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.     

Environmental and species‐specific controls on δ13C and δ15N in dominant woody plants from central‐western Argentinian drylands

Spatial variation in mean annual precipitation is the principal driver of plant water and nitrogen status in drylands. The natural abundance of carbon stable isotopes (δ¹³C) in photosynthetic tissues of C3 plants is an indicator of time‐integrated behaviour of stomatal conductance; while that of nitrogen stable isotopes (δ¹⁵N) is an indicator of the main source of plant N (soil N vs. atmospheric N₂). Previous studies in drylands have documented that plant δ¹³C and δ¹⁵N values increase with decreasing mean annual precipitation due to reductions in stomatal conductance, and soil enriched in ¹⁵N, respectively. However, evidence for this comes from studies focused on stable isotopes measurements integrated at the plant community level or on dominant plants at the site level, but little effort has been made to study C and N isotope variations within a species growing along rainfall gradients. We analysed plant δ¹³C, δ¹⁵N and C/N values of three woody species having different phenological leaf traits (deciduous, perennial and aphyllous) along a regional mean annual precipitation gradient from the central‐western Argentinian drylands. Noticeably, plant δ¹³C and δ¹⁵N values in the three woody species did not increase towards sites with low precipitation or at the start of the growing season (drier period), as we expected. These results suggest that environmental factors other than mean annual precipitation may be affecting plant δ¹³C and δ¹⁵N. The short‐term environmental conditions may interact with species‐specific plant traits related to water and nitrogen use strategies and override the predictive influence of the mean annual precipitation on plant δ¹³C and δ¹⁵N widely reported in drylands.     

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.     

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.     

Annual variability in dentin δ15N and δ13C reveal sex differences in weaning age and feeding habits in Risso's dolphins (Grampus griseus)

Teeth of odontocetes accumulate annual dentinal growth layer groups (GLGs) that record isotope ratios, which reflect the time of their synthesis. Collectively, they provide lifetime records of individual feeding patterns from which life history traits can be inferred. We subsampled the prenatal dentin and postnatal GLGs in Risso's dolphins (Grampus griseus) (n = 65) that stranded or were collected as bycatch in Taiwan (1994–2014) and analyzed them for δ¹⁵N and δ¹³C. Age‐specific δ¹⁵N and δ¹³C values were corrected for effects of calendar year, stranding site, C/N, and sex. δ¹⁵N values were higher in prenatal layers (14.94‰ ± 0.74‰) than in adult female GLGs (12.58‰ ± 0.20‰), suggesting fetal enrichment during gestation. Decreasing δ¹⁵N values in early GLGs suggested changes in dietary protein sources during transition to complete weaning. Weaning age was earlier in males (1.09 yr) than in females (1.81 yr). Significant differences in δ¹⁵N values between weaned males and females suggest potential sexual segregation in feeding habits. δ¹³C values increased from the prenatal to the 4th GLG by ~1.0‰, indicative of a diet shift from ¹³C‐depleted milk to prey items. Our results provide novel insights into the sex‐specific ontogenetic changes in feeding patterns and some life history traits of Risso's dolphins.     

Nitrogen and carbon contents and δ15N and δ13C signatures in six bryophyte species: assessment of long‐term deposition changes (1980–2010) in Spanish beech forests

In this study we used recent (2010) and herbarium material (1980) of six bryophyte species to assess long‐term atmospheric deposition in natural forested areas in northern Spain. For this purpose, tissue nitrogen and carbon content, as well as δ¹³C and δ¹⁵N signatures of samples of Hypnum cupressiforme, Polytrichastrum formosum, Leucobryum juniperoideum, Rhytidiadelphus loreus, Homalothecium lutescens and Diplophyllum albicans were analysed and comparisons made between years and species. In addition, the usefulness of each of the six species was evaluated. The range of values observed was similar to that in other studies carried out in rural areas. Significantly lower values were found in 2010 for N (H. cupressiforme), δ¹⁵N (R. loreus and D. albicans), C (R. loreus) and δ¹³C (all except L. juniperoideum). Our natural areas are thus now less influenced by atmospheric pollutants than they were, most probably due to changes in some traditional local activities. Differences were observed between species for all the four parameters studied, so different species must not be analysed together. Finally, R. loreus and H. lutescens seem to be good bioindicators, sensitive even with a few samples, although further studies are needed to corroborate their usefulness.     

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.     

Relationships between growth traits and scale stable isotopes (δ13C, δ15N) of adult chum salmon Oncorhynchus keta in Hokkaido,Japan

Stable isotope analysis (SIA) in combination with growth analysis using scales collected from adult chum salmon Oncorhynchus keta migrating back to Hokkaido, Japan, was performed to describe the variation of isotopic composition of carbon (δ¹³C) and nitrogen (δ¹⁵N) in scales and to examine relationships with growth traits [age, fork length (FL), and relative growth ratio in the last growth period [(RGR^last)]. Scale stable isotope (SI) values in 3‐ to 6‐year‐old fish were highly variable, ranging from ?17.6‰ to ?14.3‰ for δ¹³C and 9.5‰ to 13.4‰ for δ¹⁵N. The δ¹⁵N was positively correlated with FL, and this tendency may indicate changes in trophic level with growth. Significant effect was not detected between δ¹⁵N and RGR^last, it can be inferred that factors potentially yielding high δ¹⁵N may not necessarily result in higher growth rates. No trend found between FL and δ¹³C may imply that there is no clear segregation in feeding locations between the 3‐ to 6‐year groups. This study provided basic information for scale SI values of chum salmon adults and indicated that SIA using scales could be a new approach to elucidating the trophic ecology of chum salmon.     

IMPACT OF TAXONOMY,GEOGRAPHY, AND DEPTH ON δ13C AND δ15N VARIATION IN A LARGE COLLECTION OF MACROALGAE1

The natural abundance of carbon stable isotopes (δ¹³C) of marine macrophytes has been measured in previous studies and used to analyze differences in C_i assimilation among the three macroalgal phyla, Chlorophyta, Ochrophyta, and Rhodophyta, and seagrasses, distinguishing diffusive CO₂ entry from the operation of a CO₂‐concentrating mechanisms (CCM). The work reported here further resolves the patterns of δ¹³C variation in aquatic macrophytes related to their taxonomy, geographic location (and consequently climatic conditions), and vertical zonation. Analyses of δ¹³C for 87 species are reported, including eight that have not been previously examined, belonging to taxa in the three macroalgal phyla, plus two species of seagrasses, collected at different latitudes. For one species of each phylum, analyses were also conducted through a vertical depth gradient. Representative species were used in a pH drift experiment, in order to compare the mechanism of C_i acquisition for photosynthesis with the δ¹³C subsequently determined on the same specimen. Our results suggest that the δ¹³C values were mostly determined by taxonomy. Depth effects on C stable isotope composition differed among taxa. The parallel measurements of δ¹⁵N are more difficult to interpret mechanistically; there are no robust phylogenetic and large‐scale biogeographic correlations; local factors of natural (e.g., upwellings) and anthropogenic (e.g., sewage outfall) inputs predominate in determining the macrophyte δ¹⁵N.     

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.     

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

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VARIATION IN INTERNAL δ15N AND δ13C DISTRIBUTIONS AND THEIR BULK VALUES IN THE BROWN MACROALGA PADINA AUSTRALIS GROWING IN SUBTROPICAL OLIGOTROPHIC WATERS1

The utility of δ¹⁵N measurements in Padina australis Hauck as a probe for its external nitrogen (N) sources was tested by monitoring the bulk values of chemical components [δ¹⁵N, δ¹³C, and N and carbon (C) contents] and their internal distributions during a 12 d incubation in a controlled environment. Under the saturated conditions of isotopically heavier nitrate than that of original algal tissue, the bulk δ¹⁵N in P. australis was enriched, but less than what was predicted from a simple mixing model, signaling possible isotopic discrimination during N assimilation and subsequent N efflux from the cells. The enhanced N content (%), which occurred simultaneously with this δ¹⁵N shift, was a useful signal indicating this phenomenon. Bulk δ¹⁵N was enriched, especially around the meristem, in tissues growing under conditions of higher irradiance and temperature, probably due in part to dissolved organic nitrogen (DON) excretion. The δ¹³C enhancement in bulk algal tissues, also associated with high photosynthetic activity, may be an additional signal indicating this unbalanced internal δ¹⁵N distribution. However, in summer and winter environmental conditions with periodic nitrate supplies simulating typical fringing reef waters, the difference in measured algal bulk δ¹⁵N from theoretical predictions was within ±1.0‰. This difference is very small compared with the variation in δ¹⁵N in possible N sources in coastal areas. In the field, therefore, δ¹⁵N in Padina can be used effectively to trace N sources in both space and time after determining algal N content and δ¹³C to determine whether large alterations occur in algal δ¹⁵N.     

Use of a δ13C–δ15N relationship to determine animal trophic positions in a tropical Australian estuarine wetland

Stable isotope composition of organisms from different trophic groups collected from a semi‐isolated wetland pool in the Ross River estuary, northern Australia, was analysed to determine if there was a consistent relationship between δ¹³C, δ¹⁵N and trophic level that could be used to assign trophic positions. A strong linear negative relationship between δ¹³C and δ¹⁵N was detected for the three trophic levels considered (primary producers, primary consumers and secondary consumers). This relationship was consistent among trophic levels, differing only in height, that is, on δ¹⁵N values, which indicate trophic positions. A difference of 3.6–3.8‰ between trophic levels was present, suggesting a δ¹⁵N fractionation of approximately 3.7‰, a value slightly higher than the commonly assumed δ¹⁵N fractionation of approximately 3.4‰. The relationship between δ¹³C and δ¹⁵N was similar for invertebrate and fish primary consumers, indicating similar δ¹⁵N trophic fractionation for both groups, meaning trophic positions and trophic length could be reliably calculated based on either invertebrates or fish.     

Water chemistry,landscape, and spatial controls of δ13C and δ15N of zooplankton taxa in boreal lakes: One size does not fit all

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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.     

The effects of tissue type and body size on δ13C and δ15N values in parrotfish (Labridae) from Zanzibar,Tanzania

Differences between the stable isotopic ratios (δ¹³C and δ¹⁵N) of two tissues (blood and muscle) from four species of East African coral reef parrotfishes (family: Labridae, tribe: Scarini) were analysed across a broad spectrum of body sizes. Comparison of isotopic ratios between the tissues allowed the assessment of using blood as an alternative tissue to muscle. In 2010–2011, constant differences between tissues (δ_blood minus δ_muscle) were found across a broad range of sampled fish lengths. Linear relationships between the tissues, specific for an isotope, indicate that constants could be generated for converting blood isotope into muscle isotope values. Only one species, Chlorurus sordidus, displayed an inconsistent difference between tissues in δ¹⁵N, indicating that this ratio was dependent on fish length. The δ¹³C of both tissues was positively related linearly to fish length for three species, while δ¹⁵N showed no relationship with body length. The results are interpreted as indicating dietary consistency over days to weeks, the time of tissue turnover for blood and muscle, respectively. Lastly, differences among the species, even closely related species, show that the generation of tissue conversion constants is species‐specific.     

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.     

A Comparative Study by δ13C-Analysis of Crassulacean Acid Metabolism (CAM) in Kalanchoë (Crassulaceae) Species of Africa and Madagascar

The carbon isotope ratios (δ¹³C values) of samples of Kalanchoë species collected in Africa were compared with previous data obtained with species from Madagascar. In contrast to the Malagasy species which cover the whole range of δ¹³C values from ?10 to ? 30%_o, indicating high inter- and intraspecific diversity of CAM performance, in the African species nearly all δ¹³C values were less negative than ?18%₀. Thus, in the African species the CAM behaviour is characterized by CO₂ uptake proceeding mainly during the night. The distribution of δ¹³C values among the species clearly mirrors the taxonomic groups and the three sections of the genus Kalanchoë sensu lato. The Kitchingia section comprises only groups having CAM with a high proportion of carbon acquisition by the C₃-pathway of photosynthesis. The same holds true for the first three groups of the Bryophyllum section, whereas in the following groups of the section CAM with CO₂ proceeding mainly during the night is common. The latter CAM mode is typical also for the majority of groups and species in the section Eukalanchoë. The African Kalanchoë species belong to the Eukalanchoë section, whereas in Madagascar all three sections are abundant. The data support the view that the centre of adaptive radiation of the genus is located in Madagascar. They also suggest that high CAM variability is abundant in the more primitive taxa of the genus, whereas the phylogenetically more derived taxa show a stereotype CAM with CO₂ uptake taking place only during the night.     

Foliar δ13C response patterns along a moisture gradient arising from genetic variation and phenotypic plasticity in grassland species of Inner Mongolia

Plants depend upon both genetic differences and phenotypic plasticity to cope with environmental variation over different timescales. The spatial variation in foliar δ¹³C levels along a moisture gradient represents an overlay of genetic and plastic responses. We hypothesized that such a spatial variation would be more obvious than the variation arising purely from a plastic response to moisture change. Leymus chinensis and Stipa spp. were sampled from Inner Mongolia along a dry‐wet transect, and some of these species were transplanted to an area with a moisture gradient. For Stipa spp., the slope of foliar δ¹³C and mean annual precipitation along the transect was significantly steeper than that of foliar δ¹³C and mean annual precipitation after the watering treatment. For L. chinensis, there was a general decreasing trend in foliar δ¹³C under the different (increasing) watering levels; however, its populations showed an irregular relationship between foliar δ¹³C and moisture origin. Therefore, support for our hypothesis was obtained from Stipa spp., but not from L. chinensis.