Diverse moth prey identified in the diet of the critically endangered southern bent-wing bat (Miniopterus orianae bassanii) using DNA metabarcoding of scats
Johanna G. Kuhne
A * , Jeremy J. Austin B , Terry B. Reardon C and Thomas A. A. Prowse D
+ Author Affiliations
- Author Affiliations
A School of Biological Sciences, The University of Adelaide, Adelaide, SA 5005, Australia.
B Australian Centre for Ancient DNA, School of Biological Sciences, University of Adelaide, Darling Building, North Terrace Campus, SA 5005, Australia.
C South Australian Museum, North Terrace, Adelaide, SA 5000, Australia.
D School of Mathematical Sciences, The University of Adelaide, Adelaide, SA 5005, Australia.
Wildlife Research 49(6) 571-582 https://doi.org/10.1071/WR21052
Submitted: 11 February 2021 Accepted: 25 January 2022 Published: 26 April 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing.
Abstract
Context: Globally, insectivorous bats are important moderators of insect populations, including agricultural pests. However, in human-modified environments, changes to insect diversity and abundance may have detrimental impacts on bat populations. The southern bent-wing bat (SBWB; Miniopterus orianae bassanii), is a critically endangered, cave-dwelling bat with a restricted distribution across south-eastern Australia, an area now dominated by agricultural land uses. Understanding SBWB diet may highlight the role of bats in influencing insect populations in surrounding agricultural land, while simultaneously providing crucial data for conservation management of this critically endangered species.
Aim: To investigate the SBWB’s diet using arthropod DNA metabarcoding of scats and guano collected from seven caves across the species’ range.
Methods: We collected scats from bat roosts and from guano piles on cave floors during late summer and early autumn of 2019. We used PCR to amplify two short, overlapping arthropod mtDNA cytochrome oxidase subunit 1 barcodes and sequenced these using the Illumina MiSeq to identify arthropod diet species.
Key results: Moths (order Lepidoptera) were the most prevalent insect identified in all samples and from all sites. Many of the 67 moth species identified were associated with agricultural land use (e.g. pasture webworm (Hednota pedionoma) and armyworm (Persectania dyscrita)), and several, including the bogong moth (Agrotis infusa), are migratory, suggesting the SBWB’s diet changes seasonally.
Conclusion: By describing the diet of the SBWB, we have fulfilled one recommendation of the national recovery plan for the species. The SBWB preys predominantly on moths, and its diet has likely been impacted by the increase in agricultural land use across its range. Further research is required to understand its foraging habitat requirements.
Implications: Our findings suggest the SBWB may play a role in controlling populations of moth species considered to be agricultural pests. The wide variety of moths consumed by SBWBs could afford the species some resilience to landscape changes affecting moth assemblages. The methodological framework developed here could be applied to investigate how land-use changes may contribute to bat population declines, but also how insectivorous bats may provide important ecosystem services by controlling pest insect species in modified landscapes.
Keywords: agriculture, bent-wing bats, Chiroptera, Miniopterus, molecular diet analysis, non-invasive sampling, pest invertebrates.
References
Aizpurua, O, Budinski, I, Georgiakakis, P, Gopalakrishnan, S, Ibañez, C, Mata, V, Rebelo, H, Russo, D, Szodoray-Parádi, F, Zhelyazkova, V, Zrncic, V, Gilbert, MTP, and 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, 815–825.| Agriculture shapes the trophic niche of a bat preying on multiple pest arthropods across Europe: evidence from DNA metabarcoding.Crossref | GoogleScholarGoogle Scholar | 29290102PubMed |
Andújar, C, Arribas, P, Yu, DW, Vogler, AP, and Emerson, BC (2018). Why the COI barcode should be the community DNA metabarcode for the Metazoa. Molecular Ecology 27, 3968–3975.
| Why the COI barcode should be the community DNA metabarcode for the Metazoa.Crossref | GoogleScholarGoogle Scholar | 30129071PubMed |
Arrizabalaga-Escudero, A, Garin, I, García-Mudarra, JL, Alberdi, A, Aihartza, J, and Goiti, U (2015). Trophic requirements beyond foraging habitats: the importance of prey source habitats in bat conservation. Biological Conservation 191, 512–519.
| Trophic requirements beyond foraging habitats: the importance of prey source habitats in bat conservation.Crossref | GoogleScholarGoogle Scholar |
Arulandhu, AJ, Staats, M, Hagelaar, R, Voorhuijzen, MM, Prins, TW, Scholtens, I, Costessi, A, Duijsings, D, Rechenmann, F, Gaspar, FB, Barreto Crespo, MT, Holst-Jensen, A, Birck, M, Burns, M, Haynes, E, Hochegger, R, Klingl, A, Lundberg, L, Natale, C, Niekamp, H, Perri, E, Barbante, A, Rosec, J-P, Seyfarth, R, Sovová, T, Van Moorleghem, C, van Ruth, S, Peelen, T, and Kok, E (2017). Development and validation of a multi-locus DNA metabarcoding method to identify endangered species in complex samples. GigaScience 6, 1–18.
| Development and validation of a multi-locus DNA metabarcoding method to identify endangered species in complex samples.Crossref | GoogleScholarGoogle Scholar | 29020743PubMed |
Australian Bureau of Agricultural and Resource Economics and Sciences (2017) ‘Catchment Scale Land Use of Australia – Secondary ALUM Classification – Update September 2017.’ (Australian Department of Agriculture and Water Resources: Canberra, ACT, Australia). Available at https://www.agriculture.gov.au/abares/aclump/land-use [Verified 7 January 2021]
Barnosky, AD, Matzke, N, Tomiya, S, Wogan, GOU, Swartz, B, Quental, TB, Marshall, C, McGuire, JL, Lindsey, EL, Maguire, KC, Mersey, B, and Ferrer, EA (2011). Has the Earth’s sixth mass extinction already arrived? Nature 471, 51–57.
| Has the Earth’s sixth mass extinction already arrived?Crossref | GoogleScholarGoogle Scholar | 21368823PubMed |
Bellati, J, Austin, AD, and Stevens, NB (2004). Arthropod diversity of a guano and non-guano cave at the Naracoorte Caves World Heritage Area, South Australia. Records of the South Australian Museum, Monograph Series 7, 257–265.
Bergstrom, BJ, and Smith, MT (2017). Bats as predominant food Items of nesting barred owls. Southeastern Naturalist 16, N1–N4.
| Bats as predominant food Items of nesting barred owls.Crossref | GoogleScholarGoogle Scholar |
Bilney, RJ, White, JG, and Cooke, R (2011). Reversed sexual dimorphism and altered prey base: the effect on sooty owl (Tyto tenebricosa tenebricosa) diet. Australian Journal of Zoology 599, 302.
| Reversed sexual dimorphism and altered prey base: the effect on sooty owl (Tyto tenebricosa tenebricosa) diet.Crossref | GoogleScholarGoogle Scholar |
Blanckenhorn, WU, Rohner, PT, Bernasconi, MV, Haugstetter, J, and Buser, A (2016). Is qualitative and quantitative metabarcoding of dung fauna biodiversity feasible? Environmental Toxicology and Chemistry 35, 1970–1977.
| Is qualitative and quantitative metabarcoding of dung fauna biodiversity feasible?Crossref | GoogleScholarGoogle Scholar | 26450644PubMed |
Bohmann, K, Gopalakrishnan, S, Nielsen, M, Nielsen, LSB, Jones, G, Streicker, DG, and Gilbert, MTP (2018). Using DNA metabarcoding for simultaneous inference of common vampire bat diet and population structure. Molecular Ecology Resources 18, 1050–1063.
| Using DNA metabarcoding for simultaneous inference of common vampire bat diet and population structure.Crossref | GoogleScholarGoogle Scholar |
Boyles, JG, and Storm, JJ (2007). The perils of picky eating: dietary breadth is related to extinction risk in insectivorous bats. PLoS One 2, e672.
| The perils of picky eating: dietary breadth is related to extinction risk in insectivorous bats.Crossref | GoogleScholarGoogle Scholar | 17653286PubMed |
Boyles, JG, Cryan, PM, McCracken, GF, and Kunz, TH (2011). Economic importance of bats in agriculture. Science 332, 41–42.
| Economic importance of bats in agriculture.Crossref | GoogleScholarGoogle Scholar | 21454775PubMed |
Braga, L, and Diniz, IR (2015). Importance of habitat heterogeneity in richness and diversity of moths (Lepidoptera) in Brazilian savanna. Environmental Entomology 44, 499–508.
| Importance of habitat heterogeneity in richness and diversity of moths (Lepidoptera) in Brazilian savanna.Crossref | GoogleScholarGoogle Scholar | 26313955PubMed |
Cardinal, BR, and Christidis, L (2000). Mitochondrial DNA and morphology reveal three geographically distinct lineages of the large bentwing bat (Miniopterus schreibersii) in Australia. Australian Journal of Zoology 48, 1–19.
| Mitochondrial DNA and morphology reveal three geographically distinct lineages of the large bentwing bat (Miniopterus schreibersii) in Australia.Crossref | GoogleScholarGoogle Scholar |
Clare, EL, Fraser, EE, Braid, HE, Fenton, MB, and Hebert, PDN (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.
| Species on the menu of a generalist predator, the eastern red bat (Lasiurus borealis): using a molecular approach to detect arthropod prey.Crossref | GoogleScholarGoogle Scholar | 19457192PubMed |
Clare, EL, Barber, BR, Sweeney, BW, Hebert, PDN, and Fenton, MB (2011). Eating local: influences of habitat on the diet of little brown bats (Myotis lucifugus). Molecular Ecology 20, 1772–1780.
| Eating local: influences of habitat on the diet of little brown bats (Myotis lucifugus).Crossref | GoogleScholarGoogle Scholar | 21366747PubMed |
Common IFB (1990) ‘Moths of Australia.’ (Melbourne University Press; Melbourne, Vic., Australia)
Corse, E, Tougard, C, Archambaud‐Suard, G, Agnèse, J-F, Messu mandeng, FD, Bilong bilong, CF, Duneau, D, Zinger, L, Chappaz, R, Xu, CCY, Meglécz, E, and Dubut, V (2019). One-locus-several-primers: a strategy to improve the taxonomic and haplotypic coverage in diet metabarcoding studies. Ecology and Evolution 9, 4603–4620.
| One-locus-several-primers: a strategy to improve the taxonomic and haplotypic coverage in diet metabarcoding studies.Crossref | GoogleScholarGoogle Scholar | 31031930PubMed |
Davidai, N, Westbrook, JK, Lessard, J-P, Hallam, TG, and McCracken, GF (2015). The importance of natural habitats to Brazilian free-tailed bats in intensive agricultural landscapes in the Winter Garden region of Texas, United States. Biological Conservation 190, 107–114.
| The importance of natural habitats to Brazilian free-tailed bats in intensive agricultural landscapes in the Winter Garden region of Texas, United States.Crossref | GoogleScholarGoogle Scholar |
Deiner, K, Bik, HM, Mächler, E, Seymour, M, Lacoursière‐Roussel, A, Altermatt, F, Creer, S, Bista, I, Lodge, DM, Vere, Nd, Pfrender, ME, and Bernatchez, L (2017). Environmental DNA metabarcoding: transforming how we survey animal and plant communities. Molecular Ecology 26, 5872–5895.
| 28921802PubMed |
Edwards, CE, Swift, JF, Lance, RF, Minckley, TA, and Lindsay, DL (2019). Evaluating the efficacy of sample collection approaches and DNA metabarcoding for identifying the diversity of plants utilized by nectivorous bats. Genome 62, 19–29.
| Evaluating the efficacy of sample collection approaches and DNA metabarcoding for identifying the diversity of plants utilized by nectivorous bats.Crossref | GoogleScholarGoogle Scholar | 30481069PubMed |
Ekrem, T, Willassen, E, and Stur, E (2007). A comprehensive DNA sequence library is essential for identification with DNA barcodes. Molecular Phylogenetics and Evolution 43, 530–542.
| A comprehensive DNA sequence library is essential for identification with DNA barcodes.Crossref | GoogleScholarGoogle Scholar | 17208018PubMed |
Fenton MB (1983) Predation and mortality. In ‘Just Bats’. (Ed MB Fenton) pp. 112–114. (University of Toronto Press: Toronto)
Forbes, RJ, Watson, SJ, O’Connor, E, Wescott, W, and Steinbauer, MJ (2019). Diversity and abundance of Lepidoptera and Coleoptera in multiple-species reforestation plantings to offset emissions of carbon dioxide. Australian Forestry 82, 89–106.
| Diversity and abundance of Lepidoptera and Coleoptera in multiple-species reforestation plantings to offset emissions of carbon dioxide.Crossref | GoogleScholarGoogle Scholar |
Fukui, D, and Agetsuma, N (2010). Seasonal change in the diet composition of the Asian parti-coloured bat Vespertilio sinensis. Mammal Study 35, 227–233.
| Seasonal change in the diet composition of the Asian parti-coloured bat Vespertilio sinensis.Crossref | GoogleScholarGoogle Scholar |
Galan, M, Pons, J-B, Tournayre, O, Pierre, É, Leuchtmann, M, Pontier, D, and 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, 474–489.
| Metabarcoding for the parallel identification of several hundred predators and their prey: application to bat species diet analysis.Crossref | GoogleScholarGoogle Scholar | 29288544PubMed |
Gordon, R, Ivens, S, Ammerman, LK, Fenton, MB, Littlefair, JE, Ratcliffe, JM, and Clare, EL (2019). Molecular diet analysis finds an insectivorous desert bat community dominated by resource sharing despite diverse echolocation and foraging strategies. Ecology and Evolution 9, 3117–3129.
| Molecular diet analysis finds an insectivorous desert bat community dominated by resource sharing despite diverse echolocation and foraging strategies.Crossref | GoogleScholarGoogle Scholar | 30962885PubMed |
Grant C (2004) ‘Radiotracking of Miniopterus schreibersii at Naracoorte, South Australia.’ (Department for Environment and Heritage: Mount Gambier, SA, Australia)
Green, K (2011). The transport of nutrients and energy into the Australian Snowy Mountains by migrating bogong moths Agrotis infusa. Austral Ecology 36, 25–34.
| The transport of nutrients and energy into the Australian Snowy Mountains by migrating bogong moths Agrotis infusa.Crossref | GoogleScholarGoogle Scholar |
Gregg, PC, Fitt, GP, Coombs, M, and Henderson, GS (1993). Migrating moths (Lepidoptera) collected in tower-mounted light traps in northern New South Wales, Australia: species composition and seasonal abundance. Bulletin of Entomological Research 83, 563–578.
| Migrating moths (Lepidoptera) collected in tower-mounted light traps in northern New South Wales, Australia: species composition and seasonal abundance.Crossref | GoogleScholarGoogle Scholar |
Holz, P, Hufschmid, J, Boardman, WSJ, Cassey, P, Firestone, S, Lumsden, LF, Prowse, TAA, Reardon, T, and Stevenson, M (2019). Does the fungus causing white-nose syndrome pose a significant risk to Australian bats? Wildlife Research 46, 657–668.
| Does the fungus causing white-nose syndrome pose a significant risk to Australian bats?Crossref | GoogleScholarGoogle Scholar |
Joseph, GS, Mauda, EV, Seymour, CL, Munyai, TC, Dippenaar-Schoeman, A, and Foord, SH (2018). Landuse change in savannas disproportionately reduces functional diversity of invertebrate predators at the highest trophic levels: spiders as an example. Ecosystems 21, 930–942.
| Landuse change in savannas disproportionately reduces functional diversity of invertebrate predators at the highest trophic levels: spiders as an example.Crossref | GoogleScholarGoogle Scholar |
Jusino, MA, Banik, MT, Palmer, JM, Wray, AK, Xiao, L, Pelton, E, Barber, JR, Kawahara, AY, Gratton, C, Peery, MZ, and Lindner, DL (2019). An improved method for utilizing high-throughput amplicon sequencing to determine the diets of insectivorous animals. Molecular Ecology Resources 19, 176–190.
| An improved method for utilizing high-throughput amplicon sequencing to determine the diets of insectivorous animals.Crossref | GoogleScholarGoogle Scholar | 30281913PubMed |
Kemp, J, López-Baucells, A, Rocha, R, Wangensteen, OS, Andriatafika, Z, Nair, A, and Cabeza, M (2019). Bats as potential suppressors of multiple agricultural pests: a case study from Madagascar. Agriculture, Ecosystems & Environment 269, 88–96.
| Bats as potential suppressors of multiple agricultural pests: a case study from Madagascar.Crossref | GoogleScholarGoogle Scholar |
Kolkert, H, Andrew, R, Smith, R, Rader, R, and Reid, N (2020). Insectivorous bats selectively source moths and eat mostly pest insects on dryland and irrigated cotton farms. Ecology and Evolution 10, 371–388.
| Insectivorous bats selectively source moths and eat mostly pest insects on dryland and irrigated cotton farms.Crossref | GoogleScholarGoogle Scholar | 31988733PubMed |
Kunz, TH, Braun de Torrez, E, Bauer, D, Lobova, T, and Fleming, TH (2011). Ecosystem services provided by bats. Annals of the New York Academy of Sciences 1223, 1–38.
| Ecosystem services provided by bats.Crossref | GoogleScholarGoogle Scholar | 21449963PubMed |
Lobo, J, Shokralla, S, Costa, MH, Hajibabaei, M, and Costa, FO (2017). DNA metabarcoding for high-throughput monitoring of estuarine macrobenthic communities. Scientific Reports 7, 15618.
| DNA metabarcoding for high-throughput monitoring of estuarine macrobenthic communities.Crossref | GoogleScholarGoogle Scholar | 29142319PubMed |
López-Roig, M, and Serra-Cobo, J (2014). Impact of human disturbance, density, and environmental conditions on the survival probabilities of pipistrelle bat (Pipistrellus pipistrellus) Population Ecology 56, 471–480.
| Impact of human disturbance, density, and environmental conditions on the survival probabilities of pipistrelle bat (Pipistrellus pipistrellus)Crossref | GoogleScholarGoogle Scholar |
Lumsden LF, Jemison ML (2015) National recovery plan for the southern bent-wing bat Miniopterus schreibersii bassanii. Department of Environment, Land, Water and Planning, Melbourne, Vic., Australia
Maine, JJ, and Boyles, JG (2015). Land cover influences dietary specialization of insectivorous bats globally. Mammal Research 60, 343–351.
| Land cover influences dietary specialization of insectivorous bats globally.Crossref | GoogleScholarGoogle Scholar |
Marquina, D, Andersson, AF, and Ronquist, F (2019). New mitochondrial primers for metabarcoding of insects, designed and evaluated using in silico methods. Molecular Ecology Resources 19, 90–104.
| New mitochondrial primers for metabarcoding of insects, designed and evaluated using in silico methods.Crossref | GoogleScholarGoogle Scholar | 30226026PubMed |
Maslo, B, Valentin, R, Leu, K, Kerwin, K, Hamilton, GC, Bevan, A, Fefferman, NH, and Fonseca, DM (2017). Chirosurveillance: the use of native bats to detect invasive agricultural pests. PLoS One 12, e0173321.
| Chirosurveillance: the use of native bats to detect invasive agricultural pests.Crossref | GoogleScholarGoogle Scholar | 28355216PubMed |
McCracken, GF, Westbrook, JK, Brown, VA, Eldridge, M, Federico, P, and Kunz, TH (2012). Bats track and exploit changes in insect pest populations. PLoS One 7, e43839.
| Bats track and exploit changes in insect pest populations.Crossref | GoogleScholarGoogle Scholar | 22952782PubMed |
McInnes, JC, Alderman, R, Deagle, BE, Lea, M-A, Raymond, B, and Jarman, SN (2017). Optimised scat collection protocols for dietary DNA metabarcoding in vertebrates. Methods in Ecology and Evolution 8, 192–202.
| Optimised scat collection protocols for dietary DNA metabarcoding in vertebrates.Crossref | GoogleScholarGoogle Scholar |
Merckx, T, Marini, L, Feber, RE, and Macdonald, DW (2012). Hedgerow trees and extended-width field margins enhance macro-moth diversity: implications for management. Journal of Applied Ecology 49, 1396–1404.
| Hedgerow trees and extended-width field margins enhance macro-moth diversity: implications for management.Crossref | GoogleScholarGoogle Scholar |
Mickleburgh, SP, Hutson, AM, and Racey, PA (2002). A review of the global conservation status of bats. Oryx 36, 18–34.
| A review of the global conservation status of bats.Crossref | GoogleScholarGoogle Scholar |
Moulds, T (2004). Review of Australian Cave Guano Ecosystems with a Checklist of Guano Invertebrates. Proceedings of the Linnean Society of New South Wales 125, 1.
Nash, MA, and Hoffmann, AA (2012). Effective invertebrate pest management in dryland cropping in southern Australia: The challenge of marginality. Crop Protection 42, 289–304.
| Effective invertebrate pest management in dryland cropping in southern Australia: The challenge of marginality.Crossref | GoogleScholarGoogle Scholar |
Pavey, CR, and Burwell, CJ (2005). Cohabitation and predation by insectivorous bats on eared moths in subterranean roosts. Journal of Zoology 265, 141–146.
| Cohabitation and predation by insectivorous bats on eared moths in subterranean roosts.Crossref | GoogleScholarGoogle Scholar |
Perović, D, Gámez-Virués, S, Börschig, C, Klein, A-M, Krauss, J, Steckel, J, Rothenwöhrer, C, Erasmi, S, Tscharntke, T, and Westphal, C (2015). Configurational landscape heterogeneity shapes functional community composition of grassland butterflies. Journal of Applied Ecology 52, 505–513.
| Configurational landscape heterogeneity shapes functional community composition of grassland butterflies.Crossref | GoogleScholarGoogle Scholar |
Piñol, J, Senar, MA, and Symondson, WOC (2019). The choice of universal primers and the characteristics of the species mixture determine when DNA metabarcoding can be quantitative. Molecular Ecology 28, 407–419.
| The choice of universal primers and the characteristics of the species mixture determine when DNA metabarcoding can be quantitative.Crossref | GoogleScholarGoogle Scholar | 29939447PubMed |
Put, JE, Mitchell, GW, and Fahrig, L (2018). Higher bat and prey abundance at organic than conventional soybean fields. Biological Conservation 226, 177–185.
| Higher bat and prey abundance at organic than conventional soybean fields.Crossref | GoogleScholarGoogle Scholar |
Ratnasingham, S, and Hebert, PDN (2007). BOLD: the Barcode of Life Data System (https://www.boldsystems.org/). Molecular Ecology Notes 7, 355–364.
| BOLD: the Barcode of Life Data System (https://www.boldsystems.org/).Crossref | https://www.boldsystems.org/).&journal=Molecular Ecology Notes&volume=7&pages=355-364&publication_year=2007&author=S%20Ratnasingham&hl=en&doi=10.1111/j.1471-8286.2007.01678.x" target="_blank" rel="nofollow noopener noreferrer" class="reftools">GoogleScholarGoogle Scholar | 18784790PubMed |
Rodhouse, TJ, Philippi, TE, Monahan, WB, and Castle, KT (2016). A macroecological perspective on strategic bat conservation in the U.S. National Park Service. Ecosphere 7, e01576.
| A macroecological perspective on strategic bat conservation in the U.S. National Park Service.Crossref | GoogleScholarGoogle Scholar |
Ruppert, KM, Kline, RJ, and Rahman, MS (2019). Past, present, and future perspectives of environmental DNA (eDNA) metabarcoding: a systematic review in methods, monitoring, and applications of global eDNA. Global Ecology and Conservation 17, e00547.
| Past, present, and future perspectives of environmental DNA (eDNA) metabarcoding: a systematic review in methods, monitoring, and applications of global eDNA.Crossref | GoogleScholarGoogle Scholar |
Russo, D, Bosso, L, and Ancillotto, L (2018). Novel perspectives on bat insectivory highlight the value of this ecosystem service in farmland: research frontiers and management implications. Agriculture, Ecosystems & Environment 266, 31–38.
| Novel perspectives on bat insectivory highlight the value of this ecosystem service in farmland: research frontiers and management implications.Crossref | GoogleScholarGoogle Scholar |
Salsamendi, E, Garin, I, Almenar, D, Goiti, U, Napal, M, and Aihartza, J (2008). Diet and prey selection in Mehelyi’s horseshoe bat Rhinolophus mehelyi (Chiroptera, Rhinolophidae) in the south-western Iberian Peninsula. Acta Chiropterologica 10, 279–286.
| Diet and prey selection in Mehelyi’s horseshoe bat Rhinolophus mehelyi (Chiroptera, Rhinolophidae) in the south-western Iberian Peninsula.Crossref | GoogleScholarGoogle Scholar |
Schloss, PD, Westcott, SL, Ryabin, T, Hall, JR, Hartmann, M, Hollister, EB, Lesniewski, RA, Oakley, BB, Parks, DH, Robinson, CJ, Sahl, JW, Stres, B, Thallinger, GG, Van Horn, DJ, and Weber, CF (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology 75, 7537–7541.
| Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities.Crossref | GoogleScholarGoogle Scholar | 19801464PubMed |
Stefanni, S, Stanković, D, Borme, D, De olazabal, A, Juretić, T, Pallavicini, A, and Tirelli, V (2018). Multi-marker metabarcoding approach to study mesozooplankton at basin scale. Scientific Reports 8, 12085.
| Multi-marker metabarcoding approach to study mesozooplankton at basin scale.Crossref | GoogleScholarGoogle Scholar | 30108256PubMed |
Swift, JF, Lance, RF, Guan, X, Britzke, ER, Lindsay, DL, and Edwards, CE (2018). Multifaceted DNA metabarcoding: validation of a noninvasive, next-generation approach to studying bat populations. Evolutionary Applications 11, 1120–1138.
| Multifaceted DNA metabarcoding: validation of a noninvasive, next-generation approach to studying bat populations.Crossref | GoogleScholarGoogle Scholar | 30026801PubMed |
Taylor, PJ, Matamba, E, Steyn, JN, Nangammbi, T, Zepeda-Mendoza, ML, and Bohmann, K (2017). Diet determined by next generation sequencing reveals pest consumption and opportunistic foraging by bats in macadamia orchards in South Africa. Acta Chiropterologica 19, 239–254.
| Diet determined by next generation sequencing reveals pest consumption and opportunistic foraging by bats in macadamia orchards in South Africa.Crossref | GoogleScholarGoogle Scholar |
Valtonen, A, Hirka, A, Szőcs, L, Ayres, MP, Roininen, H, and Csóka, G (2017). Long-term species loss and homogenization of moth communities in Central Europe. Journal of Animal Ecology 86, 730–738.
| Long-term species loss and homogenization of moth communities in Central Europe.Crossref | GoogleScholarGoogle Scholar |
Vasseur, C, Joannon, A, Aviron, S, Burel, F, Meynard, J-M, and Baudry, J (2013). The cropping systems mosaic: How does the hidden heterogeneity of agricultural landscapes drive arthropod populations? Agriculture, Ecosystems & Environment 166, 3–14.
| The cropping systems mosaic: How does the hidden heterogeneity of agricultural landscapes drive arthropod populations?Crossref | GoogleScholarGoogle Scholar |
Vestjens, W, and Hall, L (1977). Stomach contents of forty-two species of bats From the Australasian region. Wildlife Research 4, 25–35.
| Stomach contents of forty-two species of bats From the Australasian region.Crossref | GoogleScholarGoogle Scholar |
Warrant, E, Frost, B, Green, K, Mouritsen, H, Dreyer, D, Adden, A, Brauburger, K, and Heinze, S (2016). The Australian Bogong moth Agrotis infusa: a long-distance nocturnal navigator. Frontiers in Behavioral Neuroscience 10, 77.
| The Australian Bogong moth Agrotis infusa: a long-distance nocturnal navigator.Crossref | GoogleScholarGoogle Scholar | 27147998PubMed |
Weinstein, P, and Edwards, ED (1994). Troglophilic moths in Australia: first record of a self-sustaining population. Australian Journal of Entomology 33, 377–379.
| Troglophilic moths in Australia: first record of a self-sustaining population.Crossref | GoogleScholarGoogle Scholar |
Wilson DE, Mittermeier RA, Marti’nez-Vilalta A (2019) ‘Handbook of the Mammals of the World. Volume 9, Bats.’ (Lynx Edicons: Barcelona, Spain)
Zalucki, M, Daglish, G, Firempong, S, and Twine, P (1986). The biology and ecology of Heliothis armigera (Hubner) and Heliothis punctigera Wallengren (Lepidoptera, Noctuidae) in Australia – what do we know. Australian Journal of Zoology 34, 779–814.
| The biology and ecology of Heliothis armigera (Hubner) and Heliothis punctigera Wallengren (Lepidoptera, Noctuidae) in Australia – what do we know.Crossref | GoogleScholarGoogle Scholar |
Zeale, MRK, Butlin, RK, Barker, GLA, Lees, DC, and Jones, G (2011). Taxon-specific PCR for DNA barcoding arthropod prey in bat faeces. Molecular Ecology Resources 11, 236–244.
| Taxon-specific PCR for DNA barcoding arthropod prey in bat faeces.Crossref | GoogleScholarGoogle Scholar |
Zhang, GK, Chain, FJJ, Abbott, CL, and Cristescu, ME (2018). Metabarcoding using multiplexed markers increases species detection in complex zooplankton communities. Evolutionary Applications 11, 1901–1914.
| Metabarcoding using multiplexed markers increases species detection in complex zooplankton communities.Crossref | GoogleScholarGoogle Scholar | 30459837PubMed |
