Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-04T22:01:58.219Z Has data issue: false hasContentIssue false
  • English
  • Français

Individual differences in behavior affect total tract fiber digestibility: the example of collared peccary

Published online by Cambridge University Press:  29 June 2020

R. M. Borges ,
S. L. G. Nogueira-Filho ,
P. L. G. Cairo ,
S. S. C. Nogueira ,
A. Mendes ,
L. G. Aldrigui ,
M. Vandenheede  and
J. Bindelle Open the ORCID record for J. Bindelle [Opens in a new window]
R. M. Borges
Affiliation:
Laboratory of Neotropical Animal Nutrition, Department of Agricultural and Environmental Sciences, Universidade Estadual de Santa Cruz, Rodovia Jorge Amado, km 16, Ilhéus, Bahia45662-900, Brazil
S. L. G. Nogueira-Filho
Affiliation:
Laboratory of Neotropical Animal Nutrition, Department of Agricultural and Environmental Sciences, Universidade Estadual de Santa Cruz, Rodovia Jorge Amado, km 16, Ilhéus, Bahia45662-900, Brazil National Institute of Science and Technology in Interdisciplinary and Transdisciplinary Studies in Ecology and Evolution (INCT IN-TREE), Instituto de Biologia, Universidade Federal da Bahia, Rua Barão do Geremoabo, s/n, Salvador, Bahia40110-909, Brazil
P. L. G. Cairo
Affiliation:
Laboratory of Neotropical Animal Nutrition, Department of Agricultural and Environmental Sciences, Universidade Estadual de Santa Cruz, Rodovia Jorge Amado, km 16, Ilhéus, Bahia45662-900, Brazil
S. S. C. Nogueira
Affiliation:
Laboratory of Neotropical Animal Nutrition, Department of Agricultural and Environmental Sciences, Universidade Estadual de Santa Cruz, Rodovia Jorge Amado, km 16, Ilhéus, Bahia45662-900, Brazil National Institute of Science and Technology in Interdisciplinary and Transdisciplinary Studies in Ecology and Evolution (INCT IN-TREE), Instituto de Biologia, Universidade Federal da Bahia, Rua Barão do Geremoabo, s/n, Salvador, Bahia40110-909, Brazil
A. Mendes
Affiliation:
Laboratory of Neotropical Animal Nutrition, Department of Agricultural and Environmental Sciences, Universidade Estadual de Santa Cruz, Rodovia Jorge Amado, km 16, Ilhéus, Bahia45662-900, Brazil
L. G. Aldrigui
Affiliation:
Laboratory of Neotropical Animal Nutrition, Department of Agricultural and Environmental Sciences, Universidade Estadual de Santa Cruz, Rodovia Jorge Amado, km 16, Ilhéus, Bahia45662-900, Brazil
M. Vandenheede
Affiliation:
Department of Veterinary Management of Animal Resources, Faculty of Veterinary Medicine, Liège University (ULiège), Boulevard de Colonster, 20, Liège4000, Belgium
J. Bindelle*
Affiliation:
Department of AgroBioChem/Precision Livestock and Nutrition Unit, AgricultureIsLife/TERRA, Gembloux Agro-Bio Tech, Liège University (ULiège), Passage des Déportés, 2, Gembloux5030, Belgium
*
†E-mail: [email protected]
Get access

Abstract

Differences in how individuals cope with stressful conditions (e.g. novel/unfamiliar environment, social isolation and increases in human contact) can explain the variability in data collection from nutrient digestibility trials. We used the collared peccary (Pecari tajacu), which is under process of domestication and shows high individual behavioral distinctiveness in reactions toward humans, to test the hypothesis that behavioral differences play a role in nutrient digestibility. We assessed the individual behavioral traits of 24 adult male collared peccaries using both the ‘behavioral coding’ and the ‘subjective ratings’ approaches. For the behavioral coding assessment, we recorded the hourly frequency of behaviors potentially indicative of stress during the 30-day habituation period to the experimental housing conditions. The subjective ratings were performed based on the individuals’ reactions to three short-term challenge tests (novel environment, novel object and threat from a capture net) over a period of 56 days. During the last 26 days, the collared peccaries were fed diets either high (n = 12) or low (n = 12) in dietary fiber levels, and we determined the total tract apparent digestibility of nutrients. The individual subjective ratings showed consistency in the correlated measures of ‘relaxedness’, ‘quietness’ and ‘satisfaction’ across the three challenge tests, which were combined to produce z score ratings of one derived variable (‘calmness’). Individual frequency of BPIS/h and calmness scores were negatively correlated and both predicted the total tract digestibility of acid detergent fiber (ADF), which ranged from 0.41 to 0.79. The greater the calmness z scores (i.e. calmer individuals), the greater the total tract digestibility of ADF. In contrast, the higher the frequency of BPIS/h, the lower the total tract digestibility of ADF. Therefore, our results provide evidence that by selecting calmer collared peccaries, there will be an increase in their capacity to digest dietary fiber.

Keywords

coping stylesdigestive physiologyfeed evaluationPecari tajacustress
Type
Research Article
Information
animal , Volume 14 , Issue 12 , December 2020 , pp. 2570 - 2579
Copyright
© The Author(s), 2020. Published by Cambridge University Press on behalf of The Animal Consortium

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

a

Present address: Departamento de Ciências Agrárias, Ambientais e Biológicas, Universidade Federal do Recôncavo da Bahia (UFRB), 44380000, Cruz das Almas, Brazil.

*

Both authors contributed equally to this work.

References

Altmann, J 1974. Observational study of behavior: sampling methods. Behaviour 49, 227–266.CrossRefGoogle ScholarPubMed
Association of Official Analytical Chemists (AOAC) 2012. Official methods of analysis, 18th edition. AOAC, Arlington, VA, USA.Google Scholar
Bindelle, J, Buldgen, A, Delacollette, M, Wavreille, J, Agneessens, R, Destain, JP and Leterme, P 2009. Influence of source and concentrations of dietary fiber on in vivo nitrogen excretion pathways in pigs as reflected by in vitro fermentation and nitrogen incorporation by fecal bacteria. Journal of Animal Science 87, 583–593.CrossRefGoogle ScholarPubMed
Borges, RM, Mendes, A, Nogueira, SSC, Bindelle, J and Nogueira-Filho, SLG 2017. Protein requirements of collared peccary (Pecari tajacu). Tropical Animal Health and Production 49, 1353–1359.CrossRefGoogle Scholar
Byers, JA and Bekoff, M 1981. Social, spacing, and cooperative behavior of the collared peccary, Tayassu tajacu. Journal of Mammalogy 62, 767–785.Google Scholar
Cafe, LM, Robinson, DL, Ferguson, DM, McIntyre, BL, Geesink, GH and Greenwood, PL 2011. Cattle temperament: persistence of assessments and associations with productivity, efficiency, carcass and meat quality traits. Journal of Animal Science 89, 1452–1465.CrossRefGoogle ScholarPubMed
Cairo, PLG 2018. The microbiota of the collared peccary (Pecari tajacu). PhD thesis State University of Santa Cruz, Ilhéus, Bahia, Brazil.Google Scholar
Carter, AJ, Marshall, HH, Heinsohn, R and Cowlishaw, G 2012. Evaluating animal personalities: do observer assessments and experimental tests measure the same thing? Behavioral Ecology and Sociobiology 66, 153–160.CrossRefGoogle Scholar
Comizzoli, P, Peiniau, J, Dutertre, C, Planquette, P and Aumaitre, A 1997. Digestive utilization of concentrated and fibrous diets by two peccary species (Tayassu peccari, Tayassu tajacu) raised in French Guyana. Animal Feed Science and Technology 64, 215–226.CrossRefGoogle Scholar
Dingemanse, NJ and Réale, D 2005. Natural selection and animal personality. Behaviour 142, 1159–1184.CrossRefGoogle Scholar
Elston, JJ, Klinksiek, EA and Hewitt, DG 2005. Digestive efficiency of collared peccaries and wild pigs. The Southwestern Naturalist 50, 515–519.CrossRefGoogle Scholar
Feaver, J, Mendl, M and Bateson, P 1986. A method for rating the individual distinctiveness of domestic cats. Animal Behaviour 34, 1016–1025.CrossRefGoogle Scholar
Finkemeier, MA, Langbein, J and Puppe, B 2018. Personality research in mammalian farm animals: concepts, measures, and relationship to welfare. Frontiers in Veterinary Science 5, 131.CrossRefGoogle ScholarPubMed
Fürtbauer, I, Solman, C and Fry, A 2019. Sheep wool cortisol as a retrospective measure of long-term HPA axis activity and its links to body mass. Domestic Animal Endocrinology 68, 39–46.CrossRefGoogle Scholar
Hänninen, L and Pastell, M 2009. CowLog: Open-source software for coding behaviors from digital video. Behavior Research Methods 41, 472–476.CrossRefGoogle ScholarPubMed
Hervé, J, Terenina, E, Haurogné, K, Bacou, E, Kulikova, E, Allard, M, Billon, Y, Bach, JM, Mormède, P and Lieubeau, B 2019. Effects of divergent selection upon adrenocortical activity on immune traits in pig. BMC Veterinary Research 15, 71.CrossRefGoogle ScholarPubMed
Holl, JW, Rohrer, GA and Brown-Brandl, TM 2010. Estimates of genetic parameters among scale activity scores, growth, and fatness in pigs. Journal of Animal Science 88, 455–459.CrossRefGoogle ScholarPubMed
Horback, K and Parsons, T 2018. Ontogeny of behavioral traits in commercial sows. Animal 12, 2365–2372.CrossRefGoogle ScholarPubMed
Keuroghlian, A and Eaton, DP 2008. Fruit availability and peccary frugivory in an isolated Atlantic forest fragment: effects on peccary ranging behavior and habitat use. Biotropica 40, 62–70.Google Scholar
Kiltie, RA 1981. Stomach contents of rain-forest peccaries (Tayassu tajacu and Tayassu pecari). Biotropica 13, 234–236.CrossRefGoogle Scholar
Koolhaas, JM 2008. Coping style and immunity in animals: making sense of individual variation. Brain Behavior and Immunity 22, 662–667.CrossRefGoogle ScholarPubMed
Koolhaas, JM, De Boer, SF, Coppens, CM, and Buwalda, B 2010. Neuroendocrinology of coping styles: towards understanding the biology of individual variation. Frontiers in Neuroendocrinology 31, 307–321.CrossRefGoogle ScholarPubMed
Langer, P 1978. Anatomy of the stomach of the collared peccary, Dicotyles tajacu (L., 1758) (Artiodactyla: Mammalia). Zeitschrift für Säugetierkunde 43, 42–59.Google Scholar
Langer, P 1979. Adaptational significance of the forestomach of the collared peccary, Dicotyles tajacu (L. 1758) (Mammalia: Artiodactyla). Mammalia 43, 235–246.CrossRefGoogle Scholar
Llonch, P, Somarriba, M, Duthie, CA, Haskell, MJ, Rooke, JA, Troy, S and Turner, SP 2016. Association of temperament and acute stress responsiveness with productivity, feed efficiency, and methane emissions in beef cattle: an observational study. Frontiers in Veterinary Science 3, 43.CrossRefGoogle ScholarPubMed
MacKay, JRD and Haskell, MJ 2015. Consistent individual behavioral variation: the difference between temperament, personality and behavioral syndromes. Animals 5, 455–478.CrossRefGoogle ScholarPubMed
Mazza, V, Dammhahn, M, Eccard, JA, Palme, R, Zaccaroni, M and Jacob, J 2019. Coping with style: individual differences in responses to environmental variation. Behavioral Ecology and Sociobiology 73, 142.CrossRefGoogle Scholar
Meagher, RK 2009. Observer ratings: validity and value as a tool for animal welfare research. Applied Animal Behaviour Science 119, 1–14.CrossRefGoogle Scholar
Neave, HW, Weary, DM, Von Keyserlingk, MAG 2018. Individual variability in feeding behavior of domesticated ruminants. Animal 12 (suppl. 2), 419–430.CrossRefGoogle ScholarPubMed
Negesse, T, Datt, C and Kundu, SS 2016. Variability in residual feed intake and nutrient utilization in Murrah buffalo heifers. Tropical Animal Health and Production 48, 1577–1584.CrossRefGoogle ScholarPubMed
Nogueira, SSC, Silva, MG, Dias, CTS, Pompéia, S, Cetra, M and Nogueira-Filho, SLG 2010. Social behaviour of collared peccaries (Pecari tajacu) under three space allowances. Animal Welfare 19, 243–248.Google Scholar
Nogueira, SSC and Nogueira-Filho, SLG 2011. Wildlife farming: an alternative to unsustainable hunting and deforestation in Neotropical forests? Biodiversity and Conservation 20, 1385–1397.CrossRefGoogle Scholar
Nogueira, SSC, Macedo, JF, Sant’Anna, AC, Nogueira-Filho, SLG and da Costa, MJP 2015. Assessment of temperament traits of white-lipped (Tayassu pecari) and collared peccaries (Pecari tajacu) during handling in a farmed environment. Animal Welfare 24, 291–298.CrossRefGoogle Scholar
Nogueira-Filho, SLG 2005. The effects of increasing levels of roughage on coefficients of nutrient digestibility in the collared peccary (Tayassu tajacu). Animal Feed Science and Technology 120, 151–157.CrossRefGoogle Scholar
Nogueira-Filho, SLG, Martins, K, Borges, RM, Mendes, A, Nogueira, SSC and Bindelle, J 2018. Intake and digestion of non-traditional feedstuffs by farmed collared peccary (Mammalia, Tayassuidae). Revista Brasileira de Zootecnia, https://doi.org//10.1590/rbz4720170288, Published online by Sociedade Brasileira de Zootecnia 4 October 2018.CrossRefGoogle Scholar
Oliveira, EG, Santos, ACF, Dias, JCT, Rezende, RP, Nogueira-Filho, SLG and Gross, E 2009. The influence of urea feeding on the bacterial and archaeal community in the forestomach of collared peccary (Artiodactyla, Tayassuidae). Journal of Applied Microbiology 107, 1711–1718.CrossRefGoogle Scholar
Oliveira, FR, Nogueira-Filho, SLG, Sousa, MB, Dias, CTS, Mendl, M and Nogueira, SSC 2016. Measurement of cognitive bias and cortisol levels to evaluate the effects of space restriction on captive collared peccary (Mammalia, Tayassuidae). Applied Animal Behaviour Science 181, 76–82.CrossRefGoogle Scholar
Olmos, F 1993. Diet of sympatric Brazilian caatinga peccaries (Tayassu tajacu and T. pecari). Journal of Tropical Ecology 9, 255–258.CrossRefGoogle Scholar
Ouweltjes, W, Verschuren, LMG, Pijlman, J, Bergsma, R, Schokker, D, Knol, EF, van der Aar, PJ, Molist, F and Calus, MPL 2018. The repeatability of individual nutrient digestibility in pigs. Livestock Science 207, 63–67.CrossRefGoogle Scholar
Pérez de Nanclares, M, Trudeau, MP, Hansen, JØ, Mydland, LT, Urriola, PE, Shurson, GC, Piercey Åkessonc, C, Kjosa, NP, Arntzend, MØ, Øverlanda, M 2017. High-fiber rapeseed co-product diet for Norwegian Landrace pigs: effect on digestibility. Livestock Science 203, 1–9.CrossRefGoogle Scholar
Rauw, WM, Johnson, AK, Gomez-Raya, L and Dekkers, J 2017. A hypothesis and review of the relationship between selection for improved production efficiency, coping behavior, and domestication. Frontiers in Genetics 8, 134.CrossRefGoogle ScholarPubMed
Réale, D, Reader, SM, Sol, D, McDougall, PT and Dingemanse, NJ 2007. Integrating animal temperament within ecology and evolution. Biological Reviews 82, 291–318.CrossRefGoogle ScholarPubMed
Robert, S, Dancosse, J and Dallaire, A 1987. Some observations on the role of environment and genetics in behaviour of wild and domestic forms of Sus scrofa (European wild boars and domestic pigs). Applied Animal Behaviour Science 17, 253–262.CrossRefGoogle Scholar
Robbins, CT 1993. Wildlife feeding and nutrition, 2nd edition. Academic Press Inc., San Diego, CA, USA.Google Scholar
Rohrer, GA, Brown-Brandl, TM, Rempel, LA, Schneider, JF and Holl, JW 2013. Genetic analysis of behavior traits in swine production. Livestock Science 157, 28–37.CrossRefGoogle Scholar
Ruis, MA, te Brake, JH, Engel, B, Buist, WG, Blokhuis, HJ and Koolhaas, JM 2002. Implications of coping characteristics and social status for welfare and production of paired growing gilts. Applied Animal Behaviour Science 75, 207–231.CrossRefGoogle Scholar
Sant’Anna, AC and Paranhos da Costa, MJP 2013. Validity and feasibility of qualitative behavior assessment for the evaluation of Nellore cattle temperament. Livestock Science, 157, 254–262.CrossRefGoogle Scholar
Sih, A, Bell, A and Johnson, JC 2004. Behavioral syndromes: an ecological and evolutionary overview. Trends in Ecology & Evolution 19, 372–378.CrossRefGoogle ScholarPubMed
Sowls, LK 1997. Javelinas and other peccaries: their biology, management, and use, 2nd edition. Texas A&M University Press, College Station, TX, USA.Google Scholar
Van Oers, K, De Jong, G, Van Noordwijk, AJ, Kempenaers, B and Drent, PJ 2005. Contribution of genetics to the study of animal personalities: a review of case studies. Behaviour 142, 1185–1206.Google Scholar
Vazire, S, Gosling, SD, Dickey, AS and Schapiro, SJ 2007. Measuring personality in nonhuman animals. In Handbook of research methods in personality psychology (ed. Robins, RW, Fraley, RC and Krueger, RF), pp. 190–206. Guilford Press, New York, NY, USA.Google Scholar
Voisinet, BD, Grandin, T, Tatum, JD, O’connor, SF and Struthers, JJ 1997. Feedlot cattle with calm temperaments have higher average daily gains than cattle with excitable temperaments. Journal of Animal Science 75, 892–896.CrossRefGoogle ScholarPubMed
Wemelsfelder, F, Hunter, TEA, Mendl, MT and Lawrence, AB 2001. Assessing the ‘whole animal’: a free choice profiling approach. Animal Behaviour 62, 209–220.CrossRefGoogle Scholar
Westrick, SE, van Kesteren, F, Palme, R, Boonstra, R, Lane, JE, Boutin, S, McAdam, AG, Dantzer, B 2019. Stress activity is not predictive of coping style in North Americanmred squirrels Behavioral Ecology and Sociobiology 73, 113.CrossRefGoogle Scholar
Yoder, CL, Maltecca, C, Cassady, JP, Flowers, WL, Price, S and See, MT 2011. Breed differences in pig temperament scores during a performance test and their phenotypic relationship with performance. Livestock Science 136, 93–101.CrossRefGoogle Scholar