Visually assessed body condition shows high heritability in a pedigreed great ape population.
animal models
body condition score
bonobo
relative fat mass
Journal
American journal of primatology
ISSN: 1098-2345
Titre abrégé: Am J Primatol
Pays: United States
ID NLM: 8108949
Informations de publication
Date de publication:
10 2023
10 2023
Historique:
revised:
28
06
2023
received:
09
02
2023
accepted:
18
07
2023
medline:
13
9
2023
pubmed:
29
7
2023
entrez:
28
7
2023
Statut:
ppublish
Résumé
Body condition, a measure for relative fat mass, is associated with primate health, fitness, and overall welfare. Body condition is often influenced by dietary factors, age, and/or sex, but several body condition measures (body weight, weight-to-height ratios, and so on) also show high heritability across primate species, indicating a role of genetic effects. Although different measures for body condition exist, many require direct handling of animals, which is invasive, time-consuming, and expensive, making them impractical in wild and captive settings. Therefore, noninvasive visual body condition score (BCS) systems were developed for various animal species, including macaques and chimpanzees, to visually assess relative fat mass. Here we evaluate the utility of a visual BCS system in bonobos by assessing (1) inter-rater reliability, (2) links with body mass, a traditional hands-on measure of condition, and (3) the factors driving individual variation in BCS. We adapted the chimpanzee BCS system to rate 76 bonobos in 11 European zoos (92% of the adult population). Inter-rater reliability was high (s* = 0.948), BCSs were positively associated with body mass (β = 0.075) and not predicted by diet, sex, or age, nor were they associated with a higher abundance of obesity-related diseases. Instead, BCSs showed high levels of heritability (h
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e23540Informations de copyright
© 2023 Wiley Periodicals LLC.
Références
Alapati, A., Kapa, S. R., Jeepalyam, S., Rangappa, S. M. P., & Yemireddy, K. R. (2010). Development of the body condition score system in Murrah buffaloes: Validation through ultrasonic assessment of body fat reserves. Journal of Veterinary Science, 11(1), 1-8. https://doi.org/10.4142/jvs.2010.11.1.1
Arango, J. A., Cundiff, L. V., & Van Vleck, L. D. (2002). Comparisons of Angus-, Braunvieh-, Chianina-, Hereford-, Gelbvieh-, Maine Anjou-, and Red Poll-sired cows for weight, weight adjusted for body condition score, height, and body condition score. Journal of Animal Science, 80(12), 3133-3141. https://doi.org/10.2527/2002.80123133x
Bales, K., O'Herron, M., Baker, A. J., & Dietz, J. M. (2001). Sources of variability in numbers of live births in wild golden lion tamarins (Leontopithecus rosalia). American Journal of Primatology, 54(4), 211-221. https://doi.org/10.1002/ajp.1031
Bauer, S. A., Pearl, D. L., Leslie, K. E., Fournier, J., & Turner, P. V. (2012). Causes of obesity in captive cynomolgus macaques: Influence of body condition, social and management factors on behaviour around feeding. Laboratory Animals, 46(3), 193-199. https://doi.org/10.1258/la.2012.011120
Bercovitch, F. B., Lebron, M. R., Martinez, H. S., & Kessler, M. J. (1998). Primigravidity, body weight, and costs of rearing first offspring in rhesus macaques. American Journal of Primatology, 46(2), 135-144. https://doi.org/10.1002/(SICI)1098-2345(1998)46:2<135::AID-AJP3>3.0.CO;2-X
Berghänel, A., Stevens, J., Hohmann, G., Deschner, T., & Behringer, V. (2023). Adolescent length growth spurts in bonobos and other primates: Mind the scale. eLife, 12, RP86635. https://doi.org/10.7554/eLife.86635
Berman, C. M., & Schwartz, S. (1988). A nonintrusive method for determining relative body fat in free-ranging monkeys. American Journal of Primatology, 14(1), 53-64. https://doi.org/10.1002/ajp.1350140105
Berry, D. P., Buckley, F., Dillon, P., Evans, R. D., Rath, M., & Veerkamp, R. F. (2002). Genetic parameters for level and change of body condition score and body weight in dairy cows. Journal of Dairy Science, 85(8), 2030-2039. https://doi.org/10.3168/jds.S0022-0302(02)74280-X
Borg, R. C., Notter, D. R., & Kott, R. W. (2009). Phenotypic and genetic associations between lamb growth traits and adult ewe body weights in western range sheep. Journal of Animal Science, 87(11), 3506-3514. https://doi.org/10.2527/jas.2008-1622
Cai, G., Cole, S. A., Tejero, M. E., Proffitt, J. M., Freeland-Graves, J. H., Blangero, J., & Comuzzie, A. G. (2004). Pleiotropic effects of genes for insulin resistance on adiposity in baboons. Obesity Research, 12(11), 1766-1772. https://doi.org/10.1038/oby.2004.219
Clauss, M., Wilkins, T., Hartley, A., & Hatt, J.-M. (2009). Diet composition, food intake, body condition, and fecal consistency in captive tapirs (Tapirus spp.) in UK collections. Zoo Biology, 28(4), 279-291. https://doi.org/10.1002/zoo.20225
Clavadetscher, I., Bond, M., Martin, L., Schiffmann, C., Hatt, J.-M., & Clauss, M. (2021). Development of an image-based body condition score for giraffes Giraffa camelopardalis and a comparison of zoo-housed and free-ranging individuals. Journal of Zoo and Aquarium Research, 9(3), 170-185. https://doi.org/10.19227/jzar.v9i3.615
Clingerman, K. J., & Summers, L. (2005). Development of a body condition scoring system for nonhuman primates using Macaca mulatta as a model. Lab Animal, 34(5), 31-36. https://doi.org/10.1038/laban0505-31
Clingerman, K. J., & Summers, L. (2012). Validation of a body condition scoring system in rhesus macaques (Macaca mulatta): Inter- and intrarater variability. Journal of the American Association for Laboratory Animal Science: JAALAS, 51(1), 31-36.
Cocks, L. (2007). Factors influencing the well-being and longevity of captive female orangutans. International Journal of Primatology, 28(2), 429-440.
Colman, R. J., Hudson, J. C., Barden, H. S., & Kemnitz, J. W. (1999). A comparison of dual-energy X-ray absorptiometry and somatometrics for determining body fat in rhesus macaques. Obesity Research, 7(1), 90-96. https://doi.org/10.1002/j.1550-8528.1999.tb00395.x
Comuzzie, A. G., Cole, S. A., Martin, L., Carey, K. D., Mahaney, M. C., Blangero, J., & VandeBerg, J. L. (2003). The baboon as a nonhuman primate model for the study of the genetics of obesity. Obesity Research, 11(1), 75-80. https://doi.org/10.1038/oby.2003.12
Dal Zotto, R., De Marchi, M., Dalvit, C., Cassandro, M., Gallo, L., Carnier, P., & Bittante, G. (2007). Heritabilities and genetic correlations of body condition score and calving interval with yield, somatic cell score, and linear type traits in brown Swiss cattle. Journal of Dairy Science, 90(12), 5737-5743. https://doi.org/10.3168/jds.2007-0280
Dechow, C. D., Rogers, G. W., & Clay, J. S. (2001). Heritabilities and correlations among body condition scores, production traits, and reproductive performance. Journal of Dairy Science, 84(1), 266-275. https://doi.org/10.3168/jds.S0022-0302(01)74476-1
Deschner, T., Kratzsch, J., & Hohmann, G. (2008). Urinary C-peptide as a method for monitoring body mass changes in captive bonobos (Pan paniscus). Hormones and Behavior, 54(5), 620-626. https://doi.org/10.1016/j.yhbeh.2008.06.005
Domecq, J. J., Skidmore, A. L., Lloyd, J. W., & Kaneene, J. B. (1995). Validation of body condition scores with ultrasound measurements of subcutaneous fat of dairy cows. Journal of Dairy Science, 78(10), 2308-2313. https://doi.org/10.3168/jds.S0022-0302(95)76857-6
Dong, T. S., Mayer, E. A., Osadchiy, V., Chang, C., Katzka, W., Lagishetty, V., Gonzalez, K., Kalani, A., Stains, J., Jacobs, J. P., Longo, V. D., & Gupta, A. (2020). A distinct brain-gut-microbiome profile exists for females with obesity and food addiction. Obesity, 28(8), 1477-1486.
Drews, B., Harmann, L. M., Beehler, L. L., Bell, B., Drews, R. F., & Hildebrandt, T. B. (2011). Ultrasonographic monitoring of fetal development in unrestrained bonobos (Pan paniscus) at the Milwaukee County Zoo. Zoo Biology, 30(3), 241-253. https://doi.org/10.1002/zoo.20304
Druelle, F., Schoonaert, K., Aerts, P., Nauwelaerts, S., Stevens, J. M. G., & D'Août, K. (2018). Segmental morphometrics of bonobos (Pan paniscus): Are they really different from chimpanzees (Pan troglodytes)? Journal of Anatomy, 233(6), 843-853. https://doi.org/10.1111/joa.12894
Edes, A. N., & Brand, C. M. (2021). Age, sex, and inflammatory markers predict chronic conditions, cardiac disease, and mortality among captive western lowland gorillas (Gorilla gorilla gorilla). Primates, 62, 931-943. https://doi.org/10.1007/s10329-021-00942-6
Elia, M. (2001). Obesity in the elderly. Obesity Research, 9(S11), 244S-248S. https://doi.org/10.1038/oby.2001.126
Elks, C. E., Den Hoed, M., Zhao, J. H., Sharp, S. J., Wareham, N. J., Loos, R. J. F., & Ong, K. K. (2012). Variability in the heritability of body mass index: A systematic review and meta-regression. Frontiers in Endocrinology, 3, 29. https://www.frontiersin.org/articles/10.3389/fendo.2012.00029
Ellis, K. J., Scheimann, A., & Lee, P. D. K. (2000). Body composition measurements: Clinical and technical considerations. The Endocrinologist, 10(4), 57S-62S.
Ely, J. J., Zavaskis, T., & Lammey, M. L. (2013). Hypertension increases with aging and obesity in chimpanzees (Pan troglodytes). Zoo Biology, 32(1), 79-87. https://doi.org/10.1002/zoo.21044
Ezenwa, V. O., Jolles, A. E., & O'Brien, M. P. (2009). A reliable body condition scoring technique for estimating condition in African buffalo. African Journal of Ecology, 47(4), 476-481. https://doi.org/10.1111/j.1365-2028.2008.00960.x
Fernandes, A. F. A., Neves, H. H. R., Carvalheiro, R., Oliveira, J. A., & Queiroz, S. A. (2015). Body condition score of Nellore beef cows: A heritable measure to improve the selection of reproductive and maternal traits. Animal, 9(8), 1278-1284. https://doi.org/10.1017/S1751731115000154
Fernando, P., Janaka, H. K., Ekanayaka, S. K. K., Nishantha, H. G., & Pastorini, J. (2009). A simple method for assessing elephant body condition. Gajah, 31, 29-31. https://doi.org/10.5167/uzh-32262
Fried, L. P., Ferrucci, L., Darer, J., Williamson, J. D., & Anderson, G. (2004). Untangling the concepts of disability, frailty, and comorbidity: Implications for improved targeting and care. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 59(3), M255-M263. https://doi.org/10.1093/gerona/59.3.M255
German, A. J., Holden, S. L., Moxham, G. L., Holmes, K. L., Hackett, R. M., & Rawlings, J. M. (2006). A simple, reliable tool for owners to assess the body condition of their dog or cat. The Journal of Nutrition, 136(7), 2031S-2033S. https://doi.org/10.1093/jn/136.7.2031S
Hadfield, J. D. (2010). MCMC methods for multi-response generalized linear mixed models: The MCMCglmm R package. Journal of Statistical Software, 33, 1-22. https://doi.org/10.18637/jss.v033.i02
Hämäläinen, A., Dammhahn, M., Aujard, F., Eberle, M., Hardy, I., Kappeler, P. M., Perret, M., Schliehe-Diecks, S., & Kraus, C. (2014). Senescence or selective disappearance? age trajectories of body mass in wild and captive populations of a small-bodied primate. Proceedings of the Royal Society B: Biological Sciences, 281(1791), 20140830. https://doi.org/10.1098/rspb.2014.0830
Heidegger, E. M., von Houwald, F., Steck, B., & Clauss, M. (2016). Body condition scoring system for greater one-horned rhino (Rhinoceros unicornis): Development and application: Rhinoceros bicornis body condition. Zoo Biology, 35(5), 432-443. https://doi.org/10.1002/zoo.21307
Jaquish, C. E., Dyer, T., Williams-Blangero, S., Dyke, B., Leland, M., & Blangero, J. (1997). Genetics of adult body mass and maintenance of adult body mass in captive baboons (Papio hamadryas subspecies). American Journal of Primatology, 42(4), 281-288. https://doi.org/10.1002/(SICI)1098-2345(1997)42:4<281::AID-AJP3>3.0.CO;2-T
Joganic, J. L., Willmore, K. E., Richtsmeier, J. T., Weiss, K. M., Mahaney, M. C., Rogers, J., & Cheverud, J. M. (2018). Additive genetic variation in the craniofacial skeleton of baboons (genus Papio) and its relationship to body and cranial size. American Journal of Physical Anthropology, 165(2), 269-285. https://doi.org/10.1002/ajpa.23349
Johnston, D., Chandler, H., & Graser, H. (1996). Genetic parameters for cow weight and condition score in Angus, Hereford, and Poll Hereford cattle. Australian Journal of Agricultural Research, 47(8), 1251-1260. https://doi.org/10.1071/ar9961251
Kadarmideen, H. N., & Wegmann, S. (2003). Genetic parameters for body condition score and its relationship with type and production traits in Swiss Holsteins. Journal of Dairy Science, 86(11), 3685-3693. https://doi.org/10.3168/jds.S0022-0302(03)73974-5
Kavanagh, K., Fairbanks, L. A., Bailey, J. N., Jorgensen, M. J., Wilson, M., Zhang, L., Rudel, L. L., & Wagner, J. D. (2007). Characterization and heritability of obesity and associated risk factors in vervet monkeys. Obesity, 15(7), 1666-1674. https://doi.org/10.1038/oby.2007.199
Kemnitz, J. W., & Francken, G. A. (1986). Characteristics of spontaneous obesity in male rhesus monkeys. Physiology & Behavior, 38(4), 477-483. https://doi.org/10.1016/0031-9384(86)90414-2
Kempe, R., Koskinen, N., Mäntysaari, E., & Strandén, I. (2010). The genetics of body condition and leg weakness in the blue fox (Alopex lagopus). Acta Agriculturae Scandinavica Section A-Animal Science, 60(3), 141-150. https://doi.org/10.1080/09064702.2010.515241
Kimock, C. M., Dubuc, C., Brent, L. J. N., & Higham, J. P. (2019). Male morphological traits are heritable but do not predict reproductive success in a sexually-dimorphic primate. Scientific Reports, 9(1), 19794. https://doi.org/10.1038/s41598-019-52633-4
Koenig, A., Borries, C., Chalise, M. K., & Winkler, P. (1997). Ecology, nutrition, and timing of reproductive events in an Asian primate, the Hanuman langur (Presbytis entellus). Journal of Zoology, 243(2), 215-235. https://doi.org/10.1111/j.1469-7998.1997.tb02778.x
Kuznetsova, A., Brockhoff, P. B., & Christensen, R. H. B. (2017). lmerTest package: Tests in linear mixed effects models. Journal of Statistical Software, 82, 1-26. https://doi.org/10.18637/jss.v082.i13
Landis, J. R., & Koch, G. G. (1977). The measurement of observer agreement for categorical data. Biometrics, 33(1), 159-174. https://doi.org/10.2307/2529310
Lee, J., Kolonel, L. N., & Hinds, M. W. (1982). Use of an inappropriate weight-height derived index of obesity can produce misleading results. International Journal of Obesity, 6(3), 233-239.
Lowenstine, L. J., McManamon, R., & Terio, K. A. (2016). Comparative pathology of aging great apes: Bonobos, chimpanzees, gorillas, and orangutans. Veterinary Pathology, 53(2), 250-276. https://doi.org/10.1177/0300985815612154
Lundgren, H., Zumbach, B., Lundeheim, N., Grandinson, K., Vangen, O., Olsen, D., & Rydhmer, L. (2012). Heritability of shoulder ulcers and genetic correlations with mean piglet weight and sow body condition. Animal, 6(1), 1-8. https://doi.org/10.1017/S1751731111001170
Marasini, D., Quatto, P., & Ripamonti, E. (2016). Assessing the inter-rater agreement for ordinal data through weighted indexes. Statistical Methods in Medical Research, 25(6), 2611-2633. https://doi.org/10.1177/0962280214529560
Martinez, J. A., Navas-Carretero, S., Saris, W. H. M., & Astrup, A. (2014). Personalized weight loss strategies-The role of macronutrient distribution. Nature Reviews Endocrinology, 10(12), 749-760. https://doi.org/10.1038/nrendo.2014.175
Martinsen, K. H., Ødegård, J., Aasmundstad, T., Olsen, D., & Meuwissen, T. H. E. (2016). Genetic relationships between boar feed efficiency and sow piglet production, body condition score, and stayability in Norwegian Landrace pigs. Journal of Animal Science, 94(8), 3159-3168. https://doi.org/10.2527/jas.2015-0247
Mattison, J. A., Colman, R. J., Beasley, T. M., Allison, D. B., Kemnitz, J. W., Roth, G. S., Ingram, D. K., Weindruch, R., de Cabo, R., & Anderson, R. M. (2017). Caloric restriction improves health and survival of rhesus monkeys. Nature Communications, 8(1), 14063. https://doi.org/10.1038/ncomms14063
Mirza, R. H., Javed, K., Abdullah, M., & Pasha, T. N. (2013). Genetic and non genetic factors affecting body condition score in Nili Ravi buffaloes and its correlation with milk yield. JAPS, Journal of Animal and Plant Sciences, 23(6), 1486-1490.
Morbeck, M. E., & Zihlman, A. L. (1988). Body composition and proportions, Orangutan Biology (pp. 285-297). Oxford University Press. https://apeanatomyevolution.com/wp-content/uploads/2019/03/1988-orangutans.pdf
Morfeld, K. A., Meehan, C. L., Hogan, J. N., & Brown, J. L. (2016). Assessment of body condition in African (Loxodonta africana) and Asian (Elephas maximus) elephants in North American zoos and management practices associated with high body condition scores. PLoS One, 11(7), e0155146. https://doi.org/10.1371/journal.pone.0155146
Murphy, H. W., Danforth, M. D., & Clyde, V. L. (2018). The great ape heart project. International Zoo Yearbook, 52(1), 103-112. https://doi.org/10.1111/izy.12180
Newman, T. M., Shively, C. A., Register, T. C., Appt, S. E., Yadav, H., Colwell, R. R., Fanelli, B., Dadlani, M., Graubics, K., Nguyen, U. T., Ramamoorthy, S., Uberseder, B., Clear, K. Y. J., Wilson, A. S., Reeves, K. D., Chappell, M. C., Tooze, J. A., & Cook, K. L. (2021). Diet, obesity, and the gut microbiome as determinants modulating metabolic outcomes in a non-human primate model. Microbiome, 9(1), 100.
Ndrepepa, G. (2018). Uric acid and cardiovascular disease. Clinica Chimica Acta, 484, 150-163. https://doi.org/10.1016/j.cca.2018.05.046
Nunamaker, E. A., Lee, D. R., & Lammey, M. L. (2012). Chronic diseases in captive geriatric female chimpanzees (Pan troglodytes). Comparative Medicine, 62(2), 131-136.
Obanda, V., Omondi, G. P., & Chiyo, P. I. (2014). The influence of body mass index, age and sex on inflammatory disease risk in semi-captive chimpanzees. PLOS ONE, 9(8), e104602. https://doi.org/10.1371/journal.pone.0104602
Peig, J., & Green, A. J. (2009). New perspectives for estimating body condition from mass/length data: The scaled mass index as an alternative method. Oikos, 118(12), 1883-1891. https://doi.org/10.1111/j.1600-0706.2009.17643.x
Public Health England. (2021). Composition of foods integrated dataset (CoFID). GOV.UK. https://www.gov.uk/government/publications/composition-of-foods-integrated-dataset-cofid
Quatto, P., & Ripamonti, E. (2022). raters: A modification of Fleiss' kappa in case of nominal and ordinal variables (2.0.2) [R]. https://CRAN.R-project.org/package=raters
R Core Team. (2022). R: A language and environment for statistical computing (4.2.2). R Foundation for Statistical Computing. https://www.R-project.org/
Reamer, L. A., Neal Webb, S. J., Jones, R., Thiele, E., Haller, R. L., Schapiro, S. J., Lambeth, S. P., & Hanley, P. W. (2020). Validation and utility of a body condition scoring system for chimpanzees (Pan troglodytes). American Journal of Primatology, 82(10), e23188. https://doi.org/10.1002/ajp.23188
Richard, A. F., Dewar, R. E., Schwartz, M., & Ratsirarson, J. (2000). Mass change, environmental variability and female fertility in wild Propithecus verreauxi. Journal of Human Evolution, 39(4), 381-391. https://doi.org/10.1006/jhev.2000.0427
Sánchez-Guerrero, M. J., Ramos, J., Valdés, M., Rivero, J.-L. L., & Valera, M. (2019). Prevalence, environmental risk factors and heritability of body condition in Pura Raza Español horses. Livestock Science, 230, 103851. https://doi.org/10.1016/j.livsci.2019.103851
Sawaswong, V., Praianantathavorn, K., Chanchaem, P., Khamwut, A., Kemthong, T., Hamada, Y., Malaivijitnond, S., & Payungporn, S. (2021). Comparative analysis of oral-gut microbiota between captive and wild long-tailed macaque in Thailand. Scientific Reports, 11(1), 14280.
Schiffmann, C., Clauss, M., Pastorini, J., Wendler, P., Ertl, N., Hoby, S., Hatt, J.-M., & Fernando, P. (2018). Body condition scores in European zoo elephants (Elephas maximus and Loxodonta africana) - Status quo and influencing factors. Journal of Zoo and Aquarium. Research, 6(3), 91-103. https://doi.org/10.19227/jzar.v6i3.355
Schmitt, C. A., Service, S. K., Jasinska, A. J., Dyer, T. D., Jorgensen, M. J., Cantor, R. M., Weinstock, G. M., Blangero, J., Kaplan, J. R., & Freimer, N. B. (2018). Obesity and obesogenic growth are both highly heritable and modified by diet in a nonhuman primate model, the African green monkey (Chlorocebus aethiops sabaeus). International Journal of Obesity, 42(4), 765-774. https://doi.org/10.1038/ijo.2017.301
Shapiro, S. S., & Wilk, M. B. (1965). An analysis of variance test for normality (complete samples. Biometrika, 52(3/4), 591-611. https://doi.org/10.2307/2333709
Sterck, E. H. M., Zijlmans, D. G. M., Vries, H., den Berg, L. M., Schaik, C. P., & Langermans, J. A. M. (2019). Determining overweight and underweight with a new weight-for-height index in captive group-housed macaques. American Journal of Primatology, 81(6), e22996. https://doi.org/10.1002/ajp.22996
Stevens, J. M. G., Pereboom, J. J. M., & Lafaut, S. (2022). Bonobo (Pan paniscus). International Studbook.
Stevens, J. M. G., Vervaecke, H., de Vries, H., & van Elsacker, L. (2007). Sex differences in the steepness of dominance hierarchies in captive bonobo groups. International Journal of Primatology, 28(6), 1417-1430. https://doi.org/10.1007/s10764-007-9186-9
Suleman, M. A., Wango, E., Farah, I. O., & Hau, J. (2000). Adrenal cortex and stomach lesions associated with stress in wild male African green monkeys (Cercopithecus aethiops) in the post-capture period. Journal of Medical Primatology, 29(5), 338-342.
Summers, L., Clingerman, K. J., & Yang, X. (2012). Validation of a body condition scoring system in rhesus macaques (Macaca mulatta): Assessment of body composition by using dual-energy X-ray absorptiometry. Journal of the American Association for Laboratory Animal Science: JAALAS, 51(1), 88-93.
Tait, I. M., Kenyon, P. R., Garrick, D. J., Pleasants, A. B., & Hickson, R. E. (2018). Genetic and phenotypic correlations between production traits and adult body condition scores in New Zealand merino ewes. New Zealand Journal of Animal Science and Production, 78, 71-75.
Takahashi, T., Higashino, A., Takagi, K., Kamanaka, Y., Abe, M., Morimoto, M., Kang, K. H., Goto, S., Suzuki, J., Hamada, Y., & Kageyama, T. (2006). Characterization of obesity in Japanese monkeys (Macaca fuscata) in a pedigreed colony. Journal of Medical Primatology, 35(1), 30-37. https://doi.org/10.1111/j.1600-0684.2005.00138.x
Terio, K. A., Kinsel, M. J., Raphael, J., Mlengeya, T., Lipende, I., Kirchhoff, C. A., Gilagiza, B., Wilson, M. L., Kamenya, S., Estes, J. D., Keele, B. F., Rudicell, R. S., Liu, W., Patton, S., Collins, A., Hahn, B. H., Travis, D. A., & Lonsdorf, E. V. (2011). Pathologic lesions in chimpanzees (Pan trogylodytes schweinfurthii) from Gombe National Park, Tanzania, 2004-2010. Journal of Zoo and Wildlife Medicine: Official Publication of the American Association of Zoo Veterinarians, 42(4), 597-607.
Toshniwal, J. K., Dechow, C. D., Cassell, B. G., Appuhamy, J. A. D. R. N., & Varga, G. A. (2008). Heritability of electronically recorded daily body weight and correlations with yield, dry matter intake, and body condition score. Journal of Dairy Science, 91(8), 3201-3210. https://doi.org/10.3168/jds.2007-0627
Turnbaugh, P. J., Ley, R. E., Mahowald, M. A., Magrini, V., Mardis, E. R., & Gordon, J. I. (2006). An obesity-associated gut microbiome with increased capacity for energy harvest. Nature, 444(7122), 7122.
Veerkamp, R. F., Koenen, E. P. C., & De Jong, G. (2001). Genetic correlations among body condition score, yield, and fertility in first-parity cows estimated by random regression models. Journal of Dairy Science, 84(10), 2327-2335. https://doi.org/10.3168/jds.S0022-0302(01)74681-4
Verspeek, J., & Stevens, J. M. G. (2020). Food preference and nutrient composition in captive bonobos (Pan paniscus). Primates, 61(5), 661-671. https://doi.org/10.1007/s10329-020-00813-6
Vervaecke, H., de Vries, H., & van Elsacker, L. (2000). Dominance and its behavioral measures in a captive group of bonobos (Pan paniscus). International Journal of Primatology, 21(1), 47-68. https://doi.org/10.1023/A:1005471512788
Videan, E. N., Heward, C. B., Chowdhury, K., Plummer, J., Su, Y., & Cutler, R. G. (2009). Comparison of biomarkers of oxidative stress and cardiovascular disease in humans and chimpanzees (Pan troglodytes). Comparative Medicine, 59(3), 287-296.
de Villemereuil, P. (2018). Quantitative genetic methods depending on the nature of the phenotypic trait. Annals of the New York Academy of Sciences, 1422(1), 29-47. https://doi.org/10.1111/nyas.13571
White, F. J., & Wood, K. D. (2007). Female feeding priority in bonobos, Pan paniscus, and the question of female dominance. American Journal of Primatology, 69(8), 837-850. https://doi.org/10.1002/ajp.20387
Wilson, A. J. (2008). Why h2 does not always equal VA/VP? Journal of Evolutionary Biology, 21(3), 647-650. https://doi.org/10.1111/j.1420-9101.2008.01500.x
Wolden-Hanson, T., Davis, G. A., Baum, S. T., & Kemnitz, J. W. (1993). Insulin levels, physical activity, and urinary catecholamine excretion of obese and non-obese rhesus monkeys. Obesity Research, 1(1), 5-17. https://doi.org/10.1002/j.1550-8528.1993.tb00003.x
Young, S. S., Skeans, S. M., Austin, T., & Chapman, R. W. (2003). The effects of body fat on pulmonary function and gas exchange in cynomolgus monkeys. Pulmonary Pharmacology & Therapeutics, 16(5), 313-319.
Zihlman, A. L., & Bolter, D. R. (2015). Body composition in Pan paniscus compared with Homo sapiens has implications for changes during human evolution. Proceedings of the National Academy of Sciences, 112(24), 7466-7471. https://doi.org/10.1073/pnas.1505071112
Zihlman, A. L., & Cramer, D. L. (1978). Skeletal differences between pygmy (Pan paniscus) and common chimpanzees (Pan troglodytes). Folia Primatologica, 29(2), 86-94. https://doi.org/10.1159/000155830
Zihlman, A. L., & McFarland, R. K. (2000). Body mass in lowland gorillas: A quantitative analysis. American Journal of Physical Anthropology, 113(1), 61-78. https://doi.org/10.1002/1096-8644(200009)113:1<61::AID-AJPA6>3.0.CO;2-H
Zijlmans, D. G. M., van den Berg, L. M., Langermans, J. A. M., & Sterck, E. H. M. (2022). Does behaviour predict weight gain during adulthood in captive group-living rhesus macaques? Applied Animal Behaviour Science, 256, 105748. https://doi.org/10.1016/j.applanim.2022.105748