Landscape Ecology

, Volume 33, Issue 3, pp 341–352 | Cite as

How does habitat fragmentation affect the biodiversity and ecosystem functioning relationship?

  • Jiajia Liu
  • Maxwell Wilson
  • Guang Hu
  • Jinliang Liu
  • Jianguo Wu
  • Mingjian Yu
Perspective

Abstract

Context

The relationship between biodiversity and ecosystem functioning (BEF) has been a central topic in ecology for more than 20 years. While experimental and theoretical studies have produced much knowledge of how biodiversity affects ecosystem functioning, it remains poorly understood how habitat fragmentation affects the BEF relationship.

Objectives

To develop a framework that connects habitat fragmentation to the BEF relationship from a landscape perspective.

Methods

We reviewed the literature on habitat fragmentation, BEF, and related fields, and developed a framework to analyze how habitat fragmentation affects the BEF relationship through altering biodiversity, environmental conditions, and both, based on the pattern-process-scale perspective in landscape ecology.

Results

Our synthesis of the literature suggests that habitat fragmentation can alter BEF relationship through several processes. First, habitat fragmentation causes the non-random loss of species that make major contributions to ecosystem functioning (decreasing sampling effect), and reduces mutualistic interactions (decreasing complementarity effects) regardless of the changes in species richness. Second, environmental conditions within patches and ecological flows among patches vary significantly with the degree of fragmentation, which potentially contributes to and modulates the BEF relationship.

Conclusions

Habitat fragmentation can affect the BEF relationship directly by altering community composition, as well as indirectly by changing environmental conditions within and among habitat patches on both local and landscape levels. The BEF relationship obtained from small plots and over short time periods may not fully represent that in real landscapes that are fragmented, dynamic, and continuously influenced by myriad human activities on different scales in time and space.

Keywords

Complementarity effect Ecosystem properties Environment conditions Functional traits Habitat fragmentation Non-random loss 

Notes

Acknowledgements

This paper was supported by National Natural Science Foundation of China (31361123001, 31500382, 31210103908), the US National Science Foundation (DEB-1342754 and DEB-1342757) and the 521 Talent Project of Zhejiang Sci-Tech University. We thank Tommaso Jucker, Raphael Didham, Matthew Mitchell, Ping Ding, Yanping Wang and two anonymous reviewers for their helpful comments on an earlier version of this paper.

References

  1. Bai Y, Han X, Wu J, Chen Z, Li L (2004) Ecosystem stability and compensatory effects in the Inner Mongolia grassland. Nature 431:181–184PubMedCrossRefGoogle Scholar
  2. Bogoni JA, Graipel ME, Oliveira-Santos LGR, Cherem JJ, Giehl ELH, Peroni N (2017) What would be the diversity patterns of medium- to large-bodied mammals if the fragmented Atlantic Forest was a large metacommunity? Biol Conserv 211:85–94CrossRefGoogle Scholar
  3. Bregman TP, Lees AC, Seddon N, MacGregor HE, Darski B, Aleixo A, Bonsall MB, Tobias JA (2015) Species interactions regulate the collapse of biodiversity and ecosystem function in tropical forest fragments. Ecology 96:2692–2704PubMedCrossRefGoogle Scholar
  4. Brinck K, Fischer R, Groeneveld J, Lehmann S, De Paula MD, Putz S, Sexton JO, Song D, Huth A (2017) High resolution analysis of tropical forest fragmentation and its impact on the global carbon cycle. Nat Commun 8:14855PubMedPubMedCentralCrossRefGoogle Scholar
  5. Brose U, Hillebrand H (2016) Biodiversity and ecosystem functioning in dynamic landscapes. Philos Trans R Soc B Biol Sci 371:20150267CrossRefGoogle Scholar
  6. Burley HM, Mokany K, Ferrier S, Laffan SW, Williams KJ, Hardwood TD (2016) Macroecological scale effects of biodiversity on ecosystem functions under environmental change. Ecol Evol 6:2579–2593PubMedPubMedCentralCrossRefGoogle Scholar
  7. Caliman A, Carneiro LS, Leal JJ, Farjalla VF, Bozelli RL, Esteves FA (2013) Biodiversity effects of ecosystem engineers are stronger on more complex ecosystem processes. Ecology 94:1977–1985PubMedCrossRefGoogle Scholar
  8. Cardinale BJ, Ives AR, Inchausti P (2004) Effects of species richness on the primary productivity of ecosystems: extending our spatial and temporal scales of inference. Oikos 104:437–450CrossRefGoogle Scholar
  9. Cardinale BJ, Palmer MA, Collins SL (2002) Species diversity enhances ecosystem functioning through interspecific facilitation. Nature 415:426–429PubMedCrossRefGoogle Scholar
  10. Cardinale BJ, Wright JP, Cadotte MW, Carroll IT, Hector A, Srivastava DS, Loreau M, Weiss JJ (2007) Impacts of plant diversity on biomass production increase through time because of species complementarity. Proc Natl Acad Sci U S A 104:18123–18128PubMedPubMedCentralCrossRefGoogle Scholar
  11. Chaplin-Kramer R, Ramler I, Sharp R, Haddad NM, Gerber JS, West PC, Mandle L, Engstrom P, Baccini A, Sim S, Mueller C (2015) Degradation in carbon stocks near tropical forest edges. Nat Commun 6:10158PubMedPubMedCentralCrossRefGoogle Scholar
  12. Chase JM, Ryberg WA (2004) Connectivity, scale-dependence, and the productivity-diversity relationship. Ecol Lett 7:676–683CrossRefGoogle Scholar
  13. Chisholm RA, Muller-Landau HC, Abdul Rahman K, Bebber DP, Bin Y, Bohlaman SA, Bourg NA, Brinks J, Bunyavejchewin S, Butt N, Cao H (2013) Scale-dependent relationships between tree species richness and ecosystem function in forests. J Ecol 101:1214–1224CrossRefGoogle Scholar
  14. Clarke DA, York PH, Rasheed MA, Northfield TD (2017) Does biodiversity–ecosystem function literature neglect tropical ecosystems? Trends Ecol Evol 32:320–323PubMedCrossRefGoogle Scholar
  15. Cook WM, Yao J, Foster BL, Holt RD, Patrick LB (2005) Secondary succession in an experimentally fragmented landscape: community patterns across space and time. Ecology 86:1267–1279CrossRefGoogle Scholar
  16. Cordeiro NJ, Ndangalasi HJ, McEntee JP, Howe HF (2009) Disperser limitation and recruitment of an endemic African tree in a fragmented landscape. Ecology 90:1030–1041PubMedCrossRefGoogle Scholar
  17. Crockatt ME, Bebber DP (2014) Edge effects on moisture reduce wood decomposition rate in a temperate forest. Glob Chang Biol 21:698–707PubMedCrossRefGoogle Scholar
  18. De Laender F, Rohr JR, Ashauer R, Baird DJ, Berger U, Eisenhauer N, Grimm V, Hommen U, Maltby L, Melian CJ, Pomati F (2016) Reintroducing environmental change drivers in biodiversity-ecosystem functioning research. Trends Ecol Evol 31:905–915PubMedPubMedCentralCrossRefGoogle Scholar
  19. Duffy JE, Godwin CM, Cardinale BJ (2017) Biodiversity effects in the wild are common and as strong as key drivers of productivity. Nature 549:261–264PubMedCrossRefGoogle Scholar
  20. Ewers RM, Didham RK, Fahrig L, Ferraz G, Hector A, Holt RD, Kapos V, Reynolds G, Sinun W, Snaddon JL, Turner EC (2011) A large-scale forest fragmentation experiment: the Stability of altered forest ecosystems project. Philos Trans R Soc Lond B Biol Sci 366:3292–3302PubMedPubMedCentralCrossRefGoogle Scholar
  21. Fahrig L (2017) Ecological responses to habitat fragmentation per se. Annu Rev Ecol Evol Syst.  https://doi.org/10.1146/annurev-ecolsys-110316-022612 Google Scholar
  22. Ferraz G, Nichols JD, Hines JE, Stouffer PC, Bierregaard RO, Lovejoy TE (2007) A large-scale deforestation experiment: effects of patch area and isolation on Amazon birds. Science 315:238–241PubMedCrossRefGoogle Scholar
  23. Fischer M, Bossdorf O, Gockel S, Hänsel F, Hemp A, Hessenmöller D, Korte G, Nieschulze J, Pfeiffer S, Prati D, Renner S (2010) Implementing large-scale and long-term functional biodiversity research: the biodiversity exploratories. Basic Appl Ecol 11:473–485CrossRefGoogle Scholar
  24. Flynn DF, Mirotchnick N, Jain M, Palmer MI, Naeem S (2011) Functional and phylogenetic diversity as predictors of biodiversity- ecosystem-function relationships. Ecology 92:1573–1581PubMedCrossRefGoogle Scholar
  25. France KE, Duffy JE (2006) Diversity and dispersal interactively affect predictability of ecosystem function. Nature 441:1139–1143PubMedCrossRefGoogle Scholar
  26. Germain RM, Strauss SY, Gilbert B (2017) Experimental dispersal reveals characteristic scales of biodiversity in a natural landscape. Proc Natl Acad Sci 114:4447–4452PubMedPubMedCentralCrossRefGoogle Scholar
  27. Gibson L, Lynam AJ, Bradshaw CJ, He F, Bickford DP, Woodruff DS, Bumrungsri S, Laurance WF (2013) Near-complete extinction of native small mammal fauna 25 years after forest fragmentation. Science 341:1508–1510PubMedCrossRefGoogle Scholar
  28. Godbold JA, Bulling MT, Solan M (2011) Habitat structure mediates biodiversity effects on ecosystem properties. Proc Biol Sci 278:2510–2518PubMedPubMedCentralCrossRefGoogle Scholar
  29. Gonzalez A, Chaneton EJ (2002) Heterotroph species extinction, abundance in an experimentally biomass dynamics fragmented microecosystem. J Anim Ecol 71:594–602CrossRefGoogle Scholar
  30. Gonzalez A, Mouquet N, Loreau M (2009) Biodiversity as spatial insurance: the effects of habitat fragmentation and dispersal on ecosystem functioning. Biodivers Ecosyst Funct Ecosyst Serv 134–146Google Scholar
  31. Goosem M, Paz C, Fensham R, Preece N, Goosem S, Laurance SG (2016) Forest age and isolation affect the rate of recovery of plant species diversity and community composition in secondary rain forests in tropical Australia. J Veg Sci 27:504–514CrossRefGoogle Scholar
  32. Grossiord C, Granier A, Ratcliffe S, Bouriaud O, Bruelheide H, Chećko E, Forrester DI, Dawud SM, Finér L, Pollastrini M, Scherer-Lorenzen M (2014) Tree diversity does not always improve resistance of forest ecosystems to drought. Proc Natl Acad Sci USA 111:14812–14815PubMedPubMedCentralCrossRefGoogle Scholar
  33. Haddad NM, Brudvig LA, Clobert J, Davies KF, Gonzalez A, Holt RD, Lovejoy TE, Sexton JO, Austin MP, Collins CD, Cook WM (2015) Habitat fragmentation and its lasting impact on earth ecosystems. Sci Adv.  https://doi.org/10.1126/sciadv.1500052 PubMedPubMedCentralGoogle Scholar
  34. Hagen M, Kissling WD, Rasmussen C, De Aguiar MA, Brown LE, Carstensen DW, Alves-Dos-Santos I, Dupont YL, Edwards FK, Genini J, Guimaraes PR Jr (2012) Biodiversity, species interactions and ecological networks in a fragmented world. Adv Ecol Res 46:89–120CrossRefGoogle Scholar
  35. Hanski I (2015) Habitat fragmentation and species richness. J Biogeogr 42:989–994CrossRefGoogle Scholar
  36. Hautier Y, Tilman D, Isbell F, Seabloom EW, Borer ET, Reich PB (2015) Anthropogenic environmental changes affect ecosystem stability via biodiversity. Science 348:336–340PubMedCrossRefGoogle Scholar
  37. Healy C, Gotelli NJ, Potvin C (2008) Partitioning the effects of biodiversity and environmental heterogeneity for productivity and mortality in a tropical tree plantation. J Ecol 96:903–913CrossRefGoogle Scholar
  38. Hector A, Bagchi R (2007) Biodiversity and ecosystem multifunctionality. Nature 448:188–190PubMedCrossRefGoogle Scholar
  39. Helm A, Hanski I, Pärtel M (2006) Slow response of plant species richness to habitat loss and fragmentation. Ecol Lett 9:72–77PubMedGoogle Scholar
  40. Helsen K, Hermy M, Honnay O (2013) Spatial isolation slows down directional plant functional group assembly in restored semi-natural grasslands. J Appl Ecol 50:404–413CrossRefGoogle Scholar
  41. Hooper DU, Adair EC, Cardinale BJ, Byrnes JE, Hungate BA, Matulich KL, Gonzalez A, Duffy JE, Gamfeldt L, O’Connor MI (2012) A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486:105–108PubMedCrossRefGoogle Scholar
  42. Hu G, Feeley KJ, Wu J, Xu G, Yu M (2011) Determinants of plant species richness and patterns of nestedness in fragmented landscapes: evidence from land-bridge islands. Landscape Ecol 26:1405–1417CrossRefGoogle Scholar
  43. Huston MA (1997) Hidden treatments in ecological experiments: re-evalutating the ecosystem function of biodiverstiy. Oecologia 110:449–460PubMedCrossRefGoogle Scholar
  44. Isbell F, Gonzalez A, Loreau M, Cowles J, Díaz S, Hector A, Mace GM, Wardle DA, O’Connor MI, Duffy JE, Turnbull LA (2017) Linking the influence and dependence of people on biodiversity across scales. Nature 546:65–72PubMedPubMedCentralCrossRefGoogle Scholar
  45. Isbell F, Tilman D, Polasky S, Loreau M (2015) The biodiversity-dependent ecosystem service debt. Ecol Lett 18:119–134PubMedCrossRefGoogle Scholar
  46. Jansen PA, Hirsch BT, Emsens WJ, Zamora-Gutierrez V, Wikelski M, Kays R (2012) Thieving rodents as substitute dispersers of megafaunal seeds. Proc Natl Acad Sci 109:12610–12615PubMedPubMedCentralCrossRefGoogle Scholar
  47. Jucker T, Avăcăriţei D, Bărnoaiea I, Duduman G, Bouriaud O, Coomes DA (2016) Climate modulates the effects of tree diversity on forest productivity. J Ecol 104:388–398CrossRefGoogle Scholar
  48. Kahmen A, Renker C, Unsicker SB, Buchmann N (2006) Niche complementarity for nitrogen: an explanation for the biodiversity and ecosystem functioning relationship? Ecology 87:1244–1255PubMedCrossRefGoogle Scholar
  49. Kaiser-Bunbury C, Mougal J, Whittington A (2017) Ecosystem restoration strengthens pollination network resilience and function. Nature 542:223–227PubMedCrossRefGoogle Scholar
  50. Knorr UC, Gottsberger G (2012) Differences in seed rain composition in small and large fragments in the northeast Brazilian Atlantic Forest. Plant Biol 14:811–819PubMedCrossRefGoogle Scholar
  51. Laforest-Lapointe I, Paquette A, Messier C, Kembel S (2017) Leaf bacterial diversity mediates plant diversity and ecosystem function relationships. Nature 546:145–147PubMedCrossRefGoogle Scholar
  52. Lasky JR, Uriarte M, Boukili VK, Erickson DL, John Kress W, Chazdon RL (2014) The relationship between tree biodiversity and biomass dynamics changes with tropical forest succession. Ecol Lett 17:1158–1167PubMedCrossRefGoogle Scholar
  53. Latimer C, Zuckerberg B (2017) Forest fragmentation alters winter microclimates and microrefugia in human-modified landscapes. Ecography 40:158–170CrossRefGoogle Scholar
  54. Laurance WF (2000) Do edge effects occur over large spatial scales? Trends Ecol Evol 15:134–144PubMedCrossRefGoogle Scholar
  55. Laurance WF, Camargo JL, Luizão RC, Laurance SG, Pimm SL, Bruna EM (2011) The fate of Amazonian forest fragments: a 32-year investigation. Biol Conserv 144:56–67CrossRefGoogle Scholar
  56. Laurance WF, Delamônica P, Laurance SG, Vasconcelos HL, Lovejoy TE (2000) Rainforest fragmentation kills big trees. Nature 404:836PubMedCrossRefGoogle Scholar
  57. Laurance WF, Lovejoy TE, Vasconcelos HL, Bruna EM, Didham RK, Stouffer PC, Gascon C, Bierregaard RO, Laurance SG, Sampaio E (2002) Ecosystem decay of Amazonian forest fragments: a 22-year investigation. Conserv Biol 16:605–618CrossRefGoogle Scholar
  58. Laurance WF, Nascimento HE, Laurance SG, Andrade A, Ribeiro JE, Giraldo JP, Lovejoy TE, Condit R, Chave J, Harms KE, D’Angelo S (2006a) Rapid decay of tree-community composition in Amazonian forest fragments. Proc Natl Acad Sci U S A 103:19010–19014PubMedPubMedCentralCrossRefGoogle Scholar
  59. Laurance WF, Nascimento HE, Laurance SG, Andrade AC, Fearnside PM, Ribeiro JE, Capretz RL (2006b) Rain forest fragmentation and the proliferation of successional trees. Ecology 87:469–482PubMedCrossRefGoogle Scholar
  60. Liang J, Crowther TW, Picard N, Wiser S, Zhou M, Alberti G, Schulze E-D, McGuire AD, Bozzato F, Pretzsch H, de-Miguel S, Paquette A, Herault B, Scherer-Lorenzen M, Barrett CB, Glick HB, Hengeveld GM, Nabuurs GJ, Pfautsch S, Viana H, Vibrans AC, Ammer C, Schall P, Verbyla D, Tchebakova N, Fischer M, Watson JV, Chen HYH, Lei X, Schelhaas M-J, Lu H, Gianelle D, Parfenova EI, Salas C, Lee E, Lee B, Kim HS, Bruelheide H, Coomes DA, Piotto D, Sunderland T, Schmid B, Gourlet-Fleury S, Sonke B, Tavani R, Zhu J, Brandl S, Vayreda J, Kitahara F, Searle EB, Neldner VJ, Ngugi MR, Baraloto C, Frizzera L, Balazy R, Oleksyn J, Zawila-Nied wiecki T, Bouriaud O, Bussotti F, Finer L, Jaroszewicz B, Jucker T, Valladares F, Jagodzinski AM, Peri PL, Gonmadje C, Marthy W, OBrien T, Martin EH, Marshall AR, Rovero F, Bitariho R, Niklaus PA, Alvarez-Loayza P, Chamuya N, Valencia R, Mortier F, Wortel V, Engone-Obiang NL, Ferreira LV, Odeke DE, Vasquez RM, Lewis SL, Reich PB (2016) Positive biodiversity-productivity relationship predominant in global forests. Science 354(6309):aaf8957PubMedCrossRefGoogle Scholar
  61. Lôbo D, Leão T, Melo FP, Santos AM, Tabarelli M (2011) Forest fragmentation drives Atlantic forest of northeastern Brazil to biotic homogenization. Divers Distrib 17:287–296CrossRefGoogle Scholar
  62. Loreau M (2010) Linking biodiversity and ecosystems: towards a unifying ecological theory. Philos Trans R Soc Lond B Biol Sci 365:49–60PubMedPubMedCentralCrossRefGoogle Scholar
  63. Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76PubMedCrossRefGoogle Scholar
  64. Loreau M, Mouquet N, Gonzalez A (2003) Biodiversity as spatial insurance in heterogeneous landscapes. Proc Natl Acad Sci U S A 100:12765–12770PubMedPubMedCentralCrossRefGoogle Scholar
  65. Magrach A, Laurance WF, Larrinaga AR, Santamaria L (2014) Meta-analysis of the effects of forest fragmentation on interspecific interactions. Conserv Biol 28:1342–1348PubMedCrossRefGoogle Scholar
  66. Martin P, Bullock J, Newton A (2013) Carbon pools recover more rapidly than plant biodiversity in secondary tropical forests. Proc R Soc B 280:20132236PubMedPubMedCentralCrossRefGoogle Scholar
  67. Mitchell MGE, Bennett EM, Gonzalez A (2013) Linking landscape connectivity and ecosystem service provision: current knowledge and research gaps. Ecosystems 16:894–908CrossRefGoogle Scholar
  68. Mitchell MGE, Bennett EM, Gonzalez A (2015) Strong and nonlinear effects of fragmentation on ecosystem service provision at multiple scales. Environ Res Lett 10:094014CrossRefGoogle Scholar
  69. Peh KS, Lin Y, Luke SH (2014) Forest fragmentation and ecosystem function. In: Kettle CJ, Koh LP (eds) Global forest fragmentation. CABI, Wallingford, pp 96–114Google Scholar
  70. Poisot T, Mouquet N, Gravel D (2013) Trophic complementarity drives the biodiversity-ecosystem functioning relationship in food webs. Ecol Lett 16:853–861PubMedCrossRefGoogle Scholar
  71. Potapov P, Yaroshenko A, Turubanova S, Dubinin M, Laestadius L, Thies C, Aksenov D, Egorov A, Yesipova Y, Glushkov I, Karpachevskiy M (2008) Mapping the world’s intact forest landscapes by remote sensing. Ecol Soc 13:51CrossRefGoogle Scholar
  72. Pütz S, Groeneveld J, Henle K, Knogge C, Martensen AC, Metz M, Metzger JP, Ribeiro MC, De Paula MD, Huth A (2014) Long-term carbon loss in fragmented Neotropical forests. Nat Commun 5:5037PubMedCrossRefGoogle Scholar
  73. Ratcliffe S, Holzwarth F, Nadrowski K, Levick S, Wirth C (2015) Tree neighbourhood matters—tree species composition drives diversity-productivity patterns in a near-natural beech forest. For Ecol Manage 335:225–234CrossRefGoogle Scholar
  74. Reich PB, Tilman D, Isbell F, Mueller K, Hobbie SE, Flynn DF, Eisenhauer N (2012) Impacts of biodiversity loss escalate through time as redundancy fades. Science 336:589–592PubMedCrossRefGoogle Scholar
  75. Resasco J, Bruna E, Haddad N, Banks-Leite C (2016) The contribution of theory and experiments to conservation in fragmented landscapes. Ecography 40:109–118CrossRefGoogle Scholar
  76. Riitters K, Wickham J, Costanza JK, Vogt P (2016) A global evaluation of forest interior area dynamics using tree cover data from 2000 to 2012. Landscape Ecol 31:137–148CrossRefGoogle Scholar
  77. Ruiz-Guerra B, Guevara R, Mariano NA, Dirzo R (2010) Insect herbivory declines with forest fragmentation and covaries with plant regeneration mode: evidence from a Mexican tropical rain forest. Oikos 119:317–325CrossRefGoogle Scholar
  78. Schleuning M, Farwig N, Peters MK, Bergsdorf T, Bleher B, Brandl R, Dalitz H, Fischer G, Freund W, Gikungu MW, Hagen M (2011) Forest fragmentation and selective logging have inconsistent effects on multiple animal-mediated ecosystem processes in a tropical forest. PLoS ONE.  https://doi.org/10.1371/journal.pone.0027785 PubMedPubMedCentralGoogle Scholar
  79. Slik JWF, Paoli G, Mcguire K, Amaral I, Barroso J, Bastian M, Blanc L, Bongers F, Boundja P, Clark C, Collins M, Dauby G, Ding Y, Doucet JL, Eler E, Ferreira L, Forshed O, Fredriksson G, Gillet JF, Harris D, Leal M, Laumonier Y, Malhi Y, Mansor A, Martin E, Miyamoto K, Araujo-Murakami A, Nagamasu H, Nilus R, Nurtjahya E, Oliveira Á, Onrizal O, Parada-Gutierrez A, Permana A, Poorter L, Poulsen J, Ramirez-Angulo H, Reitsma J, Rovero F, Rozak A, Sheil D, Silva-Espejo J, Silveira M, Spironelo W, ter Steege H, Stevart T, Navarro-Aguilar GE, Sunderland T, Suzuki E, Tang J, Theilade I, van der Heijden G, van Valkenburg J, Van Do T, Vilanova E, Vos V, Wich S, Wöll H, Yoneda T, Zang R, Zhang MG, Zweifel N (2013) Large trees drive forest aboveground biomass variation in moist lowland forests across the tropics. Glob Ecol Biogeogr 22:1261–1271CrossRefGoogle Scholar
  80. Smith MD, Knapp AK (2003) Dominant species maintain ecosystem function with non-random species loss. Ecol Lett 6:509–517CrossRefGoogle Scholar
  81. Staddon P, Lindo Z, Crittenden PD, Gilbert F, Gonzalez A (2010) Connectivity, non-random extinction and ecosystem function in experimental metacommunities. Ecol Lett 13:543–552PubMedCrossRefGoogle Scholar
  82. Steudel B, Hector A, Friedl T, Löfke C, Lorenz M, Wesche M, Kessler M (2012) Biodiversity effects on ecosystem functioning change along environmental stress gradients. Ecol Lett 15:1397–1405PubMedCrossRefGoogle Scholar
  83. Sullivan MJP, Talbot J, Lewis SL, Phillips OL, Qie L, Begne SK, Chave J, Cuni-Sanchez A, Hubau W, Lopez-Gonzalez G, Miles L, Monteagudo-Mendoza A, Sonké B, Sunderland T, ter Steege H, White LJT, Affum-Baffoe K, Aiba S, de Almeida EC, de Oliveira EA, Alvarez-Loayza P, Dávila EÁ, Andrade A, Aragão LEOC, Ashton P, Aymard CGA, Baker TR, Balinga M, Banin LF, Baraloto C, Bastin J-F, Berry N, Bogaert J, Bonal D, Bongers F, Brienen R, Camargo JLC, Cerón C, Moscoso VC, Chezeaux E, Clark CJ, Pacheco ÁC, Comiskey JA, Valverde FC, Coronado ENH, Dargie G, Davies SJ, De Canniere C, Djuikouo KMN, Doucet J-L, Erwin TL, Espejo JS, Ewango CEN, Fauset S, Feldpausch TR, Herrera R, Gilpin M, Gloor E, Hall JS, Harris DJ, Hart TB, Kartawinata K, Kho LK, Kitayama K, Laurance SGW, Laurance WF, Leal ME, Lovejoy T, Lovett JC, Lukasu FM, Makana J-R, Malhi Y, Maracahipes L, Marimon BS, Junior BHM, Marshall AR, Morandi PS, Mukendi JT, Mukinzi J, Nilus R, Vargas PN, Camacho NCP, Pardo G, Peña-Claros M, Pétronelli P, Pickavance GC, Poulsen AD, Poulsen JR, Primack RB, Priyadi H, Quesada CA, Reitsma J, Réjou-Méchain M, Restrepo Z, Rutishauser E, Salim KA, Salomão RP, Samsoedin I, Sheil D, Sierra R, Silveira M, Slik JWF, Steel L, Taedoumg H, Tan S, Terborgh JW, Thomas SC, Toledo M, Umunay PM, Gamarra LV, Vieira ICG, Vos VA, Wang O, Willcock S, Zemagho L (2017) Diversity and carbon storage across the tropical forest biome. Sci Rep 7:39102PubMedPubMedCentralCrossRefGoogle Scholar
  84. Symstad AJ, Chapin FS, Wall DH, Gross KL, Huenneke LF, Mittelbach GG, Peters DP, Tilman D (2003) Long-term and large-scale perspectives on the relationship between biodiversity and ecosystem functioning. Bioscience 53:89–98CrossRefGoogle Scholar
  85. Tabarelli M, Aguiar AV, Girao LC, Peres CA, Lopes AV (2010) Effects of pioneer tree species hyperabundance on forest fragments in Northeastern Brazil. Conserv Biol 24:1654–1663PubMedCrossRefGoogle Scholar
  86. Terborgh J, Lopez L, Nuñez P, Rao M, Shahabuddin G, Orihuela G, Riveros M, Ascanio R, Adler GH, Lambert TD, Balbas L (2001) Ecological meltdown in predator-free forest fragments. Science 294:1923–1926PubMedCrossRefGoogle Scholar
  87. Thompson PL, Rayfield B, Gonzalez A (2017) Loss of habitat and connectivity erodes species diversity, ecosystem functioning, and stability in metacommunity networks. Ecography 40:98–108CrossRefGoogle Scholar
  88. Tilman D, Reich PB, Isbell F (2012) Biodiversity impacts ecosystem productivity as much as resources, disturbance, or herbivory. Proc Natl Acad Sci 109:10394–10397PubMedPubMedCentralCrossRefGoogle Scholar
  89. Tylianakis JM, Rand TA, Kahmen A, Klein AM, Buchmann N, Perner J, Tscharntke T (2008) Resource heterogeneity moderates the biodiversity-function relationship in real world ecosystems. PLoS Biol 6:0947–0956Google Scholar
  90. Van Der Plas F, Manning P, Soliveres S, Allan E, Scherer-Lorenzen M, Verheyen K, Wirth C, Zavala MA, Ampoorter E, Baeten L, Barbaro L, Bauhus J, Benavides R, Benneter A, Bonal D, Bouriaud O, Bruelheide H, Bussotti F, Carnol M, Castagneyrol B, Charbonnier Y, Coomes DA, Coppi A, Bestias CC, Dawud SM, De Wandeler H, Domisch T, Finér L, Gessler A, Granier A, Grossiord C, Guyot V, Hättenschwiler S, Jactel H, Jaroszewicz B, Joly F, Jucker T, Koricheva J, Milligan H, Mueller S, Muys B, Nguyen D, Pollastrini M, Ratcliffe S, Raulund-Rasmussen K, Selvi F, Stenlid J, Valladares F, Vesterdal L, Zielínski D, Fischer M (2016) Biotic homogenization can decrease landscape-scale forest multifunctionality. Proc Natl Acad Sci 113:3557–3562PubMedPubMedCentralCrossRefGoogle Scholar
  91. Vellend M, Verheyen K, Jacquemyn H, Kolb A, Van Calster H, Peterken G, Hermy M (2006) Extinction debt of forest plants persists for more than a century following habitat fragmentation. Ecology 87:542–548PubMedCrossRefGoogle Scholar
  92. Wardle DA (1997) The influence of island area on ecosystem properties. Science 277:1296–1299CrossRefGoogle Scholar
  93. Wardle DA (2016) Do experiments exploring plant diversity-ecosystem functioning relationships inform how biodiversity loss impacts natural ecosystems? J Veg Sci 27:646–653CrossRefGoogle Scholar
  94. Wardle DA, Bardgett RD, Callaway RM, Van der Putten WH (2011) Terrestrial ecosystem responses to species gains and losses. Science 332:1273–1277PubMedCrossRefGoogle Scholar
  95. Wardle D, Jonsson M (2010) Biodiversity effects in real ecosystems–a response to Duffy. Front Ecol Environ 8:10–11CrossRefGoogle Scholar
  96. Wardle DA, Zackrisson O (2005) Effects of species and functional group loss on island ecosystem properties. Nature 435:806–810PubMedCrossRefGoogle Scholar
  97. Watling JI, Nowakowski AJ, Donnelly MA, Orrock JL (2011) Meta-analysis reveals the importance of matrix composition for animals in fragmented habitat. Glob Ecol Biogeogr 20:209–217CrossRefGoogle Scholar
  98. Weigelt A, Schumacher J, Roscher C, Schmid B (2008) Does biodiversity increase spatial stability in plant community biomass? Ecol Lett 11:338–347PubMedCrossRefGoogle Scholar
  99. Wilson MC, Chen XY, Corlett RT, Didham RK, Ding P, Holt RD, Holyoak M, Hu G, Hughes AC, Jiang L, Laurance WF, Liu J, Pimm SL, Robinson SK, Russo SE, Si X, Wilcove DS, Wu J, Yu M (2016) Habitat fragmentation and biodiversity conservation: key findings and future challenges. Landscape Ecol 31:219–227CrossRefGoogle Scholar
  100. Wright AJ, Wardle DA, Callaway R, Gaxiola A (2017) The overlooked role of facilitation in biodiversity experiments. Trends Ecol Evol 32:383–390PubMedCrossRefGoogle Scholar
  101. Wu JG (2009) Ecological dynamics in fragmented landscapes. In: Levin SA (ed) The Princeton guide to ecology. Princeton University Press, Princeton, New Jersey, pp 438–444Google Scholar
  102. Wu J (2013a) Landscape sustainability science: ecosystem services and human well-being in changing landscapes. Landscape Ecol 28:999–1023CrossRefGoogle Scholar
  103. Wu J (2013b) Key concepts and research topics in landscape ecology revisited: 30 years after the Allerton Park workshop. Landscape Ecol 28:1–11CrossRefGoogle Scholar
  104. Wu J, Huang J, Han X, Xie Z, Gao X (2003) Ecology: Three-Gorges Dam–experiment in habitat fragmentation? Science 300:1239–1240PubMedCrossRefGoogle Scholar
  105. Wu J, Loucks OL (1995) From balance of nature to hierarchical patch dynamics: a paradigm shift in ecology. Q Rev Biol 70:439–466CrossRefGoogle Scholar
  106. Wu J, Naeem S, Elser J, Bai Y, Huang J, Kang L, Pan Q, Wang Q, Hao S, Han X (2015) Testing biodiversity-ecosystem functioning relationship in the world’s largest grassland: overview of the IMGRE project. Landscape Ecol 30:1723–1736CrossRefGoogle Scholar
  107. Yuan F, Wu J, Li A, Rowe H, Bai Y, Huang J, Han X (2015) Spatial patterns of soil nutrients, plant diversity, and aboveground biomass in the Inner Mongolia grassland: before and after a biodiversity removal experiment. Landscape Ecol 30:1737–1750CrossRefGoogle Scholar
  108. Zuppinger-Dingley D, Schmid B, Petermann JS, Yadav V, De Deyn GB, Flynn DF (2014) Selection for niche differentiation in plant communities increases biodiversity effects. Nature 515:108–111PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.College of Life SciencesZhejiang UniversityHangzhouChina
  2. 2.School of Life SciencesArizona State UniversityTempeUSA
  3. 3.School of Civil Engineering and ArchitectureZhejiang Sci-Tech UniversityHangzhouChina
  4. 4.School of SustainabilityArizona State UniversityTempeUSA
  5. 5.Center for Human-Environment System Sustainability (CHESS)Beijing Normal UniversityBeijingChina

Personalised recommendations