Factors affecting the detection probability of a critically endangered flying-fox: consequences for monitoring and conservation
A. Dorrestein


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Abstract
Monitoring is crucial for understanding population trends of threatened species and for assessing the effectiveness of conservation efforts. However, population monitoring is subject to detection probabilities that can vary across factors such as time, type of vegetation cover, weather conditions and observer.
In this study, we investigated the impact of environmental factors (e.g. wind and rain), spatiotemporal factors (e.g. time of night and geographical location) and observer variability, on the detection probability of Pteropus natalis (Christmas Island flying-fox), a critically endangered species that has been monitored across its single (135 km2) island range since 2006, by using active aural and visual detection of foraging individuals.
Surveys were conducted at four visits to 133 sites across Christmas Island, representing the environmental variation of the island, over a 2-month survey period. The survey was conducted in 9 years between 2006 and 2022.
Variable importance analysis showed that distance from the coast, year, and time of night were key predictors of P. natalis detection probability. Detection probability was higher on calmer nights, suggesting higher flying-fox activity or better sound transmission. Detection probability was also higher near roosts earlier and later in the night, indicating that P. natalis gradually moves away from and returns to roosts over the night. Detection probabilities varied between 2012 and 2022 across vegetation types, potentially reflecting changes in diet or phenology. Experienced observers were more likely to detect P. natalis, likely due to familiarity with their vocalisations or visual cues. Analyses excluding environmental and spatiotemporal factors suggested a slight increase in detections since 2012; however, once these factors were included, a significant decrease in detection probability between 2019 and 2022 emerged.
Our findings highlighted how environmental and spatiotemporal factors can affect detection probability and, consequently, survey results of a mobile, threatened small-island endemic.
This study demonstrated the importance of considering environmental and spatiotemporal factors when designing a monitoring program and, in subsequent analysis, to maximise the accuracy and precision of estimates derived from monitoring programs.
Keywords: bats, conservation management, detection probability, flying-foxes, island fauna, observer bias, observer variability, population monitoring, Pteropus.
References
Australian Bureau of Meteorology (2021) Weather data Christmas Island 1995–2021. Available at http://www.bom.gov.au/climate/dwo/IDCJDW6026.latest.shtml
Banack SA, Grant GS (2002) Spatial and temporal movement patterns of the flying fox, Pteropus tonganus, in American Samoa. The Journal of Wildlife Management 66(4), 1154-1163.
| Crossref | Google Scholar |
Bernard ATF, Götz A, Kerwath SE, Wilke CG (2013) Observer bias and detection probability in underwater visual census of fish assemblages measured with independent double-observers. Journal of Experimental Marine Biology and Ecology 443, 75-84.
| Crossref | Google Scholar |
Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18(1), 117-143.
| Crossref | Google Scholar |
Conenna I, López-Baucells A, Rocha R, Ripperger S, Cabeza M (2019) Movement seasonality in a desert-dwelling bat revealed by miniature GPS loggers. Movement ecology 7(1), 27.
| Crossref | Google Scholar |
Czenze ZJ, Tucker JL, Clare EL, Littlefair JE, Hemprich-Bennett D, Oliveira HFM, Mark Brigham R, Hickey AJR, Parsons S (2018) Spatiotemporal and demographic variation in the diet of New Zealand lesser short-tailed bats (Mystacina tuberculata). Ecology and Evolution 8(15), 7599-7610.
| Crossref | Google Scholar | PubMed |
Eby P (1991) Seasonal movements of grey-headed flying-foxes, Pteropus poliocephalus (Chiroptera: Pteropodidae), from two maternity camps in northern New South Wales. Wildlife Research 18(5), 547-559.
| Crossref | Google Scholar |
Erwin RM (1982) Observer variability in estimating numbers: an experiment. Journal of Field Ornithology 53(2), 159-167.
| Google Scholar |
Fahr J, Abedi-Lartey M, Esch T, Machwitz M, Suu-Ire R, Wikelski M, Dechmann DKN (2015) Pronounced seasonal changes in the movement ecology of a highly gregarious central-place forager, the African straw-coloured fruit bat (Eidolon helvum). PLoS ONE 10(10), e0138985.
| Crossref | Google Scholar | PubMed |
Fitzpatrick MC, Preisser EL, Ellison AM, Elkinton JS (2009) Observer bias and the detection of low-density populations. Ecological Applications 19(7), 1673-1679.
| Crossref | Google Scholar | PubMed |
Forsyth DM, Scroggie MP, McDonald-Madden E (2006) Accuracy and precision of grey-headed Flying-fox (Pteropus poliocephalus) flyour counts. Wildlife Research 33, 57-65.
| Crossref | Google Scholar |
Funakoshi K, Kunisaki T, Watanabe H (1991) Seasonal changes in activity of the northern Ryukyu fruit bat Pteropus dasymallus dasymallus. Journal of the Mammalogical Society of Japan 16(1), 13-25.
| Google Scholar |
Greenwell BM, Boehmke BC (2020) Variable importance plots: an introduction to the vip package. The R Journal 12(1), 343-366.
| Crossref | Google Scholar |
Hayes JP (1997) Temporal variation in activity of bats and the design of echolocation-monitoring studies. Journal of Mammalogy 78(2), 514-524.
| Crossref | Google Scholar |
Hurvich CM, Tsai C-L (1989) Regression and time series model selection in small samples. Biometrika 76(2), 297-307.
| Crossref | Google Scholar |
Jahn P, Ross JG, MacKenzie DI, Molles LE (2022) Acoustic monitoring and occupancy analysis: cost-effective tools in reintroduction programmes for roroa-great spotted kiwi. New Zealand Journal of Ecology 46(1), 3466.
| Crossref | Google Scholar |
James DJ, Dale GJ, Retallick K, Orchard K (2007) Christmas Island flying-fox Pteropus natalis Thomas 1887: an assessment of conservation status and threats. Parks Australia North Christmas Island Biodiversity Monitoring Programme. Report to Department of Finance & Administration and the Department of Environment & Water Resources, Canberra, ACT, Australia. pp. 19–23.
Jeffress MR, Paukert CP, Sandercock BK, Gipson PS (2011) Factors affecting detectability of river otters during sign surveys. The Journal of Wildlife Management 75(1), 144-150.
| Crossref | Google Scholar |
Lai J, Tang J, Li T, Zhang A, Mao L (2024) Evaluating the relative importance of predictors in generalized additive models using the gam.hp R package. Plant Diversity 46, 542-546.
| Crossref | Google Scholar |
Lisovski S, Ramenofsky M, Wingfield JC (2017) Defining the degree of seasonality and its significance for future research. Integrative and Comparative Biology 57(5), 934-942.
| Crossref | Google Scholar | PubMed |
Lotz A, Allen CR (2007) Observer bias in anuran call surveys. The Journal of Wildlife Management 71(2), 675-679.
| Crossref | Google Scholar |
Marsh DM, Trenham PC (2008) Current trends in plant and animal population monitoring. Conservation Biology 22(3), 647-655.
| Crossref | Google Scholar | PubMed |
McCarthy ED, Martin JM, Boer MM, Welbergen JA (2022) Ground-based counting methods underestimate true numbers of a threatened colonial mammal: an evaluation using drone-based thermal surveys as a reference. Wildlife Research 50, 484-493.
| Crossref | Google Scholar |
McDonald-Madden E, Schreiber ESG, Forsyth DM, Choquenot D, Clancy TF (2005) Factors affecting grey-headed Flying-fox (Pteropus poliocephalus: Pteropodidae) foraging in the Melbourne metropolitan area, Australia. Austral Ecology 30(5), 600-608.
| Crossref | Google Scholar |
Meade J, Martin JM, Welbergen JA (2021) Fast food in the city? Nomadic flying-foxes commute less and hang around for longer in urban areas. Behavioral Ecology 32(6), 1151-1162.
| Crossref | Google Scholar |
Morellet N, Bonenfant C, Börger L, Ossi F, Cagnacci F, Heurich M, Kjellander P, Linnell JDC, Nicoloso S, Urbano F, Mysterud A, Sustr P (2013) Seasonality, weather and climate affect home range size in roe deer across a wide latitudinal gradient within Europe. Journal of Animal Ecology 82(6), 1326-1339.
| Crossref | Google Scholar | PubMed |
Oedin M, Brescia F, Boissenin M, Vidal E, Cassan J-J, Hurlin J-C, Millon A (2019) Monitoring hunted species of cultural significance: estimates of trends, population sizes and harvesting rates of flying-fox (Pteropus sp.) in New Caledonia. PLoS ONE 14(12), e0224466.
| Crossref | Google Scholar | PubMed |
Otto MC, Pollock KH (1990) Size bias in line transect sampling: a field test. Biometrics 46, 239-245.
| Crossref | Google Scholar |
Padgham M, Lovelace R, Salmon M, Rudis B (2017) osmdata. Journal of Open Source Software 2, 305.
| Crossref | Google Scholar |
Palmer C, Woinarski JCZ (1999) Seasonal roosts and foraging movements of the black flying fox (Pteropus alecto) in the Northern Territory: resource tracking in a landscape mosaic. Wildlife Research 26(6), 823-838.
| Crossref | Google Scholar |
Palmer C, Price O, Bach C (2000) Foraging ecology of the black flying fox (Pteropus alecto) in the seasonal tropics of the Northern Territory, Australia. Wildlife Research 27(2), 169-178.
| Crossref | Google Scholar |
Pebesma E (2018) Simple features for R: standardized support for spatial vector data. The R Journal 10, 439-446.
| Crossref | Google Scholar |
Perks SJ, Goodenough AE (2020) Abiotic and spatiotemporal factors affect activity of European bat species and have implications for detectability for acoustic surveys. Wildlife Biology 2020(2), 1-8.
| Crossref | Google Scholar |
Pulscher LA, Dierenfeld ES, Welbergen JA, Rose KA, Phalen DN (2021) A comparison of nutritional value of native and alien food plants for a critically endangered island flying-fox. PLoS ONE 16(5), e0250857.
| Crossref | Google Scholar | PubMed |
Pyke GH, Pulliam HR, Charnov EL (1977) Optimal foraging: a selective review of theory and tests. The Quarterly Review of Biology 52(2), 137-154.
| Crossref | Google Scholar |
R Core Team (2021) ‘R: a language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria) Available at http://www.R-project.org/
Reddiex B, Forsyth DM, McDonald-Madden E, Einoder LD, Griffioen PA, Chick RR, Robley AJ (2006) Control of pest mammals for biodiversity protection in Australia. I. Patterns of control and monitoring. Wildlife Research 33(8), 691-709.
| Crossref | Google Scholar |
Reddy S, Dávalos LM (2003) Geographical sampling bias and its implications for conservation priorities in Africa. Journal of Biogeography 30(11), 1719-1727.
| Crossref | Google Scholar |
RStudio Team (2020) ‘RStudio: Integrated Development for R.’ (RStudio, Inc.: Boston, MA, USA). Available at www.rstudio.com
Shirley MH, Dorazio RM, Abassery E, Elhady AA, Mekki MS, Asran HH (2012) A sampling design and model for estimating abundance of Nile crocodiles while accounting for heterogeneity of detectability of multiple observers. The Journal of Wildlife Management 76(5), 966-975.
| Crossref | Google Scholar |
Thomas A, Speldewinde P, Roberts JD, Burbidge AH, Comer S (2020) If a bird calls, will we detect it? Factors that can influence the detectability of calls on automated recording units in field conditions. Emu – Austral Ornithology 120(3), 239-248.
| Crossref | Google Scholar |
Tidemann CR, Yorkston HD, Russack AJ (1994) The diet of cats, Felis catus, on Christmas Island, Indian Ocean. Wildlife Research 21, 279-286.
| Crossref | Google Scholar |
Todd CM, Westcott DA, Rose K, Martin JM, Welbergen JA (2018) Slow growth and delayed maturation in a Critically Endangered insular flying fox (Pteropus natalis). Journal of Mammalogy 99(6), 1510-1521.
| Crossref | Google Scholar | PubMed |
Utzurrijm RCB, Wiles GJ, Brooke AP, Worthington DJ (2003) Count methods and population trends in Pacific island flying-foxes. In ‘Monitoring trends in bat populations of the United States and territories: problems and prospects’. (Eds TJ O’Shea, MA Bogan) pp. 49–61. US Geological Survey, Biological Resources Division, Information and Technology Report, Washington, USA.
Vincenot CE, Florens FV, Kingston T (2017) Can we protect island flying foxes? Science 355(6332), 1368-1370.
| Crossref | Google Scholar | PubMed |
Wagner JL (1981) Visibility and bias in avian foraging data. The Condor 83(3), 263-264.
| Crossref | Google Scholar |
Walker K, Porritt K, Sexton M (2014) Christmas Island Vegetation and Clearing Dataset. Geoscience Australia, Canberra, ACT, Australia. Available at http://pid.geoscience.gov.au/dataset/ga/82430
Welbergen JA (2011) Fit females and fat polygynous males: seasonal body mass changes in the grey-headed flying fox. Oecologia 165(3), 629-637.
| Crossref | Google Scholar | PubMed |
Westcott DA, McKeown A (2004) Observer error in exit counts of flying-foxes (Pteropus spp.). Wildlife Research 31(5), 551-558.
| Crossref | Google Scholar |
Westcott DA, Fletcher CS, McKeown A, Murphy HT (2012) Assessment of monitoring power for highly mobile vertebrates. Ecological Applications 22(1), 374-383.
| Crossref | Google Scholar | PubMed |
Winiarska D, Szymański P, Osiejuk TS (2024) Detection ranges of forest bird vocalisations: guidelines for passive acoustic monitoring. Scientific Reports 14(1), 894.
| Crossref | Google Scholar | PubMed |
Woinarski JCZ, Flakus S, James DJ, Tiernan B, Dale GJ, Detto T (2014) An Island-wide monitoring program demonstrates decline in reporting rate for the Christmas Island Flying-Fox Pteropus melanotus natalis. Acta Chiropterologica 16, 117-127.
| Crossref | Google Scholar |
Wood SN (2011) Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. Journal of the Royal Statistical Society: Series B 73(1), 3-36.
| Crossref | Google Scholar |
Yabsley SH, Meade J, Martin JM, Welbergen JA (2021) Human-modified landscapes provide key foraging areas for a threatened flying mammal: the grey-headed flying-fox. PLoS ONE 16(11), e0259395.
| Crossref | Google Scholar | PubMed |