Abstract
Many studies assume that it is beneficial for individuals of a species to be heavier, or have a higher body condition index (BCI), without accounting for the physiological relevance of variation in the composition of different body tissues. We hypothesized that the relationship between BCI and masses of physiologically important tissues (fat and lean) would be conditional on annual patterns of energy acquisition and expenditure. We studied three species with contrasting ecologies in their respective natural ranges: an obligate hibernator (Columbian ground squirrel, Urocitellus columbianus), a facultative hibernator (black-tailed prairie dog, Cynomys ludovicianus), and a food-caching non-hibernator (North American red squirrel, Tamiasciurus hudsonicus). We measured fat and lean mass in adults of both sexes using quantitative magnetic resonance (QMR). We measured body mass and two measures of skeletal structure (zygomatic width and right hind foot length) to develop sex- and species-specific BCIs, and tested the utility of BCI to predict body composition in each species. Body condition indices were more consistently, and more strongly correlated, with lean mass than fat mass. The indices were most positively correlated with fat when fat was expected to be very high (pre-hibernation prairie dogs). In all cases, however, BCI was never better than body mass alone in predicting fat or lean mass. While the accuracy of BCI in estimating fat varied across the natural histories and annual energetic patterns of the species considered, measuring body mass alone was as effective, or superior in capturing sufficient variation in fat and lean in most cases.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data for this study (Wishart et al. 2023) are archived on FigShare: https://doi.org/10.6084/m9.figshare.21899007.
Code availability
Code for analysis is available on GitHub at https://github.com/aewishart/bci-composition.
References
Andersen R, Gaillard J-M, Linnell JD, Duncan P (2000) Factors affecting maternal care in an income breeder, the European roe deer. J Anim Ecol 69:672–682
Bairlein F (2002) How to get fat: nutritional mechanisms of seasonal fat accumulation in migratory songbirds. Naturwissenschaften 89:1–10. https://doi.org/10.1007/s00114-001-0279-6
Blackwell GL, Bassett SM, Dickman CR (2006) Measurement error associated with external measurements commonly used in small-mammal studies. J Mammal 87:216–223. https://doi.org/10.1644/05-MAMM-A-215R1.1
Boag DA, Murie JO (1981) Weight in relation to sex, age, and season in Columbian ground squirrels (Sciuridae: Rodentia). Can J Zool 59:999–1004. https://doi.org/10.1139/z81-139
Bonte D, De La Peña E (2009) Evolution of body condition-dependent dispersal in metapopulations. J Evol Biol 22:1242–1251. https://doi.org/10.1111/j.1420-9101.2009.01737.x
Boutin S, Larsen KW (1993) Does food availability affect growth and survival of males and females differently in a promiscuous small mammal, Tamiasciurus hudsonicus? J Anim Ecol 62:364–370
Boyer BB, Barnes BM (1999) Molecular and metabolic aspects of mammalian hibernation. Bioscience 49:713–724. https://doi.org/10.2307/1313595
Brigham RM, Geiser F (2012) Do red squirrels (Tamiasciurus hudsonicus) use daily torpor during winter? Écoscience 19:127–132. https://doi.org/10.2980/19-2-3464
Broussard DR, Dobson FS, Murie JO (2005) The effects of capital on an income breeder: evidence from female Columbian ground squirrels. Can J Zool 83:546–552. https://doi.org/10.1139/z05-044
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York
Chang AM, Wiebe KL (2016) Body condition in Snowy Owls wintering on the prairies is greater in females and older individuals and may contribute to sex-biased mortality. Auk 133:738–746. https://doi.org/10.1642/AUK-16-60.1
Dantzer B, McAdam AG, Humphries MM et al (2020) Decoupling the effects of food and density on life-history plasticity of wild animals using field experiments: insights from the steward who sits in the shadow of its tail, the North American red squirrel. J Anim Ecol 89:2397–2414. https://doi.org/10.1111/1365-2656.13341
Dittus WPJ (2013) Arboreal adaptations of body fat in wild toque macaques (Macaca sinica) and the evolution of adiposity in primates. Am J Phys Anthropol 152:333–344. https://doi.org/10.1002/ajpa.22351
Dobson FS (1992) Body mass, structural size, and life-history patterns of the Columbian ground squirrel. Am Nat 140:109–125
Dobson FS, Badry MJ, Geddes C (1992) Seasonal activity and body mass of Columbian ground squirrels. Can J Zool 70:1364–1368. https://doi.org/10.1139/z92-192
Fletcher QE, Boutin S, Lane JE et al (2010) The functional response of a hoarding seed predator to mast seeding. Ecology 91:2673–2683. https://doi.org/10.1890/09-1816.1
Fletcher QE, Landry-Cuerrier M, Boutin S et al (2013) Reproductive timing and reliance on hoarded capital resources by lactating red squirrels. Oecologia 173:1203–1215. https://doi.org/10.1007/s00442-013-2699-3
Fletcher QE, Speakman JR, Boutin S et al (2015) Daily energy expenditure during lactation is strongly selected in a free-living mammal. Funct Ecol 29:195–208. https://doi.org/10.1111/1365-2435.12313
Glazier DS (2005) Beyond the ‘3/4-power law’: variation in the intra- and interspecific scaling of metabolic rate in animals. Biol Rev 80:611–662. https://doi.org/10.1017/S1464793105006834
Green AJ (2001) Mass/length residuals: measures of body condition or generators of spurious results? Ecology 82:1473. https://doi.org/10.2307/2680003
Guglielmo CG, McGuire LP, Gerson AR, Seewagen CL (2011) Simple, rapid, and non-invasive measurement of fat, lean, and total water masses of live birds using quantitative magnetic resonance. J Ornithol 152:75–85. https://doi.org/10.1007/s10336-011-0724-z
Gummer DL (2005) Geographic variation in torpor patterns: the northernmost prairie dogs and kangaroo rats. Doctoral thesis, Department of Biology, University of Saskatchewan
Harris MA, Steudel K (2002) The relationship between maximum jumping performance and hind limb morphology/physiology in domestic cats (Felis silvestris catus). J Exp Biol 205:3877–3889. https://doi.org/10.1242/jeb.205.24.3877
Hawkshaw DM (2022) Covariates of intraspecific variation in hibernation expression in the northernmost population of black-tailed prairie dogs. University of Saskatchewan, Saskatoon
Humphries MM, Thomas DW, Kramer DL (2003) The role of energy availability in mammalian hibernation: a cost-benefit approach. Physiol Biochem Zool 76:165–179. https://doi.org/10.1086/367950
Humphries MM, Boutin S, Thomas DW et al (2005) Expenditure freeze: the metabolic response of small mammals to cold environments. Ecol Lett 8:1326–1333. https://doi.org/10.1111/j.1461-0248.2005.00839.x
Jacobs SR, Elliott K, Guigueno MF et al (2012) Determining seabird body condition using nonlethal measures. Physiol Biochem Zool 85:85–95. https://doi.org/10.1086/663832
Jakob EM, Marshall SD, Uetz GW, Estimating GW (1996) Estimating fitness: a comparison of body condition indices. Oikos 77:61–67
Jenni L, Jenni-Eiermann S (1998) Fuel supply and metabolic constraints in migrating birds. J Avian Biol 29:521–528
Johnson MS, Smith DL, Nagy TR et al (2009) Validation of quantitative magnetic resonance (QMR) for determination of body composition in rats. Int J Body Compos Res 7:99–107. https://doi.org/10.1097/MCA.0000000000000178
Jones AS, Johnson MS, Nagy TR (2009) Validation of quantitative magnetic resonance for the determination of body composition of mice. Int J Body Compos Res 7:67–72
Kelly CD, Tawes BR, Worthington AM (2014) Evaluating indices of body condition in two cricket species. Ecol Evol 4:4476–4487. https://doi.org/10.1002/ece3.1257
Kelsey NA, Bairlein F (2019) Migratory body mass increase in Northern Wheatears (Oenanthe oenanthe) is the accumulation of fat as proven by quantitative magnetic resonance. J Ornithol 160:389–397. https://doi.org/10.1007/s10336-018-1621-5
Krebs CJ, Singleton GR (1993) Indices of condition for small mammals. Aust J Zool 41:317–323. https://doi.org/10.1071/ZO9930317
Kusch JM, Matzke CC, Lane JE (2020) Reproductive failure predicts intracolony dispersal of female black-tailed prairie dogs (Cynomys ludovicianus) in a northern population. West North Am Nat 80:157–164. https://doi.org/10.3398/064.080.0203
Kusch JM, Conway SE, Kapchinske A, Lane JE (2021) Reproductive phenology and seasonal mass dynamics of black-tailed prairie dogs (Cynomys ludovicianus) at their northern range limit. Can J Zool 99:257–268. https://doi.org/10.1139/cjz-2020-0054
Lane JE, Czenze ZJ, Findlay-Robinson R, Bayne E (2019) Phenotypic plasticity and local adaptation in a wild hibernator evaluated through reciprocal translocation. Am Nat 194:516–528. https://doi.org/10.1086/702313
Lehmer EM, Van Horne B (2001) Seasonal changes in lipids, diet, and body composition of free-ranging black-tailed prairie dogs (Cynomys ludovicianus). Can J Zool 79:955–965. https://doi.org/10.1139/cjz-79-6-955
Lehmer EM, Savage LT, Antolin MF, Biggins DE (2006) Extreme plasticity in thermoregulatory behaviors of free-ranging black-tailed prairie dogs. Physiol Biochem Zool 79:454–467. https://doi.org/10.1086/502816
Lindström Å, Piersoma T (1993) Mass changes in migrating birds: the evidence for fat and protein storage re-examined. Ibis 135:70–78. https://doi.org/10.1111/j.1474-919X.1993.tb02811.x
Martin JGA, Festa-Bianchet M, Côté SD, Blumstein DT (2013) Detecting between-individual differences in hind-foot length in populations of wild mammals. Can J Zool 91:118–123. https://doi.org/10.1139/cjz-2012-0210
McAdam AG, Boutin S, Sykes AK, Humphries MM (2007) Life histories of female red squirrels and their contributions to population growth and lifetime fitness. Écoscience 14:362–369. https://doi.org/10.2980/1195-6860(2007)14[362:LHOFRS]2.0.CO;2
McGilvery RW (1983) Biochemistry, a functional approach. Saunders, Philadelphia
McGuire LP, Guglielmo CG (2010) Quantitative magnetic resonance: a rapid, noninvasive body composition analysis technique for live and salvaged bats. J Mammal 91:1375–1380. https://doi.org/10.1644/10-MAMM-A-051.1.Key
McGuire LP, Kelly LA, Baloun DE et al (2018) Common condition indices are no more effective than body mass for estimating fat stores in insectivorous bats. J Mammal 99:1065–1071. https://doi.org/10.1093/jmammal/gyy103
McGuire LP, Fuller NW, Haase CG et al (2022) Lean mass dynamics in hibernating bats and implications for energy and water budgets. Physiol Biochem Zool 95:317–325. https://doi.org/10.1086/720160
Mejías C, Navedo JG, Sabat P et al (2022) Body composition and energy savings by hibernation: lessons from the South American marsupial Dromiciops gliroides. Physiol Biochem Zool 95:239–250. https://doi.org/10.1086/719932
Meyers P, Master LL (1983) Reproduction by Peromyscus manuculatus: size and compromise. J Mammal 64:1–18. https://doi.org/10.2307/1380746
Molnár PK, Klanjscek T, Derocher AE et al (2009) A body composition model to estimate mammalian energy stores and metabolic rates from body mass and body length, with application to polar bears. J Exp Biol 212:2313–2323. https://doi.org/10.1242/jeb.026146
Moya-Laraño J, Macías-Ordóñez R, Blanckenhorn WU, Fernández-Montraveta C (2008) Analysing body condition: mass, volume or density? J Anim Ecol 77:1099–1108. https://doi.org/10.1111/j.1365-2656.2008.01433.x
Peig J, Green AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118:1883–1891. https://doi.org/10.1111/j.1600-0706.2009.17643.x
R Core Team (2020) R: a language and environment for statistical computing. R Core Team, Vienna
Reynolds DS, Kunz TH (2001) Standard methods for destructive body composition analysis. In: Speakman JR (ed) Body composition analysis of animals: a handbook of non-destructive methods. Cambridge University Press, Cambridge
Schulte-Hostedde AI, Millar JS, Hickling GJ (2001) Evaluating body condition in small mammals. Can J Zool 79:1021–1029. https://doi.org/10.1139/cjz-79-6-1021
Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass-size residuals: validating body condition indices. Ecology 86:155–163. https://doi.org/10.1890/04-0232
Shimer HW (1903) Adaptations to aquatic, arboreal, fossorial and cursorial habits in mammals. III. Fossorial Habitats. Am Nat 37:819–825. https://doi.org/10.1086/278368
Smith MC (1968) Red squirrel responses to spruce cone failure in interior Alaska. J Wildl Manag 32:305–317. https://doi.org/10.2307/3798975
Stevenson RD, Woods WA (2006) Condition indices for conservation: new uses for evolving tools. Integr Comp Biol 46:1169–1190. https://doi.org/10.1093/icb/icl052
Studd EK, Boutin S, McAdam AG, Humphries MM (2016) Nest attendance of lactating red squirrels (Tamiasciurus hudsonicus): influences of biological and environmental correlates. J Mammal 97:806–814. https://doi.org/10.1093/jmammal/gyw010
Swallow JG, Wroblewska AK, Waters RP et al (2010) Phenotypic and evolutionary plasticity of body composition in rats selectively bred for high endurance capacity. J Appl Physiol 109:778–785. https://doi.org/10.1152/japplphysiol.01026.2009
Taylor CR, Heglund NC, Maloiy GM (1982) Energetics and mechanics of terrestrial locomotion. I. Metabolic energy consumption as a function of speed and body size in birds and mammals. J Exp Biol 97:1–21
Tidhar WL, Speakman JR (2007) An evaluation of four non-destructive methods for predicting body composition in a small rodent. Int J Body Compos Res 5:137–145
Tinsley FC, Taicher GZ, Heiman ML (2004) Evaluation of a quantitative magnetic resonance method for mouse whole body composition analysis. Obes Res 12:150–160. https://doi.org/10.1038/oby.2004.20
Trombulak SC (1989) Running speed and body mass in Belding’s ground squirrels. J Mammal 70:194–197
Weatherhead PJ, Brown GP (1996) Measurement versus estimation of condition in snakes. Can J Zool 74:1617–1621. https://doi.org/10.1139/z96-179
Wells CP, Wilson JA, Kelt DA, Van VDH (2019) Body mass as an estimate of female body condition in a hibernating small mammal. Can Field Nat 133:34–42. https://doi.org/10.22621/cfn.v133i1.2073
Wikelski M, Cooke SJ (2006) Conservation physiology. Trends Ecol Evol 21:38–46. https://doi.org/10.1016/j.tree.2005.10.018
Wilson AJ, Nussey DH (2010) What is individual quality? An evolutionary perspective. Trends Ecol Evol 25:207–214. https://doi.org/10.1016/j.tree.2009.10.002
Wishart AE (2023) Variation in resource acquisition in a food-caching mammal, the North American red squirrel (Tamiasciurus hudsonicus). Doctoral thesis, Department of Biology, University of Saskatchewan. https://harvest.usask.ca/handle/10388/15058
Wishart AE, Guerrero-Chacón AL, Smith R, Hawkshaw DM, McAdam AG, Dantzer B, Boutin S, Lane JE (2023) Data for: inferring condition in wild mammals: body condition indices confer no benefit over measuring body mass across ecological contexts. Figshare. https://doi.org/10.6084/m9.figshare.21899007
Woodward G, Ebenman B, Emmerson M et al (2005) Body size in ecological networks. Trends Ecol Evol 20:402–409. https://doi.org/10.1016/j.tree.2005.04.005
Young PJ (1990) Hibernating patterns of free-ranging Columbian ground squirrels. Oecologia 83:504–511. https://doi.org/10.1007/BF00317201
Zanghi BM, Cupp CJ, Pan Y et al (2013) Noninvasive measurements of body composition and body water via quantitative magnetic resonance, deuterium water, and dual-energy X-ray absorptiometry in cats. Am J Vet Res 74:721–732. https://doi.org/10.2460/ajvr.74.5.733
Acknowledgements
We thank Agnes MacDonald for long-term access to her trap-line, and to the Champagne and Aishihik First Nations for allowing us to conduct fieldwork related to red squirrels within their traditional territory. Fieldwork related to prairie dogs was conducted in Treaty 4 territory, the traditional territory of the Oceti Sakowin and Niitsitpiis-stahkoii, and the homeland of the Métis Nation. Fieldwork related to ground squirrels was conducted in Treaty 7 territory, the traditional territories of the Blackfoot Confederacy (Siksika, Piikani, and Kainai First Nations), the Tsuut’ina First Nation, the Stoney Nakoda (Chiniki, Bearspaw, and Wesley First Nations) and homeland of the Métis Nation. We thank the many volunteers, graduate students, and field assistants, including Jillian Kusch, Tessie Aujla, Jack Hendrix, Ashley Mills, Emily Kelvin, Megan Miller, M. Alejandra Hurtado, and Gabriela Heyer for field data collection, and Grasslands National Park staff for assistance with permitting and logistical support. AEW thanks Dr. Kurtis Swekla and Dr. Todd Shury for professional veterinary services in developing anesthesia protocols for red squirrels.
Funding
The authors are grateful for ongoing funding from the Natural Sciences and Engineering Research Council (SB, JEL, AGM), Canadian Foundation for Innovation (AGM, JEL), and the National Science Foundation (BD, AGM). Fieldwork for this study was further supported by the Northern Scientific Training Program (AEW), Sigma Xi Grant-in-Aid-of-Research (AEW, RS), American Society of Mammalogists Grant-in-Aid-of-Research (AEW, ALGC, RS), the American Museum of Natural History Theodore Roosevelt Memorial Fund (ALGC) and the Alberta Conservation Association (ALGC, RS). This is article no. 127 of the Kluane Red Squirrel Project.
Author information
Authors and Affiliations
Contributions
AEW designed the study, collected data, performed data and statistical analysis, and drafted the manuscript. JEL participated in the design. All authors contributed to data collection, provided valuable discussion and contributions to the writing of the manuscript, and gave final approval for publication.
Corresponding author
Ethics declarations
Conflict of interest
We have no competing interests.
Ethics approval
All procedures were approved by the University of Saskatchewan Animal Research Ethics Board. Fieldwork was completed under permits issued by Yukon Territorial Government (red squirrels); Grasslands National Park and the Saskatchewan Ministry of the Environment (prairie dogs); and Alberta Parks (ground squirrels).
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Communicated by John Loehr.
The utility of body condition indices to approximate energetically significant tissues (fat and lean mass) varies with a species' natural history, and when they are measured during the annual cycle.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Wishart, A.E., Guerrero-Chacón, A.L., Smith, R. et al. Inferring condition in wild mammals: body condition indices confer no benefit over measuring body mass across ecological contexts. Oecologia 204, 161–172 (2024). https://doi.org/10.1007/s00442-023-05495-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-023-05495-7