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Ecosystems

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Ungulates Attenuate the Response of Mediterranean Mountain Vegetation to Climate Oscillations

  • Jomar Magalhães BarbosaEmail author
  • Roberto Pascual-Rico
  • Sergio Eguia Martínez
  • José A. Sánchez-Zapata
Article

Abstract

In regions with a long-standing history of grazing pressure, vegetation has co-evolved with herbivores by developing intrinsic functional dynamics. Although this type of trophic interaction has been recognised as being important for shaping how vegetation responds to climate, better knowledge about how this process occurs on the landscape scale and over a long time range is necessary. Here, we evaluated the potential roles of herbivores in modulating the response of mountainous Mediterranean vegetation to seasonal and long-term climate oscillations. To understand the relations among climate, plants and animal population, we fitted a Bayesian model to a combination of long-term (1995–2014) climate datasets, satellite greenness maps (NASA Landsat NDVI) and exotic Barbary sheep census data (breeding success and abundance of Ammotragus lervia). We also used the intrinsic mode function and Hilbert spectrum transformations to decompose NDVI time series and to evaluate their periodic oscillations. We found remarkable dissimilarities as to how climate affects the temporal oscillation of vegetation greenness between landscapes both with and without ungulates, albeit their similarities under environmental conditions. Vegetation responses to climate are particularly attenuated in landscapes with ungulates, an effect that depends on ungulate population abundance. In a world where extreme climate events are becoming frequent and intense, our results indicate that ungulates can strongly modulate how grasslands and scrublands respond to climate change. Increasing our knowledge as to how this type of trophic interaction affects vegetation responses to climate variability is of much importance for managing ungulate rewilding strategies.

Keywords

herbivore ungulates exotic animals Normalised Difference Vegetation Index primary productivity plant biomass climate change climate adaptability 

Notes

Acknowledgements

We are grateful to all the people who participated in the Barbary sheep census. This study was partially funded by the Projects CGL2015-66966-C2-1-2-R and RTI2018-099609-B-C21 (Spanish Ministry of Economy and Competitiveness and EU/ERDF) and Regional Government of Murcia, Spain (CARM).

Supplementary material

10021_2019_449_MOESM1_ESM.docx (972 kb)
Supplementary material 1 (DOCX 972 kb)

References

  1. Anadón JD, Pérez-García JM, Pérez I, Royo J, Sánchez-Zapata JA. 2018. Disentangling the effects of habitat, connectivity and interspecific competition in the range expansion of exotic and native ungulates. Landsc Ecol 33:597–608.CrossRefGoogle Scholar
  2. Augustine DJ, McNaughton SJ, Frank DA. 2003. Feedbacks between soil nutrients and large herbivores in a managed savanna ecosystem. Ecol Appl 13:1325–37.CrossRefGoogle Scholar
  3. Bakker ES, Svenning J-C. 2018. Trophic rewilding: impact on ecosystems under global change. Philos Trans R Soc B Biol Sci 373:20170432.CrossRefGoogle Scholar
  4. Bernués A, Ruiz R, Olaizola A, Villalba D, Casasús I. 2011. Sustainability of pasture-based livestock farming systems in the European Mediterranean context: synergies and trade-offs. Livest Sci 139:44–57.CrossRefGoogle Scholar
  5. Blondel J. 2006. The ‘design’ of Mediterranean landscapes: a millennial story of humans and ecological systems during the historic period. Hum Ecol 34:713–29.CrossRefGoogle Scholar
  6. Boelman NT, Stieglitz M, Rueth HM, Sommerkorn M, Griffin KL, Shaver GR, Gamon JA. 2003. Response of NDVI, biomass, and ecosystem gas exchange to long-term warming and fertilization in wet sedge tundra. Oecologia 135:414–21.PubMedCrossRefPubMedCentralGoogle Scholar
  7. Bowen ME, McAlpine CA, House APN, Smith GC. 2007. Regrowth forests on abandoned agricultural land: a review of their habitat values for recovering forest fauna. Biol Conserv 140:273–96.CrossRefGoogle Scholar
  8. Buhk C, Götzenberger L, Wesche K, Gómez PS, Hensen I. 2006. Post-fire regeneration in a Mediterranean pine forest with historically low fire frequency. Acta Oecol 30:288–98.CrossRefGoogle Scholar
  9. Cromsigt JPGM, te Beest M, Kerley GIH, Landman M, le Roux E, Smith FA. 2018. Trophic rewilding as a climate change mitigation strategy? Philos Trans R Soc B Biol Sci 373:20170440.CrossRefGoogle Scholar
  10. Derry JF, Boone RB. 2010. Grazing systems are a result of equilibrium and non-equilibrium dynamics. J Arid Environ 74:307–9.CrossRefGoogle Scholar
  11. Deutsche Akademie der Naturforscher Leopoldina, editor. 2013. Trends in extreme weather events in Europe: implications for national and European Union adaptation strategies. Halle (Saale). EASAC policy report 22. ISBN: 978-3-8047-3239-1.Google Scholar
  12. Di Marco M, Boitani L, Mallon D, Hoffmann M, Iacucci A, Meijaard E, Visconti P, Schipper J, Rondinini C. 2014. A retrospective evaluation of the global decline of carnivores and ungulates: global decline of carnivores and ungulates. Conserv Biol 28:1109–18.PubMedCrossRefPubMedCentralGoogle Scholar
  13. Doughty CE, Roman J, Faurby S, Wolf A, Haque A, Bakker ES, Malhi Y, Dunning JB, Svenning J-C. 2016. Global nutrient transport in a world of giants. Proc Natl Acad Sci 113:868–73.PubMedCrossRefPubMedCentralGoogle Scholar
  14. Doughty CE, Wolf A, Field CB. 2010. Biophysical feedbacks between the Pleistocene megafauna extinction and climate: the first human-induced global warming? Geophys Res Lett 37:1–5.CrossRefGoogle Scholar
  15. Ellis EC, Kaplan JO, Fuller DQ, Vavrus S, Klein Goldewijk K, Verburg PH. 2013. Used planet: a global history. Proc Natl Acad Sci 110:7978–85.PubMedCrossRefPubMedCentralGoogle Scholar
  16. Fernández-Olalla M, Martínez-Jauregui M, Perea R, Velamazán M, San Miguel A. 2016. Threat or opportunity? Browsing preferences and potential impact of Ammotragus lervia on woody plants of a Mediterranean protected area. J Arid Environ 129:9–15.CrossRefGoogle Scholar
  17. Foga S, Scaramuzza PL, Guo S, Zhu Z, Dilley RD, Beckmann T, Schmidt GL, Dwyer JL, Joseph Hughes M, Laue B. 2017. Cloud detection algorithm comparison and validation for operational Landsat data products. Remote Sens Environ 194:379–90.CrossRefGoogle Scholar
  18. Frank DA, Groffman PM. 1998. Ungulate vs. landscape control of soil C and N processes in grasslands of Yellowstone National Park. Ecology 79:2229–41.CrossRefGoogle Scholar
  19. Funk C, Peterson P, Landsfeld M, Pedreros D, Verdin J, Shukla S, Husak G, Rowland J, Harrison L, Hoell A, Michaelsen J. 2015. The climate hazards infrared precipitation with stations—a new environmental record for monitoring extremes. Sci Data 2:150066.PubMedPubMedCentralCrossRefGoogle Scholar
  20. González-Candela M, Léon-Vizcaíno L, Cubero-Pablo MJ. 2004. Population effects of Sarcoptic manage in Barbary sheep (Ammotragus Lervia) from Sierra Espuña Regional Park, Spain. J Wildl Dis 40:456–65.PubMedCrossRefPubMedCentralGoogle Scholar
  21. Heidinger AK, Foster H Michael J, Walther A, Zhao X, NOAA CDR Program. 2014. NOAA Climate Data Record (CDR) of Reflectance and Brightness Temperatures from AVHRR Pathfinder Atmospheres-Extended (PATMOS-x). https://www.ngdc.noaa.gov/docucomp/page?xml=NOAA/NESDIS/NCDC/Geoportal/iso/xml/C00837. Last accessed 01/03/2018.
  22. Hoegh-Guldberg O, Hughes L, McIntyre S, Lindenmayer DB, Parmesan C, Possingham HP, Thomas CD. 2008. ECOLOGY: assisted colonization and rapid climate change. Science 321:345–6.PubMedCrossRefPubMedCentralGoogle Scholar
  23. Holmes EE, Ward EJ, Scheuerell MD. 2018. Analysis of multivariate time-series using the MARSS package. https://cran.r-project.org/web/packages/MARSS/vignettes/UserGuide.pdf. Last accessed 01/04/2018.
  24. Huang NE, Shen Z, Long SR, Wu MC, Shih HH, Zheng Q, Yen N-C, Tung CC, Liu HH. 1998. The empirical mode decomposition and the Hilbert spectrum for nonlinear and non-stationary time series analysis. Proc R Soc Math Phys Eng Sci 454:903–95.CrossRefGoogle Scholar
  25. Hunter MD, Price PW. 1992. Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73:724–32.Google Scholar
  26. Huxman TE, Snyder KA, Tissue D, Leffler AJ, Ogle K, Pockman WT, Sandquist DR, Potts DL, Schwinning S. 2004. Precipitation pulses and carbon fluxes in semiarid and arid ecosystems. Oecologia 141:254–68.PubMedCrossRefPubMedCentralGoogle Scholar
  27. Isbell F, Craven D, Connolly J, Loreau M, Schmid B, Beierkuhnlein C, Bezemer TM, Bonin C, Bruelheide H, de Luca E, Ebeling A, Griffin JN, Guo Q, Hautier Y, Hector A, Jentsch A, Kreyling J, Lanta V, Manning P, Meyer ST, Mori AS, Naeem S, Niklaus PA, Polley HW, Reich PB, Roscher C, Seabloom EW, Smith MD, Thakur MP, Tilman D, Tracy BF, van der Putten WH, van Ruijven J, Weigelt A, Weisser WW, Wilsey B, Eisenhauer N. 2015. Biodiversity increases the resistance of ecosystem productivity to climate extremes. Nature 526:574–7.PubMedCrossRefPubMedCentralGoogle Scholar
  28. Jia S, Wang X, Yuan Z, Lin F, Ye J, Hao Z, Luskin MS. 2018. Global signal of top-down control of terrestrial plant communities by herbivores. PNAS 115(24):6237–42.PubMedCrossRefPubMedCentralGoogle Scholar
  29. Junsheng C, Dejie Y, Yu Y. 2006. Research on the intrinsic mode function (IMF) criterion in EMD method. Mech Syst Signal Process 20:817–24.CrossRefGoogle Scholar
  30. Kaarlejärvi E, Hoset KS, Olofsson J. 2015. Mammalian herbivores confer resilience of Arctic shrub-dominated ecosystems to changing climate. Glob Change Biol 21:3379–88.CrossRefGoogle Scholar
  31. Kim D, Oh HS. 2009. EMD: a package for empirical mode decomposition and Hilbert spectrum. R J 1:40–6.CrossRefGoogle Scholar
  32. Letnic M, Ripple WJ. 2017. Large-scale responses of herbivore prey to canid predators and primary productivity: LETNIC and RIPPLE. Glob Ecol Biogeogr 26:860–6.CrossRefGoogle Scholar
  33. Li L, Wang Y-P, Beringer J, Shi H, Cleverly J, Cheng L, Eamus D, Huete A, Hutley L, Lu X, Piao S, Zhang L, Zhang Y, Yu Q. 2017. Responses of LAI to rainfall explain contrasting sensitivities to carbon uptake between forest and non-forest ecosystems in Australia. Sci Rep 7:11720.PubMedPubMedCentralCrossRefGoogle Scholar
  34. Liu Y, Li Y, Li S, Motesharrei S. 2015. Spatial and temporal patterns of global NDVI trends: correlations with climate and human factors. Remote Sens 7:13233–50.CrossRefGoogle Scholar
  35. MacDonald D, Crabtree JR, Wiesinger G, Dax T, Stamou N, Fleury P, Gutierrez Lazpita J, Gibon A. 2000. Agricultural abandonment in mountain areas of Europe: environmental consequences and policy response. J Environ Manag 59:47–69.CrossRefGoogle Scholar
  36. Manier DJ, Thompson Hobbs N. 2006. Large herbivores influence the composition and diversity of shrub-steppe communities in the Rocky Mountains, USA. Oecologia 146:641–51.PubMedCrossRefPubMedCentralGoogle Scholar
  37. McNaughton SJ. 1985. Ecology of a grazing ecosystem: the Serengeti. Ecol Monogr 55:259–94.CrossRefGoogle Scholar
  38. Meserve PL, Kelt DA, Milstead WB, Gutierrez JR. 2003. Thirteen years of shifting top-down and bottom-up control. BioScience 53:633–46.CrossRefGoogle Scholar
  39. Milchunas DG, Lauenroth WK. 1993. Quantitative effects of grazing on vegetation and soils over a global range of environments: ecological archives M063-001. Ecol Monogr 63:327–66.CrossRefGoogle Scholar
  40. Milchunas DG, Lauenroth WK, Chapman PL, Kazempour MK. 1989. Effects of grazing, topography, and precipitation on the structure of a semiarid grassland. Vegetation 80:11–23.CrossRefGoogle Scholar
  41. Moyes K, Nussey DH, Clements MN, Guinness FE, Morris A, Morris S, Pemberton JM, Kruuk LEB, Clutton-Brock TH. 2011. Advancing breeding phenology in response to environmental change in a wild red deer population. Glob Change Biol 17:2455–69.CrossRefGoogle Scholar
  42. Murthy K, Bagchi S. 2018. Spatial patterns of long-term vegetation greening and browning are consistent across multiple scales: implications for monitoring land degradation. Land Degrad Dev 29:2485–95.CrossRefGoogle Scholar
  43. Navarro LM, Pereira HM. 2012. Rewilding abandoned landscapes in Europe. Ecosystems 15:900–12.CrossRefGoogle Scholar
  44. Nielsen A, Yoccoz NG, Steinheim G, Storvik GO, Rekdal Y, Angeloff M, Pettorelli N, Holand Ø, Mysterud A. 2012. Are responses of herbivores to environmental variability spatially consistent in alpine ecosystems? Glob Change Biol 18:3050–62.CrossRefGoogle Scholar
  45. O’brien RM. 2007. A caution regarding rules of thumb for variance inflation factors. Qual Quant 41:673–90.CrossRefGoogle Scholar
  46. Olofsson J, Post E. 2018. Effects of large herbivores on tundra vegetation in a changing climate, and implications for rewilding. Philos Trans R Soc B Biol Sci 373:20170437.CrossRefGoogle Scholar
  47. Pascual-Rico R, Morugán-Coronado A, Botella F, García-Orenes F, Sánchez-Zapata JA. 2018. Soil properties in relation to diversionary feeding stations for ungulates on a Mediterranean mountain. Appl Soil Ecol 127:136–43.CrossRefGoogle Scholar
  48. Pettorelli N, Pelletier F, von Hardenberg A, Festa-Bianchet M, Côté SD. 2007. Early onset of vegetation growth vs. rapid green-up: impacts on juvenile mountain ungulates. Ecology 88:381–90.PubMedCrossRefPubMedCentralGoogle Scholar
  49. Pettorelli N, Ryan S, Mueller T, Bunnefeld N, Jedrzejewska B, Lima M, Kausrud K. 2011. The Normalized Difference Vegetation Index (NDVI): unforeseen successes in animal ecology. Clim Res 46:15–27.CrossRefGoogle Scholar
  50. Plieninger T, Hui C, Gaertner M, Huntsinger L. 2014. The impact of land abandonment on species richness and abundance in the Mediterranean basin: a meta-analysis. PLoS ONE 9:e98355.PubMedPubMedCentralCrossRefGoogle Scholar
  51. Post E, Pedersen C. 2008. Opposing plant community responses to warming with and without herbivores. Proc Natl Acad Sci 105:12353–8.PubMedCrossRefGoogle Scholar
  52. Reichmann LG, Sala OE, Peters DPC. 2013. Precipitation legacies in desert grassland primary production occur through previous-year tiller density. Ecology 94:435–43.PubMedCrossRefGoogle Scholar
  53. Ricciardi A, Simberloff D. 2009. Assisted colonization is not a viable conservation strategy. Trends Ecol Evol 24:248–53.PubMedCrossRefGoogle Scholar
  54. Rivas-Martínez S. 1986. Mapas de las Series de Vegetación de España. Madrid: ICONA.Google Scholar
  55. Sala OE, Gherardi LA, Reichmann L, Jobbagy E, Peters D. 2012. Legacies of precipitation fluctuations on primary production: theory and data synthesis. Philos Trans R Soc B Biol Sci 367:3135–44.CrossRefGoogle Scholar
  56. Sankaran M, Augustine DJ, Ratnam J. 2013. Native ungulates of diverse body sizes collectively regulate long-term woody plant demography and structure of a semi-arid savanna. J Ecol 101:1389–99.CrossRefGoogle Scholar
  57. Schultz PA, Halpert MS. 1993. Global correlation of temperature, NDVI and precipitation. Adv Space Res 13:277–80.CrossRefGoogle Scholar
  58. Seddon PJ. 2010. From reintroduction to assisted colonization: moving along the conservation translocation spectrum. Restor Ecol 18:796–802.CrossRefGoogle Scholar
  59. Stoffer DS, Wall KD. 1991. Bootstrapping state-space models: Gaussian maximum likelihood estimation and the Kalman filter. J Am Stat Assoc 86:1024–33.CrossRefGoogle Scholar
  60. Sullivan S, Rohde R. 2002. On non-equilibrium in arid and semi-arid grazing systems. J Biogeogr 29:1595–618.CrossRefGoogle Scholar
  61. Svenning J-C, Pedersen PBM, Donlan CJ, Ejrnæs R, Faurby S, Galetti M, Hansen DM, Sandel B, Sandom CJ, Terborgh JW, Vera FWM. 2016. Science for a wilder Anthropocene: synthesis and future directions for trophic rewilding research. Proc Natl Acad Sci 113:898–906.PubMedCrossRefPubMedCentralGoogle Scholar
  62. Teillet PM, Barker JL, Markham BL, Irish RR, Fedosejevs G, Storey JC. 2001. Radiometric cross-calibration of the Landsat-7 ETM+ and Landsat-5 TM sensors based on tandem data sets. Remote Sens Environ 78:39–54.CrossRefGoogle Scholar
  63. Tilman D, Downing JA. 1994. Biodiversity and stability in grasslands. Nature 367:363.CrossRefGoogle Scholar
  64. Tilman D, Isbell F, Cowles JM. 2014. Biodiversity and ecosystem functioning. Annu Rev Ecol Evol Syst 45:471–93.CrossRefGoogle Scholar
  65. Veblen KE, Porensky LM, Riginos C, Young TP. 2016. Are cattle surrogate wildlife? Savanna plant community composition explained by total herbivory more than herbivore type. Ecol Appl 26:1610–23.PubMedCrossRefPubMedCentralGoogle Scholar
  66. Vetter S. 2005. Rangelands at equilibrium and non-equilibrium: recent developments in the debate. J Arid Environ 62:321–41.CrossRefGoogle Scholar
  67. Wittemyer G, Barner Rasmussen H, Douglas-Hamilton I. 2007. Breeding phenology in relation to NDVI variability in free-ranging African elephant. Ecography 30:42–50.CrossRefGoogle Scholar
  68. Yi C, Ricciuto D, Li R, Wolbeck J, Xu X, Nilsson M, Aires L, Albertson JD, Ammann C, Arain MA, de Araujo AC, Aubinet M, Aurela M, Barcza Z, Barr A, Berbigier P, Beringer J, Bernhofer C, Black AT, Bolstad PV, Bosveld FC, Broadmeadow MSJ, Buchmann N, Burns SP, Cellier P, Chen J, Chen J, Ciais P, Clement R, Cook BD, Curtis PS, Dail DB, Dellwik E, Delpierre N, Desai AR, Dore S, Dragoni D, Drake BG, Dufrêne E, Dunn A, Elbers J, Eugster W, Falk M, Feigenwinter C, Flanagan LB, Foken T, Frank J, Fuhrer J, Gianelle D, Goldstein A, Goulden M, Granier A, Grünwald T, Gu L, Guo H, Hammerle A, Han S, Hanan NP, Haszpra L, Heinesch B, Helfter C, Hendriks D, Hutley LB, Ibrom A, Jacobs C, Johansson T, Jongen M, Katul G, Kiely G, Klumpp K, Knohl A, Kolb T, Kutsch WL, Lafleur P, Laurila T, Leuning R, Lindroth A, Liu H, Loubet B, Manca G, Marek M, Margolis HA, Martin TA, Massman WJ, Matamala R, Matteucci G, McCaughey H, Merbold L, Meyers T, Migliavacca M, Miglietta F, Misson L, Mölder M, Moncrieff J, Monson RK, Montagnani L, Montes-Helu M, Moors E et al. 2010. Climate control of terrestrial carbon exchange across biomes and continents. Environ Res Lett 5:034007.CrossRefGoogle Scholar
  69. Zhang L, Fu D, Sun X, Chen H, She X. 2016. A spatial-temporal-spectral blending model using satellite images. IOP Conf Ser Earth Environ Sci 34:012042.CrossRefGoogle Scholar
  70. Zhao M, Running SW. 2010. Drought-induced reduction in global terrestrial net primary production from 2000 through 2009. Science 329:940–3.PubMedCrossRefPubMedCentralGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Conservation BiologyEstación Biológica de Doñana (CSIC)SevilleSpain
  2. 2.Department of Applied BiologyMiguel Hernández University, ElcheAlicanteSpain
  3. 3.Mendijob S.L.MurciaSpain

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