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Ecoscience 13(1):11-22. 2006
doi: 10.2980/1195-6860(2006)13[11:MDFCAN]2.0.CO;2

Models developed from δ13C and δ15N of skin tissue indicate non-specific habitat use by the big brown bat (Eptesicus fuscus)

James C. Sullivana, Kendra J. Buscettaa, Robert H. Michenerb, John O. Whitaker Jr.c, John R. Finnertyd, and Thomas H. Kunz1d

aDepartment of Biology, Boston University, Boston, Massachusetts 02215, USA

bDepartment of Biology and Stable Isotope Laboratory, Boston University, Boston, Massachusetts 02215, USA

cDepartment of Ecology and Organismal Biology, Indiana State University, Terre Haute, Indiana 47809, USA

dDepartment of Biology, Boston University, Boston, Massachusetts 02215, USA,

Abstract

Stable isotopes can be used to evaluate trophic relationships, nutrient state, and temporal and spatial variation in diet, food webs, and behaviour both within and between species. Here we describe the development and application of models to predict habitat use of a common insectivorous bat (Eptesicus fuscus) based upon δ13C and δ15N signatures of skin tissue. We used a 42-specimen sample collected from three well-characterized ecogeographic regions, disparate both in photosynthetic mechanism and fertilizer use, to generate the models. Significant univariate differences between these three sites in terms of δ13C (F2, 39 = 112.92, P < 0.0001) and δ15N (F2, 39 = 97.06, P < 0.0001), and multivariate significance of both variables (Wilk's λ = 0.032, F4, 76 = 87.02, P < 0.0001), made it possible to develop three predictive models using Fisher's linear discriminant functions: 1) a model predicting if bats forage in C3 or mixed C3/C4 sites, 2) a model predicting if bats forage in agricultural areas, and 3) a combined model using both variables to predict specific habitat use. We present the results of model application to an independent dataset of 329 bats sampled from 10 states that included a broad range of δ13C (−26.53‰ δ13C −17.20‰) and δ15N (6.36‰ δ15N 15.60‰) signatures. We validated the use of skin tissue samples (from wing membranes) in the model by comparing the sites used for model development across five tissue types, selecting skin samples for model development due to consistently low variance within this tissue type. Our results indicate non-specific habitat-use by big brown bats.

Résumé

Les isotopes stables peuvent être utilisés pour examiner les relations trophiques, l'état nutritionnel et les variations temporelles et spatiales dans la diète, les chaînes alimentaires et le comportement à l'intérieur d'une même espèce ou entre les espèces. Nous décrivons ici le développement et l'application de modèles prédictifs de l'utilisation de l'habitat chez une chauve-souris insectivore commune (Eptesicus fuscus) bases sur les signatures δ13C et δ15N de la peau. Pour générer les modèles, nous avons utilisé un échantillon de 42 spécimens récoltés dans trois régions écogéographiques très distinctes au niveau du mécanisme photosynthétique et de l'utilisation de fertilisants. Des différences univariées significatives entre les trois sites en termes de δ13C (F2, 39 = 112.92, P < 0.0001) et δ15N (F2, 39 = 97.06, P < 0.0001) et la significativité multidimensionnelle des deux variables (Wilk's λ = 0.032, F4, 76 = 87.02, P < 0.0001) ont rendu possible le développement de trois modèles prédictifs utilisant les fonctions discriminantes linéaires de Fischer : 1) un modèle prédisant si les chauves-souris se nourrissent dans des sites exclusivement C3 ou mélangés C3/C4; 2) un modèle prédisant si les chauve-souris se nourrissent dans des secteurs agricoles; et 3) un modèle synthétique utilisant les deux variables pour prédire l'utilisation d'habitats spécifiques. Nous présentons les résultats de l'application des modèles sur un échantillon indépendant de 329 chauves-souris provenant de 10 etats et presentant de grandes variations dans les signature δ13C (−6.53 ‰ δ13C −17.20 ‰) et δ15N (6.36 ‰ δ15N 15.60 ‰). Nous avons validé l'utilisation d'échantillons de peau (provenant des membranes des ailes) dans les modèles en comparant, pour cinq types de tissu, les sites utilisés pour le développement des modèles. La peau a été le tissu sélectionné pour développer les modèles à cause de sa faible variance. Nos résultats démontrent que la sérotine des maisons n'utilise pas des habitats spécifiques.

Received: March 29, 2005; Accepted: May 24, 2005

Keywords: chauves-souris insectivores, conservation, habitat d 'alimentation, conservation, foraging habitat, insectivorous bats



Literature cited

Albert, A. and J. A. Anderson. 1984. On the existence of maximum likelihood estimates in logistic regression models. Biometrika 71:1–10. CrossRef
Barboza, P. S., S. D. Farley, and C. T. Robbins. 1997. Whole-body urea cycling and protein turnover during hyperphagia and dormancy in growing bears (Ursus americanus and U. arctos). Canadian Journal of Zoology 75:2129–2136. CrossRef
Black, H. L. 1972. Differential exploitation of moths by the bats Eptesicus fuscus and Lasiurus cinereus. Journal of Mammalogy 53:598–601. CrossRef
Brigham, R. M. 1991. Flexibility in foraging and roosting behaviour by the big brown bat (Eptesicus fuscus). Canadian Journal of Zoology 69:117–121. CrossRef
Coplen, T. B. 1996. New guidelines for reporting stable hydrogen, carbon, and oxygen isotope-ratio data. Geochimica et Cosmochimica Acta 60:3359–3360. CrossRef
Craig, H. 1953. The geochemistry of the stable carbon isotopes. Geochimica et Cosmochimica Acta 3:53–92. CrossRef
Cryan, P. M., M. A. Bogan, R. O. Rye, G. P. Landis, and C. L. Kester. 2004. Stable hydrogen isotope analysis of bat hair as evidence for seasonal molt and long distance migration. Journal of Mammalogy 85:995–1001. Abstract
Dawson, T. E., S. Mambelli, A. H. Plamboeck, P. H. Templer, and K. P. Tu. 2002. Stable isotopes in plant ecology. Annual Review of Ecology and Systematics 33:507–559. CrossRef, CSA
Denton, T. M., S. Schmidt, C. Critchley, and G. R. Stewart. 2001. Natural abundance of stable carbon and nitrogen isotopes in Cannabis sativa reflects growth conditions. Functional Plant Biology 28:1005–1012. CrossRef
Des Marais, D. J., J. M. Mitchell, W. G. Meinschen, and J. M. Hayes. 1980. The carbon isotope biogeochemistry of the individual hydrocarbons in bat guano and the ecology of the insectivorous bats in the region of Carlsbad, New Mexico. Geochimica et Cosmochimica Acta 44:2075–2086. CrossRef
Duchamp, J. E., D. W. Sparks, and J. O. Whitaker Jr. 2004. Foraging-habitat selection by bats at an urban–rural interface: Comparison between a successful and less successful species. Canadian Journal of Zoology 82:1157–1164. CrossRef
Ehleringer, J. R., T. E. Cerling, and B. R. Helliker. 1997. C4 photosynthesis, atmospheric CO2, and climate. Oecologia 112:285–299. CrossRef, CSA
Farquhar, G. D., M. H. O'Leary, and J. S. Berry. 1982. On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Australian Journal of Plant Physiology 9:121–137.
Farquhar, G. D. and R. A. Richards. 1984. Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Australian Journal of Plant Physiology 11:539–522.
Fleming, T. H. 1995. The use of stable isotopes to study the diets of plant-visiting bats. Symposium of the Zoological Society of London 67:99–110.
Fleming, T. H., R. A. Nuñez, and L. S. L. Sternberg. 1993. Seasonal changes in the diets of migrant and non-migrant nectarivorous bats as revealed by carbon stable isotope analysis. Oecologia 94:72–75. CrossRef, CSA
Gannes, L. Z., C. M. del Rio, and P. Koch. 1998. Natural abundance variations in stable isotopes and their potential uses in animal physiological ecology. Comparative Biochemistry and Physiology A 119:725–737. CrossRef, PubMed, CSA
Handley, L. L. and J. A. Raven. 1992. The use of natural abundance of nitrogen isotopes in plant physiology and ecology. Plant, Cell and Environment 15:965–985. CrossRef
Herrera, L. G., T. H. Fleming, and J. S. Findley. 1993. Geographic variation in carbon composition of the pallid bat, Antrozous pallidus, and its dietary implications. Journal of Mammalogy 74:601–606. CrossRef, CSA
Herrera, L. G., K. A. Hobson, A. Manzo, D. Estrada, V. Sánchez-Cordero, and G. Méndez. 2001a. The role of fruits and insects in the nutrition of frugivorous bats: Evaluating the use of stable isotope models. Biotropica 33:520–528. CSA
Herrera, L. G., K. A. Hobson, L. Mirón, N. Ramírez, G. Méndez, and V. Sánchez-Cordero. 2001b. Sources of protein in two species of phytophagous bats in a seasonal dry forest: Evidence from stable-isotope analysis. Journal of Mammalogy 82:352–361. Abstract, CSA
Herrera, L. G., E. Guitierrez, K. A. Hobson, B. Altube, and W. G. Diaz. 2002. Sources of assimilated protein in five species of New World frugivorous bats. Oecologia 133:280–287. CrossRef, CSA
Hobson, K. A. 1999. Tracing origins and migration of wildlife using stable isotopes: A review. Oecologia 120:314–326. CrossRef, CSA
Hobson, K. A., R. T. Alisauskas, and R. G. Clark. 1993. Stable-nitrogen isotope enrichment in avian tissues due to fasting and nutritional stress: Implications for isotopic analyses of diet. Condor 95:388–394. CrossRef, CSA
Hobson, K. A., H. L. Gibbs, and M. L. Gloutney. 1997. Preservation of blood and tissue samples for stable-carbon and stable-nitrogen isotope analysis. Canadian Journal of Zoology 75:388–394. CrossRef
Hobson, K. A. and S. G. Sealy. 1991. Marine protein contributions to the diet of Northern Saw-whet Owls on the Queen Charlotte Islands, British Columbia: A stable isotope approach. Auk 108:437–440. CSA
Jardine, T. D. and R. A. Cunjak. 2005. Analytical error in stable isotope ecology. Oecologia. DOI: 10.1007/s00442-005-0013-8. [URL] http://springerlink.com/link.asp?id=kr856p3h43270625.
Koopman, K. F. 1993. Order Chiroptera. Pages. 137–241. in D.E. Wilson & D.M. Reeder (eds.). Mammal Species of the World: A Taxonomic and Geographic Reference. Smithsonian Institution Press, Washington, DC.
Kramer, C. Y. 1956. Extensions of multiple range tests to group means with unequal number of replications. Biometrics 12:309–310. CrossRef
Kunz, T. H. 2004. Foraging habits of North American insectivorous bats. Pages. 12–25. in R.M. Brigham, E.K.V. Kalko, G. Jones, S. Parsons & H.J.G.A. Limpens (eds.). Bat Echolocation Research: Tools, Techniques, and Analysis. Bat Conservation International, Austin, Texas.
Kunz, T. H. and D. S. Reynolds. 2003. Bat colonies in buildings. Pages. 91–102. in T.J. O'Shea & M.A. Bogan (eds.). Monitoring Trends in Bat Populations of the United States and Territories: Problems and Prospects. US Geological Survey, Biological Sciences Division, Information and Technology Report, Washington, DC.
Kunz, T. H. and J. O. Whitaker Jr. 1983. An evaluation of fecal analysis for determining food habits of insectivorous bats. Canadian Journal of Zoology 61:1317–1321.
Kurta, A. and R. H. Baker. 1990. Eptesicus fuscus. Mammalian Species 356:1–10. CrossRef
Macko, S. A. and N. E. Ostrom. 1994. Pollution studies using stable isotopes. Pages. 45–62. in K. Lajtha & R.H. Michener (eds.). Stable Isotopes in Ecology. Blackwell Scientific Publications, Oxford.
Mariotti, A. 1984. Natural N-15 abundance measurements and atmospheric nitrogen standard calibration. Nature 311:251–252. CrossRef, CSA
McCutchan, J. M., W. M. Lewis, C. Kendall, and C. C. McGrath. 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–390. CrossRef, CSA
Mizutani, H., D. A. McFarlane, and Y. Kabaya. 1992a. Nitrogen and carbon isotope studies of a bat guano core from Eagle Creek Cave, Arizona, USA. Mass Spectrometry 40:57–65.
Mizutani, H., D. A. McFarlane, and Y. Kabaya. 1992b. Carbon and nitrogen isotopic signatures of bat guanos as a record of past environments. Mass Spectrometry 40:67–82.
Peterson, B. J. and B. Fry. 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18:293–320. CrossRef
Phillips, G. L. 1966. Ecology of the big brown bat (Chiroptera: Vespertiliondae) in northeastern Kansas. American Midland Naturalist 75:168–198. CrossRef
Policy Research Institute 2004. Kansas Statistical Abstract 2003. Climate. University of Kansas, Lawrence, Kansas.
Post, D. M. 2002. Using stable isotopes to estimate trophic position: Models, methods, and assumptions. Ecology 83:703–718. CSA
Roth, J. D. 2003. Variability in marine resources affects arctic fox population dynamics. Journal of Animal Ecology 72:668–676. CrossRef, CSA
Rubenstein, D. R. and K. A. Hobson. 2004. From birds to butterflies: Animal movement patterns and stable isotopes. Trends in Ecology and Evolution 19:256–263. CrossRef, PubMed
Shapiro, S. S. and M. B. Wilk. 1965. An analysis of variance test for normality (complete samples). Biometrika 52:591–611.
Spatial Climate Analysis Service 2004. Oregon State University. [URL] http://www.ocs.orst.edu/pub/maps/Precipitation/Total/States/KS/ks.gif (accessed 2 February 2004).
Stewart, G. R., M. H. Turnbull, S. Schmidt, and P. D. Erskine. 1995. C natural abundance in plant communities along a rainfall gradient: A biological integrator of water availability. Australian Journal of Plant Physiology 22:51–55.
Tieszen, L. L., M. M. Senyimba, S. K. Imbamba, and J. H. Troughton. 1979. The distribution of C3 and C4 grasses and carbon isotope discrimination along an altitudinal and moisture gradient in Kenya. Oecologia 37:337–350.
Tieszen, L. L., T. W. Boutton, K. G. Tesdahl, and N. A. Slade. 1983. Fractionation and turnover of stable carbon isotopes in animal tissues: Implications for δ13C analysis of diet. Oecologia 57:32–37. CrossRef, CSA
Townsend, M. A., D. P. Young, and S. A. Macko. 2003. Kansas case study applications of nitrogen-15 natural abundance method for identification of nitrate sources. Journal of Hazardous Substance Research 4:1–22.
Voigt, C. C. and F. Matt. 2004. Nitrogen stress causes unpredictable enrichments of 15N in two nectar-feeding bat species. Journal of Experimental Biology 207:1741–1748. CrossRef, PubMed
Voigt, C. C., F. Matt, R. H. Michener, and T. H. Kunz. 2003. Low turnover of carbon isotopes in tissues of two nectar-feeding bat species. Journal of Experimental Biology 206:1419–1427. CrossRef, PubMed, CSA
Whitaker Jr, J. O. 1993. Bats, beetles, and bugs. More big brown bats mean less agricultural pests. Bats 11:23.
Whitaker Jr, J. O. 1995. Food of the big brown bat, Eptesicus fuscus, from maternity colonies in Indiana and Illinois. American Midland Naturalist 134:346–360. CrossRef, CSA
Whitaker Jr, J. O. 2004. Prey selection in a temperate zone insectivorous bat community. Journal of Mammalogy 85:460–469. Abstract
Worthington Wilmer, J. and E. Barratt. 1996. A non-lethal method of tissue-sampling for genetic studies in chiropterans. Bat Research News 37:1–3.

Figure 1. Sites used for model development. a) A C3 forested site (Martin, Indiana) abutting C4 cropland (outside frame) and b) a C3/C4 site consisting of both C3 forest (20%) and C3/C4 crops (80%, Vigo, Indiana) are pictured. The third site (Hillsborough, New Hampshire) consists exclusively of C3 forest (not pictured).

Figure 2. Mean (± SE) signatures of each tissue type by site. Sample size is presented above δ15N signature bars and below δ13C signature bars. Letters above and below each signature bar indicate results of post hoc Tukey-Kramer HSD tests and are unique for each tissue type and signature. For example, the groupings above δ15N for feces present the results of a one-way ANOVA and HSD test between sites for that tissue type signature.

Figure 3. Least squares regressions of δ13C (a–d) and δ15N (e–h) of various tissue types against signatures of skin tissues with 95% confidence intervals. While each relationship is significant, the relationship between feces and skin is poorly predictive in the case of both a) carbon and e) nitrogen signatures. All other relationships are significant and highly predictive, as indicated by the Pearson product moment correlations. Legend: triangles, Martin County, Indiana; circles, Vigo County, Indiana; squares, Hillsborough County, New Hampshire.

Figure 4. Plot of δ15N versus δ13C for dataset used for model development. Hillsborough, NH can be distinguished from Martin and Vigo, IN based on δ13C signatures (Model 1; F2, 39 = 112.92, P < 0.0001) and Vigo, IN can be distinguished from Martin, IN and Hillsborough, NH based upon δ15N signatures (Model 2; F2, 39 = 97.06, P < 0.0001). Each site is indicative of a unique ecotype (Model 3; Wilk's λ = 0.032, F4, 76 = 87.02, P < 0.0001), and groups used in discriminant analysis do not overlap in each model developed.

Figure 5. Distributions and box plots (black squares represent outliers) of a) δ13C and b) δ15N signatures showing the continuous but non-normal distributions of both δ13C and δ15N (W = 0.945, P < 0 and W = 0.963, P < 0.0001, respectively). The dashed line bisecting each plot indicates the cutoff point for each univariate model categorization, as in equations 1.1–1.3 (a) and 2.1–2.3 (b). For example, equations 1.1–1.3 (a), bats with δ13C signatures greater than −22.82 ‰ are categorized as foragers in mixed C3/C4 habitat and those with signatures below this cutoff are categorized as foragers in C3 habitat.

Figure 6. Result of model application to dataset of samples from unknown ecogeographies by state, as per a) Model 1 (Equations 1.1–1.3), b) Model 2 (equations 2.1–2.3), and c) Model 3 (equations 3.1–3.3). The y-axis indicates the fraction of total samples from each state that were categorized as foragers in each habitat type. Sample sizes are presented below the state names in each panel (key for states: CO, Colorado; KA, Kansas; KY, Kentucky; MT, Montana; NE, Nebraska; NJ, New Jersey; NM, New Mexico; NY, New York; RI, Rhode Island; WI, Wisconsin).

table

Table I. Means and variation in δ13C and δ15N of skin tissue by state. This table provides sample size and mean δ13C and δ15N signatures with standard errors for each group applied to or included in our model (*: indicates states used for model development). If only one or two counties were sampled for a state, it is listed below the state. Where more than two counties were sampled, the total number of counties is given (most counties are available from the authors). Analyses of variance were conducted on both δ13C and δ15N and between states (found significant F12, 359 = 52.18, P < 0.0001; F12, 359 = 14.48, P < 0.0001, respectively). Groupings determined by post hoc Tukey-Kramer HSD tests are superscripted after the means of both δ13C and δ15N.

table

Table II. Summary of fecal analysis. “n” indicates the number of sampled individuals that had presence of an insect order in feces. Average % by volume indicates the percentage of the total feces of each insect order and includes all bat feces collected at each site. One-way analyses of variance were used to compare the three sites in terms of % consumption of Order Coleoptera and Order Hemiptera using data from fractions transformed by an arcsine square-root function. Post hoc Tukey-Kramer HSD tests indicated that Martin and Vigo, IN are significantly different from Hillsborough, NH. The site comparisons for all other insect Orders use Chi-Square analysis. (* P 0.05, **P 0.001, *** P 0.0001, ns = non significative).

table

Table III. Tukey-Kramer HSD tests of tissue signatures by site. Groups are results of Tukey-Kramer HSD test groupings. Groups are presented in increasing order of signature for both δ13C and δ15N as are tissue types within groups. Key for tissues: a, fecal matter; b, whole blood; c, hair; d, skin; e, plasma.

table

Table IV. Results of model application pooled across sites. δ13C and δ15N values represent averages of all bats categorized into each group by each model.

1 Author for correspondence.

2 Associate Editor: Don Thomas

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