Abstract
More in-depth knowledge is required regarding the diet composition and food preferences of ungulates to improve our understanding of their different feeding strategies and mechanisms for adaptation. In particular, differences in energetic demands and feeding behaviors between the sexes, in sexually dimorphic species, may lead to significant dietary differences, which may partly explain sexual segregation patterns. Diet differences between sexes in Siberian ibex (Capra sibirica) are still poorly understood. We investigated the diet of Siberian ibex in the Tianshan Mountains (China), using fecal micro-histological analyses, to understand to what extent sex and season can explain differences in diet composition. In our study area, males and females had different diet compositions during the warm season: males preferred the most abundant plant species, with the greatest biomass, while females selected plants with higher nutritional content. Considering these results, the differences in the feeding strategies of the two sexes may indeed play a crucial role in promoting sexual segregation and preference for different habitats. During the cold season, the diet overlap between males and females was higher, coinciding with a random association between the sexes, during which males and females seem to live in both mixed and unisex groups and share the same habitats. Therefore, we concluded that sexual segregation is a result not only of differences in diet composition but also of differences in the social behaviors and habitat preferences between the sexes, leading to deferential activity budgets and habitat selection that in association with feeding strategies may explain sexual segregation in Siberian ibex.
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References
Alves J, Alves da Silva A, Soares AMVM, Fonseca C (2013) Sexual segregation in red deer: is social behaviour more important than habitat preferences? Anim Behav 85(2):501–509. https://doi.org/10.1016/j.anbehav.2012.12.018
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Aust Ecol 26(1):32–46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x
Ashraf N, Anwar M, Hussain I, Nawaz MA (2014) Competition for food between the markhor and domestic goat in Chitral, Pakistan. Turk J Zool 38(2):191–198. https://doi.org/10.3906/zoo-1306-6
Awasthi A, Uniyal KS, Rawat GS, Sathyakumar S (2003) Food plants and feeding habits of Himalayan ungulates. Curr Sci India 85(6):719–723 https://www.jstor.org/stable/24109877
Bagchi S, Mishra C, Bhatnagar YV (2004) Conflicts between traditional pastoralism and conservation of Himalayan ibex (Capra sibirica) in the trans-Himalayan mountains. Anim Conserv 7(2):121–128. https://doi.org/10.1017/S1367943003001148
Barboza TS, Bowyer RT (2000) Sexual segregation in dimorphic deer: a new gastrocentric hypothesis. J Mammal 81(2):473–489. https://doi.org/10.1644/1545-1542(2000)081<0473:SSIDDA>2.0.CO;2
Beier P, Mccullough DR (1990) Factors influencing white-tailed deer activity patterns and habitat use. Wildl Monogr:109
Bell RHV (1971) The use of the herb layer by grazing ungulates in the Serengeti. In: Watson A (ed) Animal populations in relation to their food resources. Blackwell, Oxford, pp 111–123
Belovsky GE (1978) Diet optimization in a generalist herbivore: the moose. Theor Popul Biol 14(1):105–134. https://doi.org/10.1016/0040-5809(78)90007-2
Bian K, Liu CG, Wang KF, Qi XG, Wang Y, Li BG (2011) Spring bed-site selection by Capra ibex in Mazong Mountain, Gansu Province. Sichuan J Zool 30(4):633–637. https://doi.org/10.3969/j.issn.1000-7083.2011.04.028
Bliss LM, Weckerly FW (2016) Habitat use by male and female Roosevelt elk in northwestern California. Calif Fish Game 102:8–16
Bowyer RT (1984) Sexual segregation in southern mule deer. J Mammal 65(3):410–417. https://doi.org/10.2307/1381087
Bowyer RT, Kie JG (2004) Effects of foraging activity on sexual segregation in mule deer. J Mammal 85(3):498–504. https://doi.org/10.1644/BOS-115
Campos-Arceiz A, Takatsuki S, Lhagvasuren B (2004) Food overlap between Mongolian gazelles and livestock in Omnogobi, southern Mongolia. Ecol Res 19(4):455–460. https://doi.org/10.1111/j.1440-1703.2004.00658.x
Ciuti S, Apollonio M (2008) Ecological sexual segregation in fallow deer (Dama dama): a multispatial and multitemporal approach. Behav Ecol Sociobiol 62(11):1747–1759. https://doi.org/10.1007/s00265-008-0603-7
Clauss M, Frey R, Kiefer B, Lechner-Doll M, Polster C, Rössner GE, Streich WJ (2003) The maximum attainable body size of herbivorous mammals: morphophysiological constraints on foregut, and adaptations of hindgut fermenters. Oecologia 136(1):14–27. https://doi.org/10.1007/s00442-003-1254-z
Clutton-Brock TH, Guinness FE, Albon SD (1982) Red deer: behavior and ecology of two sexes. University of Chicago Press, Chicago
Conradt L (1998) Could asynchrony in activity between the sexes cause intersexual social segregation in ruminants? Proc R Soc B 265:1359–1363. https://doi.org/10.1098/rspb.1998.0442
du Toit JT (2006) Sex differences in the foraging ecology of large mammalian herbivores. In: Ruckstuhl K, Neuhaus P (eds) Sexual segregation in vertebrates: ecology of the two sexes. Cambridge University Press, Cambridge, pp 35–52
Dunn O, Clark V (1969) Correlation coefficients measured on the same individuals. J Am Stat Assoc 64(325):366–377. https://doi.org/10.2307/2283746
Eshelman BD, Jenkins SH (1989) Food selection by Belding’s ground squirrels in relation to plant nutritional features. J Mammal 70(4):846–852. https://doi.org/10.2307/1381726
Fedosenko AK, Blank DA (2001) Capra sibirica. Mamm Species:1–13. https://doi.org/10.2307/0.675.1
Fulbright TE, Frank Robbins W, Hellgren EC, DeYoung RW, Humphreys ID (2001) Lack of diet partitioning by sex in reintroduced desert bighorn sheep. J Arid Environ 48(1):49–57. https://doi.org/10.1006/jare.2000.0738
Fury CA, Ruckstuhl KE, Harrison PL (2013) Spatial and social sexual segregation patterns in indo-pacific bottlenose dolphins (Tursiops aduncus). PLoS One 8:52987. https://doi.org/10.1371/journal.pone.0052987
Gordon IJ, Illius AW (1994) The functional significance of the browser-grazer dichotomy in African ruminants. Oecologia 98(2):167–175. https://doi.org/10.1007/BF00341469
Gross JE, Demment MW, Alkon PU, Kotzman M (1995) Feeding and chewing behaviours of Nubian ibex: compensation for sex-related differences in body size. Funct Ecol 9(3):385–393. https://doi.org/10.2307/2390001
Hanley TA (1982) The nutritional basis for food selection by ungulates. J Range Manag 35(2):146–151
Hofmann RR (1989) Evolutionary steps of ecophysiological adaptation and diversification of ruminants: a comparative view of their digestive system. Oecologia 78(4):443–457. https://doi.org/10.1007/BF00378733
Hofmann RR, Stewart DRM (1972) Grazer or browser: a classification based on the stomach-structure and feeding habits of east African ruminants. Mammalia 36(2):226–240. https://doi.org/10.1515/mamm.1972.36.2.226
Ivlev VS (1961) Experimental ecology of the feeding of fishes. Yale University Press, New Haven
Jarman P (1974) The social organisation of antelope in relation to their ecology. Behaviour 48:215–267. https://doi.org/10.1163/156853974X00345
Jiang ZG, **a WP (1985) Utilization of the food resources by plantau Pika. Acta Theriol Sin 5(4):251–262. https://doi.org/10.16829/j.slxb.1985.04.003
Johnson BK (1980) Bighorn sheep food habits; forage preferences, and habitat selection in alpine and subalpine communities. Dissertation Abstracts International B, 1:1180–1181
Johnson MK (1982) Frequency sampling for microscopic analysis of botanical compositions. J Range Manag 35(4):541–542. https://doi.org/10.2307/3898628
Kjeldahl J (1883) Neue methode zur bestimmung des stickstoffs in organischen körpern. Z Anal Chem 22(1):366–382. https://doi.org/10.1007/BF01338151
Kleiber M (1947) Body size and metabolic rate. Physiol Rev 27:511–541. https://doi.org/10.1152/physrev.1947.27.4.511
Martínez T (2001) The feeding strategy of Spanish ibex (Capra pyrenaica) in the northern sierra de Gredos (Central Spain). Folia Zool 50(4):257–270
Michelena P, Bouquet PM, Dissac A, Fourcassie V, Lauga J, Gerard JF, Bon R (2004) An experimental test of hypotheses explaining social segregation in dimorphic ungulates. Anim Behav 68(6):1371–1380. https://doi.org/10.1016/j.anbehav.2004.04.008
Mysterud A (2000) The relationship between ecological segregation and sexual body size dimorphism in large herbivores. Oecologia 124(1):40–54. https://doi.org/10.1007/s004420050023
Neuhaus P, Ruckstuhl KE (2002) Foraging behaviour in alpine ibex (Capra ibex): consequences of reproductive status, body size, age and sex. Ethol Ecol Evol 14:373–381. https://doi.org/10.1080/08927014.2002.9522738
Owen-Smith N, Novellie P (1982) What should a clever ungulate eat? Am Nat 119(2):151–178. https://doi.org/10.1086/283902
Pianka ER (1973) The structure of lizard communities. Annu Rev Ecol Sci 4:53–74. https://doi.org/10.1146/annurev.es.04.110173.000413
Post DM, Armbrust TS, Horne EA, Goheen JR (2001) Sexual segregation results in differences in content and quality of bison (Bos bison) diets. J Mammal 82(2):407–413. https://doi.org/10.1644/1545-1542(2001)082<0407:SSRIDI>2.0.CO;2
Ruckstuhl KE (1998) Foraging behaviour and sexual segregation in bighorn sheep. Anim Behav 56(1):99–106. https://doi.org/10.1006/anbe.1998.0745
Ruckstuhl KE (1999) To synchronise or not to synchronise: a dilemma for young bighorn males. Behaviour 136(6):805–818. https://doi.org/10.1163/156853999501577
Ruckstuhl KE, Kokko H (2002) Modelling sexual segregation in ungulates: effects of group size, activity budgets and synchrony. Anim Behav 64(6):909–914. https://doi.org/10.1006/anbe.2002.2015
Ruckstuhl KE, Neuhaus P (2002) Sexual segregation in ungulates: a comparative test of three hypotheses. Biol Rev 77(1):77–96. https://doi.org/10.1017/S1464793101005814
Schaller GB, Ren JR (1988) Effects of a snowstorm on Tibetan antelope. J Mammal 69(3):631–634. https://doi.org/10.2307/1381361
Schoener TW (1968) The Anolis lizards of bimini: resource partitioning in a complex fauna. Ecology 49(4):704–726. https://doi.org/10.2307/1935534
Shrestha R, Wegge P, Koirala RA (2005) Summer diets of wild and domestic ungulates in Nepal Himalaya. J Zool 266(2):111–119. https://doi.org/10.1017/S0952836905006527
Sih A, Christensen B (2001) Optimal diet theory: when does it work, and when and why does it fail? Anim Behav 61:379–390. https://doi.org/10.1006/anbe.2000.1592
Sullivan JT (1962) Evaluation of forage crops by chemical analysis. A critique. Agron J 54(6):511–514. https://doi.org/10.2134/agronj1962.00021962005400060013x
Van Soest PJ (1963) Use of detergents in the analysis of fibrous feeds. J Assoc Off Agric Chem 46:829–835
Van Soest PJ (1994) Nutritional ecology of the ruminant, 2nd edn. Cornell University Press, New York
Wang MY, Alves J, da Silva AA, Yang WK, Ruckstuhl KE (2018) The effect of male age on patterns of sexual segregation in Siberian ibex. Sci Rep-UK 8:13095. https://doi.org/10.1038/s41598-018-31463-w
Xu F, Ma M, Yang WK, Blank DA, Wu YQ (2011) Test of the activity budget hypothesis on Asiatic ibex in Tian Shan Mountains of **njiang, China. Eur J Wildl Res 58(1):71–75. https://doi.org/10.1007/s10344-011-0542-x
Xu WX, **a CJ, Lin J, Yang WK, Liu W (2012) Diet of Gazella subgutturosa (Güldenstaedt, 1780) and food overlap with domestic sheep in **njiang, China. Folia Zool 61(1):54–60. https://doi.org/10.25225/fozo.v61.i1.a9.2012
Zhou P, Zhang MJ, Li ZQ, ** S (2010) Seasonal variations of the pH and electrical conductivity in precipitation and snow on the glaciers of Tianshan Mountains, China. Arid Land Geogr 33(4):518–524. https://doi.org/10.13826/j.cnki.cn65-1103/x.2010.04.004
Zhu XS (2016) Food habits and sexual segregation of the Asiatic ibex, Capra sibirica. Dissertation, University of Chinese Academy of Sciences
Acknowledgments
We are very grateful to Dr. Peter Neuhaus and Ms. Patricia Johnston for their useful suggestions and remarks and help in English language editing. We are grateful to Prof. Li Zhongqin, Dr. Wang Wenbin, Mr. Chen Hongmo, Mr. Ma Yinghui, and staff from the Tianshan Glaciological Station, Chinese Academy of Sciences, for providing logistical support during the fieldwork.
Funding
This work was supported by the Second Tibetan Plateau Scientific Expedition and Research Program (STEP), Grant No. 2019QZKK0501, and the National Natural Science Foundation of China (31661143019). KER received the support of the Natural Sciences and Engineering Research Council of Canada (NSERC) (funding reference number 316189-2012-RGPIN); Cette recherche a été financée par le Conseil de recherches en sciences naturelles et engénie du Canada (CRSNG) (reference number 316189-2012-RGPIN), and POPH/FSE from the Portuguese Foundation for Science and Technology (FCT) through the fellowships of A.A.S. (SFRH/BD/75018/2010) and J.A. (SFRH/BPD/123087/2016).
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Lei Han, Muyang Wang, and Weikang Yang conceived and performed the experiments. Lei Han, David Blank, Muyang Wang, Joana Alves, and Kathreen Ruckstuhl wrote the manuscript. António Alves da Silva, Joana Alves, and Lei Han conducted the data analysis. David Blank and Kathreen Ruckstuhl also edited the spelling and grammar of this contribution. All authors contributed to the manuscript text and have read and approved the final version of the manuscript.
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Han, L., Blank, D., Wang, M. et al. Diet differences between males and females in sexually dimorphic ungulates: a case study on Siberian ibex. Eur J Wildl Res 66, 55 (2020). https://doi.org/10.1007/s10344-020-01387-w
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DOI: https://doi.org/10.1007/s10344-020-01387-w