Effective detection and identification of sheath-tailed bats of Australian forests and woodlands
K. N. Armstrong
A B C I , J. Broken-Brow D , G. Hoye E , G. Ford F , M. Thomas G and C. Corben H
+ Author Affiliations
- Author Affiliations
A Environment Institute, University of Adelaide, North Terrace, Adelaide, SA 5005, Australia.
B South Australian Museum, North Terrace, Adelaide, SA 5000, Australia.
C Specialised Zoological, Adelaide, SA 5000, Australia.
D School of Agriculture and Food Sciences, University of Queensland, Lawes, Qld 4343, Australia.
E Fly By Night Bat Surveys, PO Box 271, Belmont, NSW 2280, Australia.
F Balance! Environmental, PO Box 1744, Toowoomba, Qld 4350, Australia.
G Ecotone Flora Fauna Consultants, Weipa, Qld 4874, Australia.
H BatSense.
I Corresponding author. Email: kyle.armstrong@adelaide.edu.au
Australian Journal of Zoology - https://doi.org/10.1071/ZO20044
Submitted: 7 June 2020 Accepted: 5 August 2021 Published online: 15 September 2021
Abstract
Assessing the risk to threatened species of population decline from anthropogenic disturbances is challenging when there are issues with species identification, and little is known of their biology, distribution, population size, and habitat preference. The bare-rumped sheath-tailed bat (Saccolaimus saccolaimus) is one such species that has a poorly defined distribution over two broad areas of northern Australia. Environmental impact assessments are expected to consider the possibility of its presence in intervening areas outside the known distributions. Our study presents new empirical data that can assist with detection of S. saccolaimus across the entire expanse of northern Australia, provides a critical analysis of acoustics-based identification of the species, and assessed presence within the potentially high value habitat of tall Eucalyptus tetrodonta-dominated forest on the western side of Cape York Peninsula using a combination of trapping and acoustic recordings. Capture of other Saccolaimus species was the greatest of any survey conducted to date in Australia, demonstrating that the capture of these high-flying bat species in tall forest habitats can be relatively effective with mist net arrays hoisted into the tree canopy. In addition, reference echolocation call collections from the focal trapping area plus other locations across northern Australia allowed characterisation and comparison of the calls of most low-frequency-emitting (LFE) echolocating bat species of northern Australia. In addition to separation of species-specific search phase call types using multivariate statistics, a compilation of features from search phase, approach phase and feeding buzz echolocation calls will help distinguish S. saccolaimus from most other LFE species. However, the similarity of the echolocation calls of S. mixtus and S. saccolaimus prevented them from being distinguished from one another. A multi-method approach that emulates the present study and incorporates our recommendations and cautions will lead to robustness in ecological studies and greater clarity in environmental impact assessments.
Keywords: threatened species, Saccolaimus, sheathtail, echolocation, bat detector, forest bat, harmonics, classification.
References
Andreassen, T., Surlykke, A., and Hallam, J. (2014). Semi-automatic long-term acoustic surveying: a case study with bats. Ecological Informatics 21, 13–24.| Semi-automatic long-term acoustic surveying: a case study with bats.Crossref | GoogleScholarGoogle Scholar |
Armstrong, K. N. (2017). Bats. In ‘Biodiversity Assessment of the PNG LNG Upstream Project Area, Southern Highlands and Hela Provinces, Papua New Guinea’. (Ed. S. J. Richards.) pp. 209–254. (ExxonMobil PNG Limited: Port Moresby.)
Armstrong, K. N., Novera, J., and Aplin, K. P. (2015a). Acoustic survey of the echolocating bats of Manus Island and Mussau Island, Papua New Guinea. In ‘A Rapid Biodiversity Survey of Papua New Guinea’s Manus and Mussau Islands’. (Ed. N. Whitmore.) pp. 69–85. (Wildlife Conservation Society Papua New Guinea Program: Goroka, Papua New Guinea.)
Armstrong, K. N., Aplin, K. P., and Lamaris, J. S. (2015b). Bats. In ‘A Rapid Biodiversity Assessment of Papua New Guinea’s Hindenburg Wall Region’. (Eds S. J. Richards and N. Whitmore.) pp. 166–180. (Wildlife Conservation Society Papua New Guinea Program: Goroka, Papua New Guinea.)
Atlas of Living Australia (2020). OZCAM records of Saccolaimus saccolaimus. Available at: http://ozcam.org.au/ [accessed 9 May 2020].
Barclay, R. M. (1983). Echolocation calls of emballonurid bats from Panama. Journal of Comparative Physiology 151, 515–520.
| Echolocation calls of emballonurid bats from Panama.Crossref | GoogleScholarGoogle Scholar |
Binary Acoustic Technology (2014). SCAN’R™ Snapshot Characterization and Analysis software manual version 1.8 (Binary Acoustic Technology LLC). Available at: http://binaryacoustictech.com/batpages_files/scanr.htm
Churchill, S. K. (2008). ‘Australian Bats.’ (Allen & Unwin: Sydney.)
Coles, R. B., and Lumsden, L. (1993). Report on the survey of bats in the Heathlands area of Cape York Peninsula. Cape York Peninsula Scientific Expedition Wet Season 1992 Report, Volume 2. The Royal Geographical Society of Queensland, Inc.
Coles, R., Britton, A., Boonman, A., and Clague, C. (2012). Discovery of a highly unusual alternating call frequency pattern used by the echolocating emballonurid bat Saccolaimus saccolaimus during foraging. Oral presentation at the 15th Australasian Bat Society Conference, Melbourne, Australia, 11–13 April 2012. The Australasian Bat Society Newsletter 38, 35–36. Available at: http://ausbats.org.au/abs-newsletters/4553514675
Coles, R., Lane, D., and Kovachev, I. (2014). Echolocation ecology and distribution of the bare-rumped sheathtail bat Saccolaimus saccolaimus: the Bornean–Australian connection. Oral presentation at the 16th Australasian Bat Society Conference 22–25 April 2014, Townsville, Queensland. The Australasian Bat Society Newsletter 42, 33. Available at: http://ausbats.org.au/abs-newsletters/4553514675
Commonwealth of Australia (2012). Interim Biogeographic Regionalisation for Australia, Version 7. Map produced by ERIN, Australian Government Department of the Environment and Energy, Canberra, October 2016. Available at: https://www.environment.gov.au/land/nrs/science/ibra/australias-bioregions-maps
Corben, C. (2010). Acoustic identification of Saccolaimus. Oral presentation at the 14th Australasian Bat Society conference, Darwin, Northern Territory, 12–14 July 2010. The Australasian Bat Society Newsletter 35, 26. Available at: http://ausbats.org.au/abs-newsletters/4553514675
Corben, C. (2011). Bat calls of Borneo. Available at: http://users.lmi.net/corben/BatsOfBorneo.htm#Bat%20Calls%20of%20Borneo
DEWHA (2010). Survey guidelines for Australia’s threatened bats. Guidelines for detecting bats listed as threatened under the Environment Protection and Biodiversity Conservation Act 1999. Department of the Environment, Water, Heritage and the Arts, Canberra. Available at: http://www.environment.gov.au/resource/survey-guidelines-australias-threatened-bats-guidelines-detecting-bats-listed-threatened
Ford, G., Thomson, B., and Macdonald, S. (2012). The ongoing challenge of characterising the echolocation calls of a rare tropical bat. Oral presentation at the 15th Australasian Bat Society Conference, Melbourne, Australia, 11–13 April 2012. The Australasian Bat Society Newsletter 38, 35. Available at: http://ausbats.org.au/abs-newsletters/4553514675
Fox, J., and Weisberg, S. (2019). ‘An R Companion to Applied Regression.’ 3rd edn. [R package car version 3.0–7] (Sage: Thousand Oaks, CA.)
Gannon, W. L., O’Farrell, M. J., Corben, C., and Bedrick, E. J. (2004). Call character lexicon and analysis of field recorded bat echolocation calls. In ‘Echolocation in Bats and Dolphins’. (Eds J. A. Thomas, C. F. Moss and M. Vater.) pp. 478–484. (University of Chicago Press: Chicago.)
Hall, T. A. (1999). Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.
Hall, L., Thomson, B. G., and Milne, D. J. (2008). Bare-rumped sheath-tailed bat Saccolaimus saccolaimus. In ‘Mammals of Australia’ 3rd edn. (Eds S. Van Dyck and R. Strahan.) pp. 475–476. (Australian Museum: Sydney.)
Hill, D. A., Armstrong, K. N., and Barden, P. A. (2015). Preliminary assessment suggests that acoustic lures can increase capture rates of Australian echolocating bats. Australian Mammalogy 37, 104–106.
| Preliminary assessment suggests that acoustic lures can increase capture rates of Australian echolocating bats.Crossref | GoogleScholarGoogle Scholar |
Jackson, S. M., and Groves, C. P. (2015). ‘Taxonomy of Australian Mammals.’ (CSIRO Publishing: Victoria.)
Jung, K., Kalko, E. A. V., and Von Helversen, O. (2007). Echolocation calls in Central American emballonurid bats: signal design and call frequency alternation. Journal of Zoology 272, 125–137.
| Echolocation calls in Central American emballonurid bats: signal design and call frequency alternation.Crossref | GoogleScholarGoogle Scholar |
Kale, E., Armstrong, K. N., Amick, P., and Woxvold, I. A. (2018a). Chapter 1.6. Mammals of the Wau Creek proposed Wildlife Management Area, Gulf Province, Papua New Guinea. In ‘Rapid Biological Assessments of Wau Creek, Uro Creek and Lake Kutubu: Documenting Biodiversity Values to Promote Forest Conservation in the Kikori River basin, Papua New Guinea’. (Ed. S. J. Richards.) pp. 125–151. (ExxonMobil PNG Limited: Port Moresby.)
Kale, E., Armstrong, K. N., Amick, P., and Woxvold, I. A. (2018b). Chapter 2.6. Mammals of the Uro Creek catchment, Gulf Province, Papua New Guinea. In ‘Rapid Biological Assessments of Wau Creek, Uro Creek and Lake Kutubu: Documenting Biodiversity Values to Promote Forest Conservation in the Kikori River basin, Papua New Guinea’. (Ed. S. J. Richards.) pp. 245–270. (ExxonMobil PNG Limited: Port Moresby.)
Kale, E., Armstrong, K. N., Amick, P., and Woxvold, I. A. (2018c). Chapter 3.6. Mammals of the Lake Kutubu Wildlife Management Area, Southern Highlands Province, Papua New Guinea. In ‘Rapid Biological Assessments of Wau Creek, Uro Creek and Lake Kutubu: Documenting Biodiversity Values to Promote Forest Conservation in the Kikori River basin, Papua New Guinea’. (Ed. S. J. Richards.) pp. 353–378. (ExxonMobil PNG Limited: Port Moresby.)
Katunzi, T, Soisook, P, Webala, P. W., Armstrong, K. N., and Bumrungsri, S (2021). Bat activity and species richness in different land‐use types in and around Chome Nature Forest Reserve, Tanzania. African Journal of Ecology 59, 117–131.
| Bat activity and species richness in different land‐use types in and around Chome Nature Forest Reserve, Tanzania.Crossref | GoogleScholarGoogle Scholar |
Kunz, T. H., Hodgkison, R., and Weise, C. D. (2009). Methods of capturing and handling bats. In ‘Ecological and Behavioral Methods for the Study of Bats’. 2nd edn. (Eds T. H. Kunz and S. Parsons.) pp. 3–35. (Johns Hopkins University Press: Baltimore.)
Lumsden, L. (2017). Saccolaimus saccolaimus. The IUCN Red List of Threatened Species 2017: e.T19802A22004019. Available at:
Mahoney, J. A., and Walton, D. W. (1988). Emballonuridae. In ‘Mammalia’ Vol. 5 (Eds J. A. Mahoney and D. W. Walton.) pp. 114–118. (Australian Government Publishing Service: Canberra.)
McKenzie, N. L., and Bullen, R. D. (2003). Identifying Little Sandy Desert bat species from their echolocation calls. Australian Mammalogy 25, 73–80.
| Identifying Little Sandy Desert bat species from their echolocation calls.Crossref | GoogleScholarGoogle Scholar |
McKenzie, N. L., and Bullen, R. D. (2009). The echolocation calls, habitat relationships, foraging niches and communities of Pilbara microbats. Records of the Western Australian Museum 78, 123–155.
| The echolocation calls, habitat relationships, foraging niches and communities of Pilbara microbats.Crossref | GoogleScholarGoogle Scholar |
McKenzie, N. L., and Bullen, R. D. (2012). An acoustic survey of zoophagic bats on islands in the Kimberley, Western Australia, including data on the echolocation ecology, organisation and habitat relationships of regional communities. Records of the Western Australian Museum 81, 67–108.
| An acoustic survey of zoophagic bats on islands in the Kimberley, Western Australia, including data on the echolocation ecology, organisation and habitat relationships of regional communities.Crossref | GoogleScholarGoogle Scholar |
McKenzie, N. L., and Bullen, R. D. (2018). What can echolocation recordings reveal about the foraging ecology of Saccolaimus saccolaimus (Emballonuridae) in north-western Australia? Australian Journal of Zoology 66, 326–334.
| What can echolocation recordings reveal about the foraging ecology of Saccolaimus saccolaimus (Emballonuridae) in north-western Australia?Crossref | GoogleScholarGoogle Scholar |
McKenzie, N. L., and Muir, W. P. (2000). Bats of the southern Carnarvon Basin, Western Australia. Records of the Western Australian Museum 61, 465–477.
| Bats of the southern Carnarvon Basin, Western Australia.Crossref | GoogleScholarGoogle Scholar |
McKenzie, N. L., Start, A. N., and Bullen, R. D. (2002). Foraging ecology and organisation of a desert bat fauna. Australian Journal of Zoology 50, 529–548.
| Foraging ecology and organisation of a desert bat fauna.Crossref | GoogleScholarGoogle Scholar |
McKenzie, N. L., Bullen, R. D., Cowan, M. A., and Milne, D. J. (2018). Echolocation and distribution of Saccolaimus saccolaimus in north-western Australia. Records of the Western Australian Museum 33, 135–144.
| Echolocation and distribution of Saccolaimus saccolaimus in north-western Australia.Crossref | GoogleScholarGoogle Scholar |
McKenzie, N. L., Bullen, R. D., and Gibson, L. A. (2019). Habitat associations of zoophagic bat ensembles in north-western Australia. Australian Journal of Zoology 67, 243–259.
| Habitat associations of zoophagic bat ensembles in north-western Australia.Crossref | GoogleScholarGoogle Scholar |
Meutstege, R., Coles, R., and Spencer, H. (2014). Observations on the foraging and roosting behaviour of the bare-rumped sheathtail bat Saccolaimus saccolaimus in the Cape Tribulation region of Queensland, Australia. Oral presentation at the 16th Australasian Bat Society Conference, 22–25 April 2014, Townsville, Queensland. The Australasian Bat Society Newsletter 42, 34. Available at: http://ausbats.org.au/abs-newsletters/4553514675
Milne, D. J. (2002). Key to the bat calls of the Top End of the Northern Territory. Parks and Wildlife Commission of the Northern Territory, Technical Report No. 71.
Milne, D. J., Jackling, F. C., Sidhu, M., and Appleton, B. R. (2009). Shedding new light on old species identifications: morphological and genetic evidence suggest need for conservation status review of the critically endangered bat, Saccolaimus saccolaimus. Wildlife Research 36, 496–508.
| Shedding new light on old species identifications: morphological and genetic evidence suggest need for conservation status review of the critically endangered bat, Saccolaimus saccolaimus.Crossref | GoogleScholarGoogle Scholar |
Murphy, S. (2001). Observations of the ‘critically endangered’ bare-rumped sheathtail bat Saccolaimus saccolaimus Temminck (Chiroptera: Emballonuridae) on Cape York Peninsula, Queensland. Australian Mammalogy 23, 185–187.
| Observations of the ‘critically endangered’ bare-rumped sheathtail bat Saccolaimus saccolaimus Temminck (Chiroptera: Emballonuridae) on Cape York Peninsula, Queensland.Crossref | GoogleScholarGoogle Scholar |
Parsons, S., and Szewczak, J. M. (2009). Detecting, recording, and analyzing the vocalizations of bats. In ‘Ecological and Behavioral Methods for the Study of Bats’ 2nd edn. (Eds T. H. Kunz and S. Parsons) pp. 91–111. (Johns Hopkins University Press: Baltimore.)
Queensland Government (2020). WildNet database. Queensland Department of Environment and Science. Available at: https://apps.des.qld.gov.au/species-search/details/?id=1008
R Core Team (2020). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: https://www.R-project.org/
Rambaut, A. (2016). FigTree version 1.4.3 software. Available at: http://tree.bio.ed.ac.uk/software/figtree/
Reardon, T. B., Robson, S. K. A., Parsons, J. G., and Inkster, T. (2010). Review of the threatened status of microchiropteran bat species on Cape York Peninsula. Unpublished report. South Australian Museum, October 2010.
Reinhold, L., Law, B., Ford, G., and Pennay, M. (2001a). Key to the bat calls of south-east Queensland and north-east New South Wales. Forest Ecosystem Research and Assessment Technical Paper 2001-07, Department of Natural Resources and Mines, Queensland.
Reinhold, L., Herr, A., Lumsden, L., Reardon, T., Corben, C., Law, B., Prevett, P., Ford, G., Conole, L., Kutt, A., and Milne, D. (2001b). Geographic variation in the echolocation calls of Gould’s wattled bat Chalinolobus gouldii. Australian Zoologist 31, 618–624.
| Geographic variation in the echolocation calls of Gould’s wattled bat Chalinolobus gouldii.Crossref | GoogleScholarGoogle Scholar |
Roeleke, M., Bumrungsri, S., and Voigt, C. C. (2018). Bats probe the aerosphere during landscape-guided altitudinal flights. Mammal Review 48, 7–11.
| Bats probe the aerosphere during landscape-guided altitudinal flights.Crossref | GoogleScholarGoogle Scholar |
Russo, D., Ancillotto, L., and Jones, G. (2018). Bats are still not birds in the digital era: echolocation call variation and why it matters for bat species identification. Canadian Journal of Zoology 96, 63–78.
| Bats are still not birds in the digital era: echolocation call variation and why it matters for bat species identification.Crossref | GoogleScholarGoogle Scholar |
Schulz, M., and Thomson, B. (2007). National recovery plan for the bare-rumped sheathtail bat Saccolaimus saccolaimus nudicluniatus. Report to Department of the Environment and Water Resources, Canberra. Queensland Parks and Wildlife Service, Brisbane.
Simmons, N. B. (2005). Order Chiroptera. In ‘Mammal Species of the World’. (Eds D. E. Wilson and D. M. Reeder.) pp. 312–529. (The Johns Hopkins University Press: Baltimore, MD, USA.)
Swofford, D. L. (2002). ‘PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods).’ (Sinauer Associates: Sunderland, MA.)
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.
| MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.Crossref | GoogleScholarGoogle Scholar | 21546353PubMed |
Venables, W. N., and Ripley, B. D. (2002). ‘Modern Applied Statistics with S [R package MASS version 7.3–51.5].’ 4th edn. (Springer: New York.)
Woinarski, J. C. Z., Burbidge, A., and Harrison, P. (2014). ‘The Action Plan for Australian Mammals 2012.’ (CSIRO Publishing: Melbourne.)
Worthington Wilmer, J., and Barratt, E. (1996). A non-lethal method of tissue sampling for genetic studies of chiropterans. Bat Research News 37, 1–3.
