序列取样的稳定同位素研究示踪中国晚更新世亚洲象的摄食行为

doi:10.19615/j.cnki.1000-3118.190327

摘要/Abstract

摘要：

为了进一步探索亚洲象的摄食行为,运用稳定同位素的序列取样(serial/sequential sampling)新方法,首次对晚更新世笆仙洞遗址的三个亚洲象臼齿牙釉质(1个DP4, 2个M1)进行研究。结果表明,3个亚洲象个体的δ¹³C和δ¹⁸O内部差异均很小,未见季节性变化,虽然可能存在断奶及迁徙导致的数据波动,但总体来看依然表现出在牙釉质形成的长期过程中较为稳定的摄食行为。之前笆仙洞亚洲象动物群的整体取样(bulk sampling)同位素研究结果中,亚洲象的数据分布较为分散。而本次研究中较小的个体内部差异,则反向证实了宽泛分布的数据确实代表了灵活的摄食行为,并非取样位置的不同所致。这也进一步证明在气候温暖的东南亚地区,长鼻类动物的牙釉质整体取样工作可以提供可靠的古摄食行为及古生态信息。

关键词: 中国南部, 晚更新世, 亚洲象, 稳定同位素, 序列取样牙釉质, 摄食行为

Abstract:

Until now, feeding ecology has been found to play a significant role in the evolution of Asian elephant Elephas maximus. As the most widely-applied method in this field, bulk stable isotope analysis on tooth enamel had revealed important evidence on their paleodiet and paleoecology. However, it might be not skilled at reflecting the overview of the paleoecology of elephants, considering their huge tooth mophology and long dental ontogeny process. A newly-developing serial sampling strategy on tooth enamel sections could provide an effective approach to reconstruct the long-term individual life history of mammals covering the whole tooth formation time with higher precision. In this study, serial sampling isotope analysis was firstly undertaken on tooth enamel of Asian elephants from Baxian Cave, South China during the Late Pleistocene. The within-tooth isotopic variations of three teeth (one DP4 and two M1s) are all surprisingly subtle (standard deviations of δ ¹³C and δ ¹⁸O values are all less than 0.6‰), though some obvious variations might be caused by weaning and/or possible migration. No seasonal variation was observed, possibly indicating that these elephants had a stable foraging ecology. Back to our previous bulk tooth enamel isotope analysis on this same site, we could confirm that the varied bulk isotope results of Asian elephants factually represent their flexible foraging ecology. We may thereby conclude that the increasing bulk isotopic analysis in this region can provide a reliable paleoecological proxy for Pleistocene proboscidea in the warm regions of South and Southeast Asia.

Key words: South China, Late Pleistocene, Elephas maximus, stable isotopes, serial sampling,tooth enamel, foraging ecology

中图分类号:

Q915.878

马姣, 王元, 金昌柱, 张瀚文, 胡耀武. 序列取样的稳定同位素研究示踪中国晚更新世亚洲象的摄食行为. 古脊椎动物学报, 2019, 57(3): 225-240.

MA Jiao, WANG Yuan, JIN Chang-Zhu, ZHANG Han-Wen, HU Yao-Wu. A preliminary study of serial stable isotope analysis tracks foraging ecology of fossil Asian elephants in South China. Vertebrata Palasiatica, 2019, 57(3): 225-240.

图/表 2

参考文献 90

[1]	Ahrestani F S, Heitkönig I M A, Matsubayashi H et al., 2016. Grazing and browsing by large herbivores in South and Southeast Asia. In: Ahrestani F S, Sankaran M eds. The Ecology of Large Herbivores in South and Southeast Asia. Dordrecht: Springer Netherlands. 99-120
[2]	Bacon A M, Bourgon N, Dufour E et al., 2018a. Nam Lot (MIS 5) and Duoi U’Oi (MIS 4) Southeast Asian sites revisited: zooarchaeological and isotopic evidences. Palaeogeogr Palaeoclimatol Palaeoecol, 512:132-144 DOI URL
[3]	Bacon A M, Duringer P, Westaway K et al., 2018b. Testing the savannah corridor hypothesis during MIS2: the Boh Dambang hyena site in southern Cambodia. Quat Int, 464:417-439 DOI URL
[4]	Barnes R F W, 1982. Elephant feeding behaviour in Ruaha National Park, Tanzania. Afr J Ecol, 20:123-136 DOI URL
[5]	Baskaran N, Balasubramanian M, Swaminathan S et al., 2010. Feeding ecology of the Asian elephant Elephas maximus Linnaeus in the Nilgiri Biosphere Reserve, southern India. J Bombay Nat Hist Soc, 107:3-13
[6]	Baskaran N, Kanakasabai R, Desai A A, 2018a. Ranging and spacing behaviour of Asian elephant (Elephas maximus Linnaeus) in the tropical forests of Southern India. In: Sivaperuman C, Venkataraman K eds. Indian Hotspots. Singapore: Springer Singapore. 295-315
[7]	Baskaran N, Kanakasabai R, Desai A A, 2018b. Influence of ranging and hierarchy on the habitat use pattern by Asian elephant (Elephas maximus) in the tropical forests of Southern India. In: Sivaperuman C, Venkataraman K eds. Indian Hotspots. Singapore: Springer Singapore. 345-358
[8]	Biasatti D, Wang Y, Deng T, 2010. Strengthening of the East Asian summer monsoon revealed by a shift in seasonal patterns in diet and climate after 2-3 Ma in northwest China. Palaeogeogr Palaeoclimatol Palaeoecol, 297:12-25 DOI URL
[9]	Bocherens H, Schrenk F, Chaimanee Y et al., 2017. Flexibility of diet and habitat in Pleistocene South Asian mammals: implications for the fate of the giant fossil ape Gigantopithecus. Quat Int, 434:148-155 DOI URL
[10]	Britton K, Fuller B T, Tütken T et al., 2015. Oxygen isotope analysis of human bone phosphate evidences weaning age in archaeological populations. Am J Phys Anthropol, 157:226-241 DOI URL
[11]	Bryant J D, Froelich P N, 1995. A model of oxygen isotope fractionation in body water of large mammals. Geochim Cosmochim Acta, 59:4523-4537 DOI URL
[12]	Cerling T E, Harris J M, 1999. Carbon isotope fractionation between diet and bioapatite in ungulate mammals and implications for ecological and paleoecological studies. Oecologia, 120:347-363 DOI PMID
[13]	Cerling T E, Harris J M, Leakey M G, 1999. Browsing and grazing in elephants: the isotope record of modern and fossil proboscideans. Oecologia, 120:364-374 DOI PMID
[14]	Cerling T E, Passey B H, Ayliffe L K et al., 2004. Orphans’ tales: seasonal dietary changes in elephants from Tsavo National Park, Kenya. Palaeogeogr Palaeoclimatol Palaeoecol, 206:367-376 DOI URL
[15]	Cerling T E, Wittemyer G, Rasmussen H B et al., 2006. Stable isotopes in elephant hair document migration patterns and diet changes. Proc Natl Acad Sci USA, 103:371-373 DOI URL
[16]	Cerling T E, Wittemyer G, Ehleringer J R et al., 2009. History of animals using isotope records (HAIR): a 6-year dietary history of one family of African elephants. Proc Natl Acad Sci USA, 106:8093-8100 DOI URL
[17]	Chen J, Deng X, Zhang L et al., 2006. Diet composition and foraging ecology of Asian elephants in Shangyong, Xishuangbanna, China. Acta Ecol Sin, 26:309-316 DOI URL
[18]	Cherney M D, 2016. Records of growth and weaning in fossil proboscidean tusks as tests of Pleistocene extinction mechanisms. Ph. D thesis. Michigan: University of Michigan. 1-480
[19]	Codron J, 2004. An isotope comparison of elephant (Loxodonta africana) diets in the Kruger National Park and Welgevonden Game Reserve. M. S. thesis. Cape Town: University of Cape Town. 1-177
[20]	Codron J, Codron D, Sponheimer M et al., 2012. Stable isotope series from elephant ivory reveal lifetime histories of a true dietary generalist. Proc R Soc B, 279:2433-2441 DOI URL
[21]	Codron J, Kirkman K, Duffy K J et al., 2013. Stable isotope turnover and variability in tail hairs of captive and free-ranging African elephants (Loxodonta africana) reveal dietary niche differences within populations. Can J Zool, 91:124-134 DOI URL
[22]	Dutton A, Wilkinson B H, Welker J M et al., 2005. Spatial distribution and seasonal variation in ¹⁸O/¹⁶O of modern precipitation and river water across the conterminous USA. Hydrol Proc, 19:4121-4146 DOI URL
[23]	Feranec R S, MacFadden B J, 2000. Evolution of the grazing niche in Pleistocene mammals from Florida: evidence from stable isotopes. Palaeogeogr Palaeoclimatol Palaeoecol, 162:155-169 DOI URL
[24]	Fernando P, Pfrender M E, Encalada S E et al., 2000. Mitochondrial DNA variation, phylogeography and population structure of the Asian elephant. Heredity, 84:362-372 DOI URL
[25]	Fisher D C, 2018. Paleobiology of Pleistocene Proboscideans. Annu Rev Earth Planet Sci, 46:229-260 DOI URL
[26]	Forrer F A, 2017. The population status, habitat use and seasonal diet of African elephant (Loxodonta africana) in Majete Wildlife Reserve, Malawi. Ph. D thesis. Western Cape: Stellenbosch University, 1-123
[27]	Fox D L, Fisher D C, 2004. Dietary reconstruction of Miocene Gomphotherium (Mammalia, Proboscidea) from the Great Plains region, USA, based on the carbon isotope composition of tusk and molar enamel. Palaeogeogr Palaeoclimatol Palaeoecol, 206:311-335 DOI URL
[28]	Fox D L, Fisher D C, Vartanyan S et al., 2007. Paleoclimatic implications of oxygen isotopic variation in Late Pleistocene and Holocene tusks of Mammuthus primigenius from northern Eurasia. Quat Int, 170:154-165
[29]	Girdland-Flink L, Albayrak E, Lister A M, 2018. Genetic insight into an extinct population of Asian elephants (Elephas maximus) in the Near East. Open Quat, 4:1-9 DOI URL
[30]	Hillson S, 2005. Teeth. 2^nd ed. Cambridge: Cambridge University Press. 1-388
[31]	Hoppe K A, Koch P L, 2006. The biogeochemistry of the Aucilla River Fauna. In: Webb S D ed. First Floridians and Last Mastodons: the Page-Ladson Site in the Aucilla River. Dordrecht: Springer Netherlands. 379-401
[32]	Jayantha D, Dayawansa P N, Padmalal U et al., 2009. Social relationships of wild juvenile Asian elephants Elephas maximus in the Udawalawa National Park, Sri Lanka. J Threat Taxa, 1:211-214 DOI URL
[33]	Ji X, Curnoe D, Taçon P S C et al., 2016. Cave use and palaeoecology at Maludong (Red Deer Cave), Yunnan, China. J Archaeol Sci Rep, 8:277-283
[34]	Jin C, Pan W, Zhang Y et al., 2009. The Homo sapiens Cave hominin site of Mulan Mountain, Jiangzhou District, Chongzuo, Guangxi with emphasis on its age. Chin Sci Bull, 54:3848-3856 DOI URL
[35]	Koch P L, Heisinger J, Moss C et al., 1995. Isotopic tracking of change in diet and habitat use in African elephants. Science, 267:1340-1343 DOI URL
[36]	Koch P L, Hoppe K A, Webb S D, 1998. The isotopic ecology of Late Pleistocene mammals in North America: Part 1. Florida. Chem Geol, 152:119-138 DOI URL
[37]	Kusza S, Suchentrunk F, Pucher H et al., 2018. High levels of mitochondrial genetic diversity in Asian elephants (Elephas maximus) from Myanmar. Hystrix Ital J Mammal, 29:152-154
[38]	Laws R M, 1966. Age criteria for the African elephant: Loxodonta a. africana. Afr J Ecol, 4:1-37 DOI URL
[39]	Lee P C, 1996. The meanings of weaning: growth, lactation, and life history. Evol Anthropol Issues News Rev, 5:87-98 DOI URL
[40]	Lee P C, Moss C J, 1986. Early maternal investment in male and female African elephant calves. Behav Ecol Sociobiol, 18:353-361 DOI URL
[41]	Lee-Thorp J A, Sealy J C, van der Merwe N J, 1989. Stable carbon isotope ratio differences between bone collagen and bone apatite, and their relationship to diet. J Archaeol Sci, 16:585-599 DOI URL
[42]	Li D, Hu C, Wang W et al., 2017. The stable isotope record in cervid tooth enamel from Tantang Cave, Guangxi: implications for the Quaternary East Asian monsoon. Quat Int, 434:156-162 DOI URL
[43]	Liu W, Jin C, Zhang Y et al., 2010. Human remains from Zhirendong, South China, and modern human emergence in East Asia. Proc Natl Acad Sci USA, 107:19201-19206 DOI URL
[44]	Liu W, Martinón-Torres M, Cai Y et al., 2015. The earliest unequivocally modern humans in southern China. Nature, 526:696-699 DOI PMID
[45]	Ma J, Wang Y, Jin C et al., 2017. Isotopic evidence of foraging ecology of Asian elephant (Elephas maximus) in South China during the Late Pleistocene. Quat Int, 443:160-167 DOI URL
[46]	Maglio V J, 1973. Origin and evolution of the Elephantidae. Trans Am Philos Soc, 63:1-149
[47]	Metcalfe J Z, 2011. Late Pleistocene climate and proboscidean paleoecology in North America: insights from stable isotope compositions of skeletal remains. Ph. D thesis. London (Ontario): The University of Western Ontario. 1-297
[48]	Metcalfe J Z, Longstaffe F J, 2012. Mammoth tooth enamel growth rates inferred from stable isotope analysis and histology. Quat Res, 77:424-432 DOI URL
[49]	Metcalfe J Z, Longstaffe F J, 2014. Environmental change and seasonal behavior of mastodons in the Great Lakes region inferred from stable isotope analysis. Quat Res, 82:366-377 DOI URL
[50]	Metcalfe J Z, Longstaffe F J, Zazula G D, 2010. Nursing, weaning, and tooth development in woolly mammoths from Old Crow, Yukon, Canada: implications for Pleistocene extinctions. Palaeogeogr Palaeoclimatol Palaeoecol, 298:257-270 DOI URL
[51]	Mumby H S, Courtiol A, Mar K U et al., 2013. Birth seasonality and calf mortality in a large population of Asian elephants. Ecol Evol, 3:3794-3803 DOI URL
[52]	Patnaik R, 2017. Stable isotope based dietary reconstruction of some Plio-Pleistocene Siwalik and Narmada Valley elephant species of India. In: Abstracts Book of VII International Conference of Mammoths and Their Relatives. Taichung: National Museum of Natural Science. AF1-1
[53]	Patnaik R, Cerling T E, Uno K T et al., 2014. Diet and habitat of Siwalik Primates Indopithecus, Sivaladapis and Theropithecus. Ann Zool Fenn, 51:123-142 DOI URL
[54]	Pečnerová P, Díez-del-Molino D, Dussex N et al., 2017. Genome-based sexing provides clues about behavior and social structure in the woolly mammoth. Curr Biol, 27:3505-3510 DOI URL
[55]	Pederzani S, Britton K, 2019. Oxygen isotopes in bioarchaeology: principles and applications, challenges and opportunities. Earth-Sci Rev, 188:77-107 DOI PMID
[56]	Pradhan N M, Wegge P, Moe S R et al., 2008. Feeding ecology of two endangered sympatric megaherbivores: Asian elephant Elephas maximus and greater one-horned rhinoceros Rhinoceros unicornis in lowland Nepal. Wildl Biol, 14:147-154 DOI URL
[57]	Pushkina D, Bocherens H, Chaimanee Y et al., 2010. Stable carbon isotope reconstructions of diet and paleoenvironment from the late Middle Pleistocene Snake Cave in Northeastern Thailand. Naturwissenschaften, 97:299-309 DOI PMID
[58]	Qu Y, Jin C, Zhang Y et al., 2014. Preservation assessments and carbon and oxygen isotopes analysis of tooth enamel of Gigantopithecus blacki and contemporary animals from Sanhe Cave, Chongzuo, South China during the Early Pleistocene. Quat Int, 354:52-58 DOI URL
[59]	Renou J P, Deponge C, Gachon P et al., 2004. Characterization of animal products according to geographic origin and feeding diet using nuclear magnetic resonance and isotope ratio mass spectrometry: cow milk. Food Chem, 85:63-66 DOI URL
[60]	Roca A L, Ishida Y, Brandt A L et al., 2015. Elephant natural history: a genomic perspective. Annu Rev Anim Biosci, 3:139-167 DOI URL
[61]	Roth V L, Shoshani J, 1988. Dental identification and age determination in Elephas maximus. J Zool, 214:567-588 DOI URL
[62]	Rountrey A N, Fisher D C, Vartanyan S et al., 2007. Carbon and nitrogen isotope analyses of a juvenile woolly mammoth tusk: evidence of weaning. Quat Int, 169-170:166-173 DOI URL
[63]	Roy M, 2010. Habitat use and foraging ecology of the Asian elephant (Elephas maximus) in Buxa Tiger Reserve and adjoining areas of northern West Bengal. Ph. D thesis. West Bengal: Vidyasagar University, 1-132
[64]	Sanders W J, 2018. Horizontal tooth displacement and premolar occurrence in elephants and other elephantiform proboscideans. Hist Biol, 30:137-156 DOI URL
[65]	Shoshani J, 1998. Understanding proboscidean evolution: a formidable task. Trends Ecol Evol, 13:480-487 PMID
[66]	Shoshani J, Eisenberg J F, 1982. Elephas maximus. Mamm Species Archive, 182:1-8
[67]	Shoshani J, Tassy P, 1996. The Proboscidea: Evolution and Palaeoecology of Elephants and Their Relatives Oxford: Oxford University Press. 1-502
[68]	Sukumar R, 1989. Ecology of the Asian elephant in southern India. I. Movement and habitat utilization patterns. J Trop Ecol, 5:1-18 DOI URL
[69]	Sukumar R, 2003. The Living Elephants: Evolutionary Ecology, Behaviour, and Conservation. Oxford: Oxford University Press. 1-495
[70]	Sukumar R, 2006. A brief review of the status, distribution and biology of wild Asian elephants Elephas maximus. Int Zoo Yearb, 40:1-8 DOI URL
[71]	Sukumar R, Ramesh R, 1992. Stable carbon isotope ratios in Asian elephant collagen: implications for dietary studies. Oecologia, 91:536-539 DOI PMID
[72]	Sukumar R, Ramesh R, 1995. Elephant foraging: is browse or grass more important? In: Daniel J C, Datye H eds. A Week with Elephants. Oxford: Oxford University Press. 368-374
[73]	Suraprasit K, Bocherens H, Chaimanee Y et al., 2018. Late Middle Pleistocene ecology and climate in Northeastern Thailand inferred from the stable isotope analysis of Khok Sung herbivore tooth enamel and the land mammal cenogram. Quat Sci Rev, 193:24-42 DOI URL
[74]	Tong H, Deng L, Chen X, 2018. Late Pleistocene proboscideans from Yangjiawan caves in Pingxiang of Jiangxi, with discussions on the Stegodon orientalis-Elephas maximus assemblage. Vert PalAsiat, 56:306-326
[75]	Tsutaya T, Yoneda M, 2015. Reconstruction of breastfeeding and weaning practices using stable isotope and trace element analyses: a review. Am J Phys Anthropol, 156:2-21 DOI URL
[76]	Lee-Thorp J A, Lee-Thorp J A, Thackeray J F et al., 1990. Source-area determination of elephant ivory by isotopic analysis. Nature, 346:744-746 DOI URL
[77]	Vidya T N C, Fernando P, Melnick D J et al., 2005. Population differentiation within and among Asian elephant (Elephas maximus) populations in southern India. Heredity, 94:71-80 DOI URL
[78]	Vidya T N C, Sukumar R, Melnick D J, 2009. Range-wide mtDNA phylogeography yields insights into the origins of Asian elephants. Proc R Soc B, 276:893-902 DOI URL
[79]	Vogel J C, Eglington B, Auret J M, 1990. Isotope fingerprints in elephant bone and ivory. Nature, 346:747-749 DOI URL
[80]	Wang Y, Qin D, Jin C, 2017a. New Elephas remains from the Zhiren Cave of Mulan Mountain, Chongzuo, Guangxi with discussion on Quaternary proboscidean evolution in southern China. Quat Sci, 37:853-859
[81]	Wang Y, Zhao L, Du B et al., 2017b. New proboscidean remains associated with Homo sapiens from the Mawokou Cave in Bijie, Guizhou Province of south-western China. Acta Anthropol Sin, 36:414-425
[82]	Wittemyer G, Rasmussen H B, Douglas-Hamilton I, 2007a. Breeding phenology in relation to NDVI variability in free-ranging African elephant. Ecography, 30:42-50 DOI URL
[83]	Wittemyer G, Getz W M, Vollrath F et al., 2007b. Social dominance, seasonal movements, and spatial segregation in African elephants: a contribution to conservation behavior. Behav Ecol Sociobiol, 61:1919-1931 DOI URL
[84]	Wittemyer G, Cerling T E, Douglas-Hamilton I, 2009. Establishing chronologies from isotopic profiles in serially collected animal tissues: an example using tail hairs from African elephants. Chem Geol, 267:3-11 DOI URL
[85]	Wright L E, Schwarcz H P, 1998. Stable carbon and oxygen isotopes in human tooth enamel: identifying breastfeeding and weaning in prehistory. Am J Phys Anthropol, 106:1-18 PMID
[86]	Wright L E, Schwarcz H P, 1999. Correspondence between stable carbon, oxygen and nitrogen isotopes in human tooth enamel and dentine: infant diets at Kaminaljuyu. J Archaeol Sci, 26:1159-1170 DOI URL
[87]	Wu Y, Deng T, Hu Y et al., 2018. A grazing Gomphotherium in Middle Miocene Central Asia, 10 million years prior to the origin of the Elephantidae. Sci Rep, 8:7640 DOI URL
[88]	Yang F, Zhang L, 2012. Population genetic structure and population genetic diversity analysis based on mitochondrial DNA of Asian elephants (Elephas maximus) in China. Acta Theriol Sin, 32:90-100
[89]	Zazzo A, Balasse M, Patterson W P, 2006. The reconstruction of mammal individual history: refining high-resolution isotope record in bovine tooth dentine. J Archaeol Sci, 33:1177-1187 DOI URL
[90]	Zhang H, Wang Y, Janis C M et al., 2017. An examination of feeding ecology in Pleistocene proboscideans from southern China (Sinomastodon, Stegodon, Elephas), by means of dental microwear texture analysis. Quat Int, 445:60-70 DOI URL