Volume 13 Issue 1
Mar.  2022
Turn off MathJax
Article Contents
Xianglong Xu, Jiahu Jiang, Yu Lei, Chao Wang, Baoping Qing, Changqing Ding. 2022: Using stable isotope to compare the habitat use and trophic level between the new and old breeding range of wild Crested Ibis in the early breeding season. Avian Research, 13(1): 100007. doi: 10.1016/j.avrs.2022.100007
Citation: Xianglong Xu, Jiahu Jiang, Yu Lei, Chao Wang, Baoping Qing, Changqing Ding. 2022: Using stable isotope to compare the habitat use and trophic level between the new and old breeding range of wild Crested Ibis in the early breeding season. Avian Research, 13(1): 100007. doi: 10.1016/j.avrs.2022.100007

Using stable isotope to compare the habitat use and trophic level between the new and old breeding range of wild Crested Ibis in the early breeding season

doi: 10.1016/j.avrs.2022.100007
More Information
  • Corresponding author: E-mail address: cqding@bjfu.edu.cn (C. Ding)
  • Received Date: 27 Jan 2022
  • Accepted Date: 16 Feb 2022
  • Rev Recd Date: 12 Feb 2022
  • Available Online: 07 Jul 2022
  • Publish Date: 25 Feb 2022
  • The concept of foraging niche provides an insight into habitat use and dietary information of animals. Knowing intraspecific variation in foraging niche and trophic level is critical to the understanding of the species response to environmental changes during the process of range expansion, as well as the habitat management for conservation of threatened species. Using stable isotopic values of eggshell membranes (δ13C and δ15N), we examined whether there are differences in habitat use, trophic level, foraging niche width between the new and old breeding habitats (plains vs. mountains) of wild Crested Ibis (Nipponia nippon) in the early breeding season. Crested Ibis exhibited high variability in both δ13C and δ15N values, δ13C and δ15N varied as a function of habitat types. Birds breeding in plains had significantly higher δ13C but lower δ15N values compared to the birds breeding in mountains. Higher δ15N suggested that individuals in mountains consumed a great proportion of higher trophic level prey species in the early breeding season. Moreover, the isotopic niches were distinctly different in positions and showed small overlap between the two habitat types. The niche width was wider in old habitat than in the expanded new habitat. Our results demonstrated that the wild Crested Ibis had a high intraspecific variation in habitat uses and trophic levels in the early breeding season, and they could be divided into mountain and plain groups based on their different foraging niches. The difference in δ15N and niche width revealed that high trophic level food resources might be insufficient in plains. These findings stressed the importance of protecting foraging grounds in mountains and the necessity of improving foraging grounds in plains during winter and spring. Our study highlights the feasibility of investigating intraspecific variation in foraging ecology of birds through non-invasive isotopes of eggshell membranes. Understanding foraging niche variation gives us an insight into the food resource diversity in local areas and provides important information regarding particular foraging habitats that require protection.

     

  • loading
  • Angert AL, Crozier LG, Rissler LJ, Gilman SE, Tewksbury JJ, Chunco AJ. Do species' traits predict recent shifts at expanding range edges? Ecol Lett. 2011;14: 677-689. doi: 10.1111/j.1461-0248.2011.01620.x
    Auer SK, King DI. Ecological and life-history traits explain recent boundary shifts in elevation and latitude of western North American songbirds. Global Ecol Biogeogr. 2014;23: 867-875. doi: 10.1111/geb.12174
    Balasubramaniam P, Rotenberry JT. Elevation and latitude interact to drive life-history variation in precocial birds: a comparative analysis using galliformes. J Anim Ecol. 2016;85: 1528-1539. doi: 10.1111/1365-2656.12570
    Becker BH, Beissinger SR. Centennial decline in the trophic level of an endangered seabird after fisheries decline. Conserv Biol. 2006;20: 470-479. doi: 10.1111/j.1523-1739.2006.00379.x
    Bearhop S, Waldron S, Votier SC, Furness RW. Factors that influence assimilation rates and fractionation of nitrogen and carbon stable isotopes in avian blood and feathers. Physiol. Biochem. Zool. 2002;75: 451-458. doi: 10.1086/342800
    Bearhop S, Furness RW, Hilton G M, Votier S C, Waldron S. A forensic approach to understanding diet and habitat use from stable isotope analysis of (avian) claw material. Funct Ecol. 2003;17: 270-275. doi: 10.1046/j.1365-2435.2003.00725.x
    Bearhop S, Adams CE, Waldron S, Fuller RA, MacLeod H. Determining trophic niche width: a novel approach using stable isotope analysis. J Anim Ecol. 2004;73: 1007-1012. doi: 10.1111/j.0021-8790.2004.00861.x
    Bearhop S, Phillips RA, McGill R, Cherel Y, Dawson DA, Croxall JP. Stable isotopes indicate sex-specific and long-term individual foraging specialisation in diving seabirds. Mar Ecol Prog Ser. 2006;311: 157-164. doi: 10.3354/meps311157
    BirdLife International, 2018. Nipponia nippon. The IUCN Red List of Threatened Species 2018: e. T22697548A132069229. https://dx.doi.org/10.2305/IUCN.UK.2018-2.RLTS.T22697548A132069229.en. (Accessed 25 October 2021).
    Bolnick DI, Svanback R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forister ML. The ecology of individuals: incidence and implications of individual specialization. Am Nat. 2003;161: 1-28. doi: 10.1086/343878
    Brommer JE. Extent of recent polewards range margin shifts in Finnish birds depends on their body mass and feeding ecology. Ornis Fennica. 2008;85: 109-117.
    Buckley LB. Functional and phylogenetic approaches to forecasting species' responses to climate change. Annu Rev Ecol Evol S. 2012;43: 205-226. doi: 10.1146/annurev-ecolsys-110411-160516
    Ding C. Research on the crested ibis. Shanghai: Shanghai Scientific and Technological Educational Publishing House. 2004.
    Fisk AT, Tittlemier SA, Pranschke JL, Norstrom RJ. Using anthropogenic contaminants and stable isotopes to assess the feeding ecology of Greenland sharks. Ecology. 2002;83: 2162-2172. doi: 10.1890/0012-9658(2002)083[2162:UACASI]2.0.CO;2
    Francesiaz C, Yohannes E, Besnard A, Sadoul N, Blanchon T, Bechet A. Foraging niche shift maintains breeding parameters of a colonial waterbird during range expansion. Ecol Evol. 2020;10: 1988-1997. doi: 10.1002/ece3.6030
    Galimberti A, Spinelli S, Bruno A, Mezzasalma V, De Mattia F, Cortis P, Labra M. Evaluating the efficacy of restoration plantings through DNA barcoding of frugivorous bird diets. Conserv Biol. 2016;30: 763-773. doi: 10.1111/cobi.12687
    Gloutney ML, Hobson KA. Field preservation techniques for the analysis of stable-carbon and nitrogen isotope ratios in eggs. J Field Ornithol 1998;69: 223-227.
    Han, H., Wei, W., Hu, Y., Nie, Y., Ji, X., Yan, L.I., et al., 2019. Diet evolution and habitat contraction of giant pandas via stable isotope analysis. Curr. Biol. 29, 664–669. doi: 10.1016/j.cub.2018.12.051
    Heiss RS, Clark AB, & McGowan KJ. Growth and nutritional state of American crow nestlings vary between urban and rural habitats. Ecol Appl. 2009;19: 829-839. doi: 10.1890/08-0140.1
    Hobson KA, Clark RG. Assessing avian diets using stable isotopes I: turnover of 13C in tissues. Condor. 1992;94: 181-188. doi: 10.2307/1368807
    Hobson KA. Reconstructing avian diets using stable-carbon and nitrogen isotope analysis of egg components: patterns of isotopic fractionation and turnover. Condor. 1995;97: 752-762. doi: 10.2307/1369183
    Hu C. The home range and dispersal ecology of Crested Ibis (Nipponia nippon). PhD thesis, Beijing Forestry University, 2016.
    Inger R, Bearhop S. Applications of stable isotope analyses to avian ecology. Ibis. 2008;150: 447-461. doi: 10.1111/j.1474-919X.2008.00839.x
    Jackson AL, Inger R, Parnell AC, Bearhop S. Comparing isotopic niche widths among and within communities: SIBER - Stable Isotope Bayesian Ellipses in R. J Anim Ecol. 2011;80: 595-602. doi: 10.1111/j.1365-2656.2011.01806.x
    Jedlicka JA, Sharma AM, Almeida RP. Molecular tools reveal diets of insectivorous birds from predator fecal matter. Conserv Genet Resour. 2013;5: 879-885. doi: 10.1007/s12686-013-9900-1
    Jeschke JM, Strayer DL. Determinants of vertebrate invasion success in Europe and North America. Global Change Biol. 2006;12: 1608-1619. doi: 10.1111/j.1365-2486.2006.01213.x
    Kowalczyk ND, Chiaradia A, Preston TJ, Reina RD. Linking dietary shifts and reproductive failure in seabirds: a stable isotope approach. Funct Ecol. 2014;28: 755-765. doi: 10.1111/1365-2435.12216
    Kress WJ, Garcia-Robledo C, Uriarte M, Erickson DL. DNA barcodes for ecology, evolution, and conservation. Trends Ecol Evol. 2015;30: 25-35. doi: 10.1016/j.tree.2014.10.008
    Lei W, Masero JA, Dingle C, Liu Y, Chai Z, Zhu B, Peng H, Zhang Z, Piersma T. The value of coastal saltpans for migratory shorebirds: conservation insights from a stable isotope approach based on feeding guild and body size. Anim. Conserv. 2021;1-13.
    Litzow MA, Piatt JF, Abookire AA, Robards, MD. Energy density and variability in abundance of pigeon guillemot prey: Support for the quality-variability trade-off hypothesis. J Anim Ecol. 2004;73: 1149-1156. doi: 10.1111/j.0021-8790.2004.00890.x
    Liu Y. Rediscovery of crested ibis Nipponia nippon in Qinling Mountain. Chinese Journal of Zoology. 1981;27: 237.
    MacLean SA, Beissinger SR. Species' traits as predictors of range shifts under contemporary climate change: A review and meta-analysis. Global Change Biol. 2017;23: 4094-4105. doi: 10.1111/gcb.13736
    Marshall JD, Brooks JR, Lajtha K. Sources of variation in the stable isotopic composition of plants. Stable isotopes in ecology and environmental science. 2007;2: 22-60. doi: 10.1002/9780470691854.ch2
    Marshall HH, Inger R, Jackson AL, McDonald RA, Thompson FJ, Cant MA. Stable isotopes are quantitative indicators of trophic niche. Ecol let. 2019;22: 1990-2.
    Meyrier E, Jenni L, Botsch Y, Strebel S, Erne B, Tablado Z. Happy to breed in the city? Urban food resources limit reproductive output in Western Jackdaws. Ecol Evol. 2017;7: 1363-1374. doi: 10.1002/ece3.2733
    Milano S, Frahnert S, Hallau A, Topfer T, Woog F, Voigt, CC. Isotope record tracks changes in historical wintering ranges of a passerine in sub-Saharan Africa. Global Change Biol. 2021;27: 5460-5468. doi: 10.1111/gcb.15794
    Mills WF, McGill RA, Cherel Y, Votier SC, Phillips RA. Stable isotopes demonstrate intraspecific variation in habitat use and trophic level of non-breeding albatrosses. Ibis. 2021;163: 463-472. doi: 10.1111/ibi.12874
    Newsome SD, Martinez del Rio C, Bearhop S, Phillips DL. A niche for isotopic ecology. Front Ecol Environ. 2007;5: 429-436. doi: 10.1890/1540-9295(2007)5[429:ANFIE]2.0.CO;2
    Oppel S, Powell AN, O'Brien DM. Using eggshell membranes as a non-invasive tool to investigate the source of nutrients in avian eggs. J Ornithol. 2009;150;1: 109-115. doi: 10.1007/s10336-008-0325-7
    Owen M. An assessment of fecal analysis technique in waterfowl feeding studies. J Wildlife Manage. 1975;271-279. doi: 10.2307/3799903
    Post DM. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology. 2002;83: 703-718. doi: 10.1890/0012-9658(2002)083[0703:USITET]2.0.CO;2
    Rader JA, Newsome SD, Sabat P, Chesser RT, Dillon ME, Martinez del Rio C. Isotopic niches support the resource breadth hypothesis. J Anim Ecol, 2017;86: 405-413. doi: 10.1111/1365-2656.12629
    R Core Team. R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. 2019. https://www.R-project.org/.
    Sheppard, C.E., Inger, R., McDonald, R.A., Barker, S., Jackson, A.L., Thompson, F.J., et al., 2018. Intragroup competition predicts individual foraging specialisation in a groupliving mammal. Ecol. Lett. 21, 665–673. doi: 10.1111/ele.12933
    Skorka P, Lenda M, Martyka R, Tworek S. The use of metapopulation and optimal foraging theories to predict movement and foraging decisions of mobile animals in heterogeneous landscapes. Landscape Ecol. 2009;24: 599-609. doi: 10.1007/s10980-009-9333-0
    Song Z. Sex allocation pattern and reproduction strategy in the wild population of Crested Ibis (Nipponia nippon). PhD thesis, Beijing Forestry University, 2018.
    Song Z, Zou Y, Hu C, Ye Y, Wang C, Qing B, Komdeur J, Ding C. Silver spoon effects of hatching order in an asynchronous hatching bird. Behav Ecol. 2019;30: 509-517. doi: 10.1093/beheco/ary191
    Stearns SC. The evolution of life histories. Oxford, UK: Oxford University Press, 1992.
    Schmidt K, Atkinson A, Stubing D, McClelland JW, Montoya JP, Voss M. Trophic relationships among Southern Ocean copepods and krill: some uses and limitations of a stable isotope approach. Limnol Oceanogr. 2003;48: 277-289. doi: 10.4319/lo.2003.48.1.0277
    Wang C, Liu D, Qing B, Ding H, Cui Y, Ye Y, Lu J, Yan L, Ke L, Ding C. The current population and distribution of wild crested ibis Nipponia nippon. Chinese Journal of Zoology. 2014;49: 666-671.
    Wang C, Zhang Y, Zeng J, Gao J, Yan L. Liu D. Reproductive status and population size of wild crested ibis (Nipponia nippon) in China. Scientia Silvae Sinicae. 2020;56: 143-150. doi: 10.3390/catal10020143
    Weimerskirch H. Linking demographic processes and foraging ecology in wandering albatross-Conservation implications. J Anim Ecol. 2018;87: 945-955. doi: 10.1111/1365-2656.12817
    Wright J, Both C, Cotton PA, Bryant D. Quality vs. quantity: Energetic and nutritional trade-offs in parental provisioning strategies. J Anim Ecol. 1998;67: 620-634. doi: 10.1046/j.1365-2656.1998.00221.x
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(4)  / Tables(2)

    Article Metrics

    Article views (38) PDF downloads(0) Cited by()
    Proportional views

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return