An appetite for pests: Synanthropic insectivorous bats exploit cotton pest irruptions and consume various deleterious arthropods.
DNA metabarcoding
bats
conservation biological control
cotton pest
Journal
Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478
Informations de publication
Date de publication:
03 2020
03 2020
Historique:
received:
02
10
2019
revised:
11
02
2020
accepted:
14
02
2020
pubmed:
11
3
2020
medline:
2
3
2021
entrez:
11
3
2020
Statut:
ppublish
Résumé
Conservation biological control (CBC) seeks to minimize the deleterious effects of agricultural pests by enhancing the efficiency of natural enemies. Despite the documented potential of insectivorous bats to consume pests, many synanthropic bat species are still underappreciated as beneficial species. We investigated the diet of Kuhl's pipistrelle (Pipistrellus kuhlii), a common synanthropic insectivorous bat that forages in urban and agricultural areas, to determine whether it may function as a natural enemy in CBC. Faecal samples of P. kuhlii were collected throughout the cotton-growing season from five roost sites near cotton fields located in a Mediterranean agroecosystem, Israel, and analyzed using DNA metabarcoding. Additionally, data on estimated abundance of major cotton pests were collected. We found that the diet of P. kuhlii significantly varied according to sites and dates and comprised 27 species of agricultural pests that were found in 77.2% of the samples, including pests of key economic concern. The dominant prey was the widespread cotton pest, the pink bollworm, Pectinophora gossypiella, found in 31% of the samples and in all the roosts. Pink bollworm abundance was positively correlated with its occurrence in the bat diet. Furthermore, the bats' dietary breadth narrowed, while temporal dietary overlap increased, in relation to increasing frequencies of pink bollworms in the diet. This suggests that P. kuhlii exploits pink bollworm irruptions by opportunistic feeding. We suggest that synanthropic bats provide important pest suppression services, may function as CBC agents of cotton pests and potentially contribute to suppress additional deleterious arthropods found in their diet in high frequencies.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1185-1198Informations de copyright
© 2020 John Wiley & Sons Ltd.
Références
Aizpurua, O., Budinski, I., Georgiakakis, P., Gopalakrishnan, S., Ibañez, C., Mata, V., … Alberdi, A. (2018). Agriculture shapes the trophic niche of a bat preying on multiple pest arthropods across Europe: Evidence from DNA metabarcoding. Molecular Ecology, 27(3), 815-825. https://doi.org/10.1111/mec.14474
Alberdi, A., Aizpurua, O., Gilbert, M. T. P., & Bohmann, K. (2018). Scrutinizing key steps for reliable metabarcoding of environmental samples. Methods in Ecology and Evolution, 9(1), 134-147. https://doi.org/10.1111/2041-210X.12849
Ancillotto, L., Ariano, A., Nardone, V., Budinski, I., Rydell, J., & Russo, D. (2017). Effects of free-ranging cattle and landscape complexity on bat foraging: Implications for bat conservation and livestock management. Agriculture, Ecosystems and Environment, 241, 54-61. https://doi.org/10.1016/j.agee.2017.03.001
Ancillotto, L., Tomassini, A., & Russo, D. (2015). The fancy city life: Kuhl’s pipistrelle, Pipistrellus kuhlii, benefits from urbanisation. Wildlife Research, 42, 598-606.
Anderson, M. J., & Walsh, D. C. I. (2013). PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: What null hypothesis are you testing? Ecological Monographs, 83(4), 557-574.
Anderson, M. J., & Willis, T. (2003). Canonical analysis of principal coordinates: A useful method of constrained ordination for ecology. Ecology, 84, 511-525.
Anthony, E. L. P., & Kunz, T. H. (1977). Feeding strategies of the little brown bat, Myotis lucifugus, in southern New Hampshire. Ecology, 58(4), 775-786. https://doi.org/10.2307/1936213
Axelrod, M. (2014). Manipulating crop management to reduce pink bollworm (Pectinophora gossypiella) infestation and damage in cotton. M.Sc. Thesis. The Hebrew University of Jerusalem (in Hebrew with English abstract).
Barak, Y., & Yom-Tov, Y. (1987). The advantage of group hunting in Kuhl’s bat Pipistrellus kuhlii (Microchiroptera). Journal of Zoology, 219(59), 670-675.
Barbosa, P. (1998). Conservation biological control. San Diego, CA: Academic Press.
Bardou, P., Mariette, J., Escudié, F., Djemiel, C., & Klopp, C. (2014). Jvenn: An interactive Venn diagram viewer. BMC Bioinformatics, 15(1), 1-7. https://doi.org/10.1186/1471-2105-15-293
Beck, A. (1995). Fecal analysis of European bat species. Myotis, 32, 109-119.
Binladen, J., Gilbert, M. T. P., Bollback, J. P., Panitz, F., Bendixen, C., Nielsen, R., & Willerslev, E. (2007). The use of coded PCR primers enables high-throughput sequencing of multiple homolog amplification products by 454 parallel sequencing. PLoS ONE, 2(2), e197. https://doi.org/10.1371/journal.pone.0000197
Bohmann, K., Gopalakrishnan, S., Nielsen, M., Nielsen, L. D. S. B., Jones, G., Streicker, D. G., & Gilbert, M. T. P. (2018). Using DNA metabarcoding for simultaneous inference of common vampire bat diet and population structure. Molecular Ecology Resources, 18(5), 1050-1063. https://doi.org/10.1111/1755-0998.12891
Bohmann, K., Monadjem, A., Lehmkuhl Noer, C., Rasmussen, M., Zeale, M. R. K., Clare, E., … Gilbert, M. T. P. (2011). Molecular diet analysis of two African free-tailed bats (molossidae) using high throughput sequencing. PLoS ONE, 6(6), e21441. https://doi.org/10.1371/journal.pone.0021441
Boyles, J. G., Cryan, P. M., McCracken, G. F., & Kunz, T. K. (2011). Economic importance of bats in agriculture. Science, 332(6025), 41-42. https://doi.org/10.1126/science.1201366
Boyles, J. G., Sole, C. L., Cryan, P. M., & McCracken, G. F. (2013). On estimating the economic value of insectivorous bats: Prospects and priorities for biologists. In R. A. Adams, & S. C. Pedersen (Eds.), Bat evolution, ecology, and conservation. New York, NY: Springer Science.
CABI. (2020). Invasive species compendium. Wallingford, UK: CAB International. www.cabi.org/isc
Carøe, C., & Bohmann, K. (2020). Tagsteady: a metabarcoding library preparation protocol to avoid false assignment of sequences to samples. https://doi.org/10.1101/2020.01.22.915009
Carøe, C., Gopalakrishnan, S., Vinner, L., Mak, S. S. T., Sinding, M. H. S., Samaniego, J. A., … Gilbert, M. T. P. (2018). Single-tube library preparation for degraded DNA. Methods in Ecology and Evolution, 9(2), 410-419. https://doi.org/10.1111/2041-210X.12871
Chao, A., Gotelli, N. J., Hsieh, T. C., Sander, E. L., Ma, K. H., Colwell, R. K., & Ellison, A. M. (2014). Rarefaction and extrapolation with Hill numbers: A framework for sampling and estimation in species diversity studies. Ecological Monographs, 84(1), 45-67. https://doi.org/10.1890/13-0133.1
Chao, A., & Jost, L. (2012). Coverage-based rarefaction and extrapolation: Standardizing samples by completeness rather than size. Ecology, 93(12), 2533-2547.
Charbonnier, Y., Barbaro, L., Theillout, A., & Jactel, H. (2014). Numerical and functional responses of forest bats to a major insect pest in pine plantations. PLoS ONE, 9(10), e109488. https://doi.org/10.1371/journal.pone.0109488
Clare, E. L., Fraser, E. E., Braid, H. E., Fenton, M. B., & Hebert, P. D. N. (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(11), 2532-2542. https://doi.org/10.1111/j.1365-294X.2009.04184.x
Clare, E. L., Symondson, W. O. C., Broders, H., Fabianek, F., Fraser, E. E., MacKenzie, A., … Reimer, J. P. (2013). The diet of Myotis lucifugus across Canada: Assessing foraging quality and diet variability. Molecular Ecology, 23(15), 3618-3632. https://doi.org/10.1111/mec.12542
Clarke, K. R. (1993). Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology, 18(1), 117-143. https://doi.org/10.1111/j.1442-9993.1993.tb00438.x
Clarke, L. J., Soubrier, J., Weyrich, L. S., & Cooper, A. (2014). Environmental metabarcodes for insects: In silico PCR reveals potential for taxonomic bias. Molecular Ecology Resources, 14(6), 1160-1170. https://doi.org/10.1111/1755-0998.12265
Cleveland, C. J., Betke, M., Federico, P., Frank, J. D., Hallam, T. G., Horn, J., … Kunz, T. H. (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. https://doi.org/10.1890/1540-9295(2006)004[0238:EVOTPC]2.0.CO;2
Dhurua, S., & Gujar, G. T. (2011). Field-evolved resistance to Bt toxin Cry1Ac in the pink bollworm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae), from India. Pest Management Science, 67(8), 898-903. https://doi.org/10.1002/ps.2127
Ehler, L. E. (1998). Conservation biological control: Past, present and fututre. In P. Barbosa (Ed.), Conservation biological control (pp. 1-8). San Diego, CA: Academic.
Federico, P., Hallam, T. G., McCracken, G. F., Purucker, S. T., Grant, W. E., Correa-Sandoval, A. N., … Kunz, T. H. (2008). Brazilian free-tailed bats as insect pest regulators in transgenic and conventional cotton crops. Ecological Applications, 18(4), 826-837. https://doi.org/10.1890/07-0556.1
Feldman, R., Whitaker, J. O., & Yom-Tov, Y. (2000). Dietary composition and habitat use in a desert insectivorous bat community in Israel. Acta Chiropterologica, 2(1), 15-22.
Flaquer, C., Torre, I., & Ruiz-Jarillo, R. (2006). The value of bat-boxes in the conservation of Pipistrellus pygmaeus in wetland rice paddies. Biological Conservation, 128(2), 223-230. https://doi.org/10.1016/j.biocon.2005.09.030
Froidevaux, J. S. P., Boughey, K. L., Hawkins, C. L., Broyles, M., & Jones, G. (2019). Managing hedgerows for nocturnal wildlife: Do bats and their insect prey benefit from targeted agri-environment schemes? Journal of Applied Ecology, 1365-2664, 13412. https://doi.org/10.1111/1365-2664.13412
Galan, M., Pons, J. B., Tournayre, O., Pierre, É., Leuchtmann, M., Pontier, D., & Charbonnel, N. (2018). Metabarcoding for the parallel identification of several hundred predators and their prey: Application to bat species diet analysis. Molecular Ecology Resources, 18(3), 474-489. https://doi.org/10.1111/1755-0998.12749
Goiti, U., Vecin, P., Gario, I., Marta, S., & Aihartza, J. R. (2003). Diet and prey selection in Kuhl’s pipistrelle Pipistrellus kuhlii (Chiroptera: Vespertilionidae) in south-western Europe. Acta Theriologica, 48(4), 457-468.
Gurr, G. M., & You, M. (2016). Conservation biological control of pests in the molecular era: New opportunities to address old constraints. Frontiers in Plant Science, 6, 1-9. https://doi.org/10.3389/fpls.2015.01255
Haruvy, N., & Shlhevet, S. (2004). Optimal allocation of agricultural crops in the open spaces in Israel: Economic, financial and environmental considerations. Journal of Financial Management and Analysis, 17(2), 93-102.
Horowitz, A. R., Forer, G., & Ishaaya, I. (1994). Managing resistance in Bemisia tabaci in Israel with emphasis on cotton. Pesticide Science, 42(2), 113-122. https://doi.org/10.1002/ps.2780420208
Hsieh, T. C., Ma, K. H., & Chao, A. (2016). inext: An R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods in Ecology and Evolution, 7(12), 1451-1456. https://doi.org/10.1111/2041-210X.12613
Hutchison, W. D., Beasley, C. A., Henneberry, T. J., & Martin, J. M. (1988). Sampling pink bollworm (Lepidoptera: Gelechiidae) eggs: Potential for improved timing and reduced use of insecticides. Journal of Economic Entomology, 81, 673-678.
Ingram, W. R. (1995). Pectinophora gossypiella (Lepidoptera: Gelechiidae). In G. A. Matthews, & I. P. Tugstell (Eds.), Insect Pests of Cotton (pp. 107-149). Wallingford, Oxon: CAB International.
Juste, J., & Paunović, M. (2016). Pipistrellus kuhlii. The IUCN Red List of Threatened Species. e.T17314A22132946. Retrieved from https://www.iucnredlist.org/
Kahnonitch, I., Lubin, Y., & Korine, C. (2018). Insectivorous bats in semi-arid agroecosystems − effects on foraging activity and implications for insect pest control. Agriculture, Ecosystems and Environment, 261, 80-92. https://doi.org/10.1016/j.agee.2017.11.003
Korine, C., Niv, A., Axelrod, M., & Dahah, T. (2020). Species richness and activity of insectivorous bats in cotton fields in semi-arid agroecosystems. Mamalian Biology. https://doi.org/10.1007/s42991-019-00002-z
Korine, C., & Pinshow, B. (2004). Guild structure, foraging space use, and distribution in a community of insectivorous bats in the Negev Desert. Journal of Zoology, 262(2), 187-196. https://doi.org/10.1017/S0952836903004539
Krauel, J. J., Brown, V. A., Westbrook, J. K., & Mccracken, G. F. (2018). Predator - prey interaction reveals local effects of high - altitude insect migration. Oecologia, 186(1), 49-58. https://doi.org/10.1007/s00442-017-3995-0
Kruger, F., Clare, E. L., Symondson, W. O. C., Keiss, O., & Petersons, G. (2014). Diet of the insectivorous bat Pipistrellus nathusii during autumn migration and summer residence. Molecular Ecology, 23(15), 3672-3683. https://doi.org/10.1111/mec.12547
Kunz, T. H., Braun de Torrez, E., Bauer, D., Lobova, T., & Fleming, T. H. (2011). Ecosystem services provided by bats. Annals of the New York Academy of Sciences, 1223(1), 1-38. https://doi.org/10.1111/j.1749-6632.2011.06004.x
Lindell, C., Eaton, R. A., Howard, P. H., Roels, S. M., & Shave, M. E. (2018). Enhancing agricultural landscapes to increase crop pest reduction by vertebrates. Agriculture, Ecosystems and Environment, 257, 1-11. https://doi.org/10.1016/j.agee.2018.01.028
Lindgreen, S. (2012). AdapterRemoval: Easy cleaning of next-generation sequencing reads. BMC Research Notes, 5, https://doi.org/10.1186/1756-0500-5-337
López-Baucells, A., Rocha, R., & Fernández-Llamazares, Á. (2018). When bats go viral: Negative framings in virological research imperil bat conservation. Mammal Review, 48(1), 62-66. https://doi.org/10.1111/mam.12110
Maas, B., Karp, D. S., Bumrungsri, S., Darras, K., Gonthier, D., Huang, J.-C., … Williams-Guillén, K. (2016). Bird and bat predation services in tropical forests and agroforestry landscapes. Biological Reviews, 91(4), 1081-1101. https://doi.org/10.1111/brv.12211
Macgregor, C. J., Pocock, M. J. O., Fox, R., & Evans, D. M. (2015). Pollination by nocturnal Lepidoptera, and the effects of light pollution: A review. Ecological Entomology, 40(3), 187-198. https://doi.org/10.1111/een.12174
Maine, J. J., & Boyles, J. G. (2015). Bats initiate vital agroecological interactions in corn. Proceedings of the National Academy of Sciences, 112(40), 12438-12443. https://doi.org/10.1073/pnas.1505413112
Manor, S., & Hagali, Z. (2002). Survey on irrigation modernization. The Hefer Valley Water Users Association.
Matthews, G. A. (1989). Cotton insect pests and their management. Harlow, UK: Longman.
Maxinová, E., Kipson, M., Naďo, L., Hradická, P., & Uhrin, M. (2016). Foraging strategy of Kuhl’s Pipistrelle at the Northern Edge of the Species Distribution. Acta Chiropterologica, 18(1), 215-222. https://doi.org/10.3161/15081109ACC2016.18.1.012
McCracken, G. F., Westbrook, J. K., Brown, V. A., Eldridge, M., Federico, P., & Kunz, T. H. (2012). Bats track and exploit changes in insect pest populations. PLoS ONE, 7(8), https://doi.org/10.1371/journal.pone.0043839
Mercier, C., Boyer, F., Bonin, A., & Coissac, E. (2013). SUMARTA and SUMACLUST: fast and exact comparison and clustering of sequences. In Programs and Abstracts of the SeqBio 2013 workshop (pp. 27-29). https://doi.org/10.1109/RCIS.2013.6577673
Milonas, P., Gogou, C., Papadopoulou, A., Fountas, S., Liakos, V., & Papadopoulos, N. T. (2016). Spatio-temporal distribution of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) and Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae) in a cotton production area. Neotropical Entomology, 45(3), 240-251. https://doi.org/10.1007/s13744-015-0358-6
Mixão, V., Bravo Barriga, D., Parreira, R., Novo, M. T., Sousa, C. A., Frontera, E., … Almeida, A. P. G. (2016). Comparative morphological and molecular analysis confirms the presence of the West Nile virus mosquito vector, Culex univittatus, in the Iberian Peninsula. Parasites and Vectors, 9(1), 1-13. https://doi.org/10.1186/s13071-016-1877-7
Murray, D. C., Coghlan, M. L., & Bunce, M. (2015). From benchtop to desktop: Important considerations when designing amplicon sequencing workflows. PLoS ONE, 10(4), 1-21. https://doi.org/10.1371/journal.pone.0124671
Nsubuga, A. M., Robbins, M. M., Roeder, A. D., Morin, P. A., Boesch, C., & Vigilant, L. (2004). Factors affecting the amount of genomic DNA extracted from ape faeces and the identification of an improved sample storage method. Molecular Ecology, 13(7), 2089-2094. https://doi.org/10.1111/j.1365-294X.2004.02207.x
O’Bryan, C. J., Braczkowski, A. R., Beyer, H. L., Carter, N. H., Watson, J. E. M., & McDonald-Madden, E. (2018). The contribution of predators and scavengers to human well-being. Nature Ecology and Evolution, 2(2), 1-8. https://doi.org/10.1038/s41559-017-0421-2
Oerke, E. C. (2006). Crop losses to pests. Journal of Agricultural Science, 144(1), 31-43. https://doi.org/10.1017/S0021859605005708
Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., Mcglinn, D., … Oksanen, M. J. (2018). Package “vegan”.
Olimpi, E. M., & Philpott, S. M. (2018). Agroecological farming practices promote bats. Agriculture, Ecosystems and Environment, 265, 282-291. https://doi.org/10.1016/j.agee.2018.06.008
Pompanon, F., Deagle, B. E., Symondson, W. O. C., Brown, D. S., Jarman, S. N., & Taberlet, P. (2012). Who is eating what: Diet assessment using next generation sequencing. Molecular Ecology, 21(8), 1931-1950. https://doi.org/10.1111/j.1365-294X.2011.05403.x
Puig-Montserrat, X., Torre, I., López-Baucells, A., Guerrieri, E., Monti, M. M., Ràfols-García, R., … Flaquer, C. (2015). Pest control service provided by bats in Mediterranean rice paddies: Linking agroecosystems structure to ecological functions. Mammalian Biology, 80(3), 237-245. https://doi.org/10.1016/j.mambio.2015.03.008
Quetglas, J., Balvín, O., Lučan, R. K., & Benda, P. (2012). First records of the bat bug Cacodmus vicinus (Heteroptera: Cimicidae) from Europe and further data on its distribution. Vespertilio, 16, 243-248. https://doi.org/10.3846/16111699.2012.701229
Ratnasingham, S., & Hebert, P. D. N. (2007). BOLD: The Barcode of Life Data System (http://www.barcodinglife.org). Molecular Ecology Notes, 7(3), 355-364. https://doi.org/10.1111/j.1471-8286.2006.01678.x
Razgour, O., Clare, E. L., Zeale, M. R. K., Hanmer, J., Schnell, I. B., Rasmussen, M., … Jones, G. (2011). High-throughput sequencing offers insight into mechanisms of resource partitioning in cryptic bat species. Ecology and Evolution, 1(4), 556-570. https://doi.org/10.1002/ece3.49
Robinson, W. H. (2005). Handbook of urban insects and arachnids. Urban Insects and Arachnids. Cambridge, UK: Cambridge University Press. https://doi.org/10.1017/CBO9780511542718
Russo, D., Bosso, L., & Ancillotto, L. (2018). Novel perspectives on bat insectivory highlight the value of this ecosystem service in farmland: Research frontiers and management implications. Agriculture, Ecosystems and Environment, 266(July), 31-38. https://doi.org/10.1016/j.agee.2018.07.024
Schnell, I. B., Bohmann, K., & Gilbert, M. T. P. (2015). Tag jumps illuminated - reducing sequence-to-sample misidentifications in metabarcoding studies. Molecular Ecology Resources, 15(6), 1289-1303. https://doi.org/10.1111/1755-0998.12402
Serangeli, M. T., Cistrone, L., Ancillotto, L., Tomassini, A., & Russo, D. (2012). The post-release fate of hand-reared orphaned bats: Survival and habitat selection. Animal Welfare, 21(1), 9-18. https://doi.org/10.7120/096272812799129510
Sunderland, K., & Samu, F. (2000). Effects of agricultural diversification on the abundance, distribution, and pest control potential of spiders: A review. Entomologia Experimentalis Et Applicata, 95(1), 1-13. https://doi.org/10.1023/A:1003986225443
Swift, S. M., Racey, P. A., & Avery, M. I. (1985). Feeding ecology of Pipistrellus pipistrellus (Chiroptera: Vespertilionidae) during pregnancy and lactation. II. Diet. The Journal of Animal Ecology, 54, 217-225. https://doi.org/10.2307/4632
Symondson, W. O. C., Sunderland, K. D., & Greenstone, M. H. (2002). Can generalist predators be effective biocontrol agents? Annual Review Entomology, 47, 561-594. https://doi.org/10.1146/annurev.ento.47.091201.145240
Tabashnik, B. E., Dennehy, T. J., & Carriere, Y. (2005). Delayed resistance to transgenic cotton in pink bollworm. Proceedings of the National Academy of Sciences, 102(43), 15389-15393. https://doi.org/10.1073/pnas.0507857102
Taberlet, P., Coissac, E., Pompanon, F., Brochmann, C., & Willerslev, E. (2012). Towards next-generation biodiversity assessment using DNA metabarcoding. Molecular Ecology, 21(8), 2045-2050. https://doi.org/10.1111/j.1365-294X.2012.05470.x
Taylor, P. G. (1996). Reproducibility of ancient DNA sequences from extinct Pleistocene fauna. Molecular Biology and Evolution, 13(1), 283-285. https://doi.org/10.1093/oxfordjournals.molbev.a025566
Taylor, P. J., Grass, I., Alberts, A. J., Joubert, E., & Tscharntke, T. (2018). Economic value of bat predation services - A review and new estimates from macadamia orchards. Ecosystem Services, 30, 372-381. https://doi.org/10.1016/j.ecoser.2017.11.015
Tscharntke, T., Bommarco, R., Clough, Y., Crist, T. O., Kleijn, D., Rand, T. A., … Vidal, S. (2007). Conservation biological control and enemy diversity on a landscape scale. Biological Control, 43(3), 294-309. https://doi.org/10.1016/j.biocontrol.2007.08.006
Voigt, C. C., & Kingston, T. (2016). Bats in the Anthropocene: Conservation of bats in a changing world. Springer Open. https://doi.org/10.1007/978-3-319-25220-9
Whitaker, J. O. (1988). Food habits analysis of insectivorous bats. In T. H. Kunz, & S. Parsons (Eds.), Ecological and behavioral methods for the study of bats (pp. 171-190). Washington, DC: Smithsonian Institution Press.
Whitaker Jr., J. O., Shalmon, B., & Kunz, T. H. (1994). Food and feeding habits of insectivorous bats from Israel. Zeitschrift fur Saugetierkunde, 59(2), 74-81.
Zeale, M. R. K., Butlin, R. K., Barker, G. L. A., Lees, D. C., & Jones, G. (2011). Taxon-specific PCR for DNA barcoding arthropod prey in bat faeces. Molecular Ecology Resources, 11(2), 236-244. https://doi.org/10.1111/j.1755-0998.2010.02920.x
Zepeda-Mendoza, M. L., Bohmann, K., Carmona Baez, A., & Gilbert, M. T. P. (2016). DAMe: A toolkit for the initial processing of datasets with PCR replicates of double-tagged amplicons for DNA metabarcoding analyses. BMC Research Notes, 9(1), 1-13. https://doi.org/10.1186/s13104-016-2064-9