Volume 44 Issue 2
Mar.  2023
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Article Contents
Meng Wang, Yong-Gang Nie, Ronald R. Swaisgood, Wei Wei, Wen-Liang Zhou, Ze-Jun Zhang, Gui-Ming Wang, Fu-Wen Wei. Stable seasonal migration patterns in giant pandas. Zoological Research, 2023, 44(2): 341-348. doi: 10.24272/j.issn.2095-8137.2022.421
Citation: Meng Wang, Yong-Gang Nie, Ronald R. Swaisgood, Wei Wei, Wen-Liang Zhou, Ze-Jun Zhang, Gui-Ming Wang, Fu-Wen Wei. Stable seasonal migration patterns in giant pandas. Zoological Research, 2023, 44(2): 341-348. doi: 10.24272/j.issn.2095-8137.2022.421

Stable seasonal migration patterns in giant pandas

doi: 10.24272/j.issn.2095-8137.2022.421
Permission for field surveys in Foping National Nature Reserve was granted by the National Forestry and Grassland Administration and the Foping National Nature Reserve.
Supplementary data to this article can be found online.
The authors declare that they have no competing interests.
M.W., F.W.W., and Y.G.N. conceived and designed the study. Y.G.N., W.W., W.L.Z., and Z.J.Z. conducted the surveys. M.W. and Y.G.N. prepared the data. M.W. and G.M.W. analyzed the data. M.W. and R.R.S. wrote the paper. All authors read and approved the final version of the manuscript.
Funds:  This work was supported by the National Natural Science Foundation of China (31821001) and Strategic Priority Research Program of the Chinese Academy of Sciences (XDB3100000)
More Information
  • Corresponding author: E-mail: weifw@ioz.ac.cn
  • Received Date: 2022-12-02
  • Accepted Date: 2023-02-20
  • Published Online: 2023-02-20
  • Publish Date: 2023-03-18
  • A critical function of animal movement is to maximize access to essential resources in temporally fluctuating and spatially heterogeneous environments. Seasonally mediated resource fluctuations may influence animal movements, enabling them to track changing resource distributions, resulting in annual migration patterns. The conservation-dependent giant panda (Ailuropoda melanoleuca) displays seasonal movement patterns; however, the key factor driving these seasonal migration patterns remains poorly understood. Here, we used GPS tracking collars to monitor the movements of six giant pandas over a 12-year period across different elevations, and performed statistical analysis of seasonal migration directions, routes, habitat revisitation, home range overlap, first arrival events, and stability. Our results revealed a compelling pattern of seasonal migrations that facilitated the ability of the pandas to forage at the appropriate time and place to maximize nutritional intake. Our results indicated that pandas utilize spatial memory to locate reliable food resources, as evidenced by their annual return to the same or similar winter and summer home ranges and the consistently maintained percentage of home range overlap. These novel insights into giant panda foraging and movement ecology not only enhance our understanding of its ability to adapt to nutritionally poor dietary resources but also provide important information for the development of resource utilization-based protection and management strategies.
  • Permission for field surveys in Foping National Nature Reserve was granted by the National Forestry and Grassland Administration and the Foping National Nature Reserve.
    Supplementary data to this article can be found online.
    The authors declare that they have no competing interests.
    M.W., F.W.W., and Y.G.N. conceived and designed the study. Y.G.N., W.W., W.L.Z., and Z.J.Z. conducted the surveys. M.W. and Y.G.N. prepared the data. M.W. and G.M.W. analyzed the data. M.W. and R.R.S. wrote the paper. All authors read and approved the final version of the manuscript.
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  • [1]
    Abrahms B, Hazen EL, Aikens EO, et al. 2019. Memory and resource tracking drive blue whale migrations. Proceedings of the National Academy of Sciences of the United States of America, 116(12): 5582−5587. doi: 10.1073/pnas.1819031116
    [2]
    Aikens EO, Kauffman MJ, Merkle JA, et al. 2017. The greenscape shapes surfing of resource waves in a large migratory herbivore. Ecology Letters, 20(6): 741−750. doi: 10.1111/ele.12772
    [3]
    Aikens EO, Mysterud A, Merkle JA, et al. 2020. Wave-like patterns of plant phenology determine ungulate movement tactics. Current Biology, 30(17): 3444−3449.e4. doi: 10.1016/j.cub.2020.06.032
    [4]
    Albon SD, Langvatn R. 1992. Plant phenology and the benefits of migration in a temperate ungulate. Oikos, 65(3): 502−513. doi: 10.2307/3545568
    [5]
    Avgar T, Baker JA, Brown GS, et al. 2015. Space-use behaviour of woodland caribou based on a cognitive movement model. Journal of Animal Ecology, 84(4): 1059−1070. doi: 10.1111/1365-2656.12357
    [6]
    Avgar T, Street G, Fryxell JM. 2014. On the adaptive benefits of mammal migration. Canadian Journal of Zoology, 92(6): 481−490. doi: 10.1139/cjz-2013-0076
    [7]
    Bailey H, Mate BR, Palacios DM, et al. 2009. Behavioural estimation of blue whale movements in the Northeast Pacific from state-space model analysis of satellite tracks. Endangered Species Research, 10: 93−106. doi: 10.3354/esr00239
    [8]
    Barboza PS, Parker KL. 2008. Allocating protein to reproduction in Arctic reindeer and caribou. Physiological and Biochemical Zoology, 81(6): 835−855. doi: 10.1086/590414
    [9]
    Ben-David M. 1997. Timing of reproduction in wild mink: the influence of spawning Pacific salmon. Canadian Journal of Zoology, 75(3): 376−382. doi: 10.1139/z97-047
    [10]
    Betts MG, Rodenhouse NL, Sillett TS, et al. 2008. Dynamic occupancy models reveal within-breeding season movement up a habitat quality gradient by a migratory songbird. Ecography, 31(5): 592−600. doi: 10.1111/j.0906-7590.2008.05490.x
    [11]
    Bolger DT, Newmark WD, Morrison TA, et al. 2008. The need for integrative approaches to understand and conserve migratory ungulates. Ecology Letters, 11(1): 63−77.
    [12]
    Bracis C, Gurarie E, Van Moorter B, et al. 2015. Memory effects on movement behavior in animal foraging. PLoS One, 10(8): e0136057. doi: 10.1371/journal.pone.0136057
    [13]
    Bracis C, Mueller T. 2017. Memory, not just perception, plays an important role in terrestrial mammalian migration. Proceedings of the Royal Society B:Biological Sciences, 284(1855): 20170449. doi: 10.1098/rspb.2017.0449
    [14]
    Connor T, Hull V, Liu JG. 2016. Telemetry research on elusive wildlife: a synthesis of studies on giant pandas. Integrative Zoology, 11(4): 295−307. doi: 10.1111/1749-4877.12197
    [15]
    Deacy WW, Erlenbach JA, Leacock WB, et al. 2018. Phenological tracking associated with increased salmon consumption by brown bears. Scientific Reports, 8(1): 11008. doi: 10.1038/s41598-018-29425-3
    [16]
    Fagan WF, Lewis MA, Auger-Méthé M, et al. 2013. Spatial memory and animal movement. Ecology Letters, 16(10): 1316−1329. doi: 10.1111/ele.12165
    [17]
    Fryxell JM, Greever J, Sinclair ARE. 1988. Why are migratory ungulates so abundant?. The American Naturalist, 131(6): 781−798. doi: 10.1086/284822
    [18]
    Fryxell JM, Sinclair ARE. 1988. Causes and consequences of migration by large herbivores. Trends in Ecology & Evolution, 3(9): 237−241.
    [19]
    Han H, Wei W, Hu YB, et al. 2019. Diet evolution and habitat contraction of giant pandas via stable isotope analysis. Current Biology, 29(4): 664−669.e2. doi: 10.1016/j.cub.2018.12.051
    [20]
    He K, Dai Q, Foss-Grant A, et al. 2019. Movement and activity of reintroduced giant pandas. Ursus, 29(2): 163−174. doi: 10.2192/URSUS-D-17-00030.1
    [21]
    Huang GP, Wang X, Hu YB, et al. 2021. Diet drives convergent evolution of gut microbiomes in bamboo-eating species. Science China Life Sciences, 64(1): 88−95. doi: 10.1007/s11427-020-1750-7
    [22]
    Jesmer BR, Merkle JA, Goheen JR, et al. 2018. Is ungulate migration culturally transmitted? Evidence of social learning from translocated animals. Science, 361(6406): 1023−1025. doi: 10.1126/science.aat0985
    [23]
    Jones MC, Marron JS, Sheather SJ. 1996. A brief survey of bandwidth selection for density estimation. Journal of the American Statistical Association, 91(433): 401−407. doi: 10.1080/01621459.1996.10476701
    [24]
    Kernohan BJ, Gitzen RA, Millspaugh JJ. 2001. Chapter 5 - Analysis of animal space use and movements. In: Millspaugh JJ, Marzluff JM. Radio Tracking and Animal Populations. San Diego: Academic Press, 125–166.
    [25]
    Lai XL, Zhou WL, Gao HL, et al. 2020. Impact of sympatric carnivores on den selection of wild giant pandas. Zoological Research, 41(3): 273−280. doi: 10.24272/j.issn.2095-8137.2020.027
    [26]
    Li C, Bao ZQ, Luo XR, et al. 2022. Does high vegetation coverage equal high giant panda density?. Zoological Research, 43(4): 608−611. doi: 10.24272/j.issn.2095-8137.2022.005
    [27]
    Li YX, Swaisgood RR, Wei W, et al. 2017. Withered on the stem: is bamboo a seasonally limiting resource for giant pandas?. Environmental Science and Pollution Research, 24(11): 10537−10546. doi: 10.1007/s11356-017-8746-6
    [28]
    Merkle JA, Fortin D, Morales JM. 2014. A memory-based foraging tactic reveals an adaptive mechanism for restricted space use. Ecology Letters, 17(8): 924−931. doi: 10.1111/ele.12294
    [29]
    Merkle JA, Sawyer H, Monteith KL, et al. 2019. Spatial memory shapes migration and its benefits: evidence from a large herbivore. Ecology Letters, 22(11): 1797−1805. doi: 10.1111/ele.13362
    [30]
    Mettke-Hofmann C, Gwinner E. 2003. Long-term memory for a life on the move. Proceedings of the National Academy of Sciences of the United States of America, 100(10): 5863−5866. doi: 10.1073/pnas.1037505100
    [31]
    Middleton AD, Merkle JA, McWhirter DE, et al. 2018. Green-wave surfing increases fat gain in a migratory ungulate. Oikos, 127(7): 1060−1068. doi: 10.1111/oik.05227
    [32]
    Monteith KL, Bleich VC, Stephenson TR, et al. 2014. Life-history characteristics of mule deer: effects of nutrition in a variable environment. Wildlife Monographs, 186(1): 1−62. doi: 10.1002/wmon.1011
    [33]
    Mueller T, Fagan WF. 2008. Search and navigation in dynamic environments: from individual behaviors to population distributions. Oikos, 117(5): 654−664. doi: 10.1111/j.0030-1299.2008.16291.x
    [34]
    Mueller T, Fagan WF, Grimm V. 2011. Integrating individual search and navigation behaviors in mechanistic movement models. Theoretical Ecology, 4(3): 341−355. doi: 10.1007/s12080-010-0081-1
    [35]
    National Forestry and Grassland Administration. 2021. 4th National Survey Report on Giant Panda in China. Beijing: Science Press. (in Chinese)
    [36]
    Nie YG, Wei FW, Zhou WL, et al. 2019. Giant pandas are macronutritional carnivores. Current Biology, 29(10): 1677−1682.e2. doi: 10.1016/j.cub.2019.03.067
    [37]
    Nie YG, Zhang ZJ, Raubenheimer D, et al. 2015. Obligate herbivory in an ancestrally carnivorous lineage: the giant panda and bamboo from the perspective of nutritional geometry. Functional Ecology, 29(1): 26−34. doi: 10.1111/1365-2435.12302
    [38]
    Pan WS, Lv Z, Zhu XJ, et al. 2001. A Chance for Lasting Survival. Beijing: Peking University Press. (in Chinese)
    [39]
    Piper WH. 2011. Making habitat selection more “familiar”: a review. Behavioral Ecology and Sociobiology, 65(7): 1329−1351. doi: 10.1007/s00265-011-1195-1
    [40]
    Polansky L, Kilian W, Wittemyer G. 2015. Elucidating the significance of spatial memory on movement decisions by African savannah elephants using state–space models. Proceedings of the Royal Society B:Biological Sciences, 282(1805): 20143042. doi: 10.1098/rspb.2014.3042
    [41]
    Powell RA. 2000. Animal home ranges and territories and home range estimators. In: Boitani L, Fuller T. Research Techniques in Animal Ecology: Controversies and Consequences. New York: Columbia University Press, 65–110.
    [42]
    Ranc N, Moorcroft PR, Ossi F, et al. 2021. Experimental evidence of memory-based foraging decisions in a large wild mammal. Proceedings of the National Academy of Sciences of the United States of America, 118(15): e2014856118. doi: 10.1073/pnas.2014856118
    [43]
    Riotte-Lambert L, Benhamou S, Bonenfant C, et al. 2017. Spatial memory shapes density dependence in population dynamics. Proceedings of the Royal Society B:Biological Sciences, 284(1867): 20171411. doi: 10.1098/rspb.2017.1411
    [44]
    Rolandsen CM, Solberg EJ, Saether BE, et al. 2017. On fitness and partial migration in a large herbivore - migratory moose have higher reproductive performance than residents. Oikos, 126(4): 547−555. doi: 10.1111/oik.02996
    [45]
    Sahanatien V, Peacock E, Derocher AE. 2015. Population substructure and space use of Foxe Basin polar bears. Ecology and Evolution, 5(14): 2851−2864. doi: 10.1002/ece3.1571
    [46]
    Schaller GB, Hu JC, Pan WS, et al. 1985. The Giant Pandas of Wolong. Chicago: University of Chicago Press.
    [47]
    Schindler DE, Armstrong JB, Bentley KT, et al. 2013. Riding the crimson tide: mobile terrestrial consumers track phenological variation in spawning of an anadromous fish. Biology Letters, 9(3): 20130048. doi: 10.1098/rsbl.2013.0048
    [48]
    Singh NJ, Grachev IA, Bekenov AB, et al. 2010. Tracking greenery across a latitudinal gradient in central Asia - the migration of the saiga antelope. Diversity and Distributions, 16(4): 663−675. doi: 10.1111/j.1472-4642.2010.00671.x
    [49]
    Spencer WD. 2012. Home ranges and the value of spatial information. Journal of Mammalogy, 93(4): 929−947. doi: 10.1644/12-MAMM-S-061.1
    [50]
    Stamps J. 1995. Motor learning and the value of familiar space. The American Naturalist, 146(1): 41−58. doi: 10.1086/285786
    [51]
    Swaisgood RR, Wang DJ, Wei FW. 2016 (2016-10-12). Ailuropoda melanoleuca. IUCN Red List of Threatened Species, http://hubaogy.cn/index/news/show/id/107.html.
    [52]
    Swaisgood RR, Wang DJ, Wei FW. 2018. Panda downlisted but not out of the woods. Conservation Letters, 11(1): e12355. doi: 10.1111/conl.12355
    [53]
    Terborgh J. 1986. Keystone plant resources in the tropical forest. In: Soulé M. Conservation Biology - the Science of Scarcity and Diversity. Sunderland: Sinauer Associates, Inc.
    [54]
    Tucker MA, Böhning-Gaese K, Fagan WF, et al. 2018. Moving in the Anthropocene: global reductions in terrestrial mammalian movements. Science, 359(6374): 466−469. doi: 10.1126/science.aam9712
    [55]
    Van Der Graaf AJ, Stahl J, Klimkowska A, et al. 2006. Surfing on a green wave - how plant growth drives spring migration in the barnacle goose Branta leucopsis. Ardea, 94(3): 567–577.
    [56]
    Van Moorter B, Visscher D, Benhamou S, et al. 2009. Memory keeps you at home: a mechanistic model for home range emergence. Oikos, 118(5): 641−652. doi: 10.1111/j.1600-0706.2008.17003.x
    [57]
    Walter WD, Fischer JW, Baruch-Mordo S, et al. 2011. What is the proper method to delineate home range of an animal using today’s advanced GPS telemetry systems: the initial step. USDA Wildlife Services-Staff Publications, 1375.
    [58]
    Wand MP, Jones MC. 1995. Kernel Smoothing. London: Chapman & Hall.
    [59]
    Wang F, Liu JG. 2017. Conservation planning beyond giant pandas: the need for an innovative telecoupling framework. Science China Life Sciences, 60(5): 551−554. doi: 10.1007/s11427-016-0349-0
    [60]
    Wei FW, Hu YB, Yan L, et al. 2015a. Giant pandas are not an evolutionary cul-de-sac: evidence from multidisciplinary research. Molecular Biology and Evolution, 32(1): 4−12. doi: 10.1093/molbev/msu278
    [61]
    Wei FW, Swaisgood R, Hu YB, et al. 2015b. Progress in the ecology and conservation of giant pandas. Conservation Biology, 29(6): 1497−1507. doi: 10.1111/cobi.12582
    [62]
    Wei FW, Wang X, Wu Q. 2015c. The giant panda gut microbiome. Trends in Microbiology, 23(8): 450−452. doi: 10.1016/j.tim.2015.06.004
    [63]
    Wei W, Nie YG, Zhang ZJ, et al. 2015d. Hunting bamboo: foraging patch selection and utilization by giant pandas and implications for conservation. Biological Conservation, 186: 260−267. doi: 10.1016/j.biocon.2015.03.023
    [64]
    Wolf M, Frair J, Merrill E, et al. 2009. The attraction of the known: the importance of spatial familiarity in habitat selection in wapiti Cervus elaphus. Ecography, 32(3): 401–410.
    [65]
    Wood SN. 2017. Generalized Additive Models: An Introduction with R. 2nd ed. New York: Chapman and Hall/CRC.
    [66]
    Xu WH, Viña A, Kong LQ, et al. 2017. Reassessing the conservation status of the giant panda using remote sensing. Nature Ecology & Evolution, 1(11): 1635−1638.
    [67]
    Yang ZS, Gu XD, Nie YG, et al. 2018. Reintroduction of the giant panda into the wild: A good start suggests a bright future. Biological Conservation, 217: 181−186. doi: 10.1016/j.biocon.2017.08.012
    [68]
    Zhang ZJ, Sheppard JK, Swaisgood RR, et al. 2014. Ecological scale and seasonal heterogeneity in the spatial behaviors of giant pandas. Integrative Zoology, 9(1): 46−60. doi: 10.1111/1749-4877.12030
    [69]
    Zhou WL, Wang M, Gao K, et al. 2022a. Behavioural thermoregulation by montane ungulates under climate warming. Diversity and Distributions, 28(10): 2229−2238. doi: 10.1111/ddi.13626
    [70]
    Zhou WL, Wang M, Ma YJ, et al. 2022b. Community structure of the solitary giant pandas is maintained by indirect social connections. Movement Ecology, 10(1): 53. doi: 10.1186/s40462-022-00354-1
    [71]
    Zhu LF, Wu Q, Dai JY, et al. 2011a. Evidence of cellulose metabolism by the giant panda gut microbiome. Proceedings of the National Academy of Sciences of the United States of America, 108(43): 17714−17719. doi: 10.1073/pnas.1017956108
    [72]
    Zhu LF, Zhang SN, Gu XD, et al. 2011b. Significant genetic boundaries and spatial dynamics of giant pandas occupying fragmented habitat across southwest China. Molecular Ecology, 20(6): 1122−1132. doi: 10.1111/j.1365-294X.2011.04999.x
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