Application of Isotopic Methods to Tracking Animal Movements

C H A P T E R

4 Application of Isotopic Methods to Tracking Animal Movements Keith A. Hobson University of Western Ontario, London, ON, Canada

4.1 INTRODUCTION

20 years did investigations start to focus on using stable isotopes to trace animal origins and movements, and this has now evolved into a diverse field of investigation with forensic as well as ecological implications. Stable isotope methods are now considered mainstream in ecology, and are well established in the diverse toolbox available to study animal movement. Fundamentally, the application of stable isotopes as a tracer of animal origin relies on three basic isotopic principles:

The application of stable isotope methods in ecology has undergone a fascinating evolution over past decades. Early applications involving carbon and nitrogen isotope analyses focused on plant physiology and photosynthetic pathways and the tracing of nitrogenous compounds in terrestrial and aquatic systems. It was not until the early 1990s that isotopic linkages were made between primary productivity and animal tissues through several trophic levels. A key development was the observation that stable isotope measurements of animal tissues provide information on source of nutrients and relative trophic position, and this led to vast improvements in the way animal ecology, physiology, and nutrition is studied. From the simplistic concept of “you are what you eat plus a few parts per mil” refinements were made involving sophisticated isotope mixing models, insights into how nutritional quality affects trophic isotope discrimination and the evolution of compound-specific versus bulk tissue isotope methods. Only in the past

Tracking Animal Migration with Stable Isotopes DOI: https://doi.org/10.1016/B978-0-12-814723-8.00004-0

1. Tissues in consumer (all animals including humans) stable isotope (CHNOS) values reflect the dietary and drinking water they are in “equilibrium” with. If diet and water used by a migratory organism differs isotopically and spatially, then isotope values in the consumer may potentially provide information on previous locations or biomes. 2. The period over which this spatial isotopic information is retained depends on the tissue type. For metabolically active tissues,

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this represents a moving window of dietary information. For metabolically inactive tissues, spatial information will be “locked in” indefinitely, but reflects the short period of growth of that tissue. 3. Mechanisms related to dietary transfer of isotopic signals to consumer tissues including isotopic discrimination, exercise, and metabolic routing are known and accounted for. In practice, it is unlikely that all three principles are satisfied or fully known with sufficient confidence. However, depending on the organism, much of the uncertainty can be constrained and, as we shall see, inferences can still be made with respect to previous provenance of individuals based on isotopic measurements of their tissues. A careful blend of knowledge of the life history of the organism, knowledge of likely dietary isotopic landscapes or “isoscapes” experienced by that organism, and the physiological parameters that can influence isotopic inferences makes up the art of using stable isotopes to accurately track migratory organisms. The devil, of course, lies in the details and assumptions made.

4.2 TOWARD ISOTOPIC ASSIGNMENT OF ORIGINS The “you are what you eat plus a few parts per mil” maxim is formalized in the equation δCt 5 δd 1 Δdt where δCt is the measured stable isotope value of a tissue in the consumer, δd is the stable isotope value of the diet, and Δdt is the diet-tissue isotope discrimination factor. We know that the isotope discrimination factor is an oversimplification, and it does not necessarily take into account metabolic routing of specific macronutrients such as proteins, lipids, and carbohydrates. Research has also shown

that diet-tissue isotope discrimination factors are influenced by quality of the diet, and so are likely not to be a static variable for wild animal populations. Because our ability to place an organism onto an isoscape map is sensitive to the true isotope discrimination factors, researchers should evaluate their estimates based on an honest assessment of how well they know such factors. Obtaining this information requires dietary experiments with the organism of interest, or, at least a sensitivity analysis to determine the effect of varying discrimination values on the outcome of GIS models or other methods used to “place” an organism onto a map.

4.2.1 Tissue and Isotopic Turnover: The Moving Window It is well known that stable isotope values in consumer tissues reflect an integration of feeding events over various time periods. Tieszen, Boutton, Tesdahl, and Slade (1983) were the first to conduct “diet switch” experiments, whereby captive animals were allowed to achieve equilibrium under one dietary regime and then being switched to an isotopically different diet (Fig. 4.1). Tissue isotopes tracked the diet switch and uptake of the new isotopic dietary signal. This approach has been applied successfully for many species, and most find an exponential uptake curve to describe the pattern of isotopic dietary change in tissues. DðtÞ 5 a 1 b expð 2ctÞ where D(t) is the stable isotope value of the tissue at time t, a is the asymptotic tissue value, b is the absolute change in tissue isotope value between initial and asymptotic conditions, and c is a rate constant defining tissue turnover. When researchers wish to consider effects of growth (k) as well as metabolic turnover (m), the overall rate constant c can be expressed as

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FIGURE 4.1 Conceptual depiction of the way in

–22 –24

which different tissues will respond to an isotopic diet switch. We expect close coupling between the diet isotope trajectory and fast turnover tissues like liver and blood plasma. Much slower response is expected for slow turnover tissues like bone collagen.

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–18 δ13C of tissues

13 δ C of diet

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–20

Muscle

–22 Collagen Liver

–24 –26 0

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100 150 Time in days

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(k 1 m). This approach works to provide estimates of elemental (C,N) turnover rates in various tissues of birds, fish, and mammals (e.g., Bosley, Witting, Chambers, & Wainright, 2002; Dalerum & Angerbjo¨rn, 2005; Hesslein, Hallard, & Ramlal, 1993). One disadvantage of these studies is they were based on sedentary, nonexercised individuals in controlled laboratory settings. Can the elemental turnover rates obtained from such sedentary experimental studies be applied to migrating individuals where, in the example of birds, undergo hours of sustained flight? Might we not expect more rapid elemental turnover in tissues of exercising versus sedentary organisms? This is still not fully clear, but Hobson and Yohannes (2007) used Rosy Starlings (Sturnus roseus) flying in a wind tunnel to provide a first approximation of this effect for the cellular fraction of blood. They performed a C3 to C4 diet switch on birds that flew for several hours per day, and then contrasted the isotopic turnover rates with those of an unexercised control group. Interestingly, no difference in isotope turnover was found for carbon isotopes between the two groups. This suggests that blood production was unaffected isotopically by exercise, at least to the level measurable in this experiment. More studies are needed and the use of

wind tunnels is clearly one effective way to explore turnover rates in migratory birds and insects. These results are encouraging and suggest published tissue isotopic turnover rates may be appropriate for isotopic studies on migratory organisms. The other good news is that elemental turnover rates across animals appear to follow expectations based on body size (Thomas & Crowther, 2015). It is possible, then, to estimate turnover rates for various tissues based on the body mass of the organism of interest even though that species has not been tested experimentally (Martı´nez del Rio & Carleton, 2012). Others have investigated a different approach to analyzing and interpreting nutrient uptake curves based on isotopic dietary switch experiments (Cerling, Bowen, Ehleringer, & Sponheimer, 2007). Instead of fitting exponential equations to estimate turnover rates, they used a decay-lapse function technique to estimate relative contributions. This approach involves the determination of the so-called “reaction progress variables” that are derived from a process that involves linearizing the decay curves. Interestingly, this approach suggests curves represent more than one source pool, with each having a different elemental turnover rate. Perhaps the best

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interpretation is that essential amino acids are transferred quickly from diet to tissues, whereas nonessential amino acids are manufactured from dietary components and so represent a lag time prior to incorporation into consumer tissues (but see Chapter 7: Amino Acid Isotope Analysis: A New Frontier in Studies of Animal Migration and Foraging Ecology). This way of looking at elemental turnover in animals shows potential for understanding how elements from diet and body stores are routed to consumer tissues, and how these differ temporally in terms of dietary integration. However, this important development by no means negates the conventional approach, and the net elemental turnover measured by fitting the exponential function provides a phenomenological estimate of the time period a given isotopic measurement of an organism represents (see also Carleton, Kelly, Anderson-Sprecher, & Martı´nez del Rio, 2008). Once we have assessed a realistic estimate of the half-life of an element for a tissue of a

migratory organism, we need to decide on a convention that best quantifies the time period represented by the isotopic measurement. Most authors have considered that a tissue realistically represents about 3 half-lives, or the time required for 87.5% of the original signal to be replaced by a new signal. Put another way, we should at least be able to detect 12.5% of the original material remaining by our isotopic measurement. While this is a rule-ofthumb, the ability to resolve between an original tissue signal and the asymptotic signal reached at a new location also depends upon the magnitude of the isotopic difference between these two signals. The greater the isotopic difference between initial and final dietary conditions (i.e., the greater the value b), and the smaller the variance associated with each equilibrium condition, the more confident we are of detecting isotopic information from a previous location (Fig. 4.2). Phillips and Eldridge (2006) explored the utility of using more than one tissue to detect Biome 2

Tissue 1 δX (per mil)

Tissue 2

Biome 1

t′1

t′2

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t2 Time (days)

FIGURE 4.2 When an organism moves from one isotopic biome to another, our ability to detect the original biome signal will depend on the tissue we choose and the magnitude of isotopic separation between the two biomes. Here, tissue 1 has a faster elemental turnover rate than tissue 2. The bands about each biome indicate the isotopic resolution or measurement error corresponding to organisms in that biome. The scenario of reducing the isotopic distance is demonstrated with the arrows. Here, we can see that the time over which we can detect the original biome signal is reduced (primed notation).

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the time an individual organism has spent in a new environment. Such information is less useful for estimating where an organism came from, but provides insights into the value of the migratory stopover environment. This approach is based on the contrast between tissues with different turnover rates, typically by comparing a fast turnover tissue like liver, plasma, or breath CO2 and a slower turnover tissue like muscle or the cellular fraction of blood. The model assumes that the researcher knows the initial and asymptotic tissue isotope values, the measured isotope value of tissues at some time after arrival, and the necessary rate constants associated with the tissues used. The model does a good job of estimating the time since diet shift and the magnitude of the isotopic difference between initial and asymptotic conditions, except in circumstances where the elapsed time was a fraction of a half-life of the slower turnover tissue, or when the diet shifts were small (i.e., less than 10 times the measurement error). Klaassen, Piersma, Korthals, Dekinga, and Dietz (2010) and Heady and Moore (2013) provide additional developments of models addressing time since arrival or diet switch. As with all models, solutions are based on assumptions. In the case of discerning previous geographical provenance of a migratory organism, we typically make the assumption that the organism was in equilibrium with its previous diet upon arrival. This will depend on the tissue, and so there would be a much higher likelihood of equilibrium conditions reached for shorter turnover tissues. Use of intermediate- or long-turnover tissues may be less useful for those migrants that move quickly among different stopover locations. There are some circumstances where we are interested in knowing if the arrival signature is different from the local food web signature, and less concerned that it can be associated with a particular location. There will also be error associated with estimates of the rate constants

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(k 1 m) and estimates of these errors are typically poorly known for most species. Finally, all models assume a direct dietary source of nutrients to tissues and do not consider situations where organisms may be metabolizing stored nutrients for maintenance. The development of stable isotope methods to tracking migratory wildlife has provided a rich literature to illustrate the breadth of applications using the light isotopes of C, N, H, O, and S (reviewed in Boecklen, Yarnes, Cook, & James, 2011; Hobson, 1999, 2005, 2008; Layman et al., 2012; Rubenstein & Hobson, 2004). With the increase in research in this field and interest in forensic tracing of plant and animal products (many studies with similar aims), it is no longer practical to provide a detailed documentation of this field. Rather, this chapter briefly summarizes key concepts and important findings, with due homage paid to the original works. In general, the isotope applications can be categorized into (1) inferences of animal origins based on biome markers using isotopes of C, N, and S and (2) those using modeled continental-scale δ2H, δ13C, and δ15N isoscapes. The use of δ2H measurements in particular has brought tremendous opportunities, but also challenges as we attempt to fill in the information gaps associated with this element, hence hydrogen isotopes are discussed separately.

4.2.2 Direct Isotope Tracers Isotopic discrimination relevant to food webs and animal movement in general is a phenomenon of the light stable isotopes (e.g., C, N, H, O, and S). For heavier elements, often little or no isotope discrimination occurs resulting in a more direct link to surficial geology, hydrology, or underlying isoscapes. There are however many exceptions and abiotic and biotic processes are involved in fractionation of several metals (e.g., Coutaud, Meheut,

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Viers, Rols, & Pokrovsky, 2014; Croal, Johnson, Beard, & Newman, 2004) and so each isotope must be considered on a case-by-case basis. Unfortunately, isotopic analyses of the heavier elements are costly and difficult because they are more involved than isotope ratio mass spectrometry and require clean labs and the use of more sophisticated instrumentation such as Inductively coupled plasma mass spectrometry (ICPMS). Nonetheless, a few elements such as Sr, Pb, and Hg show useful isotopic structure that can vary spatially and thus be applied to tracing animal movements. Sulfur is one of the light elements for which we typically expect little isotopic discrimination, but there are few S isotope studies on tissue types. Sulfur in consumer tissues is located in sulfur-bearing amino acids (e.g., cysteine and methionine) and so δ34S measurements are closely linked to dietary protein pathways. Unlike the other light isotopes, we expect little S isotopic discrimination between diets and consumer tissues because there is little opportunity for the essential amino acids to be isotopically modified in consumers (Arneson & MacAvoy, 2005; Richards, Fuller, Sponheimer, Robinson, & Ayliffe, 2003). As a result, δ34S measurements are useful direct tracers in food web and migration studies (Hebert & Wassenaar, 2005; Krouse, Stewart, & Grinenko, 1991). Proximity to coastlines influences terrestrial food web δ34S values due to the fallout of sulfur compounds derived from sea spray (Jamieson & Wadleigh, 2000; Zazzo, Monahan, Moloney, Green, & Schmidt, 2011). In terrestrial systems, δ34S values in consumer tissues are influenced by underlying geology with marine-derived sediments and volcanic rocks having relatively enriched values compared to other substrates. Animals linked to sources of sulfur in turn derived from anaerobic sediments in marshes can also show enrichment. We expect the use of δ34S measurements to increase substantially in the coming years due to the lack of discrimination involving this

isotope as well as methodological improvements making it possible to measure relatively small tissue samples (Chapter 2: Introduction to Conducting Stable Isotope Measurements for Animal Migration Studies). Natural variations in strontium isotope values of bedrock are determined by bedrock type and age varies regionally. Sr isotope signals in tissues are relatively unvarying temporally, leading to the possibility of developing permanent isoscapes useful for the study of animal movements. Sr has no discrimination occurring from soils to higher trophic levels (Flockhart, Kyser, Chipley, Miller, & Norris, 2015). Beard and Johnson (2000) modeled an expected 87Sr/86Sr isoscape for the United States based on patterns of surficial geology and applied that model to assigning human skeletal remains. We expect a general increase in the 87Sr/86Sr ratio from west to east in North America due to increasing age of bedrock and Sellick, Kyser, Wunder, Chipley, and Norris (2009) showed that adding δ87Sr measurements to δ2H in feathers of tree swallows (Tachycineta bicolor) across a longitudinal gradient in North America improved the precision of assignments to origin. Barnett-Johnson, Pearson, Ramos, Grimes, and MacFarlane (2008) successfully characterized expected δ87Sr values in watersheds supporting specific populations of Atlantic salmon. Examination of δ87Sr values in otoliths allowed these authors to identify the natal stream origin of fish taken at sea. That work underlined the amount of work required to first understand underlying δ87Sr patterns in specific regions of interest and the scale of movements of interest. By combining lithology-specific parameters in addition to bedrock age in predictive models, progress has been made in refining the δ87Sr model isoscape for the continental United States by Bataille and Bowen (2012) and for the Caribbean by Bataille et al. (2012). Like Sr, the stable isotopes of trace elements of lead (204Pb, 206Pb, 207Pb, and 208Pb) reflect

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bedrock source from which they are derived. Anthropogenic sources of Pb can be traced due to derivation from different ore sources and there has been considerable application of Pb isotope tracing because this element is an important environmental pollutant. Most notably, Pb isotopes have proven useful for tracing distributions and origins of leaded gasoline, ash from coal burning, and incineration products in the environment (reviewed by Komarek, Ettler, Chrastny, & Mihaljevic, 2008). Measurements of concentrations and stable isotopes of Pb in animals have proven useful in evaluating sources of exposure. For example, sources of incidental ingestion of Pb by raptors or scavengers consuming hunterkilled prey have been linked directly to Pb ammunition used (Finkelstein et al., 2010). An interesting application on sources of elephant ivory in Africa involved the measurement of provenance through the tracing of isotopes in ivory of several elements including Pb (Vogel, Eglington, & Auret, 1990) but few studies have used Pb isotopes to infer animal movements or provenance beyond stock identification. Stewart, Outridge, and Stern (2003) examined the 208Pb/207Pb and 206Pb/207Pb ratios in teeth of Walrus (Odobenus rosmarus) in the Canadian Arctic and were able to infer life history movements. Walrus are particularly amenable to this approach because they feed almost exclusively on sedentary bivalves and so are closely linked to the geochemical environment and localized food webs. While the lack of isotopic discrimination between biota and underlying inorganic substrates for heavier trace elements allow for direct creation of isoscapes, recent investigations into the behavior of the stable isotopes of Hg (198Hg, 199Hg, 200Hg, 201Hg, and 202Hg) highlight their complexity in nature. Mercury is deposited in polar regions through atmospheric transport and a variety of biogeochemical processes result in methylation of Hg into a bioavailable form (MeHg), which is toxic.

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Photochemical transformations of Hg compounds can result in isotopic changes that are independent of mass. The even-mass isotopes of Hg show mass dependent fractionation whereas the odd isotopes do not. Point et al. (2011) investigated Hg isotope concentrations in the eggs of seabirds occupying areas with different ice cover in coastal Alaska and found considerable isotopic variation that could be linked to the extent of photochemical breakdown of MeHg into less toxic forms. Thus the Hg isotopic composition of seabird tissues carried spatial information related to latitudinal patterns of ice cover in spring. While the focus of this book is almost entirely on the abundant light isotopes, it is worth recalling heavier isotopes such as those of Sr, Pb, and Hg and assays of the (nonisotopic) concentrations of trace elements have been used considerably to infer origins and movements of biota (Chapter 2: Introduction to Conducting Stable Isotope Measurements for Animal Migration Studies). The most useful heavy isotope situations involve improved assignment of individuals to a relatively small number of possible populations that can be well described in terms of their trace element or stable isotope composition. We will later revisit the concept of statistically combining isotopic and nonisotopic data to improve assignments of animals to their origin.

4.2.3 Tracing Involving Isotopic Discrimination Factors or Calibrations 4.2.3.1 Nitrogen Isotopes Despite extensive use of N stable isotopes in delineating animal diets and trophic relationships, the use of δ15N measurements in tracing origins of animals is rare. This is due to the fact that δ15N values in plant and animal tissues vary tremendously, regionally and at small spatial scales due to numerous natural and anthropogenic influences on the N cycle

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(Vitousek et al., 1997) which range from landuse practices, fertilizer use, sewage disposal, and the release of nitrogenous compounds into the atmosphere (Pardo & Naddlehoffer, 2010). Such N isotope variation is impossible to model in terms of predictable, continent-wide, isoscapes. However, in more natural settings, foliar δ15N has been modeled globally by Craine et al. (2009) and influences of climatic variables, N and P availability, N fixation processes, and types of mycorrhizal fungi have been identified as controlling factors. Thus while general large-scale phenomena affecting terrestrial food web δ15N values are understood, high isotopic variance at more local to regional scales is to be expected. Nonetheless, some researchers have attempted to use the foliar δ15N isoscape provided by Craine et al. (2009) to produce tissue-specific isoscapes to assist in assignment of birds to molt origins in Africa (Hobson, Møller, & Van Wilgenburg, 2012; Hobson, Van Wilgenburg, Faaborg, et al., 2014; Hobson, Van Wilgenburg, Wassenaar, & Larson, 2012; Hobson, Van Wilgenburg, Wassenaar, Powell, et al., 2012; Veen et al., 2014). More typically, however, δ15N values in animal tissues have been used to infer the type of biome supporting animals during tissue growth. Generally, marine sources of N are typically more enriched in 15N than terrestrial sources. In terrestrial systems, untilled soils are less enriched in 15N than those exposed by agriculture. Following this principle, Hobson (1999) demonstrated that feathers grown in boreal biomes are more depleted in 15N than those from agricultural landscapes. In general, hotter, dryer regions have food webs with higher δ15N values compared with those in cooler or wetter areas. Another fundamental issue complicating the application of δ15N measurements to infer animal origin is that this isotope is influenced by trophic position, with bulk tissue δ15N values increasing by about 2.5m5m with each trophic level (Layman et al., 2012; Post, 2002).

Thus inferring origins using bulk tissue N isotope analyses requires knowledge of diet and this can be a challenge for omnivores that may move across regions with changing baseline δ15N values. Tissue δ15N measurements represent a means of tracing protein pathways derived from diet because this element is largely absent in lipids and carbohydrates. This means that linking animals back to isoscapes using tissue δ15N values is theoretically more feasible for carnivores and frugivores than for omnivores. For essential amino acids, nitrogen will largely be incorporated with little isotopic discrimination into the protein pool of the consumer. Nonessential amino acids typically involve more opportunities for isotopic discrimination during protein synthesis and so the net discrimination we see for δ15N measurements in consumers will reflect the degree to which the diet meets the amino acid requirement of the consumer (Robbins, Felicetti, & Sponheimer, 2005). In general, poorer quality diets result in greater overall diet-tissue discrimination for 15 N than high-quality diets. An important derived variable in experiments designed to establish tissue-specific δ15N values in migratory animals is the elemental C:N ratio of the diet, as this ratio provides a useful indicator of diet quality and the N isotope discrimination factor to apply in natural situations. N isotopic discrimination will also depend on the means of voiding nitrogenous waste. Here, a major difference occurs between aquatic invertebrates that void nitrogen via ammonia compared to terrestrial vertebrates (Post, 2002). There is also evidence that ungulates adapted to arid conditions conserve water by recycling urea that ultimately influences whole body tissue δ15N values (Ambrose & DeNiro, 1986; Sealy, van der Merwe, Lee Thorp, & Lanham, 1987). Hobson, Alisauskas, and Clark (1993) also determined that birds that fast and undergo significant protein catabolism during incubation, like geese breeding at high

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latitudes, also experience an increase in body δ15N values. Knowledge of these sorts of physiological processes is necessary when using tissue δ15N values of migratory organisms to infer origins. The prevailing consensus is that researchers should strive to use the most parsimonious nitrogen isotope discrimination value associated with their specific organism of interest. A review of N isotopic discrimination across several taxa by Vanderklift and Ponsard (2003) identified mode of excretion and environment (marine, freshwater aquatic, and terrestrial) as important factors (see also Boecklen et al., 2011; Post, 2002). In their analysis, Caut, Angulo, and Courchamp (2009) provide a summary of δ15N discrimination factors that will prove useful and suggest that these factors are also dependent upon dietary or baseline δ15N values, but more research is needed to confirm mechanisms underlying this suggestion. A significant advance in the use of compound-specific isotope analyses (CSIAs) has been the identification of amino acids whose δ15N values largely reflect dietary source (i.e., show little change in δ15N with trophic level) compared to those that show strong trophic discrimination, the so-called trophic amino acids. For example, glutamate is a trophic amino acid compared to phenylalanine. Measuring the δ15N difference between these amino acids within the consumer can thus control any changes in baseline δ15N and trophic position. This phenomenon clearly helps resolve two of the primary limitations to using bulk tissue δ15N values to infer origins of migratory animals, the ambiguity related to an animal coming from a region of unknown baseline δ15N and unknown trophic position. It is possible then, to imagine a source amino acid (say phenylalanine) δ15N isoscape to assist with assignments. While it is possible to generate tissue δ15N isoscapes for the purposes of spatial assignment, the use of this isotope is limited and should be used with caution due to the many

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physiological and ecological factors that can influence tissue δ15N independent of location. These limitations may be partially addressed through compound-specific amino acid δ15N analyses which can inherently account for trophic position and baseline δ15N. In general, N isotopes are best considered as providing additional locational information due to biome characteristics and known land use practices in terrestrial systems. 4.2.3.2 Carbon Isotopes Unlike nitrogen and sulfur, carbon is present in all dietary macromolecules (protein, fat, and carbohydrates), hence δ13C measurements of consumer tissues reflect these various sources. The diverse sources of carbon contribute to variable diet-tissue δ13C discrimination factors compared to other light elements. However, in many cases, lipids in diets are transferred directly with little isotopic modification to lipids in the consumer. Carbohydrates are often burned directly for energy production, producing CO2 as the only carbon byproduct, and hence δ13C values in breath CO2 are used to trace origins of carbohydrates in diet. Unfortunately, we have little idea of the appropriate carbon isotopic discrimination factors that currently apply between dietary substrates and breath CO2 (McCue & Welch, 2016; Podlesak, McWilliams, & Hatch, 2005). Carbon isotope values of protein theoretically originate from all three dietary macromolecules, but is more likely associated with dietary proteins especially for carnivores. In general, we expect lower diet-tissue isotopic discrimination factors for δ13C than for δ15N. However, when using bulk tissues, researchers need to be aware of the significant intertissue differences in C isotope discrimination factors linking animals with isoscapes. For the most part, δ13C values in animal tissues are used to infer diet and biome information. The strong correspondence between δ13C values in primary production and

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photosynthetic pathway (C3, C4, and CAM) provides strong linkages to climate in terrestrial systems. In marine systems, algal growth rates influence food web δ13C values and are strongly linked to nutrient availability and sea-surface temperature (Chapter 6: Isotopic Tracking of Marine Animal Movement). Spatial information associated with food web δ13C values related to plant or primary productivity distributions form the basis for tracing animal origin and movement. A particularly useful development in generating expected plant or animal tissue δ13C isoscapes has been the modeling of expected relative distributions of C3 versus C4 plant ecozones (Still & Powell, 2010). These can be converted into spatially explicit δ13C predicted surfaces. Hobson, Van Wilgenburg, Wassenaar, and Larson (2012) applied a 1m C isotope discrimination factor between predicted plant tissue δ13C and herbivorous insects and another 1m C isotope discrimination value linking insects to feathers of insectivorous birds to produce a feather δ13C isoscape for Africa. Several sources of error are associated with continental patterns and like 15N, can be heavily influenced by anthropogenic factors such as agriculture (e.g., the extensive planting of C4 crops such as corn, sorghum, and millet), irrigation, and land use. Future δ13C isoscapes will involve year-specific agricultural crop layers for cases where migrant animals use crops such as those expected for migrant pest insects (Hobson et al., 2018). Recent advances in the use of compoundspecific δ13C analyses of plant and animal tissues opened new avenues for tracing animal movements. For example, plants, fungi, and bacteria have characteristic amino acid δ13C patterns because of unique pathways of amino acid synthesis (Larson & Hobson, 2009). Thus CSIA using δ13C analyses can be applied to infer patterns of dietary shifts of tissues synthesized at different times and geographical regions (Chapter 7: Amino Acid Isotope Analysis: A New Frontier in Studies of Animal Migration and Foraging Ecology).

4.2.3.3 Hydrogen and Oxygen As emphasized below and in Chapter 3, Isoscapes for Terrestrial Migration Research, hydrogen isotopes are particularly powerful for tracking migratory wildlife. However, this element presents challenges in terms of fully understanding how δ2H measurements of consumer tissue relate to hydrogen sources that, in most terrestrial systems, are driven by the global water cycle. Like carbon, hydrogen occurs in all three dietary macromolecules and so recognition of metabolic routing is important. As outlined in Chapter 2, Introduction to Conducting Stable Isotope Measurements for Animal Migration Studies, measurement of δ2H in the nonexchangeable fraction of hydrogen is challenging but within the consumer, a portion of the hydrogen in any tissue exchanges with body water, a component which is presumably more labile than dietary-derived hydrogen. Drinking water as well as diet thus constitutes a source of H in animals and this makes it difficult to derive linkages between precipitation δ2H and tissue δ2H that are universally applicable. Using a controlled laboratory study, Hobson et al. (1999) maintained quail (Coturnix japonica) on a single diet but exposed groups to drinking water of vastly different δ2H values. They found that H from drinking water accounted for about 20% of the total H in various tissues. Interestingly, this was the case for lipids with no exchangeable H bonds indicating that body water can exchange with H in precursor molecules involved in lipid synthesis. Because such details do not exist for most animal systems, overall H isotope discrimination factors are estimated using phenomenological approaches, as discussed below. Evidence suggests that most of the H isotope discrimination between environmental waters and animal tissues occurs at the incorporation of H from water into plant tissues with little subsequent trophic changes. The use of δ18O measurements to track wildlife remains rare because of technological constraints of routinely measuring oxygen isotopes

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in animal tissues. That situation has now changed due to online pyrolytic techniques and the development of keratin O isotope standards (Chapter 2: Introduction to Conducting Stable Isotope Measurements for Animal Migration Studies). Pekarsky et al. (2015) successfully used feather δ18O measurements to infer breeding origins of Eurasian Cranes (Grus grus) wintering in Israel. Moreover, that study clearly indicated how modeled feather δ18O isoscapes could be derived using satellite data. The tight coupling between δ18O and δ2H values in meteoric water provides opportunity to infer additional information related to climate, but that correlation between H and O isotopes breaks down in food webs involving animals, due to varying degrees based on factors affecting each isotope differently (Hobson & Koehler, 2015). Thus, in many cases, no additional information is gained from δ18O over δ2H measurements on the same tissue. As well, δ2H values typically span a much wider range than δ18O measurements in terrestrial food webs and so can potentially provide greater resolution with respect to source discrimination and an overall better signal-to-noise ratio. Oxygen occurs in proteins but not in lipids or carbohydrates. However, sources of oxygen include drinking water and air for metabolism and thus, like H, it is difficult to predict O isotopic discrimination factors associated with each contribution and “working values” will need to be derived largely from future examination of wild and captive animals.

4.3 MOVEMENTS INFERRED WITHOUT ISOSCAPES The strong link between stable isotope values in animal and plant tissues and biogeochemical processes have provided the basis for linking organisms to regions or biomes. Some of the earliest isotopic investigations revealed distinct differences between marine and

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terrestrial food webs with marine organisms having more positive δ13C, δ15N, δ34S, δ2H, and δ18O values compared to terrestrial counterparts (Hobson, 1999). As many migratory organisms use terrestrial and marine biomes throughout their annual cycles, these marine versus terrestrial isotopic differences become useful (e.g., Atkinson et al., 2005). Plant physiologists have also pioneered the use of stable isotope measurements to discern C3-, C4-, and CAM-based photosynthetic pathways using δ13C and δ2H measurements with clear implications for reconstructing animal diets and origins (Wolf & Martinez del Rio, 2000). Investigations into the effect of water-use efficiency mechanisms in C3 plants that generally leads to an enrichment of plant tissue 13C have also alluded to winter origins of migratory birds (Marra, Hobson, & Holmes, 1998; Bearhop, Furness, Hilton, Votier, & Waldron, 2003) and to the existence of carry over effects that can influence subsequent life history stages (Norris, Marra, Kyser, Sherry, & Ratcliffe, 2004). While most of these applications involve indirect spatial association through knowledge of animal life history and the biomes they use, these studies paved the way for more spatially explicit approaches to tracing animal movements and so a brief history is warranted. One of the earliest applications of stable isotope methods to investigate animal spatial movement was by Killingly (1980) who inferred the temperature of water during calcite formation of barnacles attached to the skin of California Gray Whales (Eschrichtius robustus) using δ18O measurements and by Killingly and Lutcavage (1983) who examined δ18O and δ13C measurements in barnacles on loggerhead turtles (Caretta caretta). That work has since been followed by studies on the inorganic fraction of otoliths in freshwater and marine fish to infer movements (e.g., Kennedy, Folt, Blum, & Chamberlain, 1997; Meyer-Rochow, Cook, & Hendy, 1992). Other examples of using marine

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4. APPLICATION OF ISOTOPIC METHODS TO TRACKING ANIMAL MOVEMENTS

isoscapes to infer spatial movements of marine mammals are by isotopic analyses of the baleen plates of the western Arctic population of bowhead whales (Balaena mysticetus) migrating annually between the Beaufort and Bering seas (Schell, Saupe, & Haubenstock, 1989) and southern right whales (Eubalaena australis) that annually cross the Southern ocean convergence, a zone of dramatic changes in food web δ13C and δ15N (Best & Schell, 1996). Trueman et al. (Chapter 6: Isotopic Tracking of Marine Animal Movement) provide more information on the derivation and use of marine isoscapes to infer movements of fish and marine mammals. Within terrestrial and freshwater habitats, there clearly is substantial isotopic variability that can be used to examine movements of fish. Hesslein, Capel, Fox, and Hallard (1991) used δ13C, δ15N, and δ34S measurements of muscle in broad whitefish (Coregonus nasus) and lake whitefish (Coregonus clupeaformis) in two freshwater regions of the Mackenzie Delta in Northern Canada to infer their movements. The movement of animals between marine, estuarine, and terrestrial or freshwater habitats holds great potential for inferring their past habitat use and potential migratory origins. Tietje and Teer (1988) were among the first to use stable isotope methods to investigate how wintering Northern Shoveler (Anas clypeata) ducks use coastal and inland freshwater wetlands and were able to demonstrate sedentary behavior among late wintering individuals. Other studies have primarily used δ13C measurements to infer movement of piscivorous birds between marine and freshwater habitats (Bearhop et al., 1999; Mizutani, Fukuda, Kabaya, & Wada, 1990). Hobson, Blight, and Arcese (2015) used a multiisotope approach to investigate use of terrestrial, marine, and freshwater resources by coastal wintering gulls near an urban center and the use of agricultural land by coastal shorebirds (Hobson, Slater, Lank, Milner, & Gardiner, 2013).

Migratory movements of fish with an anadromous life stage present an isotopic opportunity and, have the added advantage of carrying an isotopic record in their otoliths and scales (Nelson, Northcote, & Hendy, 1989; Trueman & Moore, 2007) and soft tissues (Hobson et al., 2007). Kennedy et al. (1997) and Harrington, Kennedy, Chamberlain, Blum, and Folt (1998) demonstrated how stable isotopes of several elements can be used on the organic and inorganic fractions of otoliths to identify natal streams of Atlantic salmon (Salmo salar) intercepted as adults at sea. Essentially, the suite of δ13C, δ15N, and δ87Sr measurements form unique combinations of values reflecting the geological substrate and land-use practices surrounding drainage basins of key salmon-producing streams (Barnett-Johnson et al., 2008, reviewed by Walther & Limburg, 2012). Recently, there has been interest in using freshwater fish tissue δ2H values because stream and river H inputs to lake systems may have very different water δ2H values (Doucett, Marks, Blinn, Caron, & Hungate, 2007). Thus freshwater systems have great potential for a multiisotope approach to trace migrations and movements of aquatic species. They also have the advantage of being reasonably tightly constrained spatially and it should be possible to literally create multiisotopic basemaps of the major aquatic space used by migrant fish (Soto, Hobson, & Wassenaar, 2016). In terrestrial systems, some of the earliest applications of isotopic measurements used for tracking origins of animals were conducted in Africa. Two simultaneous yet independent studies used stable isotope measurements of elephant (Loxodonta africana) ivory and bone collagen to infer origins of that material as a forensic tool to counter the illegal ivory trade (Van der Merwe et al., 1990; Vogel et al., 1990). Elephants feeding primarily on grasses sample a C4 food web and so have more positive δ13C values compared to those feeding in

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4.3 MOVEMENTS INFERRED WITHOUT ISOSCAPES

woodlands on C3 browse. Elephants feeding in more arid areas may also have higher δ15N values than those in more mesic habitats (Heaton, 1987). Combined with assays of Pb and Sr isotopes, these studies showed strong segregation among several African elephant populations and underlined the forensic utility of stable isotopes to infer origins of several taxa. Unfortunately, some of the early enthusiasm was later tempered by the observation of strong year-to-year variations in food web δ15N values within the Amboseli National Park presumably due to climatic variation (Koch et al., 1995). This illustrates the need to know the natural range of variation in stable isotope patterns spatially and temporally when evaluating the accuracy of the technique when inferring animal origins. Fortunately, many terrestrial systems are less erratic isotopically and show consistent isotopic patterns over decadal and longer time frames. This is especially the case with the use of δ13C measurements to track the use by animals of C3, C4, and CAM food webs. An interesting application of δ13C measurements to investigate mechanisms affecting the phenology of animal migration was that of Flemming, Nunez, and Sternberg (1993) who showed that the nectarivorous bat Leptonycteris curasoae switched from C3 flowering plants during the winter to CAM flowering columnar cacti as it migrated north in the spring. The bat tissue isotopic data revealed how the species has adapted to the phenology of CAM “nectar corridors” during northward migration. Other studies have exploited the strong C4 signal of agricultural corn to infer the origins of migratory herbivorous birds (Henaux, Powell, Vrtiska, & Hobson, 2012) and their relative dependence on C3- and C4-based food webs (Wassenaar & Hobson, 2000). However, δ13C isoscapes in North America or other areas with intense agricultural production can have a mix of C3 and C4 plants and so will be complicated to model.

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Unlike most Nearctic migratory birds, Palearctic species typically replace flight feathers on their wintering ground in Africa, so it was possible to infer aspects of the wintering habitats using isotopic analyses of these feathers. Feathers grown in mesic habitats of subSaharan West Africa are expected to have lower δ13C values than those grown in Central, East, or South Africa and that was consistent with analyses performed by Bensch, ˚ kesson (2006) on two subspeBengtsson, and A cies of flycatcher breeding in Sweden. Following the example of Møller and Hobson (2004) who examined African grown feathers of barn swallows breeding in Europe, Schmaltz, Loonstra, Wymenga, Hobson, and Piersma (2017) used blood and feather δ13C, δ15N, and δ2H values to infer likely origins of Ruffs (Philomachus pugnax) arriving in Europe during spring migration. In addition to a multivariate analysis involving three isotopes, the bivariate plot they produced of δ13C versus δ15N established quadrats inferring (1) birds wintering in Europe based on high δ15N (manure-based) agriculture and low δ13C (C3) plants; (2) birds wintering in sub-Saharan Africa and associated with livestock (high δ15N) and C4 plants (high δ13C); (3) birds from sub-Saharan Africa associated with C4 irrigated agriculture (high δ13C and low δ15N) and birds molting in unknown areas but associated with low δ13C and low δ15N (mesic or irrigated C3 biomes possibly associated with rice agriculture). The analysis of the multiisotope structure of breeding populations of animals can also be used as a means of detecting immigrants into those populations even when the isotopic structure of the landscape is unknown. For example, Hobson, Wassenaar, and Bayne (2004) used this approach to investigate minimum estimates of dispersal into breeding populations of American Redstarts and Ovenbirds (Seiurus aurocapillus), using δ2H measurements of feathers. The challenge is to

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derive statistically defensible criteria for distinguishing among local and immigrant individuals and the associated risk of making an error in assignment. The power of isotopic inference in assigning tissues of animals and plants to regions or biomes depends to a large degree on the life history of the organism in question and the confidence one can associate with isotopic patterns in nature. A more powerful approach is the use of tissue-specific isoscapes that provide predictive surfaces (isoscapes) of expected tissue isotope values.

4.4 USING ISOSCAPES The first comprehensive application of δ2H measurements in the study of migratory animals was an investigation of the isotopic structure of populations of Monarch butterflies (Danaus plexippus) wintering in Mexico. The eastern population of the Monarch Butterfly in North America overwinter in roost sites in the high-altitude Oyamel Fir (Abies religiosa) forests of central Michoacan and Mexico states. In spring, only gravid females migrate north, reaching Texas, USA, where they lay eggs on milkweed (Asclepias species) plants. The new generation emerging travels further north to repeat the process at higher latitudes. Finally, in one of the most spectacular migrations of any animal, in late summer monarchs 46 generations removed from those ancestors that migrated northward from Mexico the previous spring then return to the same roost sites that they have never seen before. Tracking origins where the overwintering butterflies were produced has emerged as a central question in the conservation of Monarchs due to their declining numbers and the real possibility their migratory phenomenon may go extinct. Only by identifying the key production zones, we can target conservation efforts effectively on the breeding grounds.

Hobson, Wassenaar, and Taylor (1999) first created an isotopic basemap corresponding to butterflies produced throughout their breeding range during the summer of 1996. An isotopic basemap is composed of isotope measurements made on individuals from known locations that spans the entire breeding range. This feat was accomplished through the aid of the nonprofit MonarchWatch organization (monarchwatch.org), who were able to solicit volunteers and educators from 86 locations across the monarch breeding range to successfully raise 412 butterflies on milkweed grown locally. Only milkweed watered by rainfall was used. From that sample, butterflies from 33 sites were selected for δ2H and δ13C analyses of wing tissue performed to produce a year-specific basemap depicting isotopic patterns for C and H isotopes. In addition to the wild-reared group of monarchs, the relationship between δ2H and δ13C of milkweed tissue and chitin in wings and the water used to raise milkweed was investigated under controlled laboratory conditions using three batches of known δ2H water. Those captive studies showed extremely tight (r2 5 0.99) relationships, demonstrating that insect wing chitin δ2H is derived exclusively from water available to plants with most of the isotopic discrimination occurring between water and plants (see also Ostrom, Colunga-Garcia, & Gage, 1997). However, in their investigation of wild monarchs, Wassenaar and Hobson (1998) applied the derived basemap based on the “outdoor” sample to portray origins of monarchs who were produced during 1996 and later collected from all known winter roost sites in Mexico that winter (i.e., 199697). The authors reasoned that the calibration based on the outdoor monarchs from known locations would better encompass natural isotopic variation. That approach resulted in the insight that the winter roost sites were panmictic, made up of butterflies from all over the breeding range, and

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most importantly, revealed that half the monarch population was produced largely in Kansas, Nebraska, Iowa, Missouri, Wisconsin, Illinois, Michigan, Indiana, and Ohio corresponding to the corn, soybean, and dairy producing region of the Midwest USA. Thus while conservation of this species was previously focused almost entirely on the precarious winter roosts in Mexico, these isotope studies pointed to the possibility that prime monarch breeding habitat was concentrated in areas of intense agricultural production in the United States where milkweed was controlled and where genetically modified corn was being used that produced BtK, a bacterium that targets Lepidoptera (Losey, Rayor, & Carter, 1999). Since these landmark studies, stable isotope measurements have been used to infer (1) patterns of monarch spring recolonization in eastern North America (Flockhart et al., 2013; Miller, Wassenaar, Hobson, & Norris, 2012), (2) the origins of wintering individuals in western North America (Yang, Ostrovsky, Rogers, & Welker, 2016), (3) the effects of natal origin on parasite loads (Altizer, Hobson, Davis, De Roode, & Wassenaar, 2015), (4) the role of wing coloration in flight distance (Hanley, Miller, Flockhart, & Norris, 2013), and (5) general conservation concerns related to areas of high productivity (Flockhart, Brower, et al., 2017; Flockhart, Dabydeen, et al., 2017). An interesting aspect of the behavior of δ2H is that deuterium in precipitation tends to rain out more at lower elevations than at higher elevations. This is a well-known phenomenon that results in an altitudinal “depletion” in 2H from 21m to 24m per 100 m rise in elevation, depending on the gradient and temperature (Clark & Fritz, 1997). Similarly, the demands of plant adaptations to harsher growing conditions at higher altitudes tend to result in plants with higher δ13C values at higher elevations. As there are several species that perform altitudinal migrations, especially in the tropics, a

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study was conducted to see if tissues grown along an altitudinal gradient reflected such patterns. Hobson et al. (2003) examined δ2H and δ13C values of feathers of hummingbirds inhabiting the Ecuadorean Andes and found good agreement between actual and predicted feather δ2H based entirely on a global model (Chapter 3: Isoscapes for Terrestrial Migration Research). As expected, feather δ13C values increased with altitude. Thus, for any given species, it may be possible to estimate approximate elevations at which feathers, and other tissues were grown. By examining different tissues with different windows of isotopic integration, the possibility exists to infer previous altitudinal movements.

4.4.1 Assignment to Bins The creation of predictive, tissue-specific, isoscapes allows for a variety of approaches to inferring past origins and movements of animals to “place them on the map.” This topic is elaborated in Chapter 6, Isotopic Tracking of Marine Animal Movement. To date, researchers have relied on assignment of individuals or populations to arbitrary spatial bins or regions of interest, or have adopted a more spatially explicit assignment approach. Both approaches rely on the ability to link individual tissues δ-values to an expected value at a given scale (ranging from thousands of km2 in the case of bins to hundreds of m2 in the case of pixels). The success of this approach clearly rests on how well modeled isoscapes represent reality. Dichotomous assignment to bins can be useful, especially if those bins represent management units or regions relevant to a question. For example, Norris et al. (2006) wanted to know the degree of migratory connectivity between breeding and wintering grounds of “populations” of the Neotropical migrant, American redstart (Setophaga ruticilla). Those authors looked at 12 wintering populations and assigned

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individuals to one of the five breeding origin bins using likelihood assignment. Each wintering population could then be categorized as representing various proportions of breeding ground origins and thereby reveal patterns of connectivity. In this case, western breeding birds clearly wintered in the western portion of their nonbreeding range and eastern birds largely in the Caribbean. Flockhart, Brower, et al. (2017) used this approach to assign monarch butterflies from the winter roost sites in Mexico to one of the six breeding regions in the United States and Canada. That approach was taken because there was considerable interest in the role of the American Midwest agricultural region to monarch production at continental scales. Ashley, Hobson, Van Wilgenburg, North, and Petrie (2010) used a hybrid approach by assigning harvested American Black Ducks (Anas rubripes) to origins in a spatially explicit way but within three distinct flyway bins (Eastern, Central, and Western).

Potential problems with the “assignment to bins” approach involve how well researchers can estimate the expected mean and variance in isotope values associated with regions. Derivation of expected isotope values associated with bins is usually accomplished by sampling isoscape points within bins and the degree to which such values are useful will depend on the nature and robustness of the underlying isoscape and the sample coverage. Problems also arise with assignments close to sharp bin boundaries.

4.4.2 Spatially Explicit Assignments Several applications using δ2H measurements have involved migratory birds in North America that had a strong conservation motivation (Figs. 4.3 and 4.4). These studies have relied on derived calibration algorithms to link individuals and populations to tissue isoscapes (reviewed in Hobson, 2008; Table 4.1). Unfortunately, there are exceptionally few

FIGURE 4.3 Migratory connectivity determined using stable isotope analyses of feathers based on the results of (A) Rubenstein et al. (2002) for the Black-throated Blue Warbler (Setophaga caerulescens) and (B) the leapfrog migration pattern of the Wilson’s Warbler (Wilsonia pusilla) discovered by Kelly, Atudorei, Sharp, and Finch (2002).

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FIGURE 4.4 Examples of spatially explicit assignment to molt origins of Golden-winged Warblers (Vermivora chrysoptera) sampled at two sites on their wintering grounds and showing strong differences in migratory connectivity. Assignment was based on δ2H measurements of feathers and subsequent assignment to a feather δ2H isoscape for North America using probabilistic assignment techniques discussed in Chapter 8, Design and Analysis for Isotope-Based Studies of Migratory Animals and Chapter 9, Isoscape Computation and Inference of Spatial Origins With Mixed Models Using the R package IsoriX. Figure legends depict the number of individuals assigned to the same pixel (see Hobson et al., 2016).

studies that have attempted to derive calibration algorithms on any continent. In North America, Hobson, Van Wilgenburg, Wassenaar, and Larson (2012) examined songbird feathers from an extensive (Monitoring Avian Productivity and Survivorship: MAPS) collection housed by the Center for Tropical research at the University of California at Los Angeles (UCLA). That study was based on 544 feathers from 40 species representing 140 known locations. In addition to choosing feathers from several guilds and across a large latitudinal gradient, the researchers specified that feathers be taken, where possible, from individuals that were philopatric to sampling site as indicated by band returns. That study showed significant within-population variance but the model accounted for B80% of the variance and suggested that foraging guild (ground, canopy, and shrub/aerial) and migratory strategy

(resident, short distance, and Neotropical) influenced the calibration. Lott and Smith (2006) provided a feather δ2H isoscape and calibration algorithm for North American raptorial birds and Cryan, Bogan, Rye, Landis, and Kester (2004), Cryan, Stricker, and Wunder (2014), and Popa-Lisseanu, So¨rgel, Luckner, Wassenaar, and Iba´n˜ez (2012) provided the first δ2H isoscapes for bat hair. Calibration algorithms for insects have been recently summarized by Hobson, Doward, Kardynal, and McNeil (2018). It is important that we increase our understanding of the isotopic variance to be expected for precipitation-based isoscapes across taxa and across geography despite the difficulty in acquiring and sampling known-origin tissues across large spatial gradients. Almost nothing is known about appropriate calibrations for Africa where millions of Palearctic-Afrotropical

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TABLE 4.1 Relationship Between Stable Hydrogen Isotope Ratios of Environmental Waters (δ2Hp) and the δ2H Values of Animal Tissues Assumed to Have Been Produced at Known Sites (See Hobson, 2008 for Additional Examples) Speciesa

Calibrationb

Source

BIRDS δ2H 5 227.8 1 0.95δ2Hp

Clark, Hobson, and Wassenaar (2006)

δ H 5 257 1 0.84δ Hp

Hebert and Wassenaar (2005)

Songbirds (NGF)

δ H 5 217.6 1 0.95δ Hp

Hobson, Møller, et al. (2012)

Songbirds (NO)

δ H 5 227.1 1 0.95δ Hp

Hobson, Møller, et al. (2012)

Songbirds (SDGF)

δ H 5 223.0 1 0.95δ Hp

Hobson, Møller, et al. (2012)

Songbirds (SDO)

δ H 5 236.9 1 0.95δ Hp

Hobson, Møller, et al. (2012)

Songbirds (RGF)

δ H 5 227.9 1 0.95δ Hp

Hobson, Møller, et al. (2012)

Songbirds (RO)

δ H 5 211.2 1 0.95δ Hp

Hobson, Møller, et al. (2012)

Raptors

δ H 5 25.6 1 0.91δ Hp

Lott and Smith (2006)

δ2H 5 225 1 0.8δ2Hp

Cryan et al. (2004)

δ H 5 242.6 1 0.73δ Hp

Cryan et al. (2014)

δ H 5 216.8 1 1.07δ Hp

Popa-Lisseanu et al. (2012)

Monarch butterfly wild

δ2H 5 279 1 0.62δ2Hp

Hobson et al. (1999)

Monarch butterfly lab

δ H 5 253 1 0.5δ Hp

Hobson et al. (1999)

Dragonfly spp

δ2H 5 242.5 1 0.91δ2Hp

Hobson, Van Wilgenburg, Wassenaar, and Larson (2012)

Beetle spp

δ2H 5 33.2 1 1.6δ2Hp

Gro¨cke, Schimmelmann, Elias, and Miller (2006)

δ H 5 34.7 1 1.4δ Hp

Gro¨cke et al. (2006)

Hoverfly

δ H 5 225.2 1 1.04δ Hp

Quin et al. (2011)

True army worm

δ H 5 295 1 0.42δ Hp

Hobson et al. (2018)

Waterfowl

2

2

2

2

2

2

2

2

2

2

2

2

2

2

2

2

C

BATS

2

2

2

2

INSECTS

2

2

2

2

2 2

2

2

a

NGF, Neotropical migrant ground forager; NO, Neotropical migrant other; RGF, resident ground forager; RO, resident other; SDGF, short-distance migrant ground forager; SDO, short-distance migrant other. b Note that δ2Hp can refer to (1) amount-weighted mean growing-season precipitation, (2) amount-weighted mean annual precipitation, or (3) laboratory waters. c See Chapter 5, Tracking of Movements of Terrestrial Mammals Using Stable Isotopes, for a more complete list.

migrant birds breeding in Europe molt their feathers in winter. The hydrogen isotope basemap for Africa shows dramatic changes seasonally. An interesting and potentially very useful feature is the more depleted values in the

southern part of the African continent and the extremely enriched region in the northeast, centered on Sudan and Ethiopia. In an investigation into potential wintering sites of the endangered aquatic warbler, Pain et al. (2004)

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did not find δ2H measurements to be particularly useful and instead advocated the use of δ15N and δ13C measurements to better define wintering areas in Africa. On the other hand, Yohannes, Hobson, Pearson, Wassenaar, and Biebach (2005), Yohannes, Hobson, and Pearson (2007) investigated δ2H together with δ15N and δ13C measurements in feathers of several migrant passerines moving through East Africa where some of them stop to molt en route to more southern wintering areas. A recent analysis of feathers from museum collections revealed a generally poor correlation with expected precipitation δ2H (Gutie´rrez-Expo´sito, Ramı´rez, Afa´n, Forero, & Hobson, 2015). Most approaches to date propagate known error associated with derived calibrations linking mean annual or growing season precipitation with animal tissues using the average of the (tissue) residuals of the calibration. An important component of deriving calibration relationships linking animal tissues with underlying isoscapes is that a measure of sitespecific isotopic variance in animal tissues can be estimated from the residuals of such regressions. Hobson, Van Wilgenburg, Wassenaar, and Larson (2012), Hobson, Van Wilgenburg, Faaborg, et al. (2014) documented the standard deviations of the residuals found for their calibration work linking feather δ2H values with expected mean growing season precipitation δ2H (δ2Hp). The overall model indicated a residual SD of B13m. Specific migratory and foraging guild residual values varied from B18m in short-distance migrant ground foragers to B10m for nonground foraging Neotropical migrants. Importantly, these estimates of variance can be propagated in assignment of individuals to origin (Chapter 8: Design and Analysis for Isotope-Based Studies of Migratory Animals). That approach provides a realistic estimate of error, but a better approach will be to use spatially explicit variance associated with both the isotope values of tissues grown at a site (i.e., within population)

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and the underlying variance associated with the precipitation surface. This is because we know that such variance changes across isoscapes. Fortunately, variance surfaces for amount weighted, mean annual or growing season δ2H and δ18O precipitation are now available (Terzer, Wassenaar, Aragua´s-Aragua´s, & Aggarwal, 2013) and analytical refinements for assignment purposes are expected (Chapter 8: Design and Analysis for Isotope-Based Studies of Migratory Animals). Regardless, we are quickly approaching the limits of refinement in our approach to using stable isotopes to assign individuals and populations to origins using a single (primarily δ2H) isotope. It should also be recognized that conclusions derived using the isotope approach have been inherently conservative, examining continent wide patterns of migratory connectivity (Hobson, Van Wilgenburg, Faaborg, et al., 2014), origins of harvested populations, derivation of migratory divides, and so on. More spatially sensitive questions regarding animal origins will require greater sophistication and almost certainly will require the addition of additional isotopic and nonisotopic information, and this will be an area of great future interest.

4.4.3 Incorporating Multiple Sources of Information As reviewed in Chapter 1, Animal Migration: A Context for Using New Techniques and Approaches, the tools for investigating animal origins and movements has never been so diverse or powerful. It helps to consider isotopic applications as part of a much larger (forensic) initiative. Chapter 8, Design and Analysis for Isotope-Based Studies of Migratory Animals, outlines in detail aspects of sample design and analysis. For example, several researchers have used multiple isotopes (δ2H, δ34S, δ13C, δ15N, and δ87Sr) in a multivariate approach to examine origins

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of migratory populations (Caccamise, Reed, Casteli, Wainright, & Nichols, 2000; Hebert & Wassenaar, 2005; Yohannes et al., 2007), but adding more isotopes is not necessarily a guarantee of better spatial resolution. As discussed, the formal incorporation of more than one isotope into migratory assignments has rarely been used. To date, this has been accomplished primarily via the use of multivariate normal distributions whereby more than one (assumed largely orthogonal) isoscape has been applied. In addition to the familiar precipitation isoscapes involving primarily δ2H measurements, other isoscapes include those based on modeled plant C3 versus C4 δ13C distributions (Still & Powell, 2010) and on soil δ15N predictions (Craine et al., 2009). Hobson, Van Wilgenburg, Wassenaar, and Larson (2012) used that approach to create expected δ2H, δ13C, and δ15N feather isoscapes and proceeded to query surfaces simultaneously to identify distinct isotopic clusters to assign European breeding birds to potential origins in Africa. That approach initially involved binning individuals to clusters (see also Lopez-Calderon et al., 2017) but later, spatially explicit assignments were used (Hobson, Van Wilgenburg, Wesolowski, et al., 2014; Veen et al., 2014). The same multiisotope approach was used to assign migratory barn swallows (Hirundo rustica) to molt origins in South America (Hobson & Kardynal, 2016). The use of prior information in Bayesian assignment models underscores one of the key advantages in this approach. Priors used in assigning individuals include expected population density distributions on the breeding grounds (Royle & Rubenstein, 2004) and the use of movement recovery vectors to constrain potential origins or destinations of migrants (Gunnarsson et al., 2012; Van Wilgenburg & Hobson, 2011). However, such applications are not necessarily straightforward, and the Bayesian prior can skew migratory origins

inappropriately (Hobson, Van Wilgenburg, Faaborg, et al., 2014; Kery & Schaub, 2012). A recent area of great promise is combining spatial structure associated with genetic markers (i.e., genescapes) and stable isotope markers (Boulet, Gibbs, & Hobson, 2006; Clegg, Kelly, Kimura, & Smith, 2003; Kelly, Ruegg, & Smith, 2005; Paxton, Yau, Moore, & Irwin, 2013). Chabot, Hobson, Van Wilgenburg, & McQuat, 2012 and Rundell et al. (2013) approached this formally by integrating genetic admixture coefficients as prior information to increase the power of isotopic assignment using Bayesianbased models. The efficacy of this approach will depend on the species in question and how well the genescape has been described for a species. Conveniently, material for stable isotope and genetic analyses is often available from the same sample (e.g., feather tip vs base). Ruegg et al. (2017) presented a formal means of combining stable isotope, genetics and habitat suitability models for assignment purposes. Rushing, Ryder, Saracco, and Marra (2014) demonstrated for Wood Thrush (Hylocichla mustelina) how combining morphometric and isotope data in assignment models can significantly improve assignment accuracy. Other means of constraining origins using stable isotope approaches involve the obvious step of delimiting potential origins by known breeding and wintering distributions before performing assignments. In addition, some stable isotopes provide important threshold information to limit samples to only those regions where the precipitation isoscape is valid (namely, terrestrial systems). Here, the use of δ15N, δ13C, and δ34S measurements can potentially reveal marine inputs to diets which would deter the use of δ2H or δ18O to assign individuals to terrestrial precipitation isoscapes (Lott, Meehan, & Heath, 2003; Table 4.1, and Fig. 4.5, see also Hobson & Kardynal, 2016). Other authors have used this threshold approach to separate origins of birds also using agricultural versus more natural biomes

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4.5 CHALLENGES

140

δDf−p (per mil)

100

Coastal bird eaters

60 20 Inland bird eaters

–20 –60

Coastal generalists

Inland generalists

–100 –15

–10

–5

0

5

10

15

20

δ34S (per mil)

FIGURE 4.5 The relationship between the difference between feather δ2H and predicted precipitation δ2H and feather δ34S for nine species of raptors breeding in North America (from Lott et al., 2003). This figure illustrates the way in which birds having access to marine protein can be distinguished by their high δ2H and δ34S values.

(Schmaltz et al., 2017; Yerkes, Hobson, Wassenaar, Macleod, & Coluccy, 2008).

4.5 CHALLENGES The development of isotopic techniques to track animal movement represents a huge breakthrough in the way we approach a suite of practical and theoretical issues associated with the ecology and conservation of migratory species. However, despite excellent advances, there are significant challenges that must be addressed. Most of these apply to the use of δ2H measurements and related isoscapes. As noted in Chapter 2, Introduction to Conducting Stable Isotope Measurements for Animal Migration Studies, the adoption of robust measurement protocols for δ2H (and to some extent δ18O) in animal tissues are paramount and practitioners must adopt

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standardized analytical approaches. Beyond issues related to measurement error, there is the ongoing issue of the appropriate precipitation to tissue calibration relationship to use to create spatially explicit isoscapes. We now realize that such calibration algorithms are sensitive to factors related to both animal physiology, diet, and ecological guild in addition to the abiotic factors driving the underlying elemental isoscapes (Hobson, Van Wilgenburg, Wassenaar, & Larson, 2012). Hydrogen is an element that will exchange with weak OH or NH bonds and this can take place with drinking water and overall body water (Hobson et al., 1999). Body δ2H values can increase from heat stress (McKechnie, Wolf, & Martinez del Rio, 2004) and presumably as a function of work or high metabolism that results in increased body evapotranspiration. Powell and Hobson (2006) found that Wood Thrush (H. mustelina) growing feathers in Georgia had higher feather δ2H values than expected from the feather δ2H isoscape, and speculated that heat stress during molt may have been a factor. While we assume that trophic 2H discrimination effects are minor and that most of the precipitation to tissue discrimination occurs between precipitation and plants, this requires further investigation (Birchall, O’Connel, Heaton, & Hedges, 2005). Notably, it is possible that feathers of birds grown in the nest differ from those of the adults feeding them due to differences in metabolism, drinking water, thermal regime, feather growth rate, and diet (Hache´, Hobson, Bayne, Van Wilgenburg, & Villard, 2014; Langin et al., 2007; Studds et al., 2012). Another concern for users of the hydrogen isotope base maps for the various continents is the variability in the IAEA GNIP dataset for any given year where organisms are sampled (Chapter 3: Isoscapes for Terrestrial Migration Research, Vander Zanden et al., 2015). As demonstrated with the monarch study, the only foolproof way to avoid impact of

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long-term variance is to create a base map for the year of interest, but this is beyond the scope of most researchers for most organisms. Second, if a study site is close to one of the IAEA GNIP sampling stations, then it may be possible for the researcher to potentially derive a year-specific tissue value for the site of interest but this would only provide local information most appropriate for discerning local from immigrant individuals (Hobson, 2005). More realistically, if researchers can obtain animal tissues from known individuals grown in the year of interest that could act as a reasonable proxy for local integrated isotope values (Van Wilgenburg, Hobson, Brewster, & Welker, 2012). Regardless, the effect of sampling year on the accuracy of assignment will vary spatially and by the degree to which climate proxies such as ENSO operate in any given system or by the degree to which food webs are supported by episodic (e.g., monsoons) versus multiple precipitation events (Ehleringer, Phillips, Schuster, & Sandquist, 1991; Rozanski, Araguas-Araguas, & Gonfiantini, 1993; Villacis, Vimeux & Taupin, 2008). Our general poor understanding of which rainfall matters in food web H flow persists. The good relationship obtained between feather δ2H and mean annual growing season δ2H in North America (Hobson, Møller, et al., 2012; Hobson, Van Wilgenburg, Wassenaar, & Larson, 2012; Hobson, Van Wilgenburg, Wassenaar, Powell, et al., 2012; Hobson & Wassenaar, 1997) was for forest birds distributed through the central region of the continent. Closed-canopy forest with shallow root systems may well integrate food web δ2H available to birds and other animals over such long periods. However, is this the case for more pulsed ecosystems like grasslands or deserts? In other riparian systems, snowmelt may have the greatest influence on local food web δ2H. In other systems where animals may be influenced by aquatic emergent insects, tissues grown later in the season may differ from those grown earlier depending

on the extent of evapotranspiration from waterbodies. However, waterfowl feather δ2H values follow closely the expected growing-season average value for at least the temperate region of North America (Clark et al., 2006), but the potential for regional departures in shallow wetland systems requires careful consideration (Coulton, Clark, Hobson, Wassenaar, & Hebert, 2009). The early years of development for the assignment of animals to origins using stable isotopes revealed problem areas. For birds, much attention focused on applications involving shorebirds (Farmer, Cade, & TorresDowdall, 2008; Rocque, Ben-David, Barry, & Winker, 2006) and raptors (Smith et al., 2009). Apart from issues involving fundamental misunderstanding of isotopic applications to tracing bird origins (Larson & Hobson, 2009) shorebirds in general can be problematic because the origin and period of molt in adults is often poorly known on and off the breeding grounds. Moreover, this group consists of birds that use a vast array of habitats during their breeding, migration, and wintering life stages. These habitats range from terrestrial upland, freshwater, brackish, and marine and so represent a formidable array of isotopic endpoints. Several species also move between temperate regions across hemispheres and this can lead to nondiagnostic feather δ2H values. In the case of raptors, apart from early issues which dealt with either methodology or a lack of understanding (Wunder et al., 2009), evidence suggests that assigning adult raptors to feather isoscapes remains particularly challenging. For birds, molt patterns are reasonably well known for most species. However, stable isotope measurements themselves have provided important qualifiers. The molt of flight feathers of northern populations of the loggerhead shrike (Lanius ludovicianus) are essentially bimodal with inner primaries, secondaries, and tail feathers usually being molted on the

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4.6 SUMMARY

breeding grounds but other feathers being grown on the wintering grounds following a suspension in molt during migration (Chabot, Hobson, Craig, & Lougheed, 2017; Perez & Hobson, 2007). Other birds undergo prealternate molt of some body feathers on the wintering grounds prior to migration allowing us to investigate aspects of winter origins or habitat use (Mazerolle & Hobson, 2005; Mehl, Alisauskas, Hobson, & Kellett, 2004). Unfortunately, information on the reliability or extent of prealternate molt or on the extent of delayed molt in migrating birds is often not available (Hobson, Brua, Hohman, & Wassenaar, 2000). Another alternative is to use claws that are continuously growing. Birds captured soon after their arrival on the breeding grounds should have claws that have retained information from the wintering grounds (Bearhop, Hilton, Votier, & Waldron, 2004; Mazerolle & Hobson, 2005). While we need more controlled studies to establish growth rates of claws for a variety of species, contrasting stable isotope values of claws against a metabolically active tissue like blood can in fact provide insight into periods where these tissues “agree” isotopically.

4.6 SUMMARY This chapter suggested that situations where the three principles needed for successful isotopic tracking of migratory animals are met will be rare. The degree to which researchers are successful in applying isotopic methods will depend on the organism of interest, its geographical range, and ecophysiology. Applications also fundamentally depend on how well we know the nature and behavior of the appropriate isoscapes. The most elegant applications will usually be situations where alternative isoscapes are different and species experience simple isotopically dichotomous situations during their travels. Here, the longstanding success in using stable carbon isotope

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analyses to delineate C3 versus C4 or CAM food webs or the use of stable hydrogen isotope analyses to further separate C4 and CAM pathways provide distinct advantages. Terrestrial organisms that also spend part of their lives in marine or estuarine situations lend themselves to isotopic tracking using several elements. Altitudinal migrants constrained by latitude and longitude also represent a useful application of δ2H and δ18O measurements providing the movement represents at least several hundred meters. We will have more trouble in cases where underlying isotopic gradients are less distinct or where alternative origins overlap isotopically. The application of deuterium measurements in animal tissues to place them on continental isoscapes undoubtedly has provided the single greatest impact in the field of isotopic tracking. Again, the success of the H isotope approach will depend very much on which part of the isoscape we are dealing with. Distinguishing between Arctic and prairie origins of migratory birds in North America or between those from Scandinavia or Spain in Europe will be relatively straightforward. We are faced with more of a challenge in distinguishing between birds or other animals originating across latitudinal bands on both continents or from regions that are more spatially restricted (e.g., Szymanski, Afton, & Hobson, 2006; Coulton et al., 2009). So, while this chapter has shown that the isotope approach has provided an exciting new tool to researchers and conservationists, it is not a “silver bullet” to be applied without full recognition of the inherent limitations. How then might the field proceed from here? We now realize that the application of a single precipitation to tissue δ2H calibration algorithm across diverse species or particular geographic regions will inherently involve error, hence a sensitivity analysis should be part of the approach in future studies (Hobson, Van Wilgenburg, Wassenaar, Moore, & Farrington, 2007). In addition, we should realize the risks

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in placing all of our eggs in one isotopic basket (i.e., explore complimentary tools). This chapter has dealt primarily with avian applications, the next chapter focuses on terrestrial mammals followed by a chapter on tracking marine animals. Chapter 7, Amino Acid Isotope Analysis: A New Frontier in Studies of Animal Migration and Foraging Ecology, provides an overview of the intriguing developments now taking place using compoundspecific methods and Chapter 8, Design and Analysis for Isotope-Based Studies of Migratory Animals, deals with the important and dynamic area of study design and statistical assignment using stable isotope and other data. Chapter 9, Isoscape Computation and Inference of Spatial Origins With Mixed Models Using the R package IsoriX, presents one of the several software packages for assignment currently available. By this point, the reader should be encouraged by the breadth of past isotopic applications to tracking migratory animals and realize the tremendous scope for future developments. The need for caution and consideration of the numerous assumptions involved are sobering (this chapter and Chapter 8: Design and Analysis for Isotope-Based Studies of Migratory Animals). Nonetheless, more and more we are coming to terms with the nature of isotopic variance in the natural world and Chapter 10, Outlook for Using Stable Isotopes in Animal Migration Studies, provides a summary of thoughts about the path ahead.

Acknowledgment Len Wassenaar provided valuable edits on an earlier version of this chapter.

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red-winged blackbirds. Ecological Applications, 10, 911916. Van Wilgenburg, S., & Hobson, K. A. (2011). Combining feather stable isotope (δD) and band recovery data to improve probabilistic assignment of migratory birds to origin. Ecological Applications, 21, 13401351. Van Wilgenburg, S. L., Hobson, K. A., Brewster, K. R., & Welker, J. M. (2012). Addressing uncertainty in assessing dispersal in threatened migratory species using stable hydrogen isotope analysis of feathers. Endangered Species Research, 16, 1729. Wunder, M., Hobson, K. A., Kelly, J., Marra, P., Wassenaar, L. I., Stricker, C., & Doucette, R. (2009). Does a lack of design and repeatability compromise scientific criticism? A response to Smith et al. Auk, 126, 922926. Wolf, B. O., & Martinez del Rio, C. (2000). Use of saguaro fruit by white-winged doves: Isotopic evidence of a tight ecological association. Oecologia, 124, 536543. Yang, L. H., Ostrovsky, D., Rogers, M. C., & Welker, J. M. (2016). Intra-population variation in the natal origins and wing morphology of overwintering western monarch butterflies Danaus plexippus. Ecography, 39, 9981007. Yerkes, T., Hobson, K. A., Wassenaar, L. I., Macleod, R., & Coluccy, J. M. (2008). Stable Isotopes (δD, δ13C, δ15N) reveal associations among geographic location and condition of Alaskan Northern Pintails. Journal of Wildlife Management, 72, 715725. Yohannes, E., Hobson, K. A., Pearson, D., Wassenaar, L. I., & Biebach, H. (2005). Stable isotope analyses of feathers help identify autumn stopover sites of three longdistance migrants in northeastern Africa. Journal of Avian Biology, 36, 235241.

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Further Reading Cormie, A. B., Schwarcz, H. P., & Gray, J. (1994). Relationship between the hydrogen and oxygen isotopes of deer bone and their use in the estimation of relative humidity. Geochimica et Cosmochimica Acta, 60, 41614166. Haramis, G. M., Jorde, D. G., Macko, S. A., & Walker, J. L. (2001). Stable isotope analysis of canvasback winter diet in Upper Chesapeake Bay. Auk, 118, 10081017. Hebert, C., & Wassenaar, L. I. (2001). Stable nitrogen isotopes in waterfowl feathers reflect agricultural land use in western Canada. Environmental Science and Technology, 35, 34823487. Hobson, K. A. (1987). Use of stable-carbon isotope analysis to estimate marine and terrestrial protein content in gull diets. Canadian Journal of Zoology, 65, 12101213.

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