to the consumption of domestic millets (Panicum miliaceum and/or Setaria italica), which are C₄ pathway plants. Conversely, individuals from the two Bronze Age sites in Southern Italy were significantly depleted in ¹³C compared to those from the north. Here, millet was absent from the diet, and protein from C₃ plants made a much greater dietary contribution than animal protein. This finding highlights the importance of cereal cultivation, most likely of wheat and barley, in the south of Italy during the Bronze Age. Overall, our results support the idea that the widespread cultivation of millet first occurred in Northern Italy, following its introduction from across the Alps in Central Europe. Finally, we found no significant differences in the stable isotope values between individuals at each site, when grouped by their sex or presence of grave goods. This leads to the conclusion that any status difference that may have existed is not reflected in the long‐term dietary record, or at least not as measurable by stable isotope analysis. Am J Phys Anthropol, 2009. © 2008 Wiley‐Liss, Inc.     

Stable isotope evidence of ontogenetic changes in the diet of gizzard shad Dorosoma cepedianum

Stable sulphur isotopic composition (δ³⁴S) of gizzard shad Dorosoma cepedianum was used to investigate the seasonal and ontogenetic variation in the diet of young and adult fish. This study evaluated fish from a hypereutrophic lake that had recently undergone a 40% reduction of large (>300 mm total length, L _T) D. cepedianum biomass as part of a biomanipulation experiment, which aimed at reducing internal nutrient loading. Dorosoma cepedianum δ³⁴S values showed evidence of ontogenetic changes with young fish (<200 mm L _T) depending more on benthic food sources than adults (>200 mm L _T). The δ³⁴S composition of the adult fish suggested an increasing importance of zooplankton in the diet, although benthic food sources remained part of the diet of all D. cepedianum collected in this study. The results indicated that benthic feeding is used by D. cepedianum of all sizes, suggesting that biomanipulation efforts may need to target all sizes of fish to realize benefits.     

Host use strategies of individual female brown-headed cowbirds Molothrus ater in a diverse avian community

Although it is well established that brown-headed cowbirds Molothrus ater are host generalists, the parasitism strategies of individual females are not well documented. Here we use microsatellite genotyping to characterize host use by individual female cowbirds. Of 205 offspring sampled at a site in northeastern Illinois during one breeding season, we identified or inferred 33 mothers of 141 offspring, with up to 13 (mean 4.72) offspring assigned to individual females. Most (83%) females were host generalists and parasitized up to five host species, indicating that community-wide patterns of parasitism do not result from different individuals specializing on different host species. However, some females (17%) parasitized a single species, suggesting that alternative host-use strategies may exist within a single population. For host generalist females, individuals often parasitized host species that differed in body mass, nest-site placement, and quality, indicating that female cowbirds exhibit extremely flexible host ranges. However, female cowbirds consistently discriminated among potential hosts, for example, by completely avoiding some common, but unsuitable species.     

Migration and wintering strategies in vulnerable Mediterranean Osprey populations

A broad range of migration strategies exist in avian species, and different strategies can occur in different populations of the same species. For the breeding Osprey Pandion haliaetus populations of the Mediterranean, sporadic observations of ringed birds collected in the past suggested variations in migratory and wintering behaviour. We used GPS tracking data from 41 individuals from Corsica, the Balearic Islands and continental Italy to perform the first detailed analysis of the migratory and wintering strategies of these Osprey populations. Ospreys showed heterogeneous migratory behaviour, with 73% of the individuals migrating and the remaining 27% staying all year round at breeding sites. For migratory individuals, an extremely short duration of migration (5.2 ± 2.6 days) was recorded. Mediterranean Ospreys were able to perform long non‐stop flights over the open sea, sometimes overnight. They also performed pre‐ and post‐migratory trips to secondary sites, before or after crossing the sea during both autumn and spring migration. Ospreys spent the winter at temperate latitudes and showed high plasticity in habitat selection, using marine bays, coastal lagoons/marshland and inland freshwater sites along the coasts of different countries of the Mediterranean basin. Movements and home‐range areas were restricted during the wintering season. The short duration of trips and high levels of variability in migratory routes and wintering grounds revealed high behavioural plasticity among individuals, probably promoted by the relatively low seasonal variability in ecological conditions throughout the year in the Mediterranean region, and weak competition for non‐breeding sites. We stress the importance of considering the diversity in migration strategies and the particular ecology of these vulnerable populations, especially in relation to proactive management measures for the species at the scale of the Mediterranean region.     

Stable isotope evidence for the localisation of phenylalanine biosynthesis in the bacterium Paracoccus denitrificans

Paracoccus denitrificans was grown on [6-13C]-glucose as the sole carbon source for growth and the extracts were fractionated and analysed by gas chromatography-mass spectrometry. The 13C-labelling pattern observed in phenylalanine indicated that the biosynthetic sequences of enzymes for phenylalanine production were unequally distributed within the cell and that there are at least 2 separate loci of phenylalanine biosynthesis. The principal locus of phenylalanine production was associated with the Entner-Doudoroff and/or the pentose phosphate pathways and it was responsible for producing 3/4 of the bacterium's phenylalanine. A second locus was associated with the G6 oxidation pathway and was responsible for producing the remaining 1/4 of the cell's phenylalanine.     

Stable isotope evidence for the localisation of some metabolic pathways in the bacterium Paracoccus denitrificans

Paracoccus denitrificans was grown on [6-13C]-glucose as the sole carbon source for growth and the extracts were fractionated and analysed by gas chromatography-mass spectrometry. The 13C-enrichments of some metabolites indicated that the "hydrolysate pools" of these metabolites were not in isotopic equilibrium with the water soluble "free pools". It was concluded that localisation of some metabolic pathways had occurred in Paracoccus during growth on [6-13C]-glucose.     

Stable isotope evidence for Turkey Vulture reliance on food subsidies from the sea

Turkey Vulture (Cathartes aura) reliance on marine subsidies in coastal Baja California peninsula was quantitatively assessed by analyzing carbon and nitrogen stable isotope ratios in its feathers. Feathers were collected in two separate roosts in a small farm, a small fishing village and an uninhabited beach. We compared among them the isotopic niches of the four populations and also with those of Yellow-footed Seagull (Larus livens), Brown Pelican (Pelecanus occidentalis) and Orange-throated Whiptail lizard (Aspidoscelis hyperythra), used as reference for sympatric marine and terrestrial species. The importance of nutrients of marine origin varied among local close subpopulations, suggesting some spatial segregation. Dominant individuals would be established near predictable sources of food (human settlements), having a mixed terrestrial–marine diet influenced by local human activities (isotopic signature of feathers also indicated the role of human-fed cattle as vulture food). Subordinate individuals would be relegated to wandering along the beaches searching for washed up food, having a diet almost exclusively marine.     

Stable isotope studies in human evolution

The discipline of human evolution usually involves the evaluation of changes in gross and molecular morphology or changes in artifact assemblages. In contrast, stable isotope analysis is an indirect line of investigation. Understanding the human evolutionary sequence requires information on nutritional, biobehavioral, and general ecology. These are the kinds of information that stable isotope analysis can provide. Such studies may not identify the mechanisms for change, but their application serves to elucidate the situations under which change occurred.     

Stable isotope evidence for impala Aepyceros melampus diets at Akagera National Park,Rwanda

Stable isotope analysis of tooth enamel was used to investigate the relative proportions of grass and browse in seasonal and overall diets of impala Aepyceros melampus at Akagera National Park, Rwanda. Bulk enamel samples suggest that on average, impala ate c. 86% C₄ grass year‐round, far more than in most previously studied impala populations across Africa. Intra‐tooth samples show that seasonal changes in the proportion of C₄ grass versus C₃ browse are minimal (c. 10%), the diet being dominated by C₄ grass year‐round in contrast to other impala populations that consume ≥50% browse during the dry season. Intra‐tooth oxygen isotope values track carbon isotope changes to a moderate degree, but are not patterned clearly enough to permit identification of wet versus dry seasons. As other studies have shown that impala select high‐protein diets, the foraging behaviour at Akagera is probably because of the availability of palatable grass for much of the year in the edaphic grasslands around the lacustrine environments of the eastern portions of Akagera National Park.     

Stable isotope analysis of dynamic lipidomics

Metabolic pathway flux is a fundamental element of biological activity, which can be quantified using a variety of mass spectrometric techniques to monitor incorporation of stable isotope-labelled substrates into metabolic products. This article contrasts developments in electrospray ionisation mass spectrometry (ESI-MS) for the measurement of lipid metabolism with more established gas chromatography mass spectrometry and isotope ratio mass spectrometry methodologies. ESI-MS combined with diagnostic tandem MS/MS scans permits the sensitive and specific analysis of stable isotope-labelled substrates into intact lipid molecular species without the requirement for lipid hydrolysis and derivatisation. Such dynamic lipidomic methodologies using non-toxic stable isotopes can be readily applied to quantify lipid metabolic fluxes in clinical and metabolic studies in vivo. However, a significant current limitation is the absence of appropriate software to generate kinetic models of substrate incorporation into multiple products in the time domain. Finally, we discuss the future potential of stable isotope-mass spectrometry imaging to quantify the location as well as the extent of lipid synthesis. This article is part of a Special Issue entitled: BBALIP_Lipidomics Opinion Articles edited by Sepp Kohlwein.     

Stable isotope ecology in the Ituri Forest

The Ituri Forest, Democratic Republic of Congo (formerly Zaire) is an example of a closed canopy forest showing extreme depletion in ¹³C. ¹³C values for plants from the canopy top, from gaps in the canopy, and from the subcanopy average –29.0±1.7, –30.4±0.9, and –34.0±1.5, respectively. The ¹³C of forest mammals show these differences, with the subcanopy browsers (okapi, dwarf antelope) having ¹³C values for tooth enamel much more negative than subcanopy frugivores who derive their food from the canopy top, and from folivores and omnivores living in gap or clearing areas. Nitrogen isotopes in plants from this ecosystem have an average ¹⁵N value of 5.4±1.8 and do not show significant differences at the 95% confidence interval between plants from the canopy top, from gaps in the canopy, and from the subcanopy. The ¹⁸O_SMOW values of surface waters in the study area are between –2.0 and –2.7. The ¹⁸O_PDB for tooth enamel ranged from –3 to +7.     

Stable isotope ecology in the Omo-Turkana Basin

Stable isotopes provide an independent assessment of paleoenvironments in the Omo-Turkana Basin. Stable isotopes track the flow of oxygen and carbon through ecosystems and accordingly are not directly related to changes in mammalian faunal composition or sedimentology. Therefore, isotope studies give insight into the paleoenvironmental conditions in which human evolutionary trends have been recorded. The development of stable isotopes as indicators of continental environmental conditions has proceeded in parallel with questions about the conditions of human environment. What was the vegetation? How hot was it? How dry? What were the diets of animals living among early humans? And most persistently, how important were "savannas" to early hominids? In this review, we take the opportunity to provide extensive background on the use of isotopes in anthropological sites. The application of stable isotope ecology to anthropological sites in the Turkana Basin has a long history, but in many ways the Omo-Turkana Basin has been a proving ground for the development of new proxy methods for understanding tropical terrestrial environments in the Neogene and Quaternary. For that reason, we also describe some of the fundamental aspects of isotope ecology that developed outside the field of paleoanthropology.     

Trophic segregation of Falkland Islands seabirds: insights from stable isotope analysis

Seabird colonies provide rare opportunities to study trophic segregation in an entire bird community. We here present data on nitrogen and carbon isotope ratios of eight species of seabirds from New Island, Falkland Islands, and compare trophic levels (TL) and foraging distributions. We included adult feathers representing the interbreeding season, as well as chick feathers or down representing the breeding season. The stable isotope ratios indicated differences in feeding areas and TLs between species, consistent with the data of previous conventional diet analyses and observations at sea. We further reviewed conventional and stable isotope seabird community studies calculating the means and ranges of TLs observed across these studies. The mean TL (3.7) of the seabird community on New Island was at the lower end of the mean value range (3.5–4.5), but not significantly different, from the reviewed seabird communities. Seabirds on New Island had a range of 1.3 TLs, which is on the upper end of ranges within a community (0.4–1.5), indicating strong trophic structuring.     

Stable isotope evidence for 1500 years of human diet at the city of York, UK

We present here the results of a large-scale diachronic palaeodietary (carbon and nitrogen isotopic measurements of bone collagen) study of humans and animals from a single site, the city of York (U.K.), dating from the Roman period to the early 19th century. The human sample comprises 313 burials from the cemeteries of Trentholme Drive and Blossom Street (Roman), Belle Vue House (Anglo-Saxon), Fishergate (High and Later Medieval), and All Saints, Pavement (Later and Post-Medieval). In addition, 145 samples of mammal, fish and bird bone from the sites of Tanner Row and Fishergate were analyzed. The isotope data suggest dietary variation between all archaeological periods, although the most significant change was the introduction of significant quantities of marine foods in the Medieval periods. These are first evident in the diet of a small group of individuals from the High Medieval cemetery at Fishergate, although they were consumed almost universally in the following periods. The human isotope values are also remarkable due to unusually elevated delta(15)N ratios that are not sufficiently explained by the comparably small enrichment in (13)C that accompanies them. We discuss the possible reasons behind this and the archaeological significance of the data set.