Tracking of Movements of Terrestrial Mammals Using Stable Isotopes

C H A P T E R

5 Tracking of Movements of Terrestrial Mammals Using Stable Isotopes Christian C. Voigt1,2 and Linn S. Lehnert1,2 1

Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany, 2Freie Universita¨t Berlin, Berlin, Germany

5.1 INTRODUCTION Isotopic tracking of movements has been used in the study of mammal biology since the 1990s. Yet only recently has this field gained momentum due to more laboratories offering their isotopic services, the standardized analysis of hydrogen stable isotope ratios of organic materials, and the importance of establishing animal movements in conservation biology. The huge benefit of isotope tracking terrestrial mammals over alternative methods such as tagging with transmitters or loggers is threefold: First, this approach depends only on the use of minute tissue samples (about 0.5 mg, depending on number and type of elements used) for measuring endogenous markers, making this technique applicable to any mammal, independent of size. This facilitates the collection of samples in a minimally invasive way, which is an important aspect for animal welfare considerations. Second, this approach does not require the recapture of the same individual. Consequently, the origin of a small-sized animal can be

Tracking Animal Migration with Stable Isotopes DOI: https://doi.org/10.1016/B978-0-12-814723-8.00005-2

estimated based on a single encounter. For example, the origin of a bat killed by a wind turbine can be assessed based on the stable hydrogen isotope ratios of its fur (Baerwald, Patterson, & Barclay, 2014; Lehnert et al., 2014; Voigt, Lindecke, Scho¨nborn, KramerSchadt, & Lehmann, 2016; Voigt, Popa-Lisseanu, Niermann, & Kramer-Schadt, 2012). Third, since the isotopic tracer is inactive in biologically inert material, such as keratin, isotopic tracking may help to unravel the movement biology of animals in historic times based on museum collections (Ossa, Kramer-Schadt, Peel, Scharf, & Voigt, 2012). This offers the unique possibility to study movements of extinct mammals and to compare the migration patterns of historic specimens with those of extant conspecifics. Previous reviews in this field focused on general aspects related to tracking migratory animals (West, Bowen, Cerling, & Ehleringer, 2006; Wunder, 2012; Chapter 4: Application of Isotopic Methods to Tracking Animal Movements) or on taxon-specific applications (Crawford, McDonald, & Bearhop, 2008). Here,

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we review published studies aimed at using stable isotopes to track terrestrial mammals, ranging from small-sized bats to elephants, covering three commonly used isotopic elements (H, C, and N) and including local, latitudinal, and elevational movements. The focus of this chapter will be on migratory movement, namely seasonal bidirectional movements, but we

mention other studies focusing on dispersal, local movements and diurnal movements as well (Table 5.1). Our chapter does not cover forensic studies for tracking the origin of animal products such as ivory from source countries; a topic that has been addressed before in other publications for wildlife (e.g., Peterson & Fry, 1987; Ziegler, Merker, Streit, Boner, & Jacob, 2016)

TABLE 5.1 Past Studies in Which Stable Isotopes Were Used to Track the Origin or Movements of Terrestrial Mammals (Sorted Following Orders) Section

Order

Climate Zone Country

Elevational migration Artiodactyla Temperate

Species

Isotopes Source

Ovis aries,

C; N

Ma¨nnel, Auerswald, and Schnyder (2007)

S

Zazzo et al. (2011)

H; C

Henaux et al. (2011)

O

Pietsch and Tu¨tken (2016)

Europe; northern part of the European Alps

Bos taurus,

Latitudinal migration Artiodactyla Temperate

Europe; Ireland

O. aries

Latitudinal migration Carnivora

Temperate; subtropical

USA; midwestern Puma concolor

Latitudinal migration Carnivora

Temperate

North America

Capra hircus

Lynx rufus, P. concolor

Latitudinal migration Carnivora

Subtropic

USA; California

Gulo gulo

C; N

Moriarty et al. (2009)

Latitudinal migration Chiroptera

Tropics; subtropics

Mexico

Leptonycteris curasoae

C

Fleming et al. (1993)

Latitudinal migration Chiroptera

Subtropics; arid

USA; Mexico

Tadarida brasiliensis

C; N

Wurster, McFarlane, and Bird (2007)

Latitudinal migration Chiroptera

Tropics

Costa Rica

Carollia castanea,

C

Voigt et al. (2012)

C; N

Segers and Broders (2015)

C; N

Reuter et al. (2016)

Glossophaga soricina

Carollia sowelli, Carollia perspicillata Latitudinal migration Chiroptera

Temperate

Canada

Myotis lucifugus, Myotis septentrionalis

Latitudinal migration Chiroptera

Tropics

Madagascar

Pteropus rufus, Eidolon dupreanum, Rousettus madagascariensis

(Continued)

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5.1 INTRODUCTION

TABLE 5.1 (Continued) Section

Order

Latitudinal migration Chiroptera

Climate Zone Country

Species

Isotopes Source

Temperate

Nyctalus noctula,

H; C; N

Voigt et al. (2016)

H

Erzberger, Popa-Lisseanu, Lehmann, and Voigt (2011)

Europe

Pipistrellus pipistrellus, Pipistrellus nathusii Elevational migration Chiroptera

Tropics

Honduras

Artibeus toltecus, Micronycteris microtis, Artibeus jamaicensis, Sturnira ludovici, Sturnira lilium, Myotis keaysi, Molossus ater

Elevational migration Chiroptera

Tropics

Tanzania

Miniopterus natalensis

H; C; N

Voigt et al. (2014)

Latitudinal migration Chiroptera

Temperate

USA

Lasiurus cinereus

H

Cryan et al. (2004)

USA

Lasiurus borealis,

H

Britzke et al. (2009)

Latitudinal migration Chiroptera

Myotis sodalist, M. septentrionalis, M. lucifugus Latitudinal migration Chiroptera

Temperate

USA; Indiana

M. sodalist

H

Britzke et al. (2012)

Latitudinal migration Chiroptera

Temperate

USA

Perimyotis subflavus

H

Fraser et al. (2012)

Latitudinal migration Chiroptera

Tropics

Africa

Eidolon helvum,

H; C; N

Ossa et al. (2012)

Rousettus aegyptiacus, Lissonycteris angolensis, Epomophorus wahlbergi, Hypsignathus monstrosus, Epomops franqueti, Epomophorus crypturus Latitudinal migration Chiroptera

Temperate

USA; Michigan

M. lucifugus

H

Sullivan et al. (2012)

Latitudinal migration Chiroptera

Temperate

USA

L. cinereus cinereus

H

Cryan et al. (2014) (Continued)

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TABLE 5.1 (Continued) Section

Order

Climate Zone Country

Species

Isotopes Source

Latitudinal migration Chiroptera

Temperate

Europe

N. noctula

H

Voigt et al. (2014)

Latitudinal migration Chiroptera

Temperate

USA

Lasionycteris noctivagans

H

Fraser et al. (2017)

Latitudinal migration Chiroptera

Temperate

Europe

N. noctula

H

Latitudinal migration Chiroptera

Temperate

Europe

P. nathusii,

H

Voigt, PopaLisseanu, et al. (2012)

H; C; N

Baerwald et al. (2014)

P. pipistrellus, N. noctula, Nyctalus leisleri Latitudinal migration Chiroptera

Temperate

Canada

L. cinereus, L. noctivagans

Latitudinal migration Chiroptera

Temperate

Europe

N. noctula

H

Lehnert et al. (2014)

Local movements

Chiroptera

Tropics

Central America

Desmodus rotundus

C

Voigt and Kelm (2006)

Local movements

Chiroptera

Tropics

Central America

C. castanea,

C

Voigt, VoigtHeucke et al. (2012)

C

Voigt (2010)

C. sowelli C. perspicillata Local movements

Chiroptera

Tropics

Central America

Phyllostomus discolor, A. jamaicensis Artibeus lituratus, Artibeus watsoni, Ectophylla alba

Local movements

Chiroptera

Tropics

Central America

More than 10 species

Local movements

Chiroptera

Tropics

Madagascar

16 bat species

N,C

Dammhahn and Goodman (2014)

Local movements

Chiroptera

Tropics

Madagascar

P. rufus,

N,C

Reuter et al. (2016)

H; C; N

Cerling et al. (2009)

Rex et al. (2011)

Eidolon helvum R. madagascariensis Latitudinal migration Proboscidea Tropics

Africa; Kenya

Loxodonta africana

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5.2 STABLE ISOTOPES AND MOVEMENTS OF TERRESTRIAL MAMMALS

and humans (Meier-Augenstein, 2011). Yet it is important to note that the approaches described in this chapter and elsewhere in this book could also be applied in wildlife forensic studies. A large proportion of isotopic papers published on mammal migration have focused on bats and using tissue δ2H measurements as the isotopic tracer. The likely reason for this taxonomic bias is that bats are elusive and difficult to track with alternative methods, such as relatively heavy GPS units and loggers, and that migratory bats cover long distances, crossing several precipitation-based δ2H isoclines during their annual latitudinal journeys. Lastly, the wind energy-wildlife conflict has stimulated several papers on bats in this field. Nonetheless, we aimed at being comprehensive in referencing and discussing also studies on non-Chiropteran species.

5.2 STABLE ISOTOPES AND MOVEMENTS OF TERRESTRIAL MAMMALS 5.2.1 Carbon and Nitrogen One of the first stable isotope papers on the ecology of a migratory mammal established δ13C values to assess the diet of nectar-feeding bat species in North America (Fleming, Nun˜ez, & Sternberg, 1993). During those early days, stable isotope measurements depended on relatively large sample mass, which forced researchers to collect muscular and skin tissue from sacrificed animals and from museum specimens. In the larger migratory Leptonycteris curasoae, δ13C values indicated a strong dependency on nectar from columnar cacti with a CAM photosynthetic pathway, whereas the smaller, nonmigratory Glossophaga soricina exhibited δ13C values indicative of a strong dependency on nectar from C3 plants. These findings confirmed that L. curasoae relied

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on a nectar corridor formed by columnar cacti from tropical Mexico to the Sonoran and Chihuahuan desert in the United States. It is important in the context of this chapter to acknowledge that the use of δ13C values in this specific case did not reveal the spatial pattern of migratory movement or the origin of animals based on probability of origin approaches, yet it highlighted the relevance of columnar cacti as a food source for migratory nectar-feeding bats. The suitability of δ13C values for use in tracing spatial origins depends on whether δ13C values vary in baseline food web samples, such as plant matter, across latitudinal, longitudinal, or elevational gradients. In contrast to hydrogen isotopes, we are missing large-scale continental maps describing spatial variation in plant δ13C and δ15N values (but see Chapter 2: Introduction to Conducting Stable Isotope Measurements for Animal Migration Studies, Chapter 3: Isoscapes for Terrestrial Migration Research). Therefore studies on mammals mostly used δ13C and δ15N values of consumer tissue or keratin in conjunction with δ2H values to confirm movement and migration patterns or to highlight the variable isotopic background of ecosystems that animals cross along their seasonal journey. For example, when covering long distances, mobile animals such as migrating bats may incorporate isotopes from a variety of food sources. Consequently, depending on the tissue chosen, variation in δ13C and δ15N values of individuals captured at a specific stopover site can be high when the catchment area of this stopover site is large (Segers & Broders, 2015). Intraindividual approaches have also been used, e.g., when comparing the variation of δ13C and δ15N values across tissues within individuals, if higher variances could best be explained by individuals encountering more habitats with variable isotopic compositions (Voigt et al., 2016). In some rare cases, baseline data on the geographic variation of δ13C and δ15N values

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in food webs leading to bats is available, so that δ13C and δ15N values in consumer tissues can be used to test movement patterns inferred from δ2H values in fur keratin. For example, bats performing elevational movements along the slopes of Mount Kilimanjaro in Tanzania were detected using isotope sampling (Voigt et al., 2016). Again, the general idea behind this approach lies in the assumption that tissues with different isotopic retention times integrate over specific retrospective periods and thus shed light over the isotopic variation of consumed food sources during the specific period of tissue formation (Chapter 4: Application of Isotopic Methods to Tracking Animal Movements). In general, continental patterns of δ13C and 15 δ N values are often too small in relation to the isotopic variation experienced by mammals at local scales. For example, in most cases differences in δ13C values between plants with a C4/CAM and C3 photosynthetic pathway are larger than most continental gradients of δ13C values for C3 plants (Chapter 3: Isoscapes for Terrestrial Migration Research). Yet, the strong contrast in δ13C values between C3 and C4/CAM plants can be used to infer local movements of mammals. For example, δ13C values in tissues or breath of vampire bats (Desmodus rotundus) suggested a diet based on C4 foods that were provided by livestock feeding on grasses even though vampires were captured in an C3 rainforest environment (Voigt, Grasse, Rex, Hetz, & Speakman, 2008; Voigt & Kelm, 2006). This indicated a commuting behavior of vampire bats between roosts in the rainforests and feeding areas on pastures. Further, C3 plants may vary in δ13C values when they are exposed to a gradient of water stress or additionally as a result of soil respiration in tropical forests, a pattern referred to as the “canopy effect” (Buchmann, Brooks, & Ehleringer, 2002). Accordingly, fruits and nectar may vary in δ13C values in relation to height. This gradient has been used to infer

feeding habits and movement of bats (Reuter, Wills, Lee, Cordes, & Sewall, 2016; Rex, Michener, Kunz, & Voigt, 2011; Voigt, VoigtHeucke, & Kretzschmar, 2012). Voigt and colleagues used breath δ13C values of fruiteating bats to assess the strata in which they foraged, since fruit-eating bats oxidize dietary carbohydrates quickly (Voigt, 2010). At the same study site, Voigt, Voigt-Heucke, et al. (2012) analyzed the movement of fruit-eating bats between rainforest and cleared areas (with expected higher δ13C values). In other studies, δ13C values of tail hair were used as a proxy to assess movements of African elephants between protected and heavily used, overgrazed communal areas, since in the latter habitat elephants switch from grass to a browse-dominated diet (Cerling, Wittemyer, Ehleringer, Remien, & Douglas-Hamilton, 2009). In an earlier study, authors also used δ13C and δ15N values in conjunction with GPS data to explain feeding behavior of GPS tagged elephants in relation to their local movements and use of crops (Cerling et al., 2006).

5.2.2 Hydrogen Initial mammalian studies using δ2H values as a tool for forensic investigations focused on the source of hydrogen in biologically inert body products, such as hair keratin. Sharp, Atudorei, Panarello, Ferna´ndez, and Douthitt (2003) demonstrated that about 31% of hydrogen in human hair originates from drinking water. They also pointed out the problem of exchangeable hydrogen in hair keratin (9% of total hydrogen in human hair, Sharp et al., 2003). The fact that hydrogen in organic molecules might exchange with ambient humidity when attached to oxygen or nitrogen, is an issue which hampered the adoption of this approach in initial years (Chapter 2: Introduction to Conducting Stable Isotope

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5.3 ISOTOPIC RETENTION IN TISSUES: THE RETROSPECTIVE MOVING TIME WINDOW

Measurements for Animal Migration Studies, Meier-Augenstein, Hobson, & Wassenaar, 2013). Importantly, spatial information derived from isotopic tracking is built on transfer functions (i.e., isotopic difference between precipitation and tissue) which require the collection of baseline data across a large geographical range (e.g., Ehleringer et al., 2008; PopaLisseanu et al., 2012). Such transfer functions are beneficial for developing and using tissuespecific isoscapes for assignment purposes (Chapter 4: Application of Isotopic Methods to Tracking Animal Movements). In the first study in which δ2H was used to assess the spatial behavior of a free-ranging mammal species, Cryan, Bogan, Rye, Landis, and Kester (2004) used keratin δ2H values of bat hair to assess the timing of molt and the migration behavior of Lasiurus cinereus, the North American hoary bat. First, they confirmed that molting occurs before migration in this species; an important point when bats captured during migration should be assigned to their summer origin (i.e., molting area) based on keratin δ2H values. Secondly, they found low variation of keratin δ2H values during the molting period, which suggested that δ2H values in keratin material are a reliable predictor of δ2H values of long-term average precipitation, one of the basic assumptions underlying this approach. Follow-up studies focusing on the same and additional North American species established information about the general migration behavior of these species for North America, yet studies varied in calibration standards (Britzke, Loeb, Hobson, Romanek, & Vonhof, 2009; Cryan, Stricker, & Wunder, 2014; Fraser, Brooks, & Longstaffe, 2017; Fraser, McGuire, Eger, Longstaffe, & Fenton, 2012). In parallel, isotopic transfer functions were established for European bats (Popa-Lisseanu et al., 2012), enabling European researchers to assign the summer origin of migratory bats as well. On both continents, most studies focused on the

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catchment areas of bats observed in hibernacula (Britzke, Loeb, Romanek, Hobson, & Vonhof, 2012; Sullivan, Bump, Kruger, & Peterson, 2012; Voigt et al., 2014) and that for bats killed at wind turbines (Baerwald et al., 2014; Lehnert et al., 2014; Voigt, Popa-Lisseanu, et al., 2012). An additional study addressed the migration behavior of the African strawcolored fruit bat, Eidolon helvum and other African flying foxes (Ossa et al., 2012).

5.3 ISOTOPIC RETENTION IN TISSUES: THE RETROSPECTIVE MOVING TIME WINDOW 5.3.1 Fur and Molting Patterns Isotopic tracking studies in mammals use mostly biologically inert material such as fur. Fur consists of various keratinous amino acids dominated by cysteine, serine, and glutamic acids (for humans: Meier-Augenstein et al., 2013). The relative contribution of amino acid composition might vary across taxa, particularly between mammalian fur keratin and avian feather keratin. In isotopic tracking studies that focus on migratory animals, it is frequently assumed that individuals molt before they migrate. This is often the case, yet poorly documented for mammals. Fraser, Longstaffe, and Fenton (2013) reviewed the literature on molting patterns in bats, particularly in context to stable isotope studies. They highlighted that molting occurs in bats mostly during a single event in summer or fall, yet with notable exceptions. Importantly, the phenology of molting may vary across species and within species (age and sex). Also, molting usually occurs gradually, i.e., body parts shade gradually their fur with areas covered by old fur adjacent to areas with regrown fur, a pattern called asynchronous fur growth. Fraser et al. (2013) concluded that fur samples should be taken dorsally from adult males to be most likely

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representative of the area of summer residency of a bat. Most information on molting in bats has been obtained from studies of the temperate zone, thus we are data deficient for the clear majority of bats in subtropical and tropical areas where the species density of Chiroptera is highest. In a detailed intraindividual study on molting patterns in free-ranging Nathusius bats, Voigt, Lindecke, Scho¨nborng, Kramer-Schadt, and Lehmann (2016) emphasized that the exact onset of molting was difficult to define. Further, individuals varied largely with respect to fur renewal, with females requiring about 50 55 days and males 25 50 days to complete molt. Molting ended around mid-July for this European migratory bat species, suggesting that δ2H values in fur keratin may integrate over a period from early June to mid-July. The high mobility of bats and the high variability in the timing of molt within and across species make it difficult to define exact periods for collecting reference data for the derivation of transfer functions (see 5.4.1). In many cases, researchers avoided any potential bias by using keratin δ2H values of nonmigratory species, i.e., those species that remain in an area presumably with similar isotopic composition throughout a year. Other non-bat mammals have also distinct molting patterns, particularly in the temperate zone where ambient temperatures vary largely between summer and winter (Ling, 1970). Species-specific molting patterns may vary according to the geographic site, taxonomy (e.g., subspecies level), sex, and age. In summary, the timing of molting is highly relevant for isotopic tracking of migratory movements based on stable hydrogen isotope ratios in fur keratin, and therefore the researcher needs to pay attention to this aspect of a species’ biology.

5.3.2 Other Keratinous Body Products In general, mammalian tail hair, whiskers, and claws consist of biologically inert keratin

material and therefore, these body products carry a constant isotopic fingerprint that can be used for dietary and spatial tracking of mammals. For example, long tail hair and whiskers can be cut into smaller segments and each of these increments record the isotopic composition of the ingesta at the time of growth (Schwertl, Auerswald, & Schnyder, 2003). For this approach, it is essential to quantify the growth rates for the specific species under study (Table 5.2). On the one hand, growth rates vary across taxa and within species, so that it is important to establish the growth rate of a selected study organism before the study. On the other hand, it seems questionable whether growth rates measured in captivity reflect those observed in free-ranging animals. Therefore these growth rate values must be treated with caution and uncertainties should be included in statistical models. Thus far, we lack studies that used the potential of hydrogen-based isotopic tracking using whisker or tail hair increments; possibly, because largesized mammals travel too slowly and thus do not cross ecosystem isoclines to make this approach fruitful. However, Henaux, Powell, Hobson, Nielsen, and LaRue (2011) developed an isotopic spatial track for cougars on a relatively small scale based on stable hydrogen isotope ratios in increments of claw material. Such an approach might be feasible if growth rates and local spatial scales are well established for the study species and area, respectively.

5.3.3 Tissue Turnover Rates Within mammals, organs differ in their isotopic retention, i.e., the rate at which stable isotopes are replaced as part of growth, maintenance, and degeneration of tissues (Martinez del Rio & Carleton, 2012). The isotopic times are usually quantified using dietswitch experiments (e.g., Ayliffe et al., 2004; Podlesak et al., 2008). Either material is

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TABLE 5.2 Growth Rates of Tail Hair and Whiskers in Selected Mammal Species Tissue

Species

Common Name

Growth Rate (mm /day)

Source

Tail hair

Equus caballus

Horse

0.63 0.88

West et al. (2004)

Tail hair

E. caballus

Horse

1.28

Sharp et al. (2003)

Tail hair

E. caballus

Horse

0.83

Dunnett (2005)

Tail hair

Loxodonta africana

African Elephant

0.55 6 0.11 (M)

Cerling et al. (2006)

0.81 6 0.13 (F)

Tail hair

L. africana

African Elephant

0.73 1.04

Cerling et al. (2009)

Tail hair

L. africana

African Elephant

0.71 1.03

Wittemyer, Cerling, and Douglas-Hamilton (2009)

Tail hair

L. africana

African Elephant

0.17 0.37

Codron et al. (2013)

Tail hair

Bos taurus

Cow

0.69 1.06

Schwertl et al. (2003)

Tail hair

B. taurus

Cow

0.51 0.63

Fisher, Wilson, Leach, and Scholz (1985)

Tail hair

E. caballus

Horse

0.39 0.87

Ayliffe et al. (2004)

Whiskers Canis lupus

Wolf

0.37 0.49

McLaren, Crawshaw, and Patterson (2015)

Whiskers Panthera leo, Panthera pardus

Lion, Leopard

0.65 (0.05 0.84)

Mutirwara, Radloff, and Codron (2017)

Whiskers Mustela erminea

Stoat

0.60

Spurr (2002)

Whiskers Meles meles

European badger

0.43 (0.23 0.83)

Robertson, McDonald, Delahay, Kelly, and Bearhop (2013)

Note that we have not listed those of pet or laboratory animals. Single numbers refer to mean growth rates (with addition of 6 1 standard devation, if possible) and two numbers to the range of observed growth rates. Abbreviations: F, females; M, males.

collected with minimal invasiveness, such as blood (separated into hematocrit and plasma) skin or muscle (using biopsy punches) or animals are euthanized during the diet switch. Currently, studies are heavily biased toward small mammals, since isotopic retention in each organ scales allometrically with body mass, i.e., for a given organ tissue isotopic retention time increases with the body mass of animals (Thomas & Crowther, 2015). Dietswitch experiments usually require a setting in which the diet of animals is under complete

control; a condition that is usually met only in captivity. However, it is important to keep in mind that the captive diet might not necessarily reflect the diet of wild animals and this flaw might affect the isotopic retention times. For example, Voigt, Matt, Michener, and Kunz (2003) found low isotopic retention times for carbon stable isotopes in nectar-feeding bats fed a low nitrogen diet, whereas Miro´n, Herrera, Ramı´rez, and Hobson (2006) showed faster isotopic retention times, when the same species was fed a nitrogen-enriched diet.

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After having gained a good understanding of organ-specific isotopic retention times in each study animal, it is possible to use stable isotopes of specific organs as tracers of diet and origin (Voigt et al., 2014). Thus far, the spatial aspect of this approach has been impaired by the inability to measure consistently (and among laboratories) δ2H values of nonexchangeable H in materials other than keratin. Development of calibration standards for metabolically active tissues like plasma, hematocrit, muscle tissues, among others are needed in the future (see Chapter 2: Introduction to Conducting Stable Isotope Measurements for Animal Migration Studies) but issues related to exchange with body water have not been resolved.

5.4 APPLICATION OF STABLE ISOTOPES TO THE STUDY OF MIGRATORY MOVEMENTS 5.4.1 Transfer Functions Several transfer functions exist linking mammalian keratin δ2H values with expected long-term precipitation δ2H values (Table 5.3). For example, one based on human hair (Ehleringer et al., 2008), several for North American bats (Cryan et al., 2004; modified in Baerwald et al., 2014), for European bats (Popa-Lisseanu et al., 2012, modified in Voigt et al., 2014; Table 5.3). So far, studies have yet to establish robust transfer functions for carnivores, probably because of specific aspects in the biology of this taxon, possibly the low dependency on surface water for drinking (Pietsch, Hobson, Wassenaar, & Tu¨tken, 2011). Two points are important in the context of isotopic transfer functions of free-ranging mammals: Large variances in regression models hamper the accuracy of the predictive model. Also, we generally lack species-specific transfer functions, which are presumed to be most

appropriate. On the one hand, isotopic transfer functions corresponding to single-species may suffer from small sample sizes. Thus transfer functions may not catch the full variation observed over the range of expected tissue δ2H values. On the other hand, multispecies transfer functions may overestimate the variance because of species-specific differences in δ2H values caused by food-web or guild-specific deviations (Voigt, Lehmann, & Greif, 2015).

5.4.2 Causes and Consequences of Variation There are numerous sources of variation in using mammal tissue δ2H values for animal tracking. Laboratory analytical measurement issues have been covered in Chapter 2, Introduction to Conducting Stable Isotope Measurements for Animal Migration Studies, and it should be mandatory now for all analyses to appropriately control for the effect of exchangeable hydrogen on δ2H values (MeierAugenstein et al., 2013). Second, food items may vary in isotopic composition and thus, tissues of consumers feeding on food items with contrasting isotopic composition may reflect these differences even though they might have been exposed to the same δ2H values of precipitation and ground water (Birchall, O’Connel, Heaton, & Hedges, 2005; Britzke et al., 2009; Voigt, Schneeberger, & Luckner, 2013). Food related differences in δ2H values across species may rather originate from contrasting δ2H values in food items in addition to those factors acting on variance in precipitation δ2H (Chapter 3: Isoscapes for Terrestrial Migration Research, Voigt et al., 2015). For example, syntopic bats showed contrasting δ2H values in fur keratin when feeding on terrestrial or limnic food items (Voigt et al., 2015), most likely because baseline δ2H values of plant matter differed between both habitats. Such differences in food web specific isotopic

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5.4 APPLICATION OF STABLE ISOTOPES TO THE STUDY OF MIGRATORY MOVEMENTS

TABLE 5.3 List of Published H Isotope Transfer Functions for a Variety of Mammal Species Taxon Chiroptera Chiroptera Chiroptera

Continent Europe Europe Europe

Species

Transfer Function

Multispecies

δ Hf 5 1.07*δ Hp 16.84

Multispecies

δ Hf 5 1.37*δ Hp 1 5.52

Multispecies

δ Hf 5 0.92*δ Hp 30.72

2 2

2

2

2

δ Hf 5 0.9*δ Hp 9.38 2

Source

2

2

scaled to A

Popa-Lisseanu et al. (2012)

scaled to A

Voigt et al. (2014)

scaled to A

δ2Hf 5 0.77*δ2Hp 1 3.44 scaled Chiroptera

Africa

to USGS

Multispecies

δ2Hf 5 1.52*δ2Hp 1 54.09 scaled

to A

Chiroptera

North America

Lasiurus cinereus

δ Hf 5 0.79*δ Hp 2 24.81

Chiroptera

North America

L. cinereus

δ2Hf 5 0.73*δ2Hp 2 42.61scaled

Chiroptera

North America

Myotis septentrionalis

δ2Hf 5 0.79*δ2Hp 2 4.73 (M)scaled

2

2

-

scaled to B

Ossa et al. (2012)

scaled to C

Cryan et al. (2004)

to C

Cryan et al. (2014)

to B and C

Britzke et al. (2009)

scaled to B and C

Britzke et al. (2009)

δ Hf 5 1.25*δ Hp 1 18.48 (F) 2

2

δ Hf 5 0.98*δ Hp 1 5.48 (M 1 F) 2

2

scaled to B

Britzke et al. (2009)

and C

Chiroptera

North America

Myotis lucifugus

δ2Hf 5 0.49*δ2Hp 2 30.90 (M)scaled to B

and C

δ Hf 5 0.33*δ Hp 40.41 (F) 2

2

scaled to B and C

δ Hf 5 0.52*δ Hp 30.82 (M 1 F) 2

2

scaled to B and

Britzke et al. (2009) Britzke et al. (2009) Britzke et al. (2009)

C

δ2Hf 5 2.69*δ2Hp 1 96.93scaled Chiroptera

North America

Myotis sodalis

to B and C

δ2Hf 5 0.90*δ2Hp 2 0.59 (M)scaled δ2Hf 5 0.71*δ2Hp 8.17 (F)scaled

to B and C

to B and C

δ2Hf 5 0.83*δ2Hp 2.97 (M 1 F)scaled

to B and

Sullivan et al. (2012) Britzke et al. (2009) Britzke et al. (2009) Britzke et al. (2009)

C

Chiroptera

North America

Perimyotis subflavius

δ2Hf 5 20.04*δ2Hp 1.79*δ2Hp 2 45.61 (M)scaled to C

Fraser et al. (2012)

δ2Hf 5 20.03*δ2Hp 1.61*δ2Hp 2 40.38 (F)scaled to C Chiroptera

North America

Lasiurus borealis

δ2Hf 5 28.2*δ2Hp 58.80 (M)scaled

to B and C

δ Hf 5 1.35*δ Hp 3.60 (F) 2

2

scaled to B and C

Britzke et al. (2009) Britzke et al. (2009)

δ Hf 5 0.48*δ Hp 26.10 (M 1 F)

Britzke et al. (2009)

δ2Hf 5 1.48*δ2Hp 1 13.95 (M)scaled to C

Pylant, Nelson, and Keller (2014)

δ2Hf 5 1.75*δ2Hp 1 18.02 (F)scaled

Pylant et al. (2014)

2

2

scaled to B and

C

to C

δ Hf 5 1.67*δ Hp 1 16.84 (M 1 F) 2

2

scaled to C

Pylant et al. (2014) (Continued)

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5. TRACKING OF MOVEMENTS OF TERRESTRIAL MAMMALS USING STABLE ISOTOPES

TABLE 5.3 (Continued) Taxon Ungulates

Continent North America

Lagomorpha North America

Species

Transfer Function

Odocoileus virginianus

δ HBoneCollagen 5 0.86*δ Hriver. scaled to B water 1 20.28

Pietsch et al. (2011)

Sylvilagus floridanus

δ2Hf 5 0.80*δ2Hp 25.46scaled

Pietsch et al. (2011)

2

Source 2

to B

Abbreviations: F, females; M, males. Information on whether data are scaled to keratin standards from the Berlin laboratory (A), the Saskatoon laboratory (B), or other standards (C).

compositions suggest that it is necessary to establish and use taxon- or guild-specific isotopic transfer functions where possible. For example, it might be necessary to use δ2H values from nonmigratory bat species from a terrestrial food web, i.e., not depending on aquatic insects, as a proxy for a migratory species that also belongs to terrestrial food webs. Third, interspecific differences in δ2H values may also stem from species-specific molting patterns that may cause fur keratin to vary according to the mean δ2H value driving the food and drinking water used by the species at the time of tissue synthesis (Britzke et al., 2009). Naturally, the protocol for collecting fur should be consistent within a study. Lastly, it is unknown how lactation changes the isotopic composition of juveniles, since suckling young assimilate hydrogen from water and nutrients in maternal milk. Since δ2H values of body water might not necessarily be correlated with δ2H values of fur keratin in mammals (Voigt et al., 2013), assimilation of hydrogen from milk by juveniles might lead to altered δ2H values in fur keratin compared to corresponding values in adult conspecifics. Indeed, lipid-rich foods, which are depleted in 2H, associated with nursing may drive dietary δ2H values more negative (Soto, Koehler, Wassenaar, & Hobson, 2017). Since juveniles carry the isotopic signature of the lactation period in their fur keratin, it is likely that this might cause additional variation in transfer functions if δ2H values of juveniles that have

been captured before the second molt are included in regression models. A large variation in the transfer function used to predict the summer origin of mammals might lead to imprecise geographical assignments of animals.

5.4.3 Case Study Here, we use a case study to describe the specific steps needed to engage in an isotopic tracking study of a migratory bat. Specifically, we elaborate on practical considerations, whereas details of the modeling are described in Chapter 9, Isoscape Computation and Inference of Spatial Origins With Mixed Models Using the R package IsoriX. The specific example deals with the geographical origin of bats killed by wind turbines in Germany. Over the past decades wind energy has become a prospering industry worldwide (Arnett et al., 2016). Wind energy poses risks to volant animals, with large numbers of birds and bats dying at wind turbines each year (Hayes, 2013; Voigt et al., 2015). Two of the main challenges in solving this dilemma are, first, to establish measures to mitigate the negative impacts on wildlife and, second, to quantify the consequences of increased mortality on affected source populations. In case of bats, it is impossible to tell whether a bat killed at a wind turbine originates from a local or distant population based on morphological or genetic traits. Therefore we applied isoscape

TRACKING ANIMAL MIGRATION WITH STABLE ISOTOPES

5.4 APPLICATION OF STABLE ISOTOPES TO THE STUDY OF MIGRATORY MOVEMENTS

origin models based on δ2H values of fur keratin collected from individual bats killed at wind turbines, specifically from the common noctule bat (Nyctalus noctula). Beforehand, we established a relationship between δ2H values in fur keratin of nonmigratory bats and that of mean annual precipitation water. This relationship enabled us to predict δ2H values in precipitation water of the most likely places of origin. Collection of samples: In most studies, fur samples are collected from the dorsal part of bats, mostly from the interscapular area. The amount of fur collected can be kept small, since the stable isotope analysis requires only a minute sample mass (e.g., 0.5 mg). However, in case of multielemental approaches, larger fur samples are required. It is important that carcasses must be relatively fresh, because decomposition of fur caused by exposure to rain and high temperature might alter the isotopic composition of keratin. Yet, this process can take considerable time and probably depends on local ambient conditions such as warm ambient temperature and rainfall that will hasten the process of decomposition. Collected fur samples should be dried and stored in a small envelope or plastic vial. To prevent any further decomposition, it is advisable to store samples in a freezer or a dry place. Preparation and analysis of samples: The laboratory based processes involved in the preparation and isotopic analysis of samples are mentioned in Chapter 2, Introduction to Conducting Stable Isotope Measurements for Animal Migration Studies. Reconstructing of the origin of animals based on stable hydrogen isotope ratios: The newly developed R-package IsoriX was used for statistical analysis and Chapter 9, Isoscape Computation and Inference of Spatial Origins With Mixed Models Using the R package IsoriX, provides details on all the different statistical substeps related to the workflow in IsoriX. Here we introduce and discuss the process and outcome of this analysis.

129

We started by fitting a δ2H precipitation isoscape for the relevant geographical area that covers the distribution range of N. noctula in Europe (and partly beyond). We used measured δ2Hp values of Europe made available via the Global Network of Isotopes in Precipitation (GNIP) to fit a pair of geostatistical models, approximating the relationship between topographic features of a location and its amount weighted mean annual δ2Hp signature. Subsequently, we built a δ2Hp isoscape for Europe using the geospatial model to predict the spatial distribution of δ2Hp values in our area of interest (Chapter 3: Isoscapes for Terrestrial Migration Research). It is important to note that the density of weather stations contributing with δ2Hp values varies spatially, which may lead to a limitation in predictive power in sparsely covered regions, such as northern regions. However, potential temporal patterns in data availability should also be explored. IsoriX provides tools to quantify the prediction variance across the area of interest (Fig. 9.4). The isotopic transfer function is required to relate the measured δ2H values in fur keratin to δ2H values in precipitation. We obtained data for this function by combining datasets of nonmigratory, insectivorous bat species from terrestrial food webs (Popa-Lisseanu et al., 2012) with those of noctule bats sampled during their nonmigratory period across Europe (Voigt et al., 2014). By using a mixedspecies transfer function we likely increased the variance within the dataset (Fig. 5.1), which might potentially lead to less accurate assignments compared with a species-specific dataset. However, to date we lack the data basis for a single species transfer function in Europe that covers the full isotopic range of possible places of origin. While acknowledging limitations in the spatial resolution of assignments, we are convinced that providing assignments based on a large multispecies dataset lead to more conservative and thus

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5. TRACKING OF MOVEMENTS OF TERRESTRIAL MAMMALS USING STABLE ISOTOPES

FIGURE 5.1 The graph shows our H isotope transfer function (IZW Berlin: blue line and black dots) relating measured δ2H values in fur keratin of nonmigratory bats to δ2H values in precipitation water across Europe. In order to demonstrate the effect different laboratory standards used in different laboratories may have on the resulting data. We additionally rescaled our dataset to two other common standards and added the resulting transfer functions to the plot (Saskatoon Laboratory: green line and green crosses; and USGS 42: red line and red triangles). δ2H values measured at the stable isotope laboratory IZW Berlin can be rescaled to USGS 42 using the following equation: 0.8388*δ2HIZW.Berlin 1 29.22. The respective formula for rescaling δ2H values measured at the Saskatoon stable isotope laboratory can be found in Soto et al. (2017). As can be seen the results differ, which is why one should exercise due care when analyzing a mixed dataset measured at different laboratories or with different standards.

also more reliable assignments than using a small but single species dataset which might be based on smaller sample sizes. Since we know that measured δ2H values in bats may vary significantly between age classes (Baerwald et al., 2014; Britzke et al., 2009), we considered adult individuals only both for the transfer function and the assignments. Results for the transfer function are shown in Fig. 5.1. For illustration, we plotted our transfer function dataset scaled to three different standards used in different laboratories (IZW Laboratory, Saskatoon Laboratory, USGS 42). The keratin standards of the IZW laboratory originate from Swedish and Spanish sheep (wool) and Tanzanian goat (pelage) and have been established using the dual-inlet method as outlined in Wassenaar and Hobson (2000, 2003).

Geographical assignments: In the case study, we aimed to assign the likely origin for 14 noctule bats killed at wind turbines. We focused on individuals found during the autumn migration period after the molting season, below wind turbines. Results of our assignments indicate that most individuals found dead below wind turbines originated from local populations, while one individual came from a distant population in Eastern Europe according to its δ2H values (Fig. 5.2). It is obvious from the derived probability maps that areas with similar δ2H values in precipitation water yield a similar probability of origin for animals. Since so-called isoclines, i.e., areas of similar isotopic composition, follow latitude reasonably closely in the northern hemisphere, isoscape origin models poorly resolve east-western movements of

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5.5 FUTURE DIRECTIONS

131

FIGURE 5.2 Predicted geographical provenance of 14 Nyctalus noctula killed at wind turbines in eastern Germany. Geographical areas marked green indicate areas of likely origin while gray areas indicate unlikely origin. Based on visual inspection of 14 individual assignments generated in IsoriX (Chapter 9: Isoscape Computation and Inference of Spatial Origins With Mixed Models Using the R package IsoriX) we decided to pool all 13 individuals for which the locality of death could not be excluded as likely origin into the category “regional bats” and provide a group assignment as a final plot (left graph). The individual assignment of the only migratory bat is shown in the right graph.

animals. However, it is possible to refine the isotopic approach by including a priori information. In a previous study, we combined the isoscape origin model with assumed heading directions and travel distances in migratory noctule bats that were obtained from banding data (Voigt et al., 2014). This example shows that it is possible to specify the area of likely origin when using such priors. Other priors could be a further set of stable isotopes, such as δ34S measurements used as a proxy for distance to the coast (Zazzo, Monahan, Moloney, Green, & Schmidt, 2011).

5.5 FUTURE DIRECTIONS We envision a promising future for the application of stable isotopes in the study of movements in terrestrial mammals. Recently, analytical developments have become widely available which will enable us to analyze hydrogen stable isotope ratios in

non-keratinous matrices (Meier-Augenstein et al., 2013; Soto et al., 2017). Further technical advances, possibly in compound specific analysis of stable hydrogen isotope ratios, may stimulate more research (Chapter 7: Amino Acid Isotope Analysis: A New Frontier in Studies of Animal Migration and Foraging Ecology). We recommend international efforts be undertaken to provide more reference material from migratory species during their molting period to serve as a global databank. By doing this, raw isotopic data would be available combined with spatial information (longitude and latitude), which would facilitate future efforts to refine isoscape origin models. This effort should include non-keratinous mammalian materials as well. Establishing small-scale isoscapes in the range of a few square kilometers could help in elucidating spatial movements of less mobile species. Lastly, isotopic tracking can be combined with other techniques such as GPS collaring or multisensor data loggers.

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5.6 SUMMARY Isotopic tracking of movements has developed as an important tool for mammal ecology. To date, the focus of research has been on highly mobile smaller mammals, such as bats, and most studies have been based on the analysis of δ2H values in keratinous materials. Almost all previous isotopic tracking studies in mammals are based on inert body products, such as fur, whiskers, tail hair, and claw material, yet the full potential of these body products has not yet been explored. For example, δ2H values in whisker material have not yet been used in isoscape origin models. Overall, research in isotopic tracking has yielded important insights into the large-scale movements of mammals, particularly in research related to conservation questions. Yet, stable isotope tracking of mammals has not reached the same momentum and widespread use as for birds and insects. Currently, we foresee four important developments that will foster new research in the area of isotopic tracking of animals in general and that of mammals in particular: New instruments for analyzing stable hydrogen isotope ratios will facilitate research on non-keratinous matrices, the availability of international organic isotopic standards will make measurements of hydrogen stable isotope ratios comparable across studies, the addition of more reference data for local food webs and for consumer tissues will facilitate the interpretation of data in future and the development of new software tools such as IsoriX and IsoMap will enable any researcher to develop assignment models with ease. In summary, we envision a multitude of possibilities to engage in isotope tracking studies of mammals and therefore encourage researchers to follow in this direction.

Acknowledgments We would like to thank the technical staff of the Stable Isotope Laboratory at the Leibniz Institute for Zoo and Wildlife Research for help with the analysis, Stephanie

Kramer-Schadt and Alexandre Courtiol for advice regarding statistical questions and the participants of the two International Summer Schools for Stable Isotopes in Animal Ecology held in 2014 and 2016 at the IZW for discussion. We thank Alexandre Courtiol, Len Wassenaar, and Keith Hobson for comments on an earlier draft of the manuscript.

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5. TRACKING OF MOVEMENTS OF TERRESTRIAL MAMMALS USING STABLE ISOTOPES

Ossa, G., Kramer-Schadt, S., Peel, A. J., Scharf, A. K., & Voigt, C. C. (2012). The movement ecology of the straw-colored fruit bat, Eidolon helvum, in sub-Saharan Africa assessed by stable isotope ratios. PLoS One, 7(9), e45729. Peterson, B. J., & Fry, B. (1987). Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics, 18 (1), 293 320. Pietsch, S. J., Hobson, K. A., Wassenaar, L. I., & Tu¨tken, T. (2011). Tracking cats: Problems with placing feline carnivores on δ18O, δD isoscapes. PLoS One, 6(9), e24601. Pietsch, S. J., & Tu¨tken, T. (2016). Oxygen isotope composition of North American bobcat (Lynx rufus) and puma (Puma concolor) bone phosphate: Implications for provenance and climate reconstruction. Isotopes in Environmental and Health Studies, 52(1 2), 164 184. Podlesak, D. W., Torregrossa, A. M., Ehleringer, J. R., Dearing, M. D., Passey, B. H., & Cerling, T. E. (2008). Turnover of oxygen and hydrogen isotopes in the body water, CO2, hair, and enamel of a small mammal. Geochimica et Cosmochimica Acta, 72(1), 19 35. Popa-Lisseanu, A. G., So¨rgel, K., Luckner, A., Wassenaar, L. I., Iba´n˜ez, C., Kramer-Schadt, S., . . . Mysłajek, R. W. (2012). A triple-isotope approach to predict the breeding origins of European bats. PLoS One, 7(1), e30388. Pylant, C. L., Nelson, D. M., & Keller, S. R. (2014). Stable hydrogen isotopes record the summering grounds of eastern red bats (Lasiurus borealis). PeerJ, 2, e629. Available from https://doi.org/10.7717/ peerj.629. Reuter, K. E., Wills, A. R., Lee, R. W., Cordes, E. E., & Sewall, B. J. (2016). Using stable isotopes to infer the impacts of habitat change on the diets and vertical stratification of frugivorous bats in Madagascar. PLoS One, 11(4), e0153192. Rex, K., Michener, R., Kunz, T. H., & Voigt, C. C. (2011). Vertical stratification of Neotropical leaf-nosed bats (Chiroptera: Phyllostomidae) revealed by stable carbon isotopes. Journal of Tropical Ecology, 27(3), 211 222. Robertson, A., McDonald, R. A., Delahay, R. J., Kelly, S. D., & Bearhop, S. (2013). Whisker growth in wild Eurasian badgers Meles meles: Implications for stable isotope and bait marking studies. European Journal of Wildlife Research, 59(3), 341 350. Rohrig. (2014). Windenergie Report Deutschland (2014) Fraunhofer-Institut fu¨r Windenergie und Energiesystemtechnik IWES Kassel. ISBN 978-38396-0854-8. Schwertl, M., Auerswald, K., & Schnyder, H. (2003). Reconstruction of the isotopic history of animal diets by hair segmental analysis. Rapid Communications in Mass Spectrometry, 17(12), 1312 1318.

Segers, J. L., & Broders, H. G. (2015). Carbon (δ13C) and nitrogen (δ15N) stable isotope signatures in bat fur indicate swarming sites have catchment areas for bats from different summering areas. PLoS One, 10(4), e0125755. Sharp, Z. D., Atudorei, V., Panarello, H. O., Ferna´ndez, J., & Douthitt, C. (2003). Hydrogen isotope systematics of hair: Archeological and forensic applications. Journal of Archaeological Science, 30(12), 1709 1716. Soto, D. X., Koehler, G., Wassenaar, L. I., & Hobson, K. A. (2017). Re-evaluation of the hydrogen stable isotopic composition of keratin calibration standards for wildlife and forensic science applications. Rapid Communications in Mass Spectrometry. Available from https://doi.org/ 10.1002/rcm.7893. Spurr, E. B. (2002). Rhodamine B as a systemic hair marker for assessment of bait acceptance by stoats (Mustela erminea). New Zealand Journal of Zoology, 29(3), 187 194. Sullivan, A. R., Bump, J. K., Kruger, L. A., & Peterson, R. O. (2012). Bat-cave catchment areas: Using stable isotopes (δD) to determine the probable origins of hibernating bats. Ecological Applications, 22(5), 1428 1434. Thomas, S. M., & Crowther, T. W. (2015). Predicting rates of isotopic turnover across the animal kingdom: A synthesis of existing data. Journal of Animal Ecology, 84(3), 861 870. Voigt, C. C. (2010). Insights into strata use of forest animals using the ‘canopy effect’. Biotropica, 42(6), 634 637. Voigt, C. C., Grasse, P., Rex, K., Hetz, S. K., & Speakman, J. R. (2008). Bat breath reveals metabolic substrate use in free-ranging vampires. Journal of Comparative Physiology B, 178(1), 9 16. Voigt, C. C., Helbig-Bonitz, M., Kramer-Schadt, S., & Kalko, E. K. (2014). The third dimension of bat migration: Evidence for elevational movements of Miniopterus natalensis along the slopes of Mount Kilimanjaro. Oecologia, 174(3), 751 764. Voigt, C. C., & Kelm, D. H. (2006). Host preference of the common vampire bat (Desmodus rotundus; Chiroptera) assessed by stable isotopes. Journal of Mammalogy, 87(1), 1 6. Voigt, C. C., Lehmann, D., & Greif, S. (2015). Stable isotope ratios of hydrogen separate mammals of aquatic and terrestrial food webs. Methods in Ecology and Evolution, 6(11), 1332 1340. Voigt, C. C., Lehnert, L. S., Popa-Lisseanu, A. G., Ciechanowski, M., Esto´k, P., Gloza-Rausch, F., . . . Teige, T. (2014). The trans-boundary importance of artificial bat hibernacula in managed European forests. Biodiversity and Conservation, 23(3), 617 631. Voigt, C. C., Lindecke, O., Scho¨nborn, S., Kramer-Schadt, S., & Lehmann, D. (2016). Habitat use of migratory bats killed during autumn at wind turbines. Ecological Applications, 26(3), 771 783.

TRACKING ANIMAL MIGRATION WITH STABLE ISOTOPES

FURTHER READING

Voigt, C. C., Matt, F., Michener, R., & Kunz, T. H. (2003). Low turnover rates of carbon isotopes in tissues of two nectar-feeding bat species. Journal of Experimental Biology, 206(8), 1419 1427. Voigt, C. C., Popa-Lisseanu, A. G., Niermann, I., & Kramer-Schadt, S. (2012). The catchment area of wind farms for European bats: A plea for international regulations. Biological Conservation, 153, 80 86. Voigt, C. C., Schneeberger, K., & Luckner, A. (2013). Ecological and dietary correlates of stable hydrogen isotope ratios in fur and body water of syntopic tropical bats. Ecology, 94(2), 346 355. Voigt, C. C., Voigt-Heucke, S. L., & Kretzschmar, A. S. (2012). Isotopic evidence for seed transfer from successional areas into forests by short-tailed fruit bats (Carollia spp.; Phyllostomidae). Journal of Tropical Ecology, 28(2), 181 186. Wassenaar, L. I., & Hobson, K. A. (2000). Improved method for determining the stable-hydrogen isotopic composition (δD) of complex organic materials of environmental interest. Environmental Science & Technology, 34(11), 2354 2360. Wassenaar, L. I., & Hobson, K. A. (2003). Comparative equilibration and online technique for determination of non-exchangeable hydrogen of keratins for use in animal migration studies. Isotopes in Environmental and Health Studies, 39(3), 211 217. West, A. G., Ayliffe, L. K., Cerling, T. E., Robinson, T. F., Karren, B., Dearing, M. D., & Ehleringer, J. R. (2004). Short-term diet changes revealed using stable carbon isotopes in horse tail-hair. Functional Ecology, 18(4), 616 624. West, J. B., Bowen, G. J., Cerling, T. E., & Ehleringer, J. R. (2006). Stable isotopes as one of nature’s ecological recorders. Trends in Ecology & Evolution, 21(7), 408 414.

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Wittemyer, G., Cerling, T. E., & Douglas-Hamilton, I. (2009). Establishing chronologies from isotopic profiles in serially collected animal tissues: An example using tail hairs from African elephants. Chemical Geology, 267(1), 3 11. Wunder, M. (2012). Determining geographic patterns of migration and dispersal using stable isotopes in keratins. Journal of Mammalogy, 93(2), 360 367. Wurster, C. M., McFarlane, D. A., & Bird, M. I. (2007). Spatial and temporal expression of vegetation and atmospheric variability from stable carbon and nitrogen isotope analysis of bat guano in the southern United States. Geochimica et Cosmochimica Acta, 71(13), 3302 3310. Zazzo, A., Monahan, F. J., Moloney, A. P., Green, S., & Schmidt, O. (2011). Sulphur isotopes in animal hair track distance to sea. Rapid Communications in Mass Spectrometry, 25, 2371 2378. Ziegler, S., Merker, S., Streit, B., Boner, M., & Jacob, D. E. (2016). Towards understanding isotope variability in elephant ivory to establish isotopic profiling and source-area determination. Biological Conservation, 197, 154 163.

Further Reading Coplen, T. B., & Qi, H. (2012). USGS42 and USGS43: Human-hair stable hydrogen and oxygen isotopic reference materials and analytical methods for forensic science and implications for published measurement results. Forensic Science International, 214(1), 135 141. Fraser, K. C., McKinnon, E. A., & Diamond, A. W. (2010). Migration, diet, or molt? Interpreting stable-hydrogen isotope values in Neotropical bats. Biotropica, 42(4), 512 517.

TRACKING ANIMAL MIGRATION WITH STABLE ISOTOPES