Host identification in unfed ticks from stable isotope compositions (δ13C and δ15N)

Determination of the ratios of natural stable isotopes (¹³C/¹²C and ¹⁵N/¹⁴N) in unfed Ixodes ricinus nymphs and adults, which, in their previous stage, fed on captive wild rodents (Apodemus sylvaticus and Myodes glareolus), wild birds (Parus major and Cyanistes caeruleus) or domestic ruminants (Ovis aries and Bos taurus), demonstrated that it is possible to identify each host category with confidence. First, the tick–blood spacing, which is the difference between values obtained from ticks and the blood of hosts that they had fed on in the previous stage, was consistent (152 spacings investigated from 15 host individuals in total). Second, potential confounding factors (tick age and sex) did not affect the discriminatory power of the isotope patterns, nor did different rearing conditions (room temperature vs. 4 °C) or the duration of development (maximum of 430 days). The findings that the tick–blood isotope spacings, across a diverse range of hosts, were similar and predictable, and that confounders had little or no effect on this, strongly support the usage of the isotope approach. Because each of the host categories has a different role in the population dynamics of I. ricinus and in tick‐borne pathogen ecology, the method described here has great potential for the clarification of tick and tick‐borne pathogen ecology in the field.     

Decrypting stable‐isotope (δ13C and δ15N) variability in aquatic plants

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Life history of the individuals buried in the St. Benedict Cemetery (Prague, 15th–18th Centuries): Insights from 14C dating and stable isotope (δ13C, δ15N, δ18O) analysis

Funerary practices and bioarchaeological (sex and age) data suggest that a mortality crisis linked to an epidemic episode occurred during the fifth phase of the St. Benedict cemetery in Prague (Czech Republic). To identify this mass mortality episode, we reconstructed individual life histories (dietary and mobility factors), assessed the population's biological homogeneity, and proposed a new chronology through stable isotope analysis (δ¹³C, δ¹⁸O and δ¹⁵N) and direct radiocarbon dating. Stable isotope analysis was conducted on the bone and tooth enamel (collagen and carbonate) of 19 individuals from three multiple graves (MG) and 12 individuals from individual graves (IG). The δ¹⁵N values of collagen and the difference between the δ¹³C values of collagen and bone carbonate could indicate that the IG individuals had a richer protein diet than the MG individuals or different food resources. The human bone and enamel carbonate and δ¹⁸O values suggest that the majority of individuals from MG and all individuals from IG spent most of their lives outside of the Bohemian region. Variations in δ¹⁸O values also indicate that all individuals experienced residential mobility during their lives. The stable isotope results, biological (age and sex) data and eight ¹⁴C dates clearly differentiate the MG and IG groups. The present work provides evidence for the reuse of the St. Benedict cemetery to bury soldiers despite the funeral protest ban (1635 AD). The Siege of Prague (1742 AD) by French‐Bavarian‐Saxon armies is identified as the cause of the St. Benedict mass mortality event. Am J Phys Anthropol 151:202–214, 2013. © 2013 Wiley Periodicals, Inc.     

Nonlethal sampling for stable isotope analysis of juvenile Chinese sturgeon (Acipenser sinensis): Comparing δ13C and δ15N signatures in muscle and fin tissues

We compared δ¹³C and δ¹⁵N values of muscle with fin from juvenile Chinese sturgeon (Acipenser sinensis), to evaluate the feasibility of using nonlethal (fin) as an alternative to lethal (muscle) sampling. Size and lipid effect on the relationship between fin and muscle were also investigated. Dorsal muscle (DM) and fin clip (FC) were collected from A. sinensis with different body length (120–373 mm) in the Yangtze Estuary for isotope analysis. The result showed that (1) muscle isotope values could estimated by the values of fin, from either use the regression model (δ¹³C_DM = 0.939 × FC ? 2.577; δ¹⁵N_DM = 0.737 × FC + 4.638) or constants factors (δ¹³C_DM = δ¹³C_FC ? 1.27; δ¹⁵N_DM = δ¹⁵N_FC + 0.59); (2) no size‐based relationships with δ¹³C and δ¹⁵N from either fin or muscle; (3) lipid extraction significantly improving the fin and muscle regression model fit for both δ¹³C and δ¹⁵N values. Therefore, this study support the use of nonlethal fin tissues for isotope analysis of juvenile A. sinensis, and will allow trophic studies to avoid the effect of lipid accumulation from muscle.     

Fatty acids and stable isotopes (δ13C and δ15N) reveal temporal changes in narwhal (Monodon monoceros) diet linked to migration patterns

Narwhals (Monodon monoceros) are sentinel species in the Arctic and to investigate marine food web changes from 1982–2011 we examined diet using fatty acids, δ¹⁵N, and δ¹³C, in narwhals from Baffin Bay (BB) and northern Hudson Bay (NHB). We predicted temporal changes would be greater in NHB due to a significant reduction in summer ice cover. In NHB, δ¹⁵N significantly increased, δ¹³C displayed a parabolic trend, and fatty acids gradually shifted, albeit not significantly, over time. δ¹⁵N was stable, δ¹³C decreased, and fatty acids significantly changed over time in BB. Stable isotope mixing models indicated a dietary reduction in capelin and increase in Greenland halibut from 1994–2000 to 2006–2011 in BB, while capelin was an important dietary component for narwhals in NHB in recent years (2006–2011). These dietary changes may be attributed to changes in sea ice and narwhal migration. Seasonal dietary changes, as evidenced by changes in blubber fatty acids and skin and muscle stable isotopes, were not as apparent in the NHB population, which may be indicative of a reduced migratory distance. Long‐term monitoring of narwhal diet and migratory patterns associated with reduced sea ice provides invaluable information about how the marine ecosystem will redistribute with global warming.     

Trophic interactions in an ant nest microcosm: a combined experimental and stable isotope (δ13C/δ15N) approach

Living in close association with other organisms has proven to be a widespread and successful strategy in nature. Some communities are completely driven by symbiotic associations and therefore, intimate relationships among the partners can be expected. Here, we analyzed in‐depth the food web of a particularly rich community of arthropods found in strict association with European red wood ants (Formica rufa group). We studied the trophic links between different ant‐associated myrmecophiles and food sources associated with the host ant, but also tested predator–prey links among myrmecophiles themselves. Our approach combined direct feeding tests and stable carbon and nitrogen isotope analyses for a large number of myrmecophiles. The results of the direct feeding tests reveal a complex food web. Most myrmecophiles were found to parasitize on ant brood. Moreover, we encountered multiple trophic predator– prey links among the myrmecophiles. The results of the stable isotope analyses complement these findings and indicate the existence of multiple trophic levels and trophic isotopic niche compartmentalization. δ¹⁵N values were strongly correlated with the trophic levels based on the direct tests, reflecting that δ¹⁵N values of myrmecophiles increased with higher trophic levels. This strong correlation underlines the strength of stable isotopes as a powerful tool to assess trophic levels. In addition, the stable isotope data suggest that most species only facultatively prey on ant brood. The presence of numerous trophic interactions among symbionts clearly contrasts with the traditional view of social insects nests as offering an enemy‐free space for symbionts. Interestingly, the ant host can indirectly benefit from these interactions because brood predators are also preyed upon by other myrmecophiles. Overall, this study provides unique insights into the complex interactions in a small symbiont microcosm system and suggests that the interactions between host and symbiont might be mediated by other symbionts in the same community.     

Carbon (δ13C) and nitrogen (δ15N) stable isotope composition in plant and soil in Southern Patagonia's native forests

Stable isotope natural abundance measurements integrate across several biogeochemical processes in ecosystem N and C dynamics. Here, we report trends in natural isotope abundance (δ¹³C and δ¹⁵N in plant and soil) along a climosequence of 33 Nothofagus forest stands located within Patagonia, Southern Argentina. We measured 28 different abiotic variables (both climatic variables and soil properties) to characterize environmental conditions at each of the 33 sites. Foliar δ¹³C values ranged from ?35.4‰ to ?27.7‰, and correlated positively with foliar δ¹⁵N values, ranging from ?3.7‰ to 5.2‰. Soil δ¹³C and δ¹⁵N values reflected the isotopic trends of the foliar tissues and ranged from ?29.8‰ to ?25.3‰, and ?4.8‰ to 6.4‰, respectively, with no significant differences between Nothofagus species (Nothofagus pumilio, Nothofagus antarctica, Nothofagus betuloides). Principal component analysis and multiple regressions suggested that mainly water availability variables (mean annual precipitation), but not soil properties, explained between 42% and 79% of the variations in foliar and soil δ¹³C and δ¹⁵N natural abundance, which declined with increased moisture supply. We conclude that a decline in water use efficiency at wetter sites promotes both the depletion of heavy C and N isotopes in soil and plant biomass. Soil δ¹³C values were higher than those of the plant tissues and this difference increased as annual precipitation increased. No such differences were apparent when δ¹⁵N values in soil and plant were compared, which indicates that climatic differences contributed more to the overall C balance than to the overall N balance in these forest ecosystems.     

Changing gull diet in a changing world: A 150‐year stable isotope (δ13C, δ15N) record from feathers collected in the Pacific Northwest of North America

The world's oceans have undergone significant ecological changes following European colonial expansion and associated industrialization. Seabirds are useful indicators of marine food web structure and can be used to track multidecadal environmental change, potentially reflecting long‐term human impacts. We used stable isotope (δ¹³C, δ¹⁵N) analysis of feathers from glaucous‐winged gulls (Larus glaucescens) in a heavily disturbed region of the northeast Pacific to ask whether diets of this generalist forager changed in response to shifts in food availability over 150 years, and whether any detected change might explain long‐term trends in gull abundance. Sampled feathers came from birds collected between 1860 and 2009 at nesting colonies in the Salish Sea, a transboundary marine system adjacent to Washington, USA and British Columbia, Canada. To determine whether temporal trends in stable isotope ratios might simply reflect changes to baseline environmental values, we also analysed muscle tissue from forage fishes collected in the same region over a multidecadal timeframe. Values of δ¹³C and δ¹⁵N declined since 1860 in both subadult and adult gulls (δ¹³C, ~ 2–6‰; δ¹⁵N, ~4–5‰), indicating that their diet has become less marine over time, and that birds now feed at a lower trophic level than previously. Conversely, forage fish δ¹³C and δ¹⁵N values showed no trends, supporting our conclusion that gull feather values were indicative of declines in marine food availability rather than of baseline environmental change. Gradual declines in feather isotope values are consistent with trends predicted had gulls consumed less fish over time, but were equivocal with respect to whether gulls had switched to a more garbage‐based diet, or one comprising marine invertebrates. Nevertheless, our results suggest a long‐term decrease in diet quality linked to declining fish abundance or other anthropogenic influences, and may help to explain regional population declines in this species and other piscivores.     

The diverse dietary profiles of MIS 3 cave bears from the Romanian Carpathians: insights from stable isotope (δ13C and δ15N) analysis

Late Pleistocene European cave bears (Ursus spelaeus ) have been considered to be largely vegetarian, although stable isotope data (δ¹³C and δ¹⁵N values) from the Romanian Carpathians has suggested considerable dietary variation. Here we evaluate previous and additional adult cave bear isotopic data from four Marine Isotope Stage 3 (MIS 3) sites in the Carpathians. Pe?tera Ur?ilor (N  =  35), Pe?tera Cioclovina (N  =  32), Pe?tera Muierilor (N  =  8), and Pe?tera cu Oase (N  =  72) provide both a dichotomy between samples suggesting vegetarian diets (from Cioclovina and Muierilor) and more omnivorous diets (from Ur?ilor and Oase), and considerable isotopic variation within samples from each site. While an inference of a strictly vegetarian diet may apply to groups that lived in ecosystems which restricted the available animal protein for these large ursids, the within and between sample isotopic variation among the Carpathian cave bears indicates considerable flexibility in their sources of protein and hence in their dietary regimes. In addition, developmental assessment of Cioclovina isotopic profiles (neonates, juveniles, sub‐adults and adults) provides patterns of transfer of stable isotope signatures throughout immature life for both δ¹³C and δ¹⁵N (increase and decrease, respectively), whereas those from Ur?ilor show little developmental shift.     

Effects of ethanol storage and lipid and urea extraction on δ15N and δ13C isotope ratios in a benthic elasmobranch,the bluespotted maskray Neotrygon kuhlii

Ethanol storage and lipid and urea extraction had no effect on bluespotted maskray Neotrygon kuhlii muscle δ¹³C values whereas urea‐removal and ethanol storage increased δ¹⁵N values. Results presented here show a significant δ¹⁵N increase post‐urea removal and provide additional support for this approach in future elasmobranch stable‐isotope analysis (SIA) studies. Further experimental work on other elasmobranch species is needed to assess extraction and preservation effects on stable‐isotope (SI) values.     

A stable isotope (δ13C and δ15N) perspective on human diet on rapa nui (Easter Island) ca. AD 1400–1900

Ecological and environmental evidence suggests that Rapa Nui was among the most marginally habitable islands in Eastern Polynesia, with only a fraction of the biotic diversity found on archipelagos to the west, and capable of sustaining many fewer cultigens traditionally transported by Polynesian colonizers. However, archaeological evidence for human dietary adaptations under such restrictions is limited. Little is known about the particulars of the subsistence base and dietary changes on Rapa Nui that may be associated with a hypothesized late prehistoric decline in the quality and diversity of food sources. To better understand prehistoric Rapa Nui diet we examined stable carbon and nitrogen isotope compositions of human teeth along with archaeological faunal material thought to comprise the Rapa Nui food web. Our results indicate that contrary to previous zooarchaeological studies diet was predominantly terrestrial throughout the entire sequence of occupation, with reliance on rats, chickens and C3 plants. While a few individuals may have had access to higher trophic level marine resources, this is evident only later in time (generally post–AD 1600). A decline in δ¹⁵N through time was observed, and may be attributed to declines in available terrestrial proteins; however, presently we cannot rule out the effect of changing soil and plant baseline δ¹⁵N. Our results also suggest differential access to higher trophic level marine resources among contemporaneous populations, but more research is required to clarify this observation. Am J Phys Anthropol 152:173–185, 2013. © 2013 Wiley Periodicals, Inc.     

Comparative response of δ13C, δ18O and δ15N in durum wheat exposed to salinity at the vegetative and reproductive stages

This study compared the performance of the stable isotope composition of carbon (δ¹³C), oxygen (δ¹⁸O) and nitrogen (δ¹⁵N) by tracking plant response and genotypic variability of durum wheat to different salinity conditions. To that end, δ¹³C, δ¹⁸O and δ¹⁵N were analysed in dry matter (dm) and the water‐soluble fraction (wsf) of leaves from plants exposed to salinity, either soon after plant emergence or at anthesis. The δ¹³C and δ¹⁸O of the wsf recorded the recent growing conditions, including changes in evaporative conditions. Regardless of the plant part (dm or wsf), δ¹³C and δ¹⁸O increased and δ¹⁵N decreased in response to stress. When the stress conditions were established just after emergence, δ¹⁵N and δ¹³C correlated positively with genotypic differences in biomass, whereas δ¹⁸O correlated negatively in the most severe treatment. When the stress conditions were imposed at anthesis, relationships between the three isotope signatures and biomass were only significant and positive within the most severe treatments. The results show that nitrogen metabolism, together with stomatal limitation, is involved in the genotypic response to salinity, with the relative importance of each factor depending on the severity and duration of the stress as well as the phenological stage that the stress occurs.     

Variations in stable isotope ratios of carbon (δ13C) and nitrogen (δ15N) in different body parts and eggs of adult stoneflies (Plecoptera)

Variations in δ¹³C and δ¹⁵N might arise from differences in nutrient allocation. Residence times of δ¹³C and δ¹⁵N vary among tissues depending on metabolic turnover rates. However, because of their small size, entire individual insects are generally used as single samples in isotope analyses. The present study aimed to determine the degree of isotope similarity among regions of the adult body and eggs in four species of Plecoptera (Amphinemura sp., Sweltsa sp., Kamimuria tibialis Pictet and Ostrovus sp.). Levels of δ¹³C and δ¹⁵N differ between the four species, being lowest in Amphinemura sp., and with δ¹⁵N being highest in Sweltsa sp. Egg masses contain consistently the lowest values of δ¹³C in the four species, with the δ¹⁵N value of eggs being highest in K. tibialis and Ostrovus sp., and lower in Amphinemura and Sweltsa spp. In Sweltsa sp., the δ¹⁵N levels of the dermal layers and cuticle are lowest, whereas the δ¹³C values of the dermal layers and cuticle are almost equal to those in other regions of the body, except egg masses. Oviposited individuals of Amphinemura and Sweltsa spp. have lower δ¹⁵N levels than individuals that have not oviposited. The rates of metabolism and incorporation of dietary metabolites will differ depending on the body regions and species. Differences in egg ecology such as egg developmental period and egg buoyancy among species are considered to impact on the values of δ¹³C and δ¹⁵N. These results will be useful for understanding the nutritional status of aquatic insects and their energy allocation.     

Differences in δ13C and δ15N stable isotopes in the pearly razorfish Xyrichtys novacula related to the sex,location and spawning period

In the present study, Xyrichtys novacula (Labridae) were sampled at five locations around the islands of Ibiza and Formentera (western Mediterranean Sea). Isotopic signatures of δ¹³C, δ¹⁵N and the C:N ratio were analysed in relation to locality, sex and size differences. δ¹³C and δ¹⁵N partitioning was also studied in the reproductive spawning period. There were significant differences in the δ¹³C signature between localities for both sexes, but not for δ¹⁵N. Sex differences were also found with a mean ±s.e . value of ?17·38 ± 0·06‰δ¹³C and 8·36 ± 0·05‰δ¹⁵N for females and ?17·17 ± 0·07‰δ¹³C and 8·80 ± 0·06‰δ¹⁵N for males. Increasing total length in both sexes was positively correlated with δ¹⁵N enrichment and a significant positive linear regression was established for both variables. During the reproductive spawning period, there were changes in δ¹³C fractioning with enrichment in postspawning females and males (with respect to prespawning and spawning periods) and δ¹⁵N impoverishment in postspawning females (with respect to prespawning and spawning periods). Xyrichtys novacula uses local food sources, as confirmed by δ¹³C and δ¹⁵N, and females and males use different food sources, thus avoiding intraspecific competition. This was confirmed by δ¹⁵N enrichment as size increased. Spawning leads to special requirements for gonad maturation, which is reflected in the isotopic signatures for both sexes.     

Spatio‐temporal isotopic signatures (δ13C and δ15N) reveal that two sympatric West African mullet species do not feed on the same basal production sources

Potential trophic competition between two sympatric mullet species, Mugil cephalus and Mugil curema, was explored in the hypersaline estuary of the Saloum Delta (Senegal) using δ¹³C and δ¹⁵N composition of muscle tissues. Between species, δ¹⁵N compositions were similar, suggesting a similar trophic level, while the difference in δ¹³C compositions indicated that these species did not feed from exactly the same basal production sources or at least not in the same proportions. This result provides the first evidence of isotopic niche segregation between two limno‐benthophageous species belonging to the geographically widespread, and often locally abundant, Mugilidae family.     

The legacy of enhanced N and S deposition as revealed by the combined analysis of δ13C, δ18O and δ15N in tree rings

This study aimed to evaluate the effects of long‐term repeated aerial nitrogen (N) and sulphur (S) misting over tree canopies of a Sitka spruce plantation in Scotland. We combined δ¹³C and δ¹⁸O in tree rings to evaluate the changes in CO₂ assimilation (A) and stomatal conductance (g_s) and to assess their contribution to variations in the intrinsic water‐use efficiency (WUE_i, i.e., the A/g_s ratio). Measurements of δ¹⁵N enabled shifts in the ecosystem N cycling following misting to be assessed. We found that: (i) N applications, with or without S, increased the ratio between A and g_s in favour of A, thus supporting a fertilizer effect of added N. (ii) After the treatments ceased, the trees quickly adjusted to the reductions of N deposition, but not to the reduction in S deposition, which had a negative effect on WUE_i by reducing A. This indicates that the beneficial role of N deposition may be negated in forests that previously received a high load of acid rain. (iii) δ¹⁵N in tree rings reflected the N dynamics caused by canopy retention, with the fingerprint also present in the litter, after the experiment stopped. (iv) Both our results (obtained using canopy applications) and a collection of published data (obtained using soil applications) showed that generally WUE_i increased in response to an increase of N applications, with the magnitude of the changes related to soil conditions and the availability of other nutrients. The shifts observed in δ¹⁵N in tree rings also suggest that both the quantity of the applied N and its quality, mediated by processes occurring during canopy N retention, are important determinants of the interactions between N and C cycles. Stable isotopes are useful probes to understand these processes and to put the results of short‐term experiments into context.     

Effects of decomposition and storage conditions on the δ13C and δ15N isotope values of killer whale (Orcinus orca) skin and blubber tissues

Several different factors in the collection and preservation of whale skin and blubber samples were examined to determine their effect on the results obtained by stable nitrogen and carbon isotope (δ¹⁵N and δ¹³C) analysis. Samples of wet killer whale skin retained their original stable isotope values for up to 14 d at 4°C or lower. However, decomposition significantly changed the δ¹⁵N value within 3 d at 20°C. Storage at ?20°C was as effective as ?80°C for the preservation of skin and blubber samples for stable isotope analysis for at least a year. By contrast, once a skin sample had been freeze‐dried and lipid extracted, the stable isotope values did not change significantly when it was stored dry at room temperature for at least 12 mo. Preservation of whale skin samples for a month in DMSO‐salt solution, frozen or at room temperature, did not significantly change the δ¹⁵N and δ¹³C values of lipid extracted tissues, although the slight changes seen could influence results of a study if only small changes are expected.     

Mother–embryo isotope (δ15N, δ13C) fractionation and mercury (Hg) transfer in aplacental deep‐sea sharks

Stable carbon (δ¹³C) and nitrogen (δ¹⁵N) isotopic values and total mercury (Hg) concentrations were analysed in muscle and liver of mothers and embryos of two aplacental shark species, Squalus megalops and Centrophorus moluccensis. Embryos of the two species had similar or lower isotopic values than their respective mothers, the only exception being for δ¹³C, which was higher in the liver of C. moluccensis embryos than in their mothers. Hg concentrations were systematically lower in embryos compared with their mothers suggesting a low transfer of this element in muscle and liver.