Dietary composition of four common chiropteran species in a bottomland hardwood forest

• Autorzy: Weinkauf C.J. , Comer C.E. , Conway W.C. , Farrell C.
• Języki publikacji: EN

Abstrakty

EN

Understanding foraging habits can be important for elucidating the ecology of any species and for designing appropriate conservation strategies. Common methods for determining bat diets, such as morphological examination of fecal material or recovery of prey fragments under feeding roosts, can be biased towards larger prey with harder exoskeletons by underestimating frequency/occurrence of smaller, softer bodied prey items. Our objectives were to determine prey selection for several common chiropteran species of bottomland hardwood forests in east Texas and to evaluate the use of DNA barcoding for dietary studies by comparing dietary composition to prey availability in four species of bats. We amplified the cytochrome coxidase subunit 1 gene from fecal samples collected from 19 bats of four species and identified arthropods by comparison to the Barcode of Life Data System database. We compared frequency of occurrence in fecal samples to frequency in concurrent night-flying insect sampling. We identified nine insect species from three orders consumed by Perimyotis subflavus, nine species from four orders consumed by Lasiurus seminolus, seven species from three orders consumed by Nycticeius humeralis, and 11 species from two orders consumed by Lasiurus borealis. Coleoptera was the most abundant order available by biomass, but beetles were never found in fecal samples from L. seminolus (n = 5) or L. borealis (n = 7) bats. However, Coleoptera comprised a substantial portion of prey identified from P. subflavus (n = 2) and N. humeralis samples (n = 5). Lepidopteran prey items were found in 13 of 19 bat fecal samples across all species but represented < 7% of arthropod biomass. Although dipteran species were a negligible portion (< 1%) of the available biomass, large numbers of dipterans were identified in fecal samples from all species of bats (13 of 19 samples across all species). Lasiurus seminolus and L. borealis may be selecting prey based on digestibility rather than availability; whereas, both N. humeralis and P. subflavus exhibited a more opportunistic approach to foraging. Based on comparison to other studies of bat diets, traditional techniques for analyzing diet from fecal samples are likely underrepresenting soft-bodied arthropods like dipterans.

• Wydawca: -
• Czasopismo: Acta Chiropterologica
• Rocznik: 2018
• Tom: 20
• Numer: 1
• Opis fizyczny: p.195-205,fig.,ref.

Twórcy

autor

Weinkauf C.J.

• Arthur Temple College of Forestry and Agriculture, Stephen F. Austin State University, Box 6109, SFA Station, Nacogdoches, TX 75962, USA

autor

Comer C.E.

• Arthur Temple College of Forestry and Agriculture, Stephen F. Austin State University, Box 6109, SFA Station, Nacogdoches, TX 75962, USA

autor

Conway W.C.

• Arthur Temple College of Forestry and Agriculture, Stephen F. Austin State University, Box 6109, SFA Station, Nacogdoches, TX 75962, USA

autor

Farrell C.

• Old Sabine Bottom Wildlife Management Area, 21187 CR 4106, Lindale, TX 75771, USA

Bibliografia

• 1. Ammerman, L. K., C. L. Hice, and D. J. Schmidly. 2012. Bats of Texas. Texas A&M University Press, College Station, Texas, 305 pp. Google Scholar
• 2. Barclay, R. M. R., and R. M. Brigham. 1991. Constraints on optimal foraging theory: a field test of prey discrimination by echolocating insectivorous bats. Animal Behaviour, 48: 1013–1021. Google Scholar
• 3. Barclay, R. M. R., and R. M. Brigham. 1994. Prey detection, dietary niche breadth, and body size in bats: why are aerial insectivores so small? American Naturalist, 137: 693–703. Google Scholar
• 4. Barclay, R. M. R., M. Dolan, and A. Dyck. 1991. The digestive efficiency of insectivorous bats. Canadian Journal of Zoology, 69: 1853–1856. Google Scholar
• 5. Bennett, A. J. 2013. Floristic and structural analysis of a mature second-growth bottomland hardwood forest impacted by severe drought in northeastern Texas. M.Sci. Thesis, Stephen F. Austin State University, Nacogdoches, Texas, 254 pp. Google Scholar
• 6. Benson, D. A., I. Karsch-Mizrachi, D. J. Lipman, J. Ostell, and E. W. Sayers. 2009. GenBank. Nucleic Acids Research, 37 (Database Issue): D26–31. Google Scholar
• 7. Black, H. 1974. A north temperate bat community: structure and prey populations. Journal of Mammalogy, 55: 138–157. Google Scholar
• 8. Bohmann, K., A. Monadjem, C. L. Noer, M. Rasmussen, M. R. K. Zeale, E. Clare, G. Jones , E. Willerslev , and M. T. P. Gilbert. 2011. Molecular diet analysis of two African free-tailed bats (Molossidae) using high throughput sequencing. PLoS ONE, 6: e21441. Google Scholar
• 9. BOLD. 2013. Barcode of Life Data Systems. Available at www.boldsystems.org. Accessed 11 November 2013. Google Scholar
• 10. Brunet-Rossinni, A. K., and G. S. Wilkinson. 2009. Methods for age estimation and the study of senescence in bats. Pp. 315–325, in Ecological and behavioral methods for the study of bats, 2nd edition ( T. H. KUNZ and S. PARSONS, eds.). Johns Hopkins University Press, Baltimore, Maryland, 901 pp. Google Scholar
• 11. Carter, T. C., M. A. Menzel, D. M. Krishon, and J. Laerm. 1998. Prey selection by five species of vespertilionid bats on Sapelo Island, Georgia. Brimleyana, 25: 158–170. Google Scholar
• 12. Carter, T. C., M. A. Menzel, B. R. Chapman, and K. V. Miller. 2004. Partitioning of food resources by syntopic eastern red (Lasiurus borealis), Seminole (L. seminolus) and evening (Nycticeius humeralis) bats. American Midland Naturalist, 151: 186–191. Google Scholar
• 13. Clare, E. L. 2011. Cryptic species? Patterns of maternal and paternal gene flow in eight Neotropical bats. PLoS ONE, 6: e21460. Google Scholar
• 14. Clare, E. L., E. E. Fraser, H. E. Braid, B. Fenton, and P. D. N. Hebert. 2009. Species on the menu of a generalist predator, the eastern red bat (Lasiurus borealis): using a molecular approach to detect arthropod prey. Molecular Ecology, 18: 2532–2542. Google Scholar
• 15. Clare, E. L., B. K. Lim, M. B. Fenton, and P. D. N. Hebert. 2011. Neotropical bats: estimating species diversity with DNA barcodes. PLoS ONE, 6: e22648. Google Scholar
• 16. Covell, C. V., Jr. 2005. A field guide to moths of eastern North America. Virginia Museum of Natural History, Martinsville, 496 pp. Google Scholar
• 17. Diggs, G. M., Jr. , B. L. Lipscomb, and R. J. O'Keenon. 1999. Illustrated flora of north central Texas. Botanical Research Institute of Texas, Fort Worth, Texas, 1626 pp. Google Scholar
• 18. Dodd, L. E., M. J. Lacki, and L. K. Rieske. 2008. Variation in moth occurrence and implications for foraging habitat of Ozark big-eared bats. Forest Ecology and Management, 255: 3866–3872. Google Scholar
• 19. Dodd, L. E., E. G. Chapman, J. D. Harwood, M. J. Lacki, and L. K. Rieske. 2012. Identification of prey of Myotis septentrionalis using DNA-based techniques. Journal of Mammalogy, 93: 1119–1128. Google Scholar
• 20. Dodd, L. E., M. J. Lacki, D. R. Cox, and L. K. Rieske. 2014. Prey consumed by bats across central Appalachia prior to detection of white-nose syndrome. Journal of the Kentucky Academy of Science, 75: 85–93. Google Scholar
• 21. Duffy, J. E., B. J. Cardinale, K. E. France, P. B. McIntyre, E. Thébault, and M. LOREAU. 2007. The functional role of biodiversity in ecosystems: incorporating trophic complexity. Ecology Letters, 10: 522–538. Google Scholar
• 22. Feldhamer, G. A., J. O. Whitaker, Jr. J. K. Krejca, and S. J. Taylor. 1995. Food of the evening bat (Nycticeius humeralis) and red bat (Lasiurus borealis) from southern Illinois. Transactions of the Illinois State Academy of Science, 88: 139–143. Google Scholar
• 23. Feldhamer, G. A., T. C. Carter, and J. O. Whitaker, Jr. 2009. Prey consumed by eight species of insectivorous bats from southern Illinois. American Midland Naturalist, 162: 43–51. Google Scholar
• 24. Freeman, P. W. 1981. Correspondence of food habits and morphology in insectivorous bats. Journal of Mammalogy, 62: 166–173. Google Scholar
• 25. Hatherly, D. T. 1993. Soil survey of Smith County, Texas. U.S. Department of Agriculture - Soil Conservation Service, Washington, D.C., 173 pp. Available at https://www.nrcs.usda.gov/Internet/FSE_MANUSCRIPTS/texas/TX423/0/ Smith.pdf Google Scholar
• 26. Hebert, P. D. N., S. Ratnasingham, and J. R. DeWaard. 2003a. Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London, 270B: S96–S99. Google Scholar
• 27. Hebert, P. D. N., A. Cywinska, S. L. Ball, and J. R. DeWaard. 2003b. Biological identifications through DNA barcodes. Proceedings of the Royal Society of London, 270B: 313–321. Google Scholar
• 28. Hill, D. A., and F. Greenaway. 2005. Effectiveness of an acoustic lure for surveying bats in British woodlands. Mammal Review, 35: 116–112. Google Scholar
• 29. Johnson, J. S., and M. J. Lacki. 2013. Habitat associations of Rafinesque's big-eared bats (Corynorhinus rafinesquii) and their lepidopteran prey in bottomland hardwood forests. Canadian Journal of Zoology, 91: 94–101. Google Scholar
• 30. Jones, G. 1990. Prey selection by the greater horseshoe bat (Rhinolophus ferrumequinum): optimal foraging by echolocation. Journal of Animal Ecology, 59: 587–602. Google Scholar
• 31. Jones, G. 1997. Acoustic signals and speciation: the roles of natural and sexual selection in the evolution of cryptic species. Advances in the Study of Behavior, 26: 317–354. Google Scholar
• 32. Ketzler, L. P., C. E. Comer, and D. J. Twedt. 2017. Nocturnal insect availability in bottomland hardwood forests managed for wildlife in the Mississippi Alluvial Valley. Forest Ecology and Management, 391: 127–134. Google Scholar
• 33. Kunz, T. H. 1988. Methods of assessing the availability of prey to insectivorous bats. Pp. 191–210, in Ecological and behavioral methods for the study of bats ( T. H. KUNZ, ed.). Smithsonian Institution Press, Washington, D.C., 533 pp. Google Scholar
• 34. 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. Google Scholar
• 35. Lacki, M. J., and L. E. DODD. 2011. Diet and foraging behavior of Corynorhinus bats in eastern North America. Pp. 39–52, in Conservation and management of eastern big-eared bats: a symposium ( S. C. LOEB, M. J. LACKI, and D.A. MIL LER, eds.). General Technical Report, SRS-145, Asheville, NC. USDA Forest Service, Southern Research Station, 157 pp. Google Scholar
• 36. Lacki, M. J., S. K. Amelon, and M. D. Baker. 2007a. Foraging ecology of bats in forests. Pp. 83–127, in Bats in forests ( M. J. LACKI, J. P. HAYES, and A. KURTA, eds.). Johns Hopkins University Press, Baltimore, Maryland, 329 pp. Google Scholar
• 37. Lacki, M. J., J. S. Johnson, L. E. Dodd, and M. D. Baker. 2007b. Prey consumption of insectivorous bats in coniferous forests of north-central Idaho. Northwest Science, 81: 199–205. Google Scholar
• 38. McDonald, J. H. 2014. Handbook of biological statistics, 3rd edition. Sparky House Publishing, Baltimore, Maryland, 313 pp. Google Scholar
• 39. Muirhead-Thomson, R. C. 1991. Trap responses of flying insects: the influence of trap design on capture efficiency. Academic Press, London, UK, 287 pp. Google Scholar
• 40. NCDC [National Climatic Data Center]. 2011. 1981–2010 daily/monthly station normals, East Texas Regional Airport, Longview, Texas. National Climatic Data Center, National Oceanic and Atmospheric Administration. Available at http://climatexas.tamu.edu/norm/2011_longview.txt. Accessed 2 August 2016. Google Scholar
• 41. Paine, R. T. 1980. Food webs: linkage, interaction strength and community Infrastructure. Journal of Animal Ecology, 49: 666–685. Google Scholar
• 42. Pearson, W. R., and D. J. Lipman. 1988. Improved tools for biological sequence comparison. Proceedings of the National Academy of Sciences of the USA, 85: 2444–2448. Google Scholar
• 43. Ratnasingham, S., and P. D. N. Hebert. 2007. BOLD: the Barcode of Life Data System ( www.barcodinglife.org). Molecular Ecology Notes, 7: 355–364. Google Scholar
• 44. Razgour, O., E. L. Clare, M. R. K. Zeale, J. Hanmer, I. B. Schnell, M. Rasmussen, T. P. Gilbert, and G. Jones. 2011. High-throughput sequencing offers insight into mechanisms of resource partitioning in cryptic bat species. Ecology and Evolution, 1: 556–570. Google Scholar
• 45. Reichard, J. D., and T. H. Kunz. 2009. White-nose syndrome inflicts lasting injuries to the wings of little brown myotis (Myotis lucifugus). Acta Chiropterologica, 11: 457–464. Google Scholar
• 46. Ross, A. 1964. Ecological aspects of the food habits of some insectivorous bats. Ph.D. Thesis, University of Arizona, Tucson, 99 pp. Google Scholar
• 47. Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proceedings of the National Academy of Sciences of the USA, 74: 5463–5467. Google Scholar
• 48. Sayers, E. W., T. Barrett, D. A. Benson, S. H. Bryant, K. Canese, V. Chetvernin, D. M. Church, M. Dicuccio, R. Edgar, S. Federhen , et al. 2009. Database resources of the National Center for Biotechnology Information. Nucleic Acids Research, 37 (Database Issue): D5–15. Google Scholar
• 49. Sheppard, S. K., and J. D. Harwood. 2005. Advances in molecular ecology: tracking trophic links through predator-prey food-webs. Functional Ecology, 19: 751–762. Google Scholar
• 50. Sih, A., and B. Christensen. 2001. Optimal diet theory: when does it work, and when and why does it fail? Animal Behaviour, 61: 379–390. Google Scholar
• 51. Sikes, R. S., W. L. Gannon, and The Animal Care and Use Committee of The American Society of Mammalogists. 2011. Guidelines of the American society of mammalogists for the use of wild mammals in research. Journal of Mammalogy, 92: 235–253. Google Scholar
• 52. Uitenbroek, D. G. 1997. SISA binomial. Available at http://www.quantitativeskills.com/sisa/distributions/binomial.htm. Accessed 7 April 2015. Google Scholar
• 53. U.S. Fish and Wildlife Service. 2012. National white-nose syndrome decontamination protocol — version 06.25.2012. U.S. Fish and Wildlife Service, Washington, D.C., 5 pp. Available at https://www.fs.usda.gov/Internet/FSE_DOCUMENTS/stelprdb5378842.pdf Google Scholar
• 54. Verlinden, C., and R. H. Wiley. 1989. The constraints of digestive rate: an alternative model of diet selection. Evolutionary Ecology, 3: 264–273. Google Scholar
• 55. Vesterinen, E. J., T. Lilley, V. N. Laine, and N. Wahlberg. 2013. Next generation sequencing of fecal DNA reveals the dietary diversity of the widespread insectivorous predator Daubenton's bat (Myotis daubentonii) in southwestern Finland. PLoS ONE, 8: e82168. Google Scholar
• 56. Weinkauf, C. 2015. Bat community composition and prey availability in bottomland hardwood forests of east Texas. M.Sci. Thesis, Stephen F. Austin State University, Nacogdoches, Texas, 140 pp. Google Scholar
• 57. Whitaker, J. O., Jr. 1972. Food habits of bats from Indiana. Canadian Journal of Zoology, 50: 877–883. Google Scholar
• 58. Whitaker, J. O., Jr. 2004. Prey selection in a temperate zone insectivorous bat community. Journal of Mammalogy, 85: 460–469. Google Scholar
• 59. Whitaker, J. O., Jr. , C. F. McCracken, and B. M. Siemers. 2009. Methods for age estimation and the study of senescence in bats. Pp. 567–592, in Ecological and behavioral methods for the study of bats, 2nd edition ( T. H. KUNZ and S. PARSONS, eds.). Johns Hopkins University Press, Baltimore, Maryland, 901 pp. Google Scholar
• 60. Zaidi, R. H., Z. Jaal, N. J. Hawkes , J. Hemingway , and W. O. C. Symondson. 1999. Can multiple-copy sequences of prey DNA be detected amongst the gut contents of invertebrate predators? Molecular Ecology, 8: 2081–2087. Google Scholar
• 61. Zeale, M. R. K., R. K. Butlin, G. L. A. Barker, D. C. Lees, and G. Jones. 2011. Taxon-specific PCR for DNA barcoding arthropod prey in bat faeces. Molecular Ecology Resources, 11: 236–244.

Identyfikatory

DOI

10.3161/15081109ACC2018.20.1.015