, Volume 174, Issue 1, pp 55–65 | Cite as

Seasonal reliance on nectar by an insectivorous bat revealed by stable isotopes

  • Winifred F. Frick
  • J. Ryan Shipley
  • Jeffrey F. Kelly
  • Paul A. HeadyIII
  • Kathleen M. Kay
Physiological ecology - Original research


Many animals have seasonally plastic diets to take advantage of seasonally abundant plant resources, such as fruit or nectar. Switches from insectivorous diets that are protein rich to fruits or nectar that are carbohydrate rich present physiological challenges, but are routinely done by insectivorous songbirds during migration. In contrast, insectivorous bat species are not known to switch diets to consume fruit or nectar. Here, we use carbon stable isotope ratios to establish the first known case of a temperate bat species consuming substantial quantities of nectar during spring. We show that pallid bats (Antrozous pallidus) switch from a diet indistinguishable from that of sympatric insectivorous bat species in winter (when no cactus nectar is present) to a diet intermediate between those of insectivorous bats and nectarivorous bats during the spring bloom of a bat-adapted cactus species. Combined with previous results that established that pallid bats are effective pollinators of the cardon cactus (Pachycereus pringlei), our results suggest that the interaction between pallid bats and cardon cacti represents the first-known plant-pollinator mutualism between a plant and a temperate bat. Diet plasticity in pallid bats raises questions about the degree of physiological adaptations of insectivorous bats for incorporation of carbohydrate-rich foods, such as nectar or fruit, into the diet.


Antrozous pallidus Insectivory Mutualism Nectarivory Pachycereus pringlei 



We thank the subject editor, two anonymous reviewers and W. N. Heady for valuable advice and comments on earlier drafts. We thank R. Michener at the Boston University Stable Isotope Laboratory for analyzing breath samples and the University of Oklahoma Stable Isotope Laboratory for analyzing blood and tissue samples. M. Badillo, U. Huesca, K. Lopez, S. Montesinos, J. Sanchez, D. Solis, M. Torres, A. Corl, and A. Davis provided valuable assistance in the field. Funding for this project was provided by a University of California Institute for Mexico and the United States (UC MEXUS) faculty grant and two UC MEXUS small grants, a Mildred Mathias Award, and by the Central Coast Bat Research Group. W. F. F. was supported by the National Science Foundation (grants DBI-0905881 and DEB-1115895).

Supplementary material

442_2013_2771_MOESM1_ESM.docx (137 kb)
Supplementary material 1 (DOCX 137 kb)


  1. Afik D, Karasov WH (1995) The trade-offs between digestion rate and efficiency in warblers and their ecological implications. Ecology 76:2247–2257CrossRefGoogle Scholar
  2. Arita HT, Fenton MB (1997) Flight and echolocation in the ecology and evolution of bats. Trends Ecol Evol 12:53–58PubMedCrossRefGoogle Scholar
  3. Arizmendi MDC, Valiente-Banuet A, Rojas-Martinez A, Dávila-Aranda P (2002) Columnar cacti and the diets of nectar-feeding bats. In: Fleming TH, Valiente-Banuet A (eds) Columnar cacti and their mutualists. The University of Arizona Press, Tucson, pp 264–282Google Scholar
  4. Arkins AM, Winnington AP, Anderson S, Clout MN (1999) Diet and nectarivorous foraging behaviour of the short-tailed bat (Mystacina tuberculata). J Zool 247:183–187CrossRefGoogle Scholar
  5. Bell G (1982) Behavioral and ecological aspects of gleaning by a desert insectivorous bat Antrozous pallidus (Chiroptera: Vespertilionidae). Behav Ecol Sociobiol 10:217–223CrossRefGoogle Scholar
  6. Bond AL, Diamond AW (2011) Recent Bayesian stable-isotope mixing models are highly sensitive to variation in discrimination factors. Ecol Appl 21:1017–1023PubMedCrossRefGoogle Scholar
  7. Caut S, Angulo E, Courchamp F (2009) Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction. J Appl Ecol 46:443–453CrossRefGoogle Scholar
  8. Fleming TH (2002) Pollination biology of four species of Sonoran Desert columnar cacti. In: Fleming TH, Valiente-Banuet A (eds) Columnar cacti and their mutualists. The University of Arizona Press, Tucson, pp 207–224Google Scholar
  9. Fleming TH, Nuñez RA, Sternberg LDSL (1993) Seasonal changes in the diets of migrant and non-migrant nectarivorous bats as revealed by carbon stable isotope analysis. Oecologia 94:72–75CrossRefGoogle Scholar
  10. Fleming TH, Tuttle MD, Horner MA (1996) Pollination biology and the relative importance of nocturnal and diurnal pollinators in three species of Sonoran Desert columnar cacti. Southwest Nat 41:257–269Google Scholar
  11. Fleming TH, Sahley CT, Holland JN et al (2001) Sonoran Desert columnar cacti and the evolution of generalized pollination systems. Ecol Monogr 71:511–530CrossRefGoogle Scholar
  12. Frick WF, Heady PA III, Hayes JP (2009) Facultative nectar-feeding behavior in a gleaning insectivorous bat (Antrozous pallidus). J Mamm 90:1157–1164CrossRefGoogle Scholar
  13. Frick WF, Price RD, Heady PA III, Kay KM (2013) Insectivorous bat pollinates columnar cactus more effectively per visit than specialized nectar bat. Am Nat 181:137–144PubMedCrossRefGoogle Scholar
  14. Geluso KN (1975) Urine concentration cycles of insectivorous bats in the laboratory. J Comp Physiol B Biochem Syst Environ Physiol 99:309–319Google Scholar
  15. Geluso KN (1978) Urine concentrating ability and renal structure of insectivorous bats. J Mamm 59:312–323CrossRefGoogle Scholar
  16. Griffiths H (1992) Carbon isotope discrimination and the integration of carbon assimilation pathways in terrestrial CAM plants. Plant Cell Environ 15:1051–1062CrossRefGoogle Scholar
  17. Hatch KA (2002) The analysis of 13C/12C ratios in exhaled CO2: its advantages and potential application to field research to infer diet, changes in diet over time, and substrate metabolism in birds. Integr Comp Biol 42:21–33PubMedCrossRefGoogle Scholar
  18. Hermanson JW, O’Shea TJ (1983) Antrozous pallidus. Mamm Species 213:1–8CrossRefGoogle Scholar
  19. Hernandez A, Martínez del Rio C (1992) Intestinal disaccharides in five species of phyllostomoid bats. Comp Biochem Physiol Part B Comp Biochem 103:105–111CrossRefGoogle Scholar
  20. Herrera CM (1984) Adaptation to frugivory of Mediterranean avian seed dispersers. Ecology 65:609–617CrossRefGoogle Scholar
  21. Herrera LG (1999) Sugar composition of fruit and nectar and preferences of bats: causes and consequences. Acta Chiropterol 1:201–208Google Scholar
  22. Herrera LG, Martínez del Rio C (1998) Pollen digestion by New World bats: effects of processing time and feeding habits. Ecology 79:2828–2838Google Scholar
  23. Herrera LG, Fleming TH, Findley JS (1993) Geographic variation in carbon composition of the pallid bat (Antrozous pallidus) and its dietary implications. J Mamm 74:601–606CrossRefGoogle Scholar
  24. Herrera LG, Martínez del Rio C, Braun E, Hobson KA (2001a) Renal structure in neotropical bats: using stable isotopes to explore relationships between diet and morphology. Isotopes Environ Health Stud 37:1–11PubMedCrossRefGoogle Scholar
  25. Herrera LG, Hobson KA, Mirón MLL et al (2001b) Sources of protein in two species of phytophagous bats in a seasonal dry forest: evidence from stable-isotope analysis. J Mamm 82:352–361CrossRefGoogle Scholar
  26. Herrera LG, Gutierrez E, Hobson K et al (2002) Sources of assimilated protein in five species of New World frugivorous bats. Oecologia 133:280–287CrossRefGoogle Scholar
  27. Herrera LG, Hobson KA, Martínez JC, Méndez CG (2006) Tracing the origin of dietary protein in tropical dry forest birds. Biotropica 38:735–742CrossRefGoogle Scholar
  28. Horner MA, Fleming TH, Sahley CT (1998) Foraging behaviour and energetics of a nectar-feeding bat, Leptonycteris curasoae (Chiroptera: Phyllostomidae). J Zool 244:575–586CrossRefGoogle Scholar
  29. Karasov WH (1996) Digestive plasticity in avian energetics and feeding ecology. In: Carey C (ed) Avian energetics and nutritional ecology. Chapman and Hall, New York, pp 61–84CrossRefGoogle Scholar
  30. Kelly JF (2000) Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can J Zool-Rev Can Zool 78:1–27CrossRefGoogle Scholar
  31. Kelly JF, Bridge ES, Fudickar AM, Wassenaar LI (2009) A test of comparative equilibration for determining non-exchangeable stable hydrogen isotope values in complex organic materials. Rapid Commun Mass Spectrom 23:2316–2320PubMedCrossRefGoogle Scholar
  32. Levey DJ, Martínez del Rio C (2001) It takes guts (and more) to eat fruit: lessons from avian nutritional ecology. Auk 118:819Google Scholar
  33. McWilliams SR, Karasov WH (2001) Phenotypic flexibility in digestive system structure and function in migratory birds and its ecological significance. Comp Biochem Physiol A Mol Integr Physiol 128:577–591CrossRefGoogle Scholar
  34. McWilliams SR, Guglielmo C, Pierce B, Klaassen M (2004) Flying, fasting, and feeding in birds during migration: a nutritional and physiological ecology perspective. J Avian Biol 35:377–393CrossRefGoogle Scholar
  35. Mirón LL, Herrera LG, Ramírez N, Hobson KA (2006) Effect of diet quality on carbon and nitrogen turnover and isotopic discrimination in blood of a New World nectarivorous bat. J Exp Biol 209:541–548CrossRefGoogle Scholar
  36. Murphy ME (1996) Nutrition and metabolism. In: Carey C (ed) Avian energetics and nutritional ecology. Chapman and Hall, New York, pp 31–60CrossRefGoogle Scholar
  37. O’Leary MH (1981) Carbon isotope fractionation in plants. Phytochemistry 20:553–567CrossRefGoogle Scholar
  38. Paritte JM, Kelly JF (2009) Effect of cleaning regime on stable-isotope ratios of feathers in Japanese quail (Coturnix japonica). Auk 126:165–174CrossRefGoogle Scholar
  39. Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS One 5:e9672PubMedCentralPubMedCrossRefGoogle Scholar
  40. Parrish JD (2000) Behavioral, energetic, and conservation implications of foraging plasticity during migration. Stud Avian Biol 20:53–70Google Scholar
  41. Perkins SE, Speakman JR (2001) Measuring natural abundance of 13C in respired CO2: variability and implications for non-invasive dietary analysis. Funct Ecol 15:791–797CrossRefGoogle Scholar
  42. Pierce BJ, McWilliams SR (2005) Seasonal changes in composition of lipid stores in migratory birds: causes and consequences. Condor 107:269CrossRefGoogle Scholar
  43. Pyke GH, Pulliam HR, Charnov EL (1977) Optimal foraging: a selective review of theory and tests. Q Rev Biol 52:137–154CrossRefGoogle Scholar
  44. Racey PA (2009) Reproductive assessment of bats. In: Kunz TH, Parsons S (eds) Ecological and behavioral methods for the study of bats, 2nd edn. John Hopkins University Press, Baltimore, pp 249–264Google Scholar
  45. Ricklefs RE (1996) Avian energetics, ecology, and evolution. In: Carey C (ed) Avian energetics and nutritional ecology. Chapman and Hall, New York, pp 1–30CrossRefGoogle Scholar
  46. Rojas-Martínez A, Valiente-Banuet A, del Coro Arizmendi M et al (1999) Seasonal distribution of the long-nosed bat (Leptonycteris curasoae) in North America: does a generalized migration pattern really exist? J Biogeogr 26:1065–1077CrossRefGoogle Scholar
  47. Sharp Z (2007) Principles of stable isotope geochemistry. Pearson Prentice Hall, Upper Saddle RiverGoogle Scholar
  48. Shreve F (1951) The vegetation of the Sonoran Desert. Carnegie Inst Wash Publ 591:698–700Google Scholar
  49. Siemers BM, Greif S, Borissov I et al (2011) Divergent trophic levels in two cryptic sibling bat species. Oecologia 166:69–78PubMedCrossRefGoogle Scholar
  50. Simmons NB, Voss RS (2009) Collection, preparation, and fixation of bat specimens and tissues. In: Kunz TH, Parsons S (eds) Ecological and behavioral methods of the study of bats. John Hopkins University Press, Baltimore, pp 849–867Google Scholar
  51. Simmons NB, Seymour KL, Habersetzer J, Gunnell GF (2008) Primitive Early Eocene bat from Wyoming and the evolution of flight and echolocation. Nature 451:818–821PubMedCrossRefGoogle Scholar
  52. Smith BN, Epstein S (1971) Two categories of 13C/12C ratios for higher plants. Plant Physiol 47:380–384PubMedCentralPubMedCrossRefGoogle Scholar
  53. Stanley RG, Linskens HF (1974) Pollen: biology, biochemistry, management. Springer, BerlinCrossRefGoogle Scholar
  54. Team RDC (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  55. Tieszen LL, Boutton TW, Tesdahl KG, Slade NA (1983) Fractionation and turnover of stable carbon isotopes in animal tissues: implications for ∂13C analysis of diet. Oecologia 57:32–37CrossRefGoogle Scholar
  56. Voigt CC, Cruz-Neto A (2009) Energetic analysis of bats. In: Kunz TH, Parsons S (eds) Ecological and behavioral methods for the study of bats, 2nd edn. John Hopkins University Press, Baltimore, pp 623–645Google Scholar
  57. Voigt CC, Speakman JR (2007) Nectar-feeding bats fuel their high metabolism directly with exogenous carbohydrates. Funct Ecol 21:913–921CrossRefGoogle Scholar
  58. Voigt CC, Matt F, Michener R, Kunz TH (2003) Low turnover rates of carbon isotopes in tissues of two nectar-feeding bat species. J Exp Biol 206:1419–1427PubMedCrossRefGoogle Scholar
  59. Voigt CC, Baier L, Speakman JR, Siemers BM (2008a) Stable carbon isotopes in exhaled breath as tracers for dietary information in birds and mammals. J Exp Biol 211:2233–2238PubMedCrossRefGoogle Scholar
  60. Voigt CC, Rex K, Michener RH, Speakman JR (2008b) Nutrient routing in omnivorous animals tracked by stable carbon isotopes in tissue and exhaled breath. Oecologia 157:31–40PubMedCrossRefGoogle Scholar
  61. Voigt CC, Zubaid A, Kunz TH, Kingston T (2011) Sources of assimilated proteins in Old and New World phytophagous bats. Biotropica 43:108–113CrossRefGoogle Scholar
  62. Welch KC, Herrera LG, Suarez RK (2008) Dietary sugar as a direct fuel for flight in the nectarivorous bat Glossophaga soricina. J Exp Biol 211:310–316PubMedCrossRefGoogle Scholar
  63. Weyandt SE, Van Den Bussche RA (2007) Phylogeographic structuring and volant mammals: the case of the pallid bat (Antrozous pallidus). J Biogeogr 34:1233–1245CrossRefGoogle Scholar
  64. Wiggins IL (1980) Flora of Baja California, 1st edn. Stanford University Press, Palo AltoGoogle Scholar
  65. Wolf BO, Martínez del Rio C (2000) Use of saguaro fruit by white-winged doves: isotopic evidence of a tight ecological association. Oecologia 124:536–543CrossRefGoogle Scholar
  66. Wolf BO, Martínez del Rio C (2003) How important are columnar cacti as sources of water and nutrients for desert consumers? A review. Isotopes Environ Health Stud 39:53–67PubMedCrossRefGoogle Scholar
  67. Wolf BO, Martínez del Rio C, Babson J (2002) Stable isotopes reveal that saguaro fruit provides different resources to two desert dove species. Ecology 83:1286–1293CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Winifred F. Frick
    • 1
  • J. Ryan Shipley
    • 2
  • Jeffrey F. Kelly
    • 3
  • Paul A. HeadyIII
    • 4
  • Kathleen M. Kay
    • 1
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of California, Santa CruzSanta CruzUSA
  2. 2.Ecology and Evolutionary BiologyCornell UniversityIthacaUSA
  3. 3.Oklahoma Biological Survey and Department of BiologyUniversity of OklahomaNormanUSA
  4. 4.Central Coast Bat Research GroupAptosUSA

Personalised recommendations