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Stable Isotope Ecology

  1. Jason Newton

Published Online: 15 JAN 2010

DOI: 10.1002/9780470015902.a0021231

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Newton, J. 2010. Stable Isotope Ecology. eLS.

Author Information

  1. Scottish Universities Environmental Research Centre, NERC Life Sciences Mass Spectrometry Facility, East Kilbride, UK

Publication History

  1. Published Online: 15 JAN 2010

Introduction and Background

  1. Top of page
  2. Introduction and Background
  3. Natural Variations
  4. Applications of Stable Isotope Approaches to Ecological Problems
  5. Conclusions
  6. References
  7. Further Reading

Geochemists provided the earliest applications of stable isotope ratios to the earth sciences, including the tracing of water and fluid sources, geothermometry, palaeoclimatology, etc. Recently, ecologists have added storeys to the theoretical foundations of applied stable isotope geochemistry, constructing a large database over the past 25 years to enable the study of the interactions among plants, animals and their environment. The following discussion is restricted to ‘bulk’ stable isotope analysis, but the reader is directed to Evershed et al. 2007 for a review of compound-specific stable isotope techniques and applications. Following an account of isotope terminology and measurement, the natural variations of stable isotope ratios of the light elements are described, followed by some examples of how stable isotope approaches are applied to several broad ecological themes.

Terminology

Isotopes of a given element differ in the number of neutrons they contain, and are loosely described as ‘heavy’ if they are neutron-rich and ‘light’ if they are neutron-poor. Isotopes are divided into three types based on their stability and origin: (i) radioactive isotopes, (ii) radiogenic stable isotopes and (iii) nonradiogenic stable isotopes. Radioactive isotopes are those which spontaneously decay into ‘daughter’ isotopes. Stable isotopes are those which do not, but may form as products of radioactive decay (i.e. radiogenic stable isotopes), in which case their abundance is purely a function of time, or alternatively their abundance may be determined by stellar nucleosynthesis at the birth of the solar system (i.e. nonradiogenic stable isotopes). Nonradiogenic stable isotopes are most useful for ecological studies, and particularly those of the light elements: H, C, N, O and S, which are major constituents of organic materials, and for which there are large relative mass differences between isotopes of the same element. The small mass difference between a heavy and light isotope of a given element causes them to behave slightly differently during normal physical and chemical processes and thus changes the isotope ratio. It is this property which makes them useful to many branches of applied science. Stable isotope ratios of heavy to light isotopes are usually measured using stable isotope mass spectrometry, which comprises a gas-source isotope ratio mass spectrometer with a peripheral instrument which prepares samples into a form (i.e. a gas) suitable for mass spectrometry. More information on stable isotope techniques can be gleaned from de Groot 2004, 2009 and Matthews and Beauchemin 2010.

Since absolute isotope ratios (R=heavy isotope/light isotope) are difficult to quantify accurately and precisely, the isotope ratio (Rx) of a sample x is compared against that of an internationally agreed standard (Rstd). Thus, the delta (δ) notation is used for describing isotope ratios (McKinney et al., 1950), where δX=(Rx/Rstd−1), where X is the notation of the heavy isotope of a pair. For clarity, delta values are multiplied by a thousand to give units in ‰ (permil). It follows from this equation that each element has a primary international standard with a value of 0‰. Deviations towards the positive and negative imply enrichments and depletions in the heavy isotope with respect to the standard. Note that in some cases the primary international standards have now expired; however, the delta scales for each element remain the same, and there are secondary international standards with nonzero delta values.

Mixing and fractionation

In terms of modelling/tracing various ecological processes, there are two themes – mixing and fractionation. Mixing is self-explanatory, and mixing of two or more components with different isotope ratios can be modelled using a mass-balance approach, in an identical manner to mixing solutions of differing concentrations:

  • mathml alt image

where δ1, δ2, …, δn and m1, m2, …, mn are, respectively, the delta values and mass of that element in separates 1, 2, …, n in the mix.

Isotope fractionation, which is essentially partitioning of isotopes into different phases/compounds/reservoirs in a system, results from the subtle differences in the properties of two isotopes of a given element. Several rules may be determined:

  • (i)
    in kinetic reactions, light isotopes usually react faster and
  • (ii)
    in equilibrium reactions, heavy isotopes preferentially partition into components involving strong chemical bonds.

Fractionations may be practically quantified by subtracting the delta value of a reactant from that of a product.

Natural Variations

  1. Top of page
  2. Introduction and Background
  3. Natural Variations
  4. Applications of Stable Isotope Approaches to Ecological Problems
  5. Conclusions
  6. References
  7. Further Reading

Carbon and δ13C

Carbon has two stable isotopes: the more common 12C and the minor isotope 13C, with the primary international standard being V-PDB, derived from the carbonate skeleton of a Cretaceous cephalopod (Pee Dee Belemnite). The natural δ13C variations of terrestrial material span a 100‰ range, from biogenic methane and other reduced carbon compounds with very negative values, through soft animal and plant tissues, to carbonates with δ13C values just into the positive portion of the δ13C scale. The largest reactive pool in the carbon cycle is marine dissolved inorganic carbon (DIC), which controls the δ13C of carbonate-secreting organisms; both lie close to 0‰. One of the seminal discoveries in stable isotope ecology was that terrestrial plants using disparate photosynthetic pathways could be differentiated using δ13C (Smith and Epstein, 1971). C3 plants generally have values of around −35‰ to −20‰, whereas C4 plants have a δ13C range of about −18‰ to −7‰, with the resulting soil organic δ13C reflecting the respective photosynthetic process. The disparity between the δ13C of C3 and C4 plants is stark, given that the precursor for both photosynthetic pathways is atmospheric CO2. The difference is caused by the fact that the ribulose-1,5-bisphosphate carboxylase (Rubisco) catalyst involved in the C3 pathway strongly discriminates against 13CO2 compared with phosphoenolpyruvate(PEP) carboxylase, the C4 catalyst. The δ13C of CAM (crassulacean acid metabolism) plants overlaps with C3 and C4 plants, with a range of −10‰ to −22‰ (O'Leary, 1988). See also Photosynthesis: Ecology

Another application of stable isotopes has been to derive water-use efficiency (WUE) estimates of plants. Both WUE and the δ13C of plants are controlled by intracellular carbon dioxide concentrations; this led Farquhar et al. 1982 to demonstrate that the δ13C of plant tissue could be used as a reliable indicator of WUE. Investigations of WUE in plant systems using the isotope approach are numerous, for example Marshall and Zhang 1994 modelled WUE in deciduous and evergreen plants over a large altitudinal gradient. In the marine environment, photosynthesis proceeds via the C3 pathway; however, the δ13C of marine plants and algae do not resemble terrestrial C3 plants, since here the carbon source is mainly DIC rather than atmospheric carbon dioxide. Marine phytoplanktons have a wide range of δ13C values from about −30‰ to −18‰, the lighter values associated with higher latitudes (Rau et al., 1982). Freshwater phytoplanktons encompass a similar but slightly larger range of δ13C values. Marine and freshwater vascular plants macroalgae have a wide range of δ13C reflecting the use of carbon dioxide or HCO3 for photosynthesis (Maberly et al., 1992).

Nitrogen and δ15N

Nitrogen has two isotopes, the more common 14N and the minor isotope 15N. By far the largest reservoir of nitrogen above the geosphere is atmospheric nitrogen, and its uniform isotope ratio is the reason for its choice as the international standard for δ15N, atmospheric isotope reservoir (AIR). Nitrogen fixation involves very little nitrogen isotope fractionation, such that N-fixing plants have δ15N values very close to 0‰. Non-nitrogen-fixing plants have a slightly more varying range of δ15N compositions, depending on their particular source of nitrogen. The successive oxidation steps involved in nitrification are associated with varying amounts of fractionation, which is kinetically controlled. Given that most of the organic nitrogen in soils is slowly converted into ammonium, this is generally the rate-determining step in the nitrification process and the resulting nitrate is quite similar in terms of δ15N to the organic starting materials. However, when large amounts of ammonium are available, the oxidation steps to nitrite and nitrate are rate limiting, and the nitrate formed may be depleted in 15N by up to 35‰. Denitrification back to molecular nitrogen gas involves a 15N depletion of up to −20‰. All the fractionations in the pedospheric part of the nitrogen cycle are heavily dependent on nitrogen concentrations. Synthetic fertilizers, since being produced from air via the Haber process, are close to 0‰. Volatilization of ammonium compounds to ammonia from manure, however, involves a fractionation of up to −40‰, such that the residue may be very 15N-enriched. This has proved quite useful in detecting sewage pollution (Costanzo et al., 2001). Högberg, 1997 provides a comprehensive review of nitrogen isotope fractionations in plants and soils.

Hydrogen (δ2H) and oxygen (δ18O)

Hydrogen has two stable isotopes – the minor isotope deuterium or 2H and the more common isotope protium or 1H. Oxygen has three stable isotopes, though the minor 17O is of less importance from an ecological standpoint; as with the other elements mentioned here, 16O is more common than its heavy counterpart, 18O. Both hydrogen and oxygen isotope scales use standard mean ocean water (V-SMOW) as their primary international standards. Ocean water is a fairly uniform 0‰ in terms of both δ2H and δ18O scales, with the exception of where there is mixing with freshwater or ice sheets. During both evaporation and condensation of water, the fractionation of hydrogen and oxygen isotopes are correlated, such that precipitation isotope ratios form a linear relationship which approximates δ2H=8δ18O+10‰, called the global meteoric water line. As a result, there are strong spatial patterns of δ2H and δ18O in precipitation on a global scale, and seasonal patterns in the same location. Models have been put forward to predict the isotopic composition of precipitation at a given geographic location (http://www.waterisotopes.org). The natural range of waters is around 600‰, stretching from the Antarctic ice which is close to −500‰, to over +100‰ in the Saharan basin lakes which are subject to extreme evaporation. The source of hydrogen for plants is local water, which enters the plant with negligible fractionation, such that bulk plant water δ2H is consistent with environmental water. In higher terrestrial plants, however, evapotranspiration in the leaf increases both δ2H and δ18O of plant cell water compared with environmental water. Organic compounds, particularly lipids, resulting from biosynthesis in plants are depleted in 2H compared with water.

Interest in the hydrogen and oxygen isotope systematics of plant tissues has been driven by the possibility of deriving historical climate data, and empirical correlations have been derived between tree-ring cellulose isotope data and various environmental factors including temperature, humidity and rainfall. Hydrogen isotopes in animal tissues also reflect local precipitation, despite the complication of hydrogen incorporation via diet as well as drinking water. Given the complexity, detailed knowledge of how hydrogen isotopes are exchanged during tissue synthesis is still lacking.

Sulfur and δ34S

Sulfur has four stable isotopes – 32S, 33S, 34S and 36S, with 32S and 34S being the most abundant (c. 95% and 4% respectively). The δ34S scale is measured with respect to Cañon Diablo Troilite (V-CDT). The vast majority of natural samples fall into a range from −40‰ to +40‰. Large deviations in δ34S are primarily caused by biologically mediated fractionation at low temperatures. In particular, dissimilatory bacterial reduction of sulfate to H2S creates large sulfur isotope effects, such that the δ34S of resulting sulfides can be up to 40‰ more negative than pre-existing sulfate. In contrast, there is little fractionation of sulfur isotopes during the assimilation of sulfate by both aqueous and terrestrial plants. Although marine sulfate is a very uniform +21‰, sulfate uptaken by terrestrial plants is more variable, and depends on the underlying geology. Animals must ingest organic sulfur compounds and convert them as necessary, though minor isotope fractionation is involved. Thus, throughout various food-web studies, 34S-enrichments are often taken as evidence of a marine influence, and δ34S measurements have been used to trace marine nutrients in freshwateSr systems (MacAvoy et al., 1998).

Applications of Stable Isotope Approaches to Ecological Problems

  1. Top of page
  2. Introduction and Background
  3. Natural Variations
  4. Applications of Stable Isotope Approaches to Ecological Problems
  5. Conclusions
  6. References
  7. Further Reading

Determining diet/food webs

Although some animals’ diets may readily be determined by observation alone, more elusive species may require a more invasive approach. In some animals it may be possible to obtain regurgitated dietary material to study, whereas in others only gut content analysis (GCA) will be possible, which is obviously a destructive technique. The main disadvantage of these conventional techniques is that they all comprise ‘snapshot analyses’: they only provide a measure of what an animal has been feeding on most recently. Stable isotope analysis integrates diet over a longer time period, and offers an alternative approach which is often nondestructive and in many cases noninvasive.

It is possible to use a theoretical approach to calculate isotope fractionations for many simple chemical reactions; however, in the real, complex, biological world, an experimental/observational approach is more feasible. Merely subtracting the original delta value from the final delta value in a particular process gives a workable approximation, Δ of the total fractionation of the process. For instance, the long-held maxim of ‘you are what you eat, plus a few ‰’ (DeNiro and Epstein, 1976) describes the general fact that the δ15N of a consumer is a few ‰ ‘heavier’ than those of its diet (Figure 1) and is the basis of all food-web ecology investigations using nitrogen isotopes. The effect for δ13C is much less, with carbon isotope ratios reflecting more the source of carbon, such that δ15N–δ13C plots (Figure 1) are a useful graphical representation of simple food webs. The arithmetic difference in the nitrogen isotope ratio of consumer and diet (Δ15N=δ15Nconsumer−δ15Ndiet, cf. Figure 1) has been termed the ‘trophic enrichment factor’ (TEF). TEFs have been calculated for many taxa, and though mean Δ15N for several compilations of taxa averages around +3‰ (Minagawa and Wada, 1984; Post, 2002; Vanderklift and Ponsard, 2003; Vander Zanden and Fetzer, 2007) in agreement with the earliest work (DeNiro and Epstein, 1981), the range of Δ15N is quite wide, and varies with the biochemical mode of excretion and diet C:N (Vanderklift and Ponsard, 2003). In some cases, for example large cetaceans, it is impractical to measure TEFs directly, and assumptions are made regarding a probable TEF for the consumer/diet in question. Diet is generally determined by stable isotope analysis of specific tissues, rather than that of the whole animal, and different tissues will partition isotopes by differing amounts, hence tissue-specific TEFs (i.e. δ15Ntissue−δ15Ndiet) have to be taken into account. Despite these complications, Δ15N has been used to make direct inferences about the diet of many consumers, and nitrogen stable isotopes have also been used to infer a variety of ecological parameters. For instance, the variance of stable isotope ratios has been used to derive a measure of trophic niche width (Bearhop et al., 2004). The δ15N value of a consumer relative to that of the base of the food web combined with the knowledge of TEFs provides a quantitative measure of the food chain length (Vander Zanden et al., 1999), which is not subject to the kind of errors involved in estimating the number of trophic levels based on the presence/absence of intermediate consumers.

thumbnail image

Figure 1. Schematic food web in which Δ15N (and Δ13C) represent the trophic enrichment factor. See text for further explanation.

The isotopic composition of an animal tissue reflects diet at the time of synthesis, and different tissues in the same animal have varying turnover rates. This provides an opportunity to obtain time-integrated dietary information. Turnover rates (and TEFs) are calculated using carefully controlled ‘diet-switch’ feeding experiments (Figure 2). These involve changing the feeding regime of a laboratory animal from an isotopically homogeneous diet to one which is isotopically disparate (e.g. from a C3-based plant diet to a C4 one). Tissues are sampled before the diet switch, and at regular intervals following the change to the new diet. In the C3–C4 diet switch example, δ13Ctissue is plotted against time, an exponential uptake curve is plotted and a half-life calculated. As an example, in one of the earliest such experiments, Tieszen et al. 1983 showed that the δ13C half-life in rat muscle is around a month, compared with a week for rat liver. Recently, the exponential-fit approach has been criticized for the assumption that these diet-switch isotope exchange reactions are subject to first-order rate kinetics. Using an analogous methodology to disentangle radionuclides of differing half-lives, Cerling et al. 2007 have determined ‘reaction progress variables’ by linearizing the exponential decay curves. Such work has been validated by the observation that there can be more than one source pool with differing half-lives, and that this method provides more realistic diet reconstruction scenarios.

thumbnail image

Figure 2. Hypothetical diet switch experiment. The animal is fed a C3 plant-based diet for some time, then switched to a C4 plant-based diet at time=0. Analysis of tissue for δ13C is carried out every 10 days. The time for complete carbon turnover is in excess of 100 days.

This approach is very useful, as it allows the researcher to look at changes in diet over time, using the isotopic composition of different tissues. As an example, for a small passerine bird, by measuring the δ15N and δ13C in blood and feathers, it is possible to glean dietary information from a few days (plasma) and weeks (red blood cells) ago, and from the time of the most recent feather moult, and all without sacrificing the bird.

In contrast to the soft tissues mentioned above, many hard tissues (feathers, baleen, hair, fingernails, teeth) are metabolically (and therefore isotopically) inert once synthesized. Some of these – tooth collagen, for example – are grown incrementally, and can be tied to temporal parameters, such as growth annuli. Stable isotope measurements on individual increments allow a high-resolution temporally explicit dietary history to be constructed. Careful measurements such as these have for instance elucidated long-term dietary changes in bowhead whales (Hobson and Schell, 1998), toothed whales (Mendes et al., 2007) and elephants (Cerling et al., 2009).

Mixed models have been developed to determine diet based on stable isotope measurements, the principal requirement that the consumer assimilates diets which are isotopically disparate. For example, Inger et al. 2006 explored marine versus terrestrial dietary choices by light-bellied Brent geese at monthly intervals over a 16-month period. One of the obstacles in obtaining dietary information from an animal tissue is that using simple mathematical models a maximum of only n+1 dietary sources can be elucidated from n isotope ratios. More advanced models (Phillips and Gregg, 2003) will provide a range of feasible solutions to systems where the number of sources is too large to provide a unique mixture of diets, but these models are parameterized with invariable figures for the isotope ratios of diet and TEFs. Recently, Bayesian models (Moore and Semmens, 2008; Parnell et al., 2008) have been proposed which incorporate uncertainty, and result in probability distributions for which the analyst can choose the most likely solution.

Animal migration

The study of animal migration is essentially an extension to dietary modelling as described above. As intrinsic markers, the stable isotope approach does not require initial marking of individuals; all that is required is that an animal moves from one isotopically distinct habitat to another. It is particularly informative for those animals which are too small to attach transmitters, for example insects and small passerines.

In terms of carbon isotopes for instance, the δ13C disparity between freshwater and marine primary production has been used to detect anadromy in fish (Adams et al., 2008).

The relationship between temperature and δ2Hprecipitation affords the potential to map the migration of terrestrial animals at a fine resolution. The rationale for hydrogen isotope tracking of animals is as follows:

  • (i)
    Temperature and rainout effects in the hydrological cycle provide a uniform relationship between δ2Hprecipitation and latitude, altitude and continentality. A description of hydrogen isotope fractionations in the hydrological cycle can be found in Clark and Fritz 1999.
  • (ii)
    There is a predictable relationship between a specific animal tissue of interest and δ2Hprecipitation.
  • (iii)
    The tissue sampled for hydrogen isotope analysis is metabolically inert once synthesized.

Feather keratin is metabolically inert once grown, and in North America, the positive relationship between δ2Hprecipitation (=geographic location) and δ2Hfeather has been used to good effect for elucidating the migratory behaviour of a number of passerine bird species (Chamberlain et al., 1997; Hobson and Wassenaar, 1997). Large compilations of δ2Hprecipitation data from global hydrological projects have been used to construct ‘isoscapes’ (Bowen and Revenaugh, 2003). Isoscapes are spatial distributions of isotope ratios incorporated into maps, which can be utilized to broadly predict the geographic location of growth of an individual feather. Europe, however, is topographically more complex than North America, and latitudinally shorter, which means that the range of δ2Hprecipitation is smaller and less predictable (Hobson et al., 2004). Nevertheless, there have been a number of successful investigations of European bird migration using hydrogen isotope measurements of feathers or claws (Bearhop et al., 2005). Where migration passes over areas differing in the relative proportions of C3 and C4 plants, the addition of δ13C increases discrimination (Neto et al., 2006).

There are other sources of variation in δ2Hfeather which confound the use of stable hydrogen isotope ratios as a geolocation device. For instance, long-term climatic variations may cause temporal changes in δ2Hprecipitation, and differing metabolic effects among species may result in a species-specific correlation between δ2Hprecipitation and δ2Hfeather. Thus, the ‘map-look-up technique’ for assigning geographic origins of populations using precipitation isoscapes and an equation involving δ2Hprecipitation and δ2Htissue is attracting some criticism (Wunder and Norris, 2008). This technique still remains popular because of its easy implementation; it is nevertheless useful in the early stages of experimental design. Isoscapes based on control conspecific or analogue individuals from known locations allow a direct comparison. Ironically, one of the first isoscapes (Hobson et al., 1999) is a classic example of this, constructed from the isotope analysis of Monarch butterflies raised in known locations across the eastern United States. This provided a template from which Monarch butterflies could be geographically assigned with some accuracy.

Isotope additions

The article so far presents processes and applications involving ‘natural abundance’ isotope ratios, that is those within the natural range of isotope compositions. It is possible to buy chemical compounds from commercial companies which are enriched in the heavy isotope such that the isotope ratio R>0.99. These compounds have obvious advantages over radioactive tracers in tracer studies in that they are nontoxic and do not require licensing. They are generally used to investigate the routing of materials and chemical transformations which occur along the way. The simplest experiments involve just adding a labelled compound to a system, and then analysing the different products to acquire knowledge about the location(s) of the products of reactions involving the labelled compound; more detailed experiments would obtain quantitative data on how the label is partitioned among the products. An example of this in the carbon cycle would be using 13C labelling to examine how carbon is allocated to different plant tissues, and eventually to components of soil. Similarly, 15N labelling has been applied to soil-plant systems. In particular, the 15N tracer has been used to elucidate the fate of different 15N-labelled fertilizers (Powlson and Barraclough, 1993) by measuring its abundance in the ammonium, nitrate, organic N and plant tissue. By measuring the 15N abundance over time, a measure of the loss of N derived from the fertilizer can be measured. Other examples of 13C and 15N labelling outwith plant and soil sciences include the application to stream basal food resources to evaluate the importance of these to consumers (Parkyn et al., 2005) and examining the fate of 13C-labelled phytodetritus among the oceanic abyssal benthic community (Witte et al., 2003).

A special example of isotope additions is that of doubly labelled water (DLW), which is water with enriched levels of 2H and 18O. The DLW method has been developed for studying the intake and loss of water and energy metabolism in animals. An animal is typically injected with DLW, weighed and blood samples are taken at the time of the injection and some specified time later. Loss of 2H in water over this period can be used to derive a measure of water flux rate through the animal. 18O is lost as both water and carbon dioxide, and thus the difference between the rate of loss of 2H and 18O is a measure of the carbon dioxide production rate, a measure of energy expenditure. DLW can be combined with other ecological measurements to investigate the energy budgets of animals in their natural environment and during specific activities, for example migration flights for birds (Kvist et al., 2001).

Conclusions

  1. Top of page
  2. Introduction and Background
  3. Natural Variations
  4. Applications of Stable Isotope Approaches to Ecological Problems
  5. Conclusions
  6. References
  7. Further Reading

The purpose of this article has been to draw the reader to the expanding subject of stable isotope ecology, and introduce several applications where stable isotopes have made a very significant contribution. Ongoing technological developments will ensure the continued involvement of stable isotopes in ecology in the future.

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  1. Top of page
  2. Introduction and Background
  3. Natural Variations
  4. Applications of Stable Isotope Approaches to Ecological Problems
  5. Conclusions
  6. References
  7. Further Reading
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Further Reading

  1. Top of page
  2. Introduction and Background
  3. Natural Variations
  4. Applications of Stable Isotope Approaches to Ecological Problems
  5. Conclusions
  6. References
  7. Further Reading
  • Fry B (2006) Stable Isotope Ecology, 308pp. New York: Springer.
  • Hobson KA and Wassenaar LI (eds) (2008) Tracking Animal Migration with Stable Isotopes, 144pp. Amsterdam, Holand: Academic Press/Elsevier.
  • Michener R and Lajtha K (eds) (2007) Stable Isotopes in Ecology and Environmental Science, 566pp. Oxford, UK: Blackwell.
  • Speakman J (1997) Doubly Labelled Water: Theory and Practice, 416pp. London: Springer.