The bigger they are, the higher they go: Australian insectivorous bats confirm Bergmann’s 175-year-old prediction
Alexander Herr A *A
Abstract
Some insectivorous bats are some of the smallest flying endotherm. They have a high energy demand to maintain body temperature. Therefore, one can expect that larger animals of a species and larger species occur in colder environments as a result of improved energy conservation related to reduced surface to volume ratio in larger endotherm animals. Evidence of this general rule is scarce in bats, although Bergmann predicted this some 175 years ago for closely related species.
In this work, I investigated whether bat body size increases with above-sea-level elevation-related temperature decrease for three closely related Australian bat species of the genus Vespadelus. The purpose of this was two-fold. First, to investigate whether there is a relationship between bat size and elevation by using more recent computational techniques of Bayesian multilevel modelling (BMM). Second, to provide an example of applying recent advances in BMMs to wildlife research and to predict potential consequences of climate warming for these bats.
I investigated whether bat size relates to elevations of bat-capture locations. I included measurement errors for elevation and forearm length measurements by using a BMM in an high-performance computing environment. This model uses measurements of 775 bats from locations in the western slopes of the Australian Alps.
The BMM analysis showed that bat forearm length increased 0.11 mm for every 100 m elevation, with a low standard error of 0.01 mm, indicating a high precision. The standard deviations of the variables species and sex within species were large. This means that they did not provide sufficient explantory power for the overall model and predictions to warrant inclusion.
This study showed that there is a linear increase of bat size with elevation. This is the first study to show that bat size is related to elevation (and associated temperature decline) in three sympatric, closely related species of the same genus and it confirmed what Bergmann predicted over 175 years ago.
Under a warming climate, the results predict that bats become smaller on average. When incorporating average temperature-lapse rate to calculate elevations that assume a 1.5 and 3°C change in future average climate, the study coarsely quantified reduction in suitable habitat for the largest of the three species, V. darlingtoni, of up to 3%.
Keywords: Australian Alps, Bayesian multilevel model, Chiroptera, forearm length, lapse rate, measurement error, size, surface to volume ratio, temperature and elevation.
References
Alston JM, Keinath DA, Willis CKR, Lausen CL, O’Keefe JM, Tyburec JD, Broders HG, Moosman PR, Carter TC, Chambers CL, Gillam EH, Geluso K, Weller TJ, Burles DW, Fletcher QE, Norquay KJO, Goheen JR (2023) Environmental drivers of body size in North American bats. Functional Ecology 37, 1020-1032.
| Crossref | Google Scholar |
Baldwin JW, Garcia-Porta J, Botero CA (2023) Complementarity in Allen’s and Bergmann’s rules among birds. Nature Communications 14, 4240.
| Crossref | Google Scholar |
Bergmann C (1848) ‘Über die Verhältnisse der Wärmeökonomie der Thiere zu ihrer Größe’. Abgedruckt aus den Göttinger studien. pp. 595–708. (Vandenhoeck und Ruprecht) Available at https://www.digitale-sammlungen.de/en/view/bsb10306637
Brown JH, Lee AK (1969) Bergmann’s rule and climatic adaptation in woodrats (Neotoma). Evolution 23, 329-338.
| Crossref | Google Scholar | PubMed |
Bürkner P-C (2017) Brms: an R package for Bayesian multilevel models using Stan. Journal of Statistical Software 80, 1-28.
| Crossref | Google Scholar |
Bürkner P-C, Gabry J, Weber S, Johnson A, Modrak M, Badr HS, Weber F, Ben-Shachar MS, Rabel H, Mills SC, Wild S (2023a) Estimating distributional models with brms. Vignette included in R package brms, version 2.20.1. Available at https://CRAN.R-Project.org/package=brms
Bürkner P-C, Gabry J, Weber S, Johnson A, Modrak M, Badr HS, Weber F, Ben-Shachar MS, Rabel H, Mills SC, Wild S (2023b) Handle missing values with brms. Vignette included in R package brms, version 2.20.1. Available at https://CRAN.R-Project.org/package=brms
Castillo-Figueroa D (2022) Does Bergmann’s rule apply in bats? Evidence from two neotropical species. Neotropical Biodiversity 8, 200-221.
| Crossref | Google Scholar |
Charmantier A, McCleery RH, Cole LR, Perrins C, Kruuk LEB, Sheldon BC (2008) Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science 320, 800-803.
| Crossref | Google Scholar | PubMed |
Chen I-C, Hill JK, Ohlemüller R, Roy DB, Thomas CD (2011) Rapid range shifts of species associated with high levels of climate warming. Science 333, 1024-1026.
| Crossref | Google Scholar | PubMed |
Chenery M, Geiser F, Stawski C (2022) Thermal biology and roost selection of free-ranging male little forest bats, Vespadelus vulturnus, during winter. Journal of Mammalogy 103, 826-834.
| Crossref | Google Scholar | PubMed |
Churchill S (2009) ‘Australian bats.’ (Allen & Unwin) Available at https://books.google.com.au/books?id=zY4ZfTWXPYoC
Clauss M, Dittmann MT, Müller DWH, Meloro C, Codron D (2013) Bergmann’s rule in mammals: a cross-species interspecific pattern. Oikos 122, 1465-1472.
| Crossref | Google Scholar |
Davy CM, von Zuben V, Kukka PM, Gerber BD, Slough BG, Jung TS (2022) Rapidly declining body size in an insectivorous bat is associated with increased precipitation and decreased survival. Ecological Applications 32, e2639.
| Crossref | Google Scholar |
de Oliveira FV (2020) Microchiroptera life history. In ‘Encyclopedia of animal cognition and behavior’. (Eds J Vonk, T Shackelford) pp. 1–15. (Springer International Publishing: Cham, Switzerland) doi:10.1007/978-3-319-47829-6_1158-1
Gabry J, Češnovar R, Johnson A (2023) Cmdstanr: R interface to ‘CmdStan’. Available at https://mc-stan.org/cmdstanr/
Galloway RW (1988) The potential impact of climate changes on Australian ski fields. In ‘Greenhouse: planning for climate change’. (Ed. G Pearman) pp. 428–437. (CSIRO Publishing: Melbourne, Vic, Australia) doi:10.1071/9780643105041
Gardner JL, Heinsohn R, Joseph L (2009) Shifting latitudinal clines in avian body size correlate with global warming in Australian passerines. Proceedings of the Royal Society B: Biological Sciences 276, 3845-3852.
| Crossref | Google Scholar |
Gonsalves L, Bicknell B, Law B, Webb C, Monamy V (2013) Mosquito consumption by insectivorous bats: does size matter? PLoS ONE 8, e77183.
| Crossref | Google Scholar | PubMed |
Green K (2014) Growing season air temperature lapse rate in the snowy mountains. Australian Meteorological and Oceanographic Journal 64, 289-291.
| Crossref | Google Scholar |
He J, Tu J, Yu J, Jiang H (2023) A global assessment of Bergmann’s rule in mammals and birds. Global Change Biology 29, 5199-5210.
| Crossref | Google Scholar | PubMed |
Herr A (1998) Aspects of the ecology of insectivorous forest-dwelling bats (Microchiroptera) in the western slopes of the Australian alps. PhD Thesis, Charles Sturt University. Available at https://doi.org/10.13140/RG.2.2.12708.94087/1
Herr A, Klomp NI, Lumsden LF (2000) Variability in measurements of microchiropteran bats caused by different investigators. Mammalian Biology 65, 51-54 Available at https://www.biodiversitylibrary.org/part/192414.
| Google Scholar |
Hutchinson SMF (2008) GEODATA 9 second DEM and D8: digital elevation model version 3 and flow direction grid 2008. Record DEM-9S.v3. (Geoscience Australia: Canberra, ACT, Australia) Available at https://pid.geoscience.gov.au/dataset/ga/66006
Ji F, Nishant N, Evans JP, Di Luca A, Di Virgilio G, Cheung KKW, Tam E, Beyer K, Riley ML (2022) Rapid warming in the Australian alps from observation and NARCliM simulations. Atmosphere 13, 1686.
| Crossref | Google Scholar |
Jiang T, Wang J, Wu H, Csorba G, Puechmaille SJ, Benda P, Boireau J, Toffoli R, Courtois J-Y, Nyssen P, Colombo R, Feng J (2019) The patterns and possible causes of global geographical variation in the body size of the greater horseshoe bat (Rhinolophus ferrumequinum). Journal of Biogeography 46, 2363-2377.
| Crossref | Google Scholar |
Körner C (2012) ‘Alpine treelines: functional ecology of the global high elevation tree limits’. (Springer: Basel, Switzerland) doi:10.1007/978-3-0348-0396-0
Kröner N, Kotlarski S, Fischer E, Lüthi D, Zubler E, Schär C (2016) Separating climate change signals into thermodynamic, lapse-rate and circulation effects: theory and application to the European summer climate. Climate Dynamics 48, 3425-3440.
| Crossref | Google Scholar |
Kunz TH, Whitaker JO, Jr, Wadanoli MD (1995) Dietary energetics of the insectivorous mexican free-tailed bat (Tadarida brasiliensis) during pregnancy and lactation. Oecologia 101, 407-415.
| Crossref | Google Scholar | PubMed |
Law BS, Anderson J (2000) Roost preferences and foraging ranges of the eastern forest bat Vespadelus pumilus under two disturbance histories in northern New South Wales, Australia. Austral Ecology 25, 352-367.
| Crossref | Google Scholar |
Law B, Anderson J, Chidel M (1998) A bat survey in State Forests on the south-west slopes region of New South Wales with suggestions of improvements for future surveys. Australian Zoologist 30, 467-479.
| Crossref | Google Scholar |
Law BS, Chidel M, Law PR (2018) Forest bat population dynamics over 14 years at a climate refuge: effects of timber harvesting and weather extremes. PLoS ONE 13, e0191471.
| Crossref | Google Scholar |
Law B, Brassil T, Chidel M (2022) Site fidelity and other attributes of infrequently trapped bats over two decades in a montane wet sclerophyll forest. Australian Mammalogy 45, 91-97.
| Crossref | Google Scholar |
Law B, Brassil T, Proud R, Potts J (2023) Estimating density of forest bats and their long-term trends in a climate refuge. Ecology and Evolution 13, e10215.
| Crossref | Google Scholar |
Lentini PE, Bird TJ, Griffiths SR, Godinho LN, Wintle BA (2015) A global synthesis of survival estimates for microbats. Biology Letters 11, 20150371.
| Crossref | Google Scholar | PubMed |
Lewandowski D, Kurowicka D, Joe H (2009) Generating random correlation matrices based on vines and extended onion method. Journal of Multivariate Analysis 100, 1989-2001.
| Crossref | Google Scholar |
McElreath R (2020) ‘Statistical rethinking: a Bayesian course with examples in r and stan’, 2nd edn. (CRC Press) Available at http://xcelab.net/rm/statistical-rethinking/
McGuire LP, Kelly LA, Baloun DE, Boyle WA, Cheng TL, Clerc J, Fuller NW, Gerson AR, Jonasson KA, Rogers EJ, Sommers AS, Guglielmo CG (2018) Common condition indices are no more effective than body mass for estimating fat stores in insectivorous bats. Journal of Mammalogy 99, 1065-1071.
| Crossref | Google Scholar |
Meiri S, Dayan T (2003) On the validity of Bergmann’s rule. Journal of Biogeography 30, 331-351.
| Crossref | Google Scholar |
Meng F, Zhu L, Huang W, Irwin DM, Zhang S (2016) Bats: body mass index, forearm mass index, blood glucose levels and SLC2A2 genes for diabetes. Scientific Reports 6, 29960.
| Crossref | Google Scholar |
Merilä J, Hendry AP (2014) Climate change, adaptation, and phenotypic plasticity: the problem and the evidence. Evolutionary Applications 7, 1-14.
| Crossref | Google Scholar | PubMed |
Minder JR, Mote PW, Lundquist JD (2010) Surface temperature lapse rates over complex terrain: lessons from the Cascade Mountains. Journal of Geophysical Research: Atmospheres 115, D14122.
| Crossref | Google Scholar |
Mokhov II, Akperov MG (2006) Tropospheric lapse rate and its relation to surface temperature from reanalysis data. Izvestiya, Atmospheric and Oceanic Physics 42, 430-438.
| Crossref | Google Scholar |
Moritz C, Patton JL, Conroy CJ, Parra JL, White GC, Beissinger SR (2008) Impact of a century of climate change on small-mammal communities in Yosemite National Park, USA. Science 322, 261-264.
| Crossref | Google Scholar | PubMed |
Morningstar DE, Robinson CV, Shokralla S, Hajibabaei M (2019) Interspecific competition in bats and diet shifts in response to white-nose syndrome. Ecosphere 10, e02916.
| Crossref | Google Scholar |
Mundinger C, Scheuerlein A, Kerth G (2021) 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. Proceedings of the Royal Society B: Biological Sciences 288, 20210508.
| Crossref | Google Scholar |
Naccarella A, Morgan JW, Cutler SC, Venn SE (2020) Alpine treeline ecotone stasis in the face of recent climate change and disturbance by fire. PLoS ONE 15, e0231339.
| Crossref | Google Scholar | PubMed |
Nalborczyk L, Batailler C, Lœvenbruck H, Vilain A, Bürkner P-C (2019) An introduction to Bayesian multilevel models using brms: a case study of gender effects on vowel variability in standard Indonesian. Journal of Speech, Language, and Hearing Research 62, 1225-1242.
| Crossref | Google Scholar | PubMed |
Novella-Fernandez R, Ibañez C, Juste J, Clare EL, Doncaster CP, Razgour O (2020) Trophic resource partitioning drives fine-scale coexistence in cryptic bat species. Ecology and Evolution 10, 14122-14136.
| Crossref | Google Scholar | PubMed |
Nunez M, Colhoun EA (1986) A note on air temperature lapse rates on Mount Wellington, Tasmania. Papers and Proceedings of The Royal Society of Tasmania 120, 11-15.
| Crossref | Google Scholar |
Pan Z, Zhu J, Liu J, Gu J, Liu Z, Qin F, Pan Y (2021) Estimation of air temperature and the mountain-mass effect in the Yellow River Basin using multi-source data. PLoS ONE 16, e0258549.
| Crossref | Google Scholar |
Radchuk V, Reed T, Teplitsky C, van de Pol M, Charmantier A, Hassall C, Adamík P, Adriaensen F, Ahola MP, Arcese P, Miguel Avilés J, Balbontin J, Berg KS, Borras A, Burthe S, Clobert J, Dehnhard N, de Lope F, Dhondt AA, Dingemanse NJ, Doi H, Eeva T, Fickel J, Filella I, Fossøy F, Goodenough AE, Hall SJG, Hansson B, Harris M, Hasselquist D, Hickler T, Joshi J, Kharouba H, Martínez JG, Mihoub J-B, Mills JA, Molina-Morales M, Moksnes A, Ozgul A, Parejo D, Pilard P, Poisbleau M, Rousset F, Rödel M-O, Scott D, Senar JC, Stefanescu C, Stokke BG, Kusano T, Tarka M, Tarwater CE, Thonicke K, Thorley J, Wilting A, Tryjanowski P, Merilä J, Sheldon BC, Pape Møller A, Matthysen E, Janzen F, Dobson FS, Visser ME, Beissinger SR, Courtiol A, Kramer-Schadt S (2019) Adaptive responses of animals to climate change are most likely insufficient. Nature Communications 10, 3109.
| Crossref | Google Scholar |
R Core Team (2021) ‘R: a language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria) Available at: https://www.R-project.org/
Roeleke M, Johannsen L, Voigt CC (2018) How bats escape the competitive exclusion principle: seasonal shift from intraspecific to interspecific competition drives space use in a bat ensemble. Frontiers in Ecology and Evolution 6, 101.
| Crossref | Google Scholar |
Rolland C (2003) Spatial and seasonal variations of air temperature lapse rates in alpine regions. Journal of Climate 16, 1032-1046.
| Crossref | Google Scholar |
Rosas-Chavoya M, López-Serrano PM, Hernández-Díaz JC, Wehenkel C, Vega-Nieva DJ (2021) Analysis of near-surface temperature lapse rates in mountain ecosystems of northern Mexico using Landsat-8 satellite images and ECOSTRESS. Remote Sensing 14, 162.
| Crossref | Google Scholar |
Salinas-Ramos VB, Ancillotto L, Bosso L, Sánchez-Cordero V, Russo D (2019) Interspecific competition in bats: state of knowledge and research challenges. Mammal Review 50, 68-81.
| Crossref | Google Scholar |
Sivula T, Magnusson M, Matamoros AA, Vehtari A (2022) Uncertainty in Bayesian leave-one-out cross-validation based model comparison. Available at https://arxiv.org/abs/2008.10296
Slatyer R (2010) Climate change impacts on Australia’s alpine ecosystems. ANU Undergraduate Research Journal 2, 81-97.
| Crossref | Google Scholar |
Spence AR, Tingley MW (2020) The challenge of novel abiotic conditions for species undergoing climate-induced range shifts. Ecography 43, 1571-1590.
| Crossref | Google Scholar |
Spence AR, LeWinter H, Tingley MW (2022) Anna’s hummingbird (Calypte anna) physiological response to novel thermal and hypoxic conditions at high elevations. Journal of Experimental Biology 225, jeb243294.
| Crossref | Google Scholar |
Stawski C, Willis CKR, Geiser F (2014) The importance of temporal heterothermy in bats. Journal of Zoology 292, 86-100.
| Crossref | Google Scholar |
Taylor RJ, Savva NM (1988) Use of roost sites by four species of bats in state forest in south-eastern Tasmania. Wildlife Research 15, 637.
| Crossref | Google Scholar |
Teplitsky C, Millien V (2013) Climate warming and Bergmann’s rule through time: is there any evidence? Evolutionary Applications 7, 156-168.
| Crossref | Google Scholar | PubMed |
Thackeray SJ, Henrys PA, Hemming D, Bell JR, Botham MS, Burthe S, Helaouet P, Johns DG, Jones ID, Leech DI, Mackay EB, Massimino D, Atkinson S, Bacon PJ, Brereton TM, Carvalho L, Clutton-Brock TH, Duck C, Edwards M, Elliott JM, Hall SJG, Harrington R, Pearce-Higgins JW, Høye TT, Kruuk LEB, Pemberton JM, Sparks TH, Thompson PM, White I, Winfield IJ, Wanless S (2016) Phenological sensitivity to climate across taxa and trophic levels. Nature 535, 241-245.
| Crossref | Google Scholar | PubMed |
Vehtari A, Gelman A, Gabry J (2017) Practical Bayesian model evaluation using leave-one-out cross-validation and WAIC. Statistics and Computing 27, 1413-1432.
| Crossref | Google Scholar |
Verrall B, Norman P, Mackey B, Fisher S, Dodd J (2023) The impact of climate change and wildfire on decadal alpine vegetation dynamics. Australian Journal of Botany 71, 231-251.
| Crossref | Google Scholar |
Voigt CC, Sörgel K, Dechmann DKN (2010) Refueling while flying: foraging bats combust food rapidly and directly to power flight. Ecology 91, 2908-2917.
| Crossref | Google Scholar | PubMed |
Wang M, Chen K, Guo D, Luo B, Wang W, Gao H, Liu Y, Feng J (2020) Ambient temperature correlates with geographic variation in body size of least horseshoe bats. Current Zoology 66, 459-465.
| Crossref | Google Scholar | PubMed |
Watt C, Mitchell S, Salewski V (2010) Bergmann’s rule; a concept cluster? Oikos 119, 89-100.
| Crossref | Google Scholar |
Wood H, Cousins SAO (2023) Variability in bat morphology is influenced by temperature and forest cover and their interactions. Ecology and Evolution 13, e9695.
| Crossref | Google Scholar |
Young J, Littleboy M (2019) Climate change impacts in the NSW and ACT alpine region: impacts on water availability. (NSW Department of Planning, Industry and Environment: Sydney, NSW, Australia) Available at https://www.climatechange.environment.nsw.gov.au/sites/default/files/2021-08/Climate change impacts Alpine - Water availability.pdf
Zylstra PJ (2018) Flammability dynamics in the Australian alps. Austral Ecology 43, 578-591.
| Crossref | Google Scholar |