Diet determined by next generation sequencing reveals pest consumption and opportunistic foraging by bats in macadamia orchards in South Africa

• Autorzy: Taylor P.J. , Matamba E. , Steyn J.N. , Nangammbi T. , Zepeda-Mendoza M.L. , Bohmann K.
• Języki publikacji: EN

Abstrakty

EN

Recent studies have documented the economically significant impact of bats as predators of agricultural pest insects. We used Next Generation Sequencing (NGS) of the cytochrome oxidase I gene to elucidate the diet of six species of bats based on faecal pellets collected from individuals and roosts in macadamia orchards at Levubu, Limpopo Province, South Africa. For five of these species, we compared the molecular data with published results from microscopic analysis of faecal pellets, culled parts and stomach contents. We provide the first description of the molecular diet of the large African molossid bat, Mops midas. Expectations from skull morphology and a single limited study of stomach contents were that this species should be a beetle-specialist. However, NGS revealed that the diet of M. midas contained a much higher prevalence and diversity of lepidopteran (81 taxa from 17 families) compared to coleopteran (two taxa) prey. While this result is predicted by the allotonic frequency hypothesis for a bat species with low echolocation frequency, it could also be explained by unequal PCR amplification, a constraint of amplicon sequencing. Apart from the above-mentioned species where our sample was probably unbiased (24 pellets from multiple roosts and occasions), sample sizes of the other five species were very low and therefore potentially biased (1–6 pellets). Nevertheless, these samples revealed for each bat species surprisingly many prey taxa spanning several insect orders, indicating that individual bats were capable of consuming a wide diversity of prey during one or two nights of foraging. Contrary to expectations, bats of all foraging groups (clutter, clutteredge and open-air) fed opportunistically on mostly-flightless cockroaches (Order Blattodea). About one third of all faecal pellets tested from five species of bats of all foraging groups contained DNA from the significant macadamia pest species, Nezara viridula (Order Heteroptera), indicating the value of intact bat communities in the biological control of pest stink bugs in macadamia orchards. Contrary to the general expectations of the allotonic frequency hypothesis, all six bat species studied fed predominantly on tympanate versus non-tympanate species of moths (57–75% of lepidopteran prey taxa), even those ‘non-allotonic’ bat species having intermediate echolocation peak frequencies that encompass the frequency sensitivity of hearing (tympanate) moths.

• Wydawca: -
• Czasopismo: Acta Chiropterologica
• Rocznik: 2017
• Tom: 19
• Numer: 2
• Opis fizyczny: p.239-254,fig.,ref.

Twórcy

autor

Taylor P.J.

• SARChI Chair on Biodiversity Value and Change in the Vhembe Biosphere Reserve and Centre for Invasion Biology, School of Mathematical and Natural Sciences, University of Venda, P. Bag X5050, Thohoyandou 0950, Republic of South Africa
• School of Life Sciences, University of KwaZulu-Natal, Durban 4001, Republic of South Africa

autor

Matamba E.

• Department of Zoology, School of Natural and Mathematical Sciences, University of Venda, P. Bag X5050, Thohoyandou 0950, Republic of South Africa

autor

Steyn J.N.

• Department of Ecology and Resource Management, School of Environmental Sciences, University of Venda, P. Bag X5050, Thohoyandou 0950, Republic of South Africa

autor

Nangammbi T.

• Department of Zoology, School of Natural and Mathematical Sciences, University of Venda, P. Bag X5050, Thohoyandou 0950, Republic of South Africa
• Department of Nature Conservation, Faculty of Science, Tshwane University of Technology, P. Bag X680, Pretoria 0001, Republic of South Africa

autor

Zepeda-Mendoza M.L.

• Section for Evolutionary Genomics, Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Oster Voldgade 5-7, 1350 Copenhagen K, Denmark

autor

Bohmann K.

• Section for Evolutionary Genomics, Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Oster Voldgade 5-7, 1350 Copenhagen K, Denmark
• School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich NR4 7TJ, United Kingdom

Bibliografia

• 1. Acharya, L., and M. B. Fenton. 1999. Bat attacks and moth defensive behaviour around streetlights. Canadian Journal of Zoology, 77: 27–33. Google Scholar
• 2. Aldridge, H. D. J. N., and I. L. Rautenbach. 1987. Morphology, echolocation and resource partitioning in insectivorous Bats, Journal of Animal Ecology, 56: 763–778. Google Scholar
• 3. Archer, A. L. 1977. Results of the Winnifred T. Carter Expedition 1975 to Botswana, Mammals — Chiroptera. Botswana Notes and Records, 9: 145–154. Google Scholar
• 4. Aspetsberger, F., D. Brandsen, and D. S. Jacobs. 2003. Geographic variation in the morphology, echolocation and diet of the little free-tailed bat, Chaerephon pumilus (Molossidae). African Zoology, 38: 245–254. Google Scholar
• 5. Binladen, J., M. T. P. Gilbert, J. P. Bollback, F. Panitz, C. Bendixen, R. Nielsen, and E. Willerslev. 2007. The use of coded PCR primers enables high-throughput sequencing of multiple homolog amplification products by parallel sequencing. PLoS ONE, 2: e197. Google Scholar
• 6. 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
• 7. Bowie, R., D. J. Jacobs, and P. J. Taylor. 1999. Resource utilization by two morphologically similar insectivorous bats (Nycteris thebaica and Hipposideros coffer). South African Journal of Zoology, 34: 27–33. Google Scholar
• 8. Boyles, J. G., P. M. Cryan, G. F. McCracken, and T. H. Kunz. 2011. Economic importance of bats in agriculture. Science, 332: 41–42. Google Scholar
• 9. Campos, G. S., A. C. Bandeira, and S. L. Sardi. 2015. Zika virus outbreak, Bahia, Brazil. Emerging Infectious Diseases, 21: 1885–1886. Google Scholar
• 10. Caporaso, J. G., J. Kuczynski, J. Stombaugh, K. Bittinger, F. D. Bushman, E. K. Costello, N. Fierer, A. G. Peña, J. K. Goodrich, J. I. Gordon, et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7: 335–336. Google Scholar
• 11. Clark, F. L,. and Smart, A. C. 1991. The diet of Tadarida (Chaerephon) pumila (Cretzschmar), Molossidae, at Lake Naivasha, Kenya. Journal of African Zoology, 105: 493–496. Google Scholar
• 12. Clarke, L. J., J. Soubrier, L. S. Weyrich, and A. Cooper. 2014. Environmental metabarcodes for insects: in silico PCR reveals potential for taxonomic bias. Molecular Ecology Resources, 14: 1160–1170. Google Scholar
• 13. Cleveland, C. J., M. Betke, P. Federico, J. D. Frank, T. G. Hallam, J. Horn, J. D. López, Jr. , G. F. McCracken, R. A. Medellín, and A. Moreno-Valdez. 2006. Economic value of the pest control service provided by Brazilian free-tailed bats in South-Central Texas. Frontiers in Ecology and the Environment, 4: 238–243. Google Scholar
• 14. Edgar, R. C. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics, 26: 2460–2461. Google Scholar
• 15. Fenton, M. B, D. H. M. Cumming, I. L. Rautenbach, G. S. Comming, L. S. Cumming, G. Ford, D. R. Taylor, J. Dunlop, M. D. Hovorka, D. S. Johnston , et al. 1998. Bats and the loss of tree canopy in African woodlands. Conservation Biology, 12: 399–407. Google Scholar
• 16. Fenton, M. B., D. S. Jacobs, E. R. Richardson, P. J. Taylor, and W. White. 2004. Individual signatures in the frequency modulated sweep calls of African large-eared free-tailed bats (Otomops martiensseni) (Chiroptera: Molossidae). Journal of Zoology (London), 262: 11–19. Google Scholar
• 17. Folmer, O., M. Black, W. Hoeh, R. Lutz, and R. Vrijenhoek. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3: 294–299. Google Scholar
• 18. Jacobs, D. S. 2000. Community level support for the allotonic frequency hypothesis. Acta Chiropterologica, 2: 197–207. Google Scholar
• 19. Jacobs, D. S., and R. M. R. Barclay. 2009. Niche differentiation in two sympatric sibling bat species, Scotophilus dingami and Scotophilus mhlanganii. Journal of Mammalogy, 90: 879–887. Google Scholar
• 20. Jones, G., D. S. Jacobs, T. H., Kunz, M. R. Willig, and P. A. Racey. 2009. Carpe noctem: the importance of bats as bioindicators. Endangered Species Research, 8: 93–115. Google Scholar
• 21. Jones, V. P., and L. C. Caprio. 1994. Southern Stinkbug (Hemiptera: Pentatomidae) feeding on Hawaiian macadamia nuts: the relative importance of damage occurring in the canopy and on the ground. Journal of Economic Entomology, 87: 431–435. Google Scholar
• 22. Kunz, T. H., E. B. De Torrez, D. Bauer, T. Lobova, and T. H. Fleming. 2011. Ecosystem services provided by bats. Annals of the New York Academy of Sciences, 1223 (2011): 1–38. Google Scholar
• 23. Lindgreen, S. 2012. Adapter Removal: easy cleaning of next-generation sequencing reads. BMC Research Notes, 5: 337. Google Scholar
• 24. LaVal, R. K., and M. L. LaVal. 1980. Prey selection by slitfaced bat Nycteris thebaica (Chiroptera: Nycteridae) in Natal, South Africa. Biotropica, 12: 241–246. Google Scholar
• 25. Lopez-Hoffman, L., R. Wiederholt, C. Sansone, K. J. Bagstad, P. Cryan, J. E. Diffendorfer, J. Goldstein, K. Lasharr, J. Loomis, G. McCracken, et al. 2014. Market forces and technological substitutes cause fluctuations in the value of bat pest-control services for cotton. PLoS ONE, 9: e87912. Google Scholar
• 26. Maas, B., Y. Clough, and T. Tscharntke. 2013. Bats and birds increase crop yield in tropical agroforestry landscapes. Ecology Letters, 16: 1480–1487. Google Scholar
• 27. Maas, B., D. S. Karp, S. Bumrungsri, K. Darras, D. Gonthier, J. C. C. Huang, C. A. Lindell, J. Maine, L. Mestre, N. L. Michel, et al. 2015. Bird and bat predation services in tropical forests and agro forestry landscapes. Biological Reviews, 91: 1081–1101. Google Scholar
• 28. Maine, J. J., and J. G. Boyles. 2015. Bats initiate vital agroecological interactions in corn. Proceedings of the National Academy of Sciences of the USA, 112: 12438–12443. Google Scholar
• 29. McCracken, G. F., J. K. Westbrook, V. A. Brown, M. Eldridge, P. Federico, and T. H. Kunz. 2012. Bats track and exploit changes in insect pest populations. PLoS ONE, 7: e43839. Google Scholar
• 30. Meyer, M., and M. Kircher. 2010. Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harbor Protocols, 2010, pdb.prot 5448. Google Scholar
• 31. Monadjem, A., P. J. Taylor, M. C. Schoeman, and F. P. D. Cotterill. 2010. Bats of southern and central Africa: a biogeographic and taxonomic synthesis. Wits University Press, Johannesburg, 596 pp. Google Scholar
• 32. Mucina, L., and M. C. Rutherford. 2006. The vegetation of South Africa, Lesotho and Swaziland. Strelitzia, 19: 1–807. Google Scholar
• 33. Noer, C. L., T. Dabelsteen, K. Bohmann, and A. Monadjem. 2012. Molossid bats in an African agro-ecosystem select sugarcane fields as foraging habitat. African Zoology, 47: 1–11. Google Scholar
• 34. Piñol, J., G. Mir, P. Gomez-Polo, and N. Agustí. 2014. Universal and blocking primer mismatches limit the use of high-throughput DNA sequencing for the quantitative metabarcoding of arthropods. Molecular Ecology Resources, 15: 819–830. Google Scholar
• 35. Pocock, M. J. O., and N. Jennings. 2008. Testing biotic indicator taxa: the sensitivity of insectivorous mammals and their prey to the intensification of lowland agriculture. Journal of Applied Ecology, 45: 151–160. Google Scholar
• 36. Pompanon, F., B. E. Deagle, W. O. C. Symondson, D. S. Brown, S. N. Jarman, and P. Taberlet. 2012. Who is eating what: diet assessment using next generation sequencing. Molecular Ecology, 21: 1931–1950. Google Scholar
• 37. Ratnasingham, S., and P. D. N. Hebert. 2007. BOLD: The Barcode of Life Data System ( http://www.barcodinglife.org). Molecular Ecology Notes, 7: 355–364. Google Scholar
• 38. R Core Team. 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at http://www.R-project.org. Accessed 10 December 2013. Google Scholar
• 39. Rydell, J. 1992. Exploitation of insects around streetlamps in Sweden. Functional Ecology, 9:744–750. Google Scholar
• 40. Rydell, J., and D. W. Yalden. 1997. The diets of two high-flying bats from Africa. Journal of Zoology (London), 242: 69–76. Google Scholar
• 41. Schal, C., and R. Hamilton. 1990. Integrated suppression of synanthropic cockroaches. Annual Review of Entomology, 35: 521–551. Google Scholar
• 42. Schnell, I. B., K. Bohmann, and M. T. P. Gilbert. 2015. Tag jumps illuminated — reducing sequence-to-sample misidentifications in metabarcoding studies. Molecular Ecology Resources, 15: 1289–1303. Google Scholar
• 43. Schoeman, M. C. 2006. The relative influence of competition and coevolution on the community structure of insectivorous bats in southern Africa. Ph.D. Thesis, University of Cape Town, Cape Town, 142 pp. Google Scholar
• 44. Schoeman, M. C. 2008. The relative influence of competition and coevolution on the community structure of insectivorous bats in southern Africa. Ph.D. Thesis, University of Cape Town, Cape Town, PLoS ONE3(11): e3715. Google Scholar
• 45. Schoeman, M. C., and D. S. Jacobs. 2003. Support for the allotonic frequency hypothesis in an insectivorous bat community. Oecologia, 134: 154–162. Google Scholar
• 46. Schoeman, M. C., and D. S. Jacobs. 2011. The relative influence of competition and prey defences on the trophic structure of animalivorous bat ensembles. Oecologia, 166: 493–506. Google Scholar
• 47. Schoeman, P. S. 2009. Key biotic components of the indigenous Tortricidae and Heteroptera complexes occurring on macadamia in South Africa. Ph.D. Thesis, North West University, Potchefstroom, 165 pp. Google Scholar
• 48. Schoeman, P. S. 2013. Phytophagous stink bugs (Hemiptera: Pentatomidae; Coreidae) associated with macadamia in South Africa. Open Journal of Animal Sciences, 3: 179–183. Google Scholar
• 49. Schoeman, P. S. 2015. Are we beating the bugs. Subtrop Quarterly Journal, 11: 18–20. Google Scholar
• 50. Seamark, E. C. J., and W. Bogdanowicz. 2002. Feeding ecology of the common slit-faced bat in KwaZulu-Natal, South Africa. Acta Chiropterologica, 4: 49–54. Google Scholar
• 51. Sierra, A., and R. Arlettaz. 1997. Barbastelle bats (Barbastella spp.) specialize in the predation of moths: implications for foraging tactics and conservation. Acta Oecologica, 18: 91–106. Google Scholar
• 52. Taylor, P. J., D. Mkhari, T. Mukwevho, A. Monadjem, M. C. Schoeman, C. Schoeman, and J. N. Steyn. 2011. Bats as potential biocontrol agents in an agricultural landscape, Levubu Valley, Limpopo Province: diet, activity and species composition of bats in macadamia orchards and neighbouring natural habitats. Southern African Avocado Growers' Association Yearbook, 34: 51–61. Google Scholar
• 53. Taylor, P. J., P. Nemudivhiso, V. Mphethe, T. Murida, A. Monadjem, M. C. Schoeman, C. Schoeman, and J. N. Steyn. 2012. Bats as biocontrol agents in macadamia orchards, Levubu Valley, Limpopo Province: Results of a pilot project and future prospects. Southern African Macadamia Growers Association Yearbook, 20: 41–51. Google Scholar
• 54. Taylor, P. J., K. Bohmann, J. N. Steyn, M. C. Schoeman, E. Matamba, M. Zepeda-mendoza, T. Nangammbi, and M. T. P. Gilbert. 2013a. Bats eat pest green vegetable stinkbugs (Nezara viridula): diet analyses of seven insectivorous species of bats roosting and foraging in macadamia orchards at Levubu, Limpopo Province, South Africa. Southern African Macadamia Growers Association Yearbook, 21: 37–43. Google Scholar
• 55. Taylor, P. J., S. Sowler, M. C. Schoeman, and A. Monadjem. 2013b. Diversity of bats in the Soutpansberg and Blouberg Mountains of northern South Africa: complementarity of acoustic and non-acoustic survey methods. South African Journal of Wildlife Research, 43: 12–26. Google Scholar
• 56. Taylor, P. J., A. Monad jem, and J. N. Steyn. 2013c. Seasonal patterns of habitat use by insectivorous bats in a subtropical African agro-ecosystem dominated by macadamia orchards. African Journal of Ecology, 51: 552–561. Google Scholar
• 57. Taylor, P. J., I. Grass, A. J. Alberts, E. Joubert, and T. Tscharntke. In press. Economic value of bat predation services — a review and new estimates from macadamia orchards. Ecosystem Services. Google Scholar
• 58. Vincent, P. J., D. M. Westcott, N. N. Finson, and R. K. Nishimoto. 2001. Relationship between community structure and Southern green stink bug (Heteroptera: Pentatomidae) damage in macadamia nuts. Environmental Entomology, 30: 1028–1035. Google Scholar
• 59. Wanger, T. C., K. Darras, S. Bumrungsri, T. Tscharntke and A.-M. Klein. 2014. Bat pest control contributes to food security in Thailand. Biological Conservation, 171: 220–223. Google Scholar
• 60. Whitaker, J. O., Jr. , and H. Black. 1976. Food habits of cave bats from Zambia, Africa. Journal of Mammalogy, 57: 199–204. Google Scholar
• 61. Whitaker, J. O., Jr. , and T. H. Kunz. 1988. Food habits analysis of insectivorous bats. Pp. 171–189, in Ecological and behavioural methods for the study of bats ( T. H. Kunz, ed.). Smithsonian Institution Press, Washington, D.C., 533 pp. Google Scholar
• 62. Whitaker, J. O., Jr. , and R. E. Mumford. 1978. Foods and ectoparasites of bats from Kenya, East Africa. Journal of Mammalogy 59: 632–634 Google Scholar
• 63. Whitaker, J. O., Jr. , G. F. McCracken, and B. M. Siemers. 2009. Food habits analysis of insectivorous bats. Pp. 567–592, in Ecological and behavioral methods for the study of bats, 2nd edition ( T. H. Kunz and S. Parsons, eds.). The Johns Hopkins University Press, Baltimore, 920 pp. Google Scholar
• 64. Wickramasinge, L. P., S. Harris, G. Jones, and N. Vaughan. 2003. Bat activity and species richness on organic and conventional farms: impact of agricultural intensification. Journal of Applied Ecology, 40: 984–993. Google Scholar
• 65. Williams-Guillén, K., I. Perfecto, and J. Vandermeer. 2008. Bats limit insects in a Neotropical agroforestry ecosystem. Science, 320: 70. Google Scholar
• 66. Zeale, M. R. K., R. K. Butein, 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. Google Scholar
• 67. Zha, Y., Q. Chen, and C. Lei. 2009. Ultrasonic hearing ins moths. Annales de la Société Entomologique de France, 45: 145–156. Google Scholar

Identyfikatory

DOI

10.3161/15081109ACC2017.19.2.003