Abstract
Animals consume, process, use, and allocate energy to survive. The rate at which individuals use energy depends on how they lose heat to the environment, which is influenced by both climate and body mass (Mb), as well as their ability to process food. Apparent digestibility of dry matter (D*m) is commonly used to estimate digestive efficiency and has been positively linked to mass-independent basal metabolic rate (hereafter, BMR) in some birds and mammals. In vespertilionid bats, D*m has been reported to be inversely related to Mb. Since Mb is negatively associated with BMR, a positive relationship between D*m and BMR is expected. However, bats from cold climates tend to exhibit lower BMRs. We measured BMR in 10 bat species from the family Vespertilionidae and gathered information from 29 additional species across a range of climates and Mb (3.4 g to 30.3 g). Using phylogenetic and additive approaches, we tested the relationship between BMR, climate and D*m mathematically modeled. We found that BMR was positive associated with D*m and that this relationship differed by climate. BMR was constant in bats with Mb ≥ 13–17 g and D*m ≤ 74–76%, while BMR increased in smaller species. Our results suggest that D*m could be critical in smaller bats from warm climates due to their high rates of energy use. The different responses we found with other studies can be explained by trade-offs in energy allocation among organs and other metabolically active tissues. We discuss morphological, physiological, and ecological mechanisms underlying D*m variation.
References
Amador LI, Giannini NP, Simmons NB, Abdala V (2018) Morphology and evolution of sesamoid elements in bats (Mammalia: Chiroptera). Am Mus Novit. https://doi.org/10.1206/3905.1
Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis. United States, New York
Ayala-Berdon J, Medina-Bello KI (2024) Torpor energetics are related to the interaction between body mass and climate in bats of the family Vespertilionidae. J Exp Biol. https://doi.org/10.1242/jeb.246824
Ayala-Berdon J, Galicia R, Flores-Ortíz C, Medellín RA, Schondube JE (2013) Digestive capacities allow the Mexican long-nosed bat (Leptonycteris nivalis) to live in cold environments. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 164:622–628. https://doi.org/10.1016/j.cbpa.2013.01.015
Ayala-Berdon J, Medina-Bello KI, Carballo-Morales JD, Saldaña-Vázquez RA, Villalobos F (2025) Thermal energetics of bats of the family Vespertilionidae: an evolutionary approach. Zoology 126271. https://doi.org/10.1016/j.zool.2025.126271
Beck C, Grieser J, Kottek M, Rubel F, Rudolf B (2005) Characterizing global climate change by means of Köppen climate classification. Klimastatusbericht 85:139–149
Bozinovic F (1995) Nutritional energetics and digestive responses of an herbivorous rodent (Octodon degus) to different levels of dietary fiber. J Mammal 76(2):627–637. https://doi.org/10.2307/1382371
Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789. https://doi.org/10.1111/j.1469-7998.2012.00927.x
Cabrera-Campos I, Carballo-Morales JD, Saldaña-Vázquez RA, Villalobos F, Ayala-Berdon J (2021) Body mass explains digestive traits in small vespertilionid bats. J Comp Physiol B 191:427–438. https://doi.org/10.1007/s00360-021-01348-y
Calder WA (1984) Size, function and life history. United States, New York
Caviedes-Vidal E, McWhorter TJ, Lavin SR, Chediack JG, Tracy CR, Karasov WH (2007) The digestive adaptation of flying vertebrates: high intestinal paracellular absorption compensates for smaller guts. Proc Natl Acad Sci U S A 104:19132–19137
Chávez SBR (2019) Comunidades componentes de helmintos parásitos de Myotis velifer chiroptera: vespertilionidae en tres refugios cavernícolas del Estado de Morelos. Master’s thesis. Universidad Autónoma del Estado de Morelos
Choshniak I, Yahav S (1987) Can desert rodents better utilize low quality roughage than their non-desert kindred? J Arid Environ 12:241–246. https://doi.org/10.1016/S0140-1963(18)31168-6
Cruz-Neto AP, Jones KE (2006) Exploring the evolution of the basal metabolic rate in bats. In: Zubaid A, McCracken GFM, Kunz TH (eds) Functional and evolutionary ecology of bats. New York, United States
Dearing MD (1997) The manipulation of plant toxins by a food-hoarding herbivore, Ochotona princeps. Ecology 78:774–781. https://doi.org/10.1890/0012-9658(1997)078[0774:TMOPTB]2.0.CO;2
Dearing MD, Cork S (1999) The role of detoxification of plant secondary com- pounds on diet breadth in mammalian herbivores. J Chem Ecol 25:1205–1220. https://doi.org/10.1023/A:1020958221803
Drent RH, Daan S (1980) The prudent parent: energetic adjustments in avian breeding 1. Ardea 55:225–252. https://doi.org/10.5253/arde.v68.p225
Fenton MB (2004) Bat natural history and echolocation. Bat Echolocation Research: tools, techniques and analysis 2
Fleming TH, Kress WJ (2019) The ornaments of life: coevolution and conservation in the tropics. United States, Chicago
Geluso K, Hayes JP (1999) Effects of dietary quality on basal metabolic rate and internal morphology of European starlings (Sturnus vulgaris). Physiol Biochem Zool 72:189–197. https://doi.org/10.1086/316654
Genoud M, Isler K, Martin RD (2018) Comparative analyses of basal rate of metabolism in mammals: data selection does matter. Biol Rev 93:404–438. https://doi.org/10.1111/brv.12350
Hastie T, Tibshirani R (1990) Exploring the nature of covariate effects in the proportional hazards model. Biometrics. https://doi.org/10.2307/2532444
INEGI (2005) ;2014;2016). Instituto Nacional de Estadística y Geografía (México). Guía para la interpretación de cartografía: uso del suelo y vegetación: escala 1:250, 000: serie VI / Instituto Nacional de Estadística y Geografía. México: INEGI, 2017. 7:204
Karasov WH, del Martínez C (2007) Physiological ecology: how animals process energy, nutrients, and toxins. New Jersey, United States
Karasov WH, Hume ID (2010) Vertebrate gastrointestinal system. Compr Physiol. https://doi.org/10.1002/cphy.cp130107
Kleiber M (1932) Body size and metabolism. Hilgardia 6:315–353
Klite PD (1965) Intestinal bacterial flora and transit time of three Neotropical bat species. J Bacteriol 90:375–379. https://doi.org/10.1128/jb.90.2.375-379.1965
Lighton JR (2018) Measuring metabolic rates: a manual for scientists, 2ed edn. edn. Oxford, United kingdom
Lighton JR, Halsey LG (2011) Flow-through respirometry applied to chamber systems: pros and cons, hints and tips. Comp Biochem Physiol Mol Integr Physiol 158:265–275. https://doi.org/10.1016/j.cbpa.2010.11.026
McNab BK (1986) The influenceof food habits on the energetics of eutherian mammals. Ecol Monogr 56:1–19. https://doi.org/10.2307/2937268
McNab BK (2000) Energy constraints on carnivore diet. Nature 407:584–584. https://doi.org/10.1038/35036695
McNab BK (2002) Minimizing energy expenditure facilitates vertebrate persistence on oceanic islands. Ecol Lett 5:693–704. https://doi.org/10.1046/j.1461-0248.2002.00365.x
McNab BK (2012) Extreme measures: the ecological energetics of birds and mammals. University of Chicago Press, EE.UU
Medellín RA, Arita AT, Sanchez-Herrera O (2008) Identificación de Los Murcieélagos de méxico: Clave de Campo. México, Ciudad de México
Medina-Bello KI, Orozco-Lugo CL, Ayala-Berdon J (2023) Differences in thermal energetics of the cave myotis (Myotis velifer) from a cool and a warm environment of central Mexico. Can J Zool 101:1115–1123. https://doi.org/10.1139/cjz-2022-0190
Munshi-South J, Wilkinson GS (2010) Bats and birds: exceptional longevity despite high metabolic rates. Ageing Res Rev 9:12–19. https://doi.org/10.1016/j.arr.2009.07.006
Oliver JE (2008) Encyclopedia of world climatology. Springer science & business media, EE.UU
Paradis E, Schliep K (2019) Ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35:526–528. https://doi.org/10.1093/bioinformatics/bty633
Perry RW, Carter SA, Thill RE (2010) Temporal patterns in capture rate and sex ratio of forest bats in Arkansas. Am Midl Nat 164:270–282. https://doi.org/10.1674/0003-0031-164.2.270
Peterson J, Bihain BE, Bengtsson-Olivecrona G, Deckelbaum RJ, Carpentier YA, Olivecrona T (1990) Fatty acid control of lipoprotein lipase: a link between energy metabolism and lipid transport. Proc Natl Acad Sci U S A 87:909–913
Pinheiro J, Bates D (2000) Mixed-effects models in S and S-PLUS. Springer science & business media, EE.UU
Porter K, Prescott D, Frye J (1973) Changes in surface morphology of Chinese hamster ovary cells during the cell cycle. J Cell Biol 57:815–836. https://doi.org/10.1083/jcb.57.3.815
Qiao GH, Yu CQ, Li JH, Yang X, Zhu XQ, Zhou XH (2013) Effect of high altitude on nutrient digestibility, rumen fermentation and basal metabolism rate in Chinese Holstein cows on the Tibetan plateau. Anim Prod Sci 53:240–246. https://doi.org/10.1071/AN12109
Ramírez-Pulido J, González-Ruiz N, Gardner AL, Arroyo-Cabrales J (2014) List of recent land mammals of Mexico, 2014
Roswag A, Becker NI, Encarnação JA (2012) Inter-and intraspecific comparisons of retention time in insectivorous bat species (Vespertilionidae). J Zool 288:85–92. https://doi.org/10.1111/j.1469-7998.2012.00927.x
Schmidt-Nielsen K (1997) Animal physiology: adaptation and environment, 5rd edn. Cambridge, United Kingdom
Speakman JR (2005) Body size, energy metabolism and lifespan. J Exp Biol 208:1717–1730. https://doi.org/10.1242/jeb.01556
Speakman JR, Thomas DW (2003) Physiological ecology and energetics of bats. In: Kunz TH, Fenton MB (eds) Bat ecology. United States, Chicago, pp 430–490
Staliński J (1994) Digestion, defecation and food passage rate in the insectivorous bat Myotis myotis. Acta Theriol 39:1–11
Stevens CE, Hume ID (1995) Comparative physiology of the vertebrate digestive system, 2ed edn. edn. North Carolina, United States
Stevens CE, Hume ID (1998) Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. Physiol Rev 78:393–427. https://doi.org/10.1152/physrev.1998.78.2.393
Vazquez-Dominguez G (2016) Plasticidad digestiva estacional del murciélago nectarívoro Glossophaga soricina (phyllostomidae: glossophaginae). Master’s thesis. Universidad Nacional Autónoma de México
Veloso C, Bozinovic F (1993) Dietary and digestive constraints on basal energy metabolism in a small herbivorous rodent. Ecology 74:2003–2010. https://doi.org/10.2307/1940843
Villers Ruiz L, García FR, Lezama PT (2006) Guia botanica Del Parque Nacional Malinche. Universidad Autónoma de México, Mexico
Warton DI, Wright ST, Wang Y (2012) Distance-based multivariate analyses confound location and dispersion effects. Methods Ecol Evol 3:89–101. https://doi.org/10.1111/j.2041-210X.2011.00127.x
West GB, Brown JH (2005) The origin of allometric scaling laws in biology from genomes to ecosystems: towards a quantitative unifying theory of biological structure and organization. J Exp Biol 208:1575–1592. https://doi.org/10.1242/jeb.01589
Wilkinson GS, Adams DM (2019) Recurrent evolution of extreme longevity in bats. Biol Lett 15:20180860. https://doi.org/10.1098/rsbl.2018.0860
Wilkinson GS, Brunet-Rossinni AK (2009) Methods for age Estimation and the study of senescence in bats. Ecological and behavioral methods for the study of bats, pp 315–325
Wood S, Docs (2017) mgcv-package Mixed GAM Computation Vehicle with GCV/AIC/REML smoothness estimation and GAMMs by REML/PQL. Docs. W3cub. Com.
Zeileis A, Hothorn T (2002) Diagnostic checking in regression relationships. R News 2:7–10
Acknowledgements
The authors acknowledge support by the program CONACYT FOSEC CB2017-2018 (A1-S-39572) Granted to JAB, to all students involved in bats’ captures, and La Malinche, La Mancha, and Quilamula Biological stations for logistical support.
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Conceptualization: Jorge Ayala-Berdon, Methodology: Jorge Ayala-Berdon and Kevin I. Medina-Bello, Formal analysis and investigation: Jorge Ayala-Berdon, Writing - original draft preparation: Jorge Ayala-Berdon, Kevin I. Medina-Bello, Lorena Orozco-Lugo, Ignacio Íñiguez-Dávalos, Antonio Guillén-Servent, and Margarita Martínez-Gómez, Funding acquisition: Jorge Ayala-Berdon.
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Bat care and housing of the bats was carried out with the permission of the Secretaria de Medio Ambiente y Recursos Naturales de México (SEMARNAT: SGPA/DGVS/06795/21).
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Ayala-Berdon, J., Medina-Bello, K.I., Orozco-Lugo, L. et al. Linking digestive efficiency and climate to basal metabolic rate in bats of the family vespertilionidae. J Comp Physiol B (2025). https://doi.org/10.1007/s00360-025-01630-3
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DOI: https://doi.org/10.1007/s00360-025-01630-3