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Novel passive detection approach reveals low breeding season survival and apparent lactation cost in a critically endangered cave bat

  • Odonnell, C. Population dynamics and survivorship in bats. In Ecology and Behavioral Methods for the Study of Bats (eds Kunz, T. H. & Parsons, S.) 158–176 (The Johns University Press, 2009).

    Google Scholar 

  • Lebreton, J.-D., Burnham, K. P., Clobert, J. & Anderson, D. R. Modeling survival and testing biological hypotheses using marked animals: A unified approach with case studies. Ecol. Monogr. 62, 67–118 (1992).

    Article 

    Google Scholar 

  • Gibbons, J. W. & Andrews, K. M. PIT tagging: Simple technology at its best. Bioscience 54, 447–454 (2004).

    Article 

    Google Scholar 

  • Ellison, L. E. et al. A comparison of conventional capture versus PIT reader techniques for estimating survival and capture probabilities of big brown bats (Eptesicus fuscus). Acta Chiropterologica 9, 149–160 (2007).

    Article 

    Google Scholar 

  • van Harten, E. et al. High detectability with low impact: Optimizing large PIT tracking systems for cave-dwelling bats. Ecol. Evol. 9, 10916–10928 (2019).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Schorr, R. A., Ellison, L. E. & Lukacs, P. M. Estimating sample size for landscape-scale mark-recapture studies of North American migratory tree bats. Acta Chiropterologica 16, 231–239 (2014).

    Article 

    Google Scholar 

  • Baker, G. B. et al. The effect of forearm bands on insectivorous bats (Microchiroptera) in Australia. Wildl. Res. 28, 229–237 (2001).

    Article 

    Google Scholar 

  • O’Shea, T. J., Ellison, L. E. & Stanley, T. R. Survival estimation in bats: Historical overview, critical appraisal, and suggestions for new approaches. In Sampling Rare or Elusive Species: Concepts, Designs, and Techniques for Estimating Population Parameters (ed. Thompson, W. L.) 297–336 (Island Press, 2004).

    Google Scholar 

  • O’Shea, T. J. et al. Recruitment in a Colorado population of big brown bats: Breeding probabilities, litter size, and first-year survival. J. Mammal. 91, 418–428 (2010).

    Article 

    Google Scholar 

  • O’Shea, T. J., Ellison, L. E. & Stanley, T. R. Adult survival and population growth rate in Colorado big brown bats (Eptesicus fuscus). J. Mammal. 92, 433–443 (2011).

    Article 

    Google Scholar 

  • Schorr, R. A. & Siemers, J. L. Population dynamics of little brown bats (Myotis lucifugus) at summer roosts: Apparent survival, fidelity, abundance, and the influence of winter conditions. Ecol. Evol. 11, 7427–7438 (2021).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • O’Donnell, C. F. J., Edmonds, H. & Hoare, J. M. Survival of PIT-tagged lesser short-tailed bats (Mystacina tuberculata) through a pest control operation using the toxin pindone in bait stations. N. Z. J. Ecol. 35, 291–295 (2011).

    Google Scholar 

  • Edmonds, H., Pryde, M. & O’Donnell, C. Survival of PIT-tagged lesser short-tailed bats (Mystacina tuberculata) through an aerial 1080 pest control operation. N. Z. J. Ecol. 41, 186–192 (2017).

    Google Scholar 

  • Reusch, C. et al. Differences in seasonal survival suggest species-specific reactions to climate change in two sympatric bat species. Ecol. Evol. 9, 7957–7965 (2019).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • IUCN. The IUCN red list of threatened species. Version 2020-2. http://www.iucnredlist.org (2020).

  • Lentini, P. E., Bird, T. J., Griffiths, S. R., Godinho, L. N. & Wintle, B. A. A global synthesis of survival estimates for microbats. Biol. Lett. 11, 20150371 (2015).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Culina, A., Linton, D. M. & Macdonald, D. W. Age, sex, and climate factors show different effects on survival of three different bat species in a woodland bat community. Glob. Ecol. Conserv. 12, 263–271 (2017).

    Article 

    Google Scholar 

  • Frick, W. F., Reynolds, D. S. & Kunz, T. H. Influence of climate and reproductive timing on demography of little brown myotis Myotis lucifugus. J. Anim. Ecol. 79, 128–136 (2010).

    PubMed 
    Article 

    Google Scholar 

  • Schorcht, W., Bontadina, F. & Schaub, M. Variation of adult survival drives population dynamics in a migrating forest bat. J. Anim. Ecol. 78, 1182–1190 (2009).

    PubMed 
    Article 

    Google Scholar 

  • Sendor, T. & Simon, M. Population dynamics of the pipistrelle bat: Effects of sex, age and winter weather on seasonal survival. J. Anim. Ecol. 72, 308–320 (2003).

    Article 

    Google Scholar 

  • Sripathi, K., Raghuram, H., Rajasekar, R., Karuppudurai, T. & Abraham, S. G. Population size and survival in the indian false vampire bat Megaderma lyra. Acta Chiropterologica 6, 145–154 (2004).

    Article 

    Google Scholar 

  • Papadatou, E., Butlin, R. K., Pradel, R. & Altringham, J. D. Sex-specific roost movements and population dynamics of the vulnerable long-fingered bat, Myotis capaccinii. Biol. Conserv. 142, 280–289 (2009).

    Article 

    Google Scholar 

  • López-Roig, M. & Serra-Cobo, J. Impact of human disturbance, density, and environmental conditions on the survival probabilities of pipistrelle bat (Pipistrellus pipistrellus). Popul. Ecol. 56, 471–480 (2014).

    Article 

    Google Scholar 

  • Wilkinson, G. S. & Adams, D. M. Recurrent evolution of extreme longevity in bats. Biol. Lett. 15, 20180860 (2019).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • DELWP. National Recovery Plan for the Southern Bent-wing Bat Miniopterus orianae bassanii (2020).

  • Lumsden, L. & Gray, P. Longevity record for a southern bent-wing bat Miniopterus schreibersii bassanii. Australas. Bat Soc. Newsl. 16, 43–44 (2001).

    Google Scholar 

  • Holz, P. H. et al. Virus survey in populations of two subspecies of bent-winged bats (Miniopterus orianae bassanii and oceanensis) in south-eastern Australia reveals a high prevalence of diverse herpesviruses. PLoS ONE 13, e0197625 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Holz, P. H., Lumsden, L. F., Marenda, M. S., Browning, G. F. & Hufschmid, J. Two subspecies of bent-winged bats (Miniopterus orianae bassanii and oceanensis) in southern Australia have diverse fungal skin flora but not Pseudogymnoascus destructans. PLoS ONE 13, e0204282 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Holz, P. H., Lumsden, L. F. & Hufschmid, J. Ectoparasites are unlikely to be a primary cause of population declines of bent-winged bats in south-eastern Australia. Int. J. Parasitol. Parasites Wildl. 7, 423–428 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Holz, P. H., Lumsden, L. F., Legione, A. R. & Hufschmid, J. Polychromophilus melanipherus and haemoplasma infections not associated with clinical signs in southern bent-winged bats (Miniopterus orianae bassanii) and eastern bent-winged bats (Miniopterus orianae oceanensis). Int. J. Parasitol. Parasites Wildl. 8, 10–18 (2019).

    PubMed 
    Article 

    Google Scholar 

  • Holz, P. H., Clark, P., McLelland, D. J., Lumsden, L. F. & Hufschmid, J. Haematology of southern bent-winged bats (Miniopterus orianae bassanii) from the Naracoorte Caves National Park, South Australia. Comp. Clin. Pathol. 29, 231–237 (2020).

    CAS 
    Article 

    Google Scholar 

  • Dwyer, P. D. The population pattern of Miniopterus schreibersii (Chiroptera) in north-eastern New South Wales. Aust. J. Zool. 14, 1073–1137 (1966).

    Article 

    Google Scholar 

  • Dwyer, P. D. Mortality factors of the bent-winged bat. Vic. Nat. 83, 31–36 (1966).

    Google Scholar 

  • Dwyer, P. D. Seasonal changes in activity and weight of Miniopterus schreibersii blepotis (Chiroptera) in north-eastern NSW. Aust. J. Zool. 12, 52–69 (1964).

    Article 

    Google Scholar 

  • Bureau of Meteorology. Drought archive. http://www.bom.gov.au/climate/drought/archive.shtml (2019).

  • Dwyer, P. D. Population ranges of Miniopterus schreibersii (Chiroptera) in south-eastern Australia. Aust. J. Zool. 17, 665–686 (1969).

    Article 

    Google Scholar 

  • Fleischer, T., Gampe, J., Scheuerlein, A. & Kerth, G. Rare catastrophic events drive population dynamics in a bat species with negligible senescence. Sci. Rep. 7, 7370 (2017).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Thomas, D. W. Hibernating bats are sensitive to nontactile human disturbance. J. Mammal. 76, 940–946 (1995).

    Article 

    Google Scholar 

  • Reeder, D. M. et al. Frequent arousal from hibernation linked to severity of infection and mortality in bats with white-nose syndrome. PLoS ONE 7, e38920 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Turbill, C., Bieber, C. & Ruf, T. Hibernation is associated with increased survival and the evolution of slow life histories among mammals. Proc. R. Soc. B Biol. Sci. 278, 3355–3363 (2011).

    Article 

    Google Scholar 

  • van Harten, E. Population Dynamics of the Critically Endangered, Southern Bent-Winged Bat Miniopterus orianae bassanii (La Trobe University, 2020).

    Google Scholar 

  • PIRSA. History of the south east drainage system – summary. https://www.pir.sa.gov.au/aghistory/natural_resources/water_resources_ag_dev/history_of_the_south_east_drainage_system_-_summary/history_of_the_south_east_drainage_system_-_summary#_ftnref2 (2017).

  • Harding, C., Herpich, D. & Cranswick, R. H. Examining temporal and spatial changes in surface water hydrology of groundwater dependent ecosystems using WOfS (Water Observations from Space): Southern Border Groundwaters Agreement area, South East South Australia. (2018).

  • Holz, P. H., Lumsden, L. F., Reardon, T., Gray, P. & Hufschmid, J. Does size matter? Morphometrics of southern bent-winged bats (Miniopterus orianae bassanii) and eastern bent-winged bats (Miniopterus orianae oceanensis). Aust. Zool. AZ https://doi.org/10.7882/AZ.2019.019 (2020).

    Article 

    Google Scholar 

  • Rashid, M. M. & Beecham, S. Characterization of meteorological droughts across South Australia. Meteorol. Appl. 26, 556–568 (2019).

    Article 

    Google Scholar 

  • Culina, A., Linton, D. M., Pradel, R., Bouwhuis, S. & Macdonald, D. W. Live fast, don’t die young: Survival–reproduction trade-offs in long-lived income breeders. J. Anim. Ecol. 88, 746–756 (2019).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Kunz, T. H., Whitaker, J. O. & Wadanoli, M. D. Dietary energetics of the insectivorous Mexican free-tailed bat (Tadarida brasiliensis) during pregnancy and lactation. Oecologia 101, 407–415 (1995).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Adams, R. A. & Hayes, M. A. Water availability and successful lactation by bats as related to climate change in arid regions of western North America. J. Anim. Ecol. 77, 1115–1121 (2008).

    PubMed 
    Article 

    Google Scholar 

  • Henry, M., Thomas, D. W., Vaudry, R. & Carrier, M. Foraging distances and home range of pregnant and lactating little brown bats (Myotis lucifugus). J. Mammal. 83, 767–774 (2002).

    Article 

    Google Scholar 

  • Lučan, R. & Radil, J. Variability of foraging and roosting activities in adult females of Daubenton’s bat (Myotis daubentonii) in different seasons. Biologia (Bratisl.) 65 (2010).

  • Amorim, F., Jorge, I., Beja, P. & Rebelo, H. Following the water? Landscape-scale temporal changes in bat spatial distribution in relation to Mediterranean summer drought. Ecol. Evol. 8, 5801–5814 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • O’Donnell, C. F. J. Timing of breeding, productivity and survival of long-tailed bats Chalinolobus tuberculatus (Chiroptera: Vespertilionidae) in cold-temperate rainforest in New Zealand. J. Zool. 257, 311–323 (2002).

    Article 

    Google Scholar 

  • Holz, P. H., Stent, A., Lumsden, L. F. & Hufschmid, J. Trauma found to be a significant cause of death in a pathological investigation of bent-winged bats (Miniopterus orianae). J. Zoo Wildl. Med. 50, 966–971 (2020).

    PubMed 
    Article 

    Google Scholar 

  • Hughes, P. M., Rayner, J. M. V. & Jonesg, G. Ontogeny of ‘true’ flight and other aspects of growth in the bat Pipistrellus pipistrellus. J. Zool. 236, 291–318 (1995).

    Article 

    Google Scholar 

  • Wund, M. A. Learning and the development of habitat-specific bat echolocation. Anim. Behav. 70, 441–450 (2005).

    Article 

    Google Scholar 

  • McGuire, L. P. et al. Common condition indices are no more effective than body mass for estimating fat stores in insectivorous bats. J. Mammal. 99, 1065–1071 (2018).

    Article 

    Google Scholar 

  • Mispagel, C. et al. DDT and metabolites residues in the southern bent-wing bat (Miniopterus schreibersii bassanii) of south-eastern Australia. Chemosphere 55, 997–1003 (2004).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Allinson, G. et al. Organochlorine and trace metal residues in adult southern bent-wing bat (Miniopterus schreibersii bassanii) in southeastern Australia. Chemosphere 64, 1464–1471 (2006).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Kolkert, H., Andrew, R., Smith, R., Rader, R. & Reid, N. Insectivorous bats selectively source moths and eat mostly pest insects on dryland and irrigated cotton farms. Ecol. Evol. https://doi.org/10.1002/ece3.5901 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Sherwin, H. A., Montgomery, W. I. & Lundy, M. G. The impact and implications of climate change for bats. Mammal Rev. 43, 171–182 (2013).

    Article 

    Google Scholar 

  • O’Shea, T. J., Cryan, P. M., Hayman, D. T. S., Plowright, R. K. & Streicker, D. G. Multiple mortality events in bats: A global review. Mammal Rev. 46, 175–190 (2016).

    Article 

    Google Scholar 

  • Mundinger, C., Scheuerlein, A. & Kerth, G. Long-term study shows that increasing body size in response to warmer summers is associated with a higher mortality risk in a long-lived bat species. Proc. R. Soc. B Biol. Sci. 288, 20210508 (2021).

    Article 

    Google Scholar 

  • Adams, R. A. & Hayes, M. A. Assemblage-level analysis of sex-ratios in Coloradan bats in relation to climate variables: A model for future expectations. Glob. Ecol. Conserv. 14, e00379 (2018).

    Article 

    Google Scholar 

  • Crichton, E. G., Seamark, R. F. & Krutzsch, P. H. The status of the corpus luteum during pregnancy in Miniopterus schreibersii (Chiroptera: Vespertilionidae) with emphasis on its role in developmental delay. Cell Tissue Res. 258, 183–201 (1989).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Olsen, I. C. The analysis of continuous mark-recapture data (Norwegian University of Science and Technology, 2006).

    Google Scholar 

  • Barbour, A. B., Ponciano, J. M. & Lorenzen, K. Apparent survival estimation from continuous mark-recapture/resighting data. Methods Ecol. Evol. 4, 846–853 (2013).

    Article 

    Google Scholar 

  • van Harten, E. et al. Recovery of southern bent-winged bats (Miniopterus orianae bassanii) after PIT-tagging and the use of surgical adhesive. Aust. Mammal. 42, 216–219 (2020).

    Article 

    Google Scholar 

  • McDonald, T. L., Amstrup, S. C. & Manly, B. F. Tag loss can bias Jolly-Seber capture-recapture estimates. Wildl. Soc. Bull. 31, 814–822 (2003).

    Google Scholar 

  • van Harten, E. et al. Low rates of PIT-tag loss in an insectivorous bat species. J. Wildl. Manag. 85, 1739–1743 (2021).

    Article 

    Google Scholar 

  • Lebl, K. & Ruf, T. An easy way to reduce PIT-tag loss in rodents. Ecol. Res. 25, 251–253 (2010).

    Article 

    Google Scholar 

  • Rigby, E. L., Aegerter, J., Brash, M. & Altringham, J. D. Impact of PIT tagging on recapture rates, body condition and reproductive success of wild Daubenton’s bats (Myotis daubentonii). Vet. Rec. 170, 101 (2012).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Locatelli, A. G., Ciuti, S., Presetnik, P., Toffoli, R. & Teeling, E. Long-term monitoring of the effects of weather and marking techniques on body condition in the Kuhl’s pipistrelle bat, Pipistrellus kuhlii. Acta Chiropterologica 21, 87–102 (2019).

    Article 

    Google Scholar 

  • Paniw, M. et al. The myriad of complex demographic responses of terrestrial mammals to climate change and gaps of knowledge: A global analysis. J. Anim. Ecol. 90, 1398–1407 (2021).

    PubMed 
    Article 

    Google Scholar 

  • Frick, W. F., Kingston, T. & Flanders, J. A review of the major threats and challenges to global bat conservation. Ann. N. Y. Acad. Sci. 1469, 5–25 (2020).

    PubMed 
    Article 

    Google Scholar 

  • Brunet-Rossinni, A. K. & Wilkinson, G. S. Methods for age estimation and the study of senescence in bats. In Ecological and Behavioral Methods for the Study of Bats (eds Kunz, T. H. & Parsons, S.) 315–325 (Johns Hopkins University Press, 2009).

    Google Scholar 

  • Churchill, S. Australian Bats (Allen and Unwin, 2008).

    Google Scholar 

  • Laake, J. L. RMark: An R interface for analysis of capture-recapture data with MARK. 25 (2013).

  • Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference (Springer, 2002). https://doi.org/10.1007/b97636.

    Book 
    MATH 

    Google Scholar 

  • Caswell, H. Matrix population models. In Encyclopedia of Environmetrics (eds El-Shaarawi, A. H. & Piegorsch, W. W.) (Wiley, Berlin, 2006). https://doi.org/10.1002/9780470057339.vam006m.

    Chapter 

    Google Scholar 

  • Dwyer, P. D. The breeding biology of Miniopterus schreibersii blepotis (Termminck) (Chiroptera) in north-eastern NSW. Aust. J. Zool. 11, 219–240 (1963).

    Article 

    Google Scholar 

  • Richardson, E. G. The biology and evolution of the reproductive cycle of Miniopterus schreibersii and M. australis (Chiroptera: Vespertilionidae). J. Zool. 183, 353–375 (1977).

    Article 

    Google Scholar 


  • Source: Ecology - nature.com

    Invasions of an obligate asexual daphnid species support the nearly neutral theory

    Succession comprises a sequence of threshold-induced community assembly processes towards multidiversity