The quest for a mechanistic understanding of biodiversity–Ecosystem services relationships

Proceedings of the Royal Society B: Biological Sciences

Volumn 282, Issue 1817, 2015, Pages

  Duncan, Clare ^a,b   Thompson, Julian R ^b   Pettorelli, Nathalie ^a  

^a INSTITUTE OF ZOOLOGY   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Biodiversity; Biodiversity ecosystem services relationships; Ecosystem function; Ecosystem services; Mechanisms; Proxies

Indexed keywords

BIODIVERSITY; ECOSYSTEM FUNCTION; ECOSYSTEM SERVICE; FUTURE PROSPECT; LANDSCAPE ECOLOGY; POLICY MAKING; PROXY CLIMATE RECORD; TRADE-OFF;

BIODIVERSITY; ECOLOGY; ECOSYSTEM; ENVIRONMENTAL PROTECTION; PROCEDURES;

BIODIVERSITY; CONSERVATION OF NATURAL RESOURCES; ECOLOGY; ECOSYSTEM;

EID: 84945208958     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2015.1348     Document Type: Review

References (106)

1. Mace GM. 2014 Whose conservation? Science 345, 1558–1560. (doi:10.1126/science.1254704)
2. Millennium Ecosystem Assessment. 2005 Ecosystems and human well-being: biodiversity synthesis. Washington, DC: World Resources Institute.
3. Hooper DU et al. 2005 Effect of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol. Monogr. 75, 3–35. (doi:10.1890/04-0922)
4. Mace GM, Norris K, Fitter AH. 2012 Biodiversity and ecosystem services: a multilayered relationship. Trends Ecol. Evol. 27, 19–26. (doi:10.1016/j.tree.2011.08.006)
5. Cardinale BJ et al. 2012 Biodiversity loss and its impact on humanity. Nature 486, 59–67. (doi:10.1038/nature11148)
6. Harrison PA et al. 2014 Linkages between biodiversity attributes and ecosystem services: a systematic review. Ecosystem Services 9, 191–203. (doi:10.1016/j.ecoser.2014.05.006)
7. Naidoo R, Balmford A, Costanza R, Fisher B, Green RE, Lehner B, Malcolm TR, Ricketts TH. 2008 Global mapping of ecosystem services and conservation priorities. Proc. Natl Acad. Sci. USA 105, 9495–9500. (doi:10.1073/pnas.0707823105)
8. Egoh B, Reyers B, Rouget M, Bode M, Richardson DM. 2009 Spatial congruence between biodiversity and ecosystem services in South Africa. Biol. Conserv. 142, 553–562. (doi:10.1016/j.biocon.2008.11.009)
9. Chan KMA, Shaw MR, Cameron DR, Underwood EC, Daily GC. 2006 Conservation planning for ecosystem services. PLoS Biol. 4, e379. (doi:10.1371/journal.pbio.0040379)
10. Sachs JD et al. 2009 Biodiversity conservation and the millennium development goals. Science 325, 1502–1503. (doi:10.1126/science.1175035)
11. Secretariat of the Convention on Biological Diversity. 2014 Global biodiversity outlook 4. Montreal, Canada: CBD.
12. McShane TO et al. 2011 Hard choices: making tradeoffs between biodiversity conservation and human well-being. Biol. Conserv. 144, 966–972. (doi:10.1016/j.biocon.2010.04.038)
13. Schroter M, van der Zanden EH, van Oudenhoven APE, Remme RP, Serna-Chavez HM, de Groot RS, Opdam P. 2014 Ecosystem services as a contested concept: a synthesis of critique and counterarguments. Conserv. Lett. 7, 514–523. (doi:10.1111/conl.12091)
14. Kremen C. 2005 Managing ecosystem services: what do we need to know about their ecology? Ecol. Lett. 8, 468–479. (doi:10.1111/j.1461-0248.2005.00751.x)
15. Maes J, Paracchini ML, Zulian G, Dunbar MB, Alkemade R. 2012 Synergies and trade-offs between ecosystem service supply, biodiversity and habitat conservation status in Europe. Biol. Conserv. 155, 1–12. (doi:10.1016/j.biocon.2012.06.016)
16. Gamfeldt L et al. 2013 Higher levels of multiple ecosystem services are found in forests with more tree species. Nat. Commun. 4, 1340. (doi:10.1038/ncomms2328)
17. Rodriguez JP, Beard Jr TD, Bennett EM, Cumming GS, Cork S, Agard J, Dobson AP, Peterson GD. 2006 Trade-offs across space, time, and ecosystem services. Ecol. Soc. 11, 28.
18. Bennett EM, Peterson GD, Gordon LJ. 2009 Understanding relationships among multiple ecosystem services. Ecol. Lett. 12, 1–11. (doi:10.1111/j.1461-0248.2009.01387.x)
19. Raudsepp-Hearne C, Peterson GD, Bennett EM. 2010 Ecosystem service bundles for analyzing tradeoffs in diverse landscapes. Proc. Natl Acad. Sci. USA 107, 5242–5247. (doi:10.1073/pnas.0907284107)
20. Lavorel S, Grigulis K. 2012 How fundamental plant functional trait relationships scale-up to trade-offs and synergies in ecosystem services. J. Ecol. 100, 128–140. (doi:10.1111/j.1365-2745.2011.01914.x)
21. Nicholson E et al. 2009 Priority research areas for ecosystem services in a changing world. J. Appl. Ecol. 46, 1139–1144. (doi:10.1111/j.1365-2664.2009.01716.x)
22. Boyd J, Banzhaf S. 2007 What are ecosystem services? The need for standardized environmental accounting units. Ecol. Econ. 63, 616–626. (doi:10.1016/j.ecolecon.2007.01.002)
23. Wallace KJ. 2007 Classification of ecosystem services: problems and solutions. Biol. Conserv. 139, 235–246. (doi:10.1016/j.biocon.2007.07.015)
24. Fisher B, Turner RK. 2008 Ecosystem services: classification for valuation. Biol. Conserv. 141, 1167–1169. (doi:10.1016/j.biocon.2008.02.019)
25. Haines-Young R, Potschin M. 2010 The links between biodiversity, ecosystem services and human well-being. In Ecosystem ecology: a new synthesis (eds D Raffaelli, C Frid), BES Ecological Reviews Series, pp. 110–139. Cambridge, UK: Cambridge University Press.
26. Eigenbrod F, Armsworth PR, Anderson BJ, Heinemeyer A, Gillings S, Roy DB, Thomas CD, Gaston KJ. 2010 The impact of proxy-based methods on mapping the distribution of ecosystem services. J. Appl. Ecol. 47, 377–385. (doi:10.1111/j.1365-2664.2010.01777.x)
27. Balvanera P et al. 2014 Linking biodiversity and ecosystem services: current uncertainties and the necessary next steps. Bioscience 64, 49–57. (doi:10.1093/biosci/bit003)
28. Stephens PA, Pettorelli N, Barlow J, Whittingham MJ, Cadotte MW. 2015 Management by proxy? The use of indices in applied ecology. J. Appl. Ecol. 52, 1–6. (doi:10.1111/1365-2664.12383)
29. Maskell LC et al. 2013 Exploring the ecological constraints to multiple ecosystem service delivery and biodiversity. J. Appl. Ecol. 50, 561–571. (doi:10.1111/1365-2664.12085)
30. Costanza R, Fisher B, Mulder K, Liu S, Christopher T. 2007 Biodiversity and ecosystem services: a multi-scale empirical study of the relationship between species richness and net primary production. Ecol. Econ. 61, 478–491. (doi:10.1016/j.ecolecon.2006.03.021)
31. Werling BP et al. 2014 Perennial grasslands enhance biodiversity and multiple ecosystem services in bioenergy landscapes. Proc. Natl Acad. Sci. USA 111, 1652–1657. (doi:10.1073/pnas.1309492111)
32. Potvin C et al. 2011 An ecosystem approach to biodiversity effects: carbon pools in a tropical tree plantation. Forest Ecol. Manag. 261, 1614–1624. (doi:10.1016/j.foreco.2010.11.015)
33. Liss KN et al. 2013 Variability in ecosystem service measurement: a pollination service case study. Front. Ecol. Environ. 11, 414–422. (doi:10.1890/120189)
34. Wong CP, Jiang B, Kinzig AP, Lee MN, Ouyang Z. 2015 Linking ecosystem characteristics to final ecosystem services for public policy. Ecol. Lett. 18, 108–118. (doi:10.1111/ele.12389)
35. Lyashevska O, Farnsworth KD. 2012 How many dimensions of biodiversity do we need? Ecol. Indic. 18, 485–492. (doi:10.1016/j.ecolind.2011.12.016)
36. Hill MO. 1973 Diversity and evenness: a unifying notation and its consequences. Ecology 54, 427–432. (doi:10.2307/1934352)
37. Jost L. 2007 Partitioning diversity into independent alpha and beta components. Ecology 88, 2427–2439. (doi:10.1890/06-1736.1)
38. Mason NWH, Mouillot D, Lee WG, Wilson JB. 2005 Functional richness, functional evenness and functional divergence: the primary components of functional diversity. Oikos 111, 112–118. (doi:10.1111/j.0030-1299.2005.13886.x)
39. Villeger S, Mason NWH, Mouillot D. 2008 New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89, 2290–2301. (doi:10.1890/07-1206.1)
40. Smith B, Wilson JB. 1996 A consumer’s guide to evenness indices. Oikos 76, 70–82. (doi:10.2307/3545749)
41. Rao CR. 1982 Diversity and dissimilarity coefficients: a united approach. Theor. Popul. Biol. 21, 24–43. (doi:10.1016/0040-5809(82)90004-1)
42. Laliberte´ E, Legendre P. 2010 A distance-based framework for measuring functional diversity from multiple traits. Ecology 91, 299–305. (doi:10.1890/08-2244.1)
43. Lavorel S, Grigulis K, Lamargue P, Colace M-P, Garden D, Girel J, Pellet G, Douzet R. 2011 Using plant functional traits to understand the landscape distribution of multiple ecosystem services. J. Ecol. 99, 135–147. (doi:10.1111/j.1365-2745.2010.01753.x)
44. Diaz S, Lavorel S, de Bello F, Quetier F, Grigulis K, Robson TM. 2007 Incorporating plant functional diversity effects in ecosystem service assessments. Proc. Natl Acad. Sci. USA 104, 20 684–20 689. (doi:10.1073/pnas.0704716104)
45. Mokany K, Ash J, Roxburgh S. 2008 Functional identity is more important than diversity in influencing ecosystem processes in a temperate native grassland. J. Ecol. 96, 884–893. (doi:10.1111/j.1365-2745.2008.01395.x)
46. Lavorel S. 2013 Plant functional effects on ecosystem services. J. Ecol. 101, 4–8. (doi:10.1111/1365-2745.12031)
47. Anderson BJ, Armsworth PR, Eigenbrod F, Thomas CD, Gillings S, Heinemeyer A, Roy DB, Gaston KJ. 2009 Spatial covariance between biodiversity and other ecosystem service priorities. J. Appl. Ecol. 46, 888–896. (doi:10.1111/j.1365-2664.2009.01666.x)
48. Strassburg BBN et al. 2010 Global congruence of carbon storage and biodiversity in terrestrial ecosystems. Conserv. Lett. 3, 98–105. (doi:10.1111/j.1755-263X.2009.00092.x)
49. Lavorel S et al. 2013 A novel framework for linking functional diversity of plants with other trophic levels for the quantification of ecosystem services. J. Veg. Sci. 24, 942–948. (doi:10.1111/jvs.12083)
50. Tilman D. 1997 Distinguishing between the effects of species diversity and species composition. Oikos 80, 185. (doi:10.2307/3546532)
51. de Bello F et al. 2010 Towards an assessment of multiple ecosystem processes and services via functional traits. Biodivers. Conserv. 19, 2873–2893. (doi:10.1007/s10531-010-9850-9)
52. Kremen C, Williams NM, Thorp RW. 2002 Crop pollination from native bees at risk from agricultural intensification. Proc. Natl Acad. Sci. USA 99, 16 812–16 816. (doi:10.1073/pnas.262413599)
53. Winfree R, Fox JW, Williams NM, Reilly JR, Cariveau DP. 2015 Abundance of common species, not species richness, drives delivery of a real-world ecosystem service. Ecol. Lett. 18, 626–635. (doi:10.1111/ele.12424)
54. Dobson A et al. 2006 Habitat loss, trophic collapse, and the decline of ecosystem services. Ecology 87, 1915–1924. (doi:10.1890/0012-9658(2006)87[1915:HLTCAT]2.0.CO;2)
55. Duffy JE, Cardinale BJ, France KE, McIntyre PB, Thebault E, Loreau M. 2007 The functional role of biodiversity in ecosystems: incorporating trophic complexity. Ecol. Lett. 10, 522–538. (doi:10.1111/j.1461-0248.2007.01037.x)
56. Ayanu YZ, Conrad C, Nauss T, Wegmann M, Koellner T. 2014 Quantifying and mapping ecosystem services supplies and demands: a review of the remote sensing applications. Environ. Sci. Technol. 46, 8529–8541. (doi:10.1021/es300157u)
57. Barbier EB et al. 2008 Coastal ecosystem-based management with nonlinear ecological functions and values. Science 319, 321–323. (doi:10.1126/science.1150349)
58. Field CB et al. 1998 Mangrove biodiversity and ecosystem function. Global Ecol. Biogeogr. Lett. 7, 3–14. (doi:10.2307/2997693)
59. Pasari JR, Levi T, Zavaleta ES, Tilman D. 2013 Several scales of biodiversity affect ecosystem multifunctionality. Proc. Natl Acad. Sci. USA 110, 10 219–10 222. (doi:10.1073/pnas.1220333110)
60. Cardinale BJ, Matulich KL, Hooper DU, Byrnes JE, Duffy JE, Gamfeldt L, Balvanera P, O’Connor MI, Gonzalez A. 2011 The functional role of producer diversity in ecosystems. Am. J. Bot. 98, 572–592. (doi: 10.3732/ajb.1000364)
61. Venail P et al. 2015 Species richness, but not phylogenetic diversity, influences community biomass production and temporal stability in a re-examination of 16 grassland biodiversity studies. Funct. Ecol. 29, 615–626. (doi:10.1111/1365-2435.12432)
62. Gamfeldt L, Lefcheck JS, Byrnes JEK, Cardinale BJ, Duffy JE, Griffin JN. 2015 Marine biodiversity and ecosystem functioning: what’s known and what’s next? Oikos 124, 252–265. (doi:10.1111/oik.01549)
63. Isbell F et al. 2011 High plant diversity is needed to maintain ecosystem services. Nature 477, 199–202. (doi:10.1038/nature10282)
64. Loreau M. 2010 Linking biodiversity and ecosystems: towards a unifying ecological theory. Phil. Trans. R. Soc. B 365, 49–60. (doi:10.1098/rstb.2009.0155)
65. Reich PB, Tilman D, Isbell F, Mueller K, Hobbie SE, Flynn DFB, Eisenhauer N. 2012 Impacts of biodiversity loss escalate through time as redundancy fades. Science 336, 589–592. (doi:10.1126/science.1217909)
66. Grime JP. 1998 Benefits of plant diversity to ecosystems: immediate, filter and founder effects. J. Ecol. 86, 902–910.(doi:10.1046/j.1365-2745.1998.00306.x)
67. Loreau M. 2000 Biodiversity and ecosystem functioning: recent theoretical advances. Oikos 91, 3–17. (doi:10.1034/j.1600-0706.2000.910101.x)
68. Lefcheck JS, Byrnes JEK, Isbell F, Gamfeldt L, Hensel JNM, Hector A, Cardinale BJ, Duffy JE. 2015 Biodiversity enhances ecosystem multifunctionality across trophic levels and habitats. Nat. Commun. 6, 6936. (doi:10.1038/ncomms7936)
69. Laughlin DC. 2011 Nitrification is linked to dominant leaf traits rather than functional diversity. J. Ecol. 99, 1091–1099. (doi:10.1111/j.1365-2745.2011.01856.x)
70. Mouillot D, Villeger S, Scherer-Lorenzen M, Mason NWH. 2011 Functional structure of biological communities predicts ecosystem multifunctionality. PLoS ONE 6, e17476. (doi:10.1371/journal.pone.0017476)
71. Conti G, Diaz S. 2013 Plant functional diversity and carbon storage—an empirical test in semi-arid forest ecosystems. J. Ecol. 101, 18–28. (doi:10.1111/1365-2745.12012)
72. Grigulis K et al. 2013 Relative contributions of plant traits and soil microbial properties to mountain grassland ecosystem services. J. Ecol. 101, 47–57. (doi:10.1111/1365-2745.12014)
73. Ruiz-Jaen MC, Potvin C. 2010 Tree diversity explains variation in ecosystem function in a neotropical forest in Panama. Biotropica 42, 638–646. (doi:10.1111/j.1744-7429.2010.00631.x)
74. Valencia E, Maestre FT, Le Bagousse-Pinguet Y, Quero JL, Tamme R, Borger L, Garcia-Gomez M, Gross N. 2015 Functional diversity enhances the resistance of ecosystem multifunctionality to aridity in Mediterranean drylands. New Phytol. 206, 660–671. (doi:10.1111/nph.13268)
75. Hector A, Bagchi R. 2007 Biodiversity and ecosystem multifunctionality. Nature 448, 188–190. (doi:10.1038/nature05947)
76. Gamfeldt L, Hillebrand H, Jonsson PR. 2008 Multiple functions increase the importance of biodiversity for overall ecosystem functioning. Ecology 89, 1223–1231. (doi:10.1890/06-2091.1)
77. Zavaleta ES, Pasari JR, Hulvey KB, Tilman GD. 2010 Sustaining multiple ecosystem functions in grassland communities requires higher biodiversity. Proc. Natl Acad. Sci. USA 107, 1443–1446. (doi:10.1073/pnas.0906829107)
78. Mouillot D et al. 2013 Rare species support vulnerable functions in high-diversity ecosystems. PLoS Biol. 11, e1001569. (doi:10.1371/journal.pbio.1001569)
79. Vila M, Vayreda J, Comas L, Ibanas JJ, Mata T, Obon B. 2007 Species richness and wood production: a positive association in Mediterranean forests. Ecol. Lett. 10, 241–250. (doi:10.1111/j.1461-0248.2007.01016.x)
80. Paquette A, Messier C. 2011 The effect of biodiversity on tree productivity: from temperate to boreal forests. Global Ecol. Biogeogr. 20, 170–180. (doi:10.1111/j.1466-8238.2010.00592.x)
81. Maestre FT et al. 2012 Plant species richness and ecosystem multifunctionality in global drylands. Science 335, 214–218. (doi:10.1126/science.1215442)
82. Zimmerman EK, Cardinale BJ. 2014 Is the relationship between algal diversity and biomass in North American lakes consistent with biodiversity experiments? Oikos 123, 267–278. (doi:10.1111/j.1600-0706.2013.00777.x)
83. Grace JB et al. 2007 Does species diversity limit productivity in natural grassland communities? Ecol. Lett. 10, 680–689. (doi:10.1111/j.1461-0248.2007.01058.x)
84. Danovaro R, Gambi C, Dell’Anno A, Corinaldesi C, Fraschetti S, Vanreusel A, Vincx M, Gooday AJ. 2008 Exponential decline of deep-sea ecosystem functioning linked to benthic biodiversity loss. Curr. Biol. 18, 1–8. (doi:10.1016/j.cub.2007.11.056)
85. Mora C, Danovaro R, Loreau M. 2014 Alternative hypotheses to explain why biodiversity–ecosystem functioning relationships are concave-up in some natural ecosystems but concave-down in manipulative experiments. Sci. Rep. 4, 5427. (doi:10.1038/srep05427)
86. Wardle DA, Zackrisson O. 2005 Effects of species and functional group loss on island ecosystem properties. Nature 435, 806–810.(doi:10.1038/nature03611)
87. Lasky JR, Uriarte M, Boukili VK, Erickson DL, Kress WJ, Chazdon RL. 2014 The relationship between tree biodiversity and biomass dynamics changes with tropical forest succession. Ecol. Lett. 17, 1158–1167. (doi:10.1111/ele.12322)
88. Ziter C, Bennett EM, Gonzalez A. 2013 Functional diversity and management mediate aboveground carbon stocks in small forest fragments. Ecosphere 4, part85. (doi:10.1890/ES13-00135.1)
89. Petchey OL, Gaston KJ. 2002 Functional diversity (FD), species richness and community composition. Ecol. Lett. 5, 402–411. (doi:10.1046/j.1461-0248.2002.00339.x)
90. Diaz S et al. 2005 Biodiversity regulation of ecosystem services. In Ecosystems and human well-being: current state and trends: findings of the Condition and Trends Working Group (eds R Hassan, R Scholes, N Ash), pp. 297–329. Washington, DC: Island Press.
91. Zhang Y, Chen HYH, Reich PB. 2012 Forest productivity increases with evenness, species richness and trait variation: a global meta-analysis. J. Ecol. 100, 742–749. (doi:10.1111/j.1365-2745.2011.01944.x)
92. Cornwell WK et al. 2008 Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecol. Lett. 11, 1065–1071. (doi:10.1111/j.1461-0248.2008.01219.x)
93. Isbell F, Tilman D, Polasky S, Loreau M. 2015 The biodiversity-dependent ecosystem service debt. Ecol. Lett. 18, 119–134. (doi:10.1111/ele.12393)
94. Van der Biest K, D’Hondt R, Jacobs S, Landuyt D, Staes J, Goethals P, Meire P. 2014 EBI: an index for delivery of ecosystem service bundles. Ecol. Indic. 37, 252–265. (doi:10.1016/j.ecolind.2013.04.006)
95. Naeem S, Bunker DE, Hector A, Loreau M, Perrings CH. 2009 Biodiversity, ecosystem functioning and human well-being: an ecological and economic perspective. Oxford, UK: Oxford University Press.
96. Byrnes JEK et al. 2014 Investigating the relationship between biodiversity and ecosystem multifunctionality: challenges and solutions. Methods Ecol. Evol. 5, 111–124. (doi:10.1111/2041-210X.12143)
97. Bradford MA et al. 2014 Discontinuity in the responses of ecosystem processes and multifunctionality to altered soil community composition. Proc. Natl Acad. Sci. USA 111, 14 478–14 483. (doi:10.1073/pnas.1413707111)
98. Nelson E et al. 2009 Modelling multiple ecosystem services, biodiversity conservation, commodity production, and tradeoffs at landscape scales. Front. Ecol. Environ. 7, 4–11. (doi:10.1890/080023)
99. Pringle RM, Goheen JR, Palmer TM, Charles GK, DeFranco E, Hohbein R, Ford AT, Tarnita CE. 2014 Low functional redundancy among mammalian browsers in regulating an encroaching shrub (Solanum campylacanthum) in African savannah. Proc. R. Soc. B 281, 20140390. (doi:10.1098/rspb.2014.0390)
100. Garcia D, Martinez D. 2012 Species richness matters for the quality of ecosystem services: a test using seed dispersal by frugivorous birds. Proc. R. Soc. B 279, 3106–3113. (doi:10.1098/rspb.2012.0175)
101. Deraison H, Badenhausser I, Borger L, Gross N. 2015 Herbivore effects and their impact on plant community biomass: an experimental test using grasshoppers. Funct. Ecol. 29, 650–661. (doi:10.1111/1365-2435.12362)
102. Muiruri EW, Milligan HT, Morath S, Koricheva J. 2015 Moose browsing alters tree diversity effects on birch growth and insect herbivory. Funct. Ecol. 29, 724–735. (doi:10.1111/1365-2435.12407)
103. Alongi DM. 2008 Mangrove forests: resilience, protection from tsunamis, and responses to global climate change. Estuar. Coast. Shelf S. 76, 1–13. (doi:10.1016/j.ecss.2007.08.024)
104. Hooper DU et al. 2012 A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486, 105–108. (doi:10.1038/nature11118)
105. Larsen TH, Williams NM, Kremen C. 2005 Extinction order and altered community structure rapidly disrupt ecosystem functioning. Ecol. Lett. 8, 538–547. (doi:10.1111/j.1461-0248.2005.00749.x)
106. Phalan B, Onial M, Balmford A, Green RE. 2014 Reconciling food production and biodiversity conservation: land sharing and land sparing compared. Science 333, 1289–1291. (doi:10.1126/science.1208742)