plant species richness and ecosystem multifunctionality in global drylands

7/25/2019 Plant Species Richness and Ecosystem Multifunctionality in Global Drylands

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DOI: 10.1126/science.1215442, 214 (2012);335Science

et al.Fernando T. MaestreDrylandsPlant Species Richness and Ecosystem Multifunctionality in Global

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wandering albatrosses, the movements of many

other species of albatrosses and petrels are strong-

ly constrained by wind conditions (8, 21), and

species richness of Procellariiformes is positively

associated to wind speed (22). Thus, future re-

search should consider wind fields as an impor-

tant driver of the distribution and migration ofthese oceanic species.

References and Notes1. C. Parmesan, Annu. Rev. Ecol. Syst. 37, 637 (2006).2. G.-R. Walther et al., Nature416 , 389 (2002).3. I. R. Young, S. Zieger, A. V. Babanin, Science332, 451

(2011).4. S. Solomon, Climate Change 2007: The Physical Science

Basis. Contribution of Working Group I to the Fourth

Assessment Report of the Intergovernmental Panel on Climate

Change (Cambridge Univ. Press, Cambridge, 2007).5. N. P. Gillett, D. W. Thompson,Science302 , 273 (2003).6. D. W. Thompson, S. Solomon,Science296 , 895 (2002).7. T. Alerstam, D. Christie, A. Ulfstrand,Bird Migration

(Cambridge Univ. Press, Cambridge, 1993).8. H. Weimerskirch, T. Guionnet, J. Martin, S. A. Shaffer,

D. P. Costa, Proc. Biol. Sci. 267 , 1869 (2000).9. A. M. Felicsimo, J. Muoz, J. Gonzlez-Solis,PLoS ONE3,e2928 (2008).

10. R. M. Suryan et al., PLoS ONE3, e4016 (2008).11. E. Wakefield et al., Ecol. Monogr. 79, 663 (2009).12. H. Weimerskirch,A. Gault,Y. Cherel, Ecology86, 2611 (2005).13. C. Pron et al., Glob. Change Biol. 16 , 1895 (2010).14. H. Weimerskirch, Oecologia 102 , 37 (1995).15. H. Weimerskirch, N. Brothers, P. Jouventin, Biol. Conserv.

79, 257 (1997).16. G. N. Tuck, T. Polacheck, J. P. Croxall, H. Weimerskirch,

J. Appl. Ecol.38 , 1182 (2001).17. G. N. Tuck, T. Polacheck, C. M. Bulman, Biol. Conserv.

114, 1 (2003).18. C. Pennycuick, Bird Flight Performance: A Practical

Calculation Manual(Oxford Univ. Press, Oxford, 1989).19. S. A. Shaffer, H. Weimerskirch, D. Costa, Funct. Ecol.15,

203 (2001).

20. T. Alerstam, G. A. Gudmundsson, B. Larsson,Philos.Trans. R. Soc. Lond. B Biol. Sci. 340 , 55 (1993).

21. J. Gonzlez-Sols etal.,Mar.Ecol. Prog. Ser. 391, 221 (2009).22. R. Davies, U. Irlich, S. Chown, K. Gaston,Glob. Ecol.

Biogeogr.19, 98 (2009).

Acknowledgments:The long-term data on the demographyand foraging ecology of wandering albatrosses at PossessionIsland, Crozet Islands, were supported by the French PolarInstitute IPEV (program no. 109 to H.W.), with additionalfunding from the Prince Albert II de Monaco Foundation.The study is a contribution to the Program ANR Biodiversit2005-11 REMIGE. We acknowledge the modeling groups, theProgram for Climate Model Diagnosis and Intercomparison(PCMDI), and the World Climate Research Programme s

(WCRPs) Working Group on Coupled Modeling (WGCM) fortheir roles in making available the WCRP CMIP-3 multimodeldata set. Support for data and model selection was providedby S. Jenouvrier. We thank the many field workers involvedin the Crozet long-term monitoring since 1966 and in trackingprograms since 1989, and D. Besson for help with themanagement of the demographic database. M.L. was funded bya postdoctoral contract of the Spanish Ministry of Education

and Science (Ref. EX2007-1148) and Marie Curie IndividualFellowship (PIEF-GA-2008-220063). We are grateful toL. Riotte-Lambert for help with data analysis and C. Barbraud,

C. A. Bost, Y. Cherel, and S. Jenouvrier for commentson the manuscript.

Supporting Online Materialwww.sciencemag.org/cgi/content/full/335/6065/211/DC1Materials and MethodsSOM TextFigs. S1 to S3

References (2325)24 June 2011; accepted 11 October 201110.1126/science.1210270

Plant Species Richness andEcosystem Multifunctionalityin Global DrylandsFernando T. Maestre,1*Jos L. Quero,1 Nicholas J. Gotelli,2 Adrin Escudero,1

Victoria Ochoa,1 Manuel Delgado-Baquerizo,3 Miguel Garca-Gmez,1,4 Matthew A. BowkerSantiago Soliveres,1 Cristina Escolar,1 Pablo Garca-Palacios,1 Miguel Berdugo,1

Enrique Valencia,1 Beatriz Gozalo,1 Antonio Gallardo,3 Lorgio Aguilera,6 Tulio Arredondo,7

Julio Blones,8 Bertrand Boeken,9 Donaldo Bran,10 Abel A. Conceio,11 Omar Cabrera,12

Mohamed Chaieb,13 Mchich Derak,14 David J. Eldridge,15 Carlos I. Espinosa,12

Adriana Florentino,16 Juan Gaitn,10 M. Gabriel Gatica,17 Wahida Ghiloufi,13

Susana Gmez-Gonzlez,18 Julio R. Gutirrez,6 Rosa M. Hernndez,19 Xuewen Huang,20

Elisabeth Huber-Sannwald,7 Mohammad Jankju,21 Maria Miriti,22 Jorge Monerris,23

Rebecca L. Mau,24 Ernesto Morici,25 Kamal Naseri,21 Abelardo Ospina,16 Vicente Polo,1

Anbal Prina,25 Eduardo Pucheta,17 David A. Ramrez-Collantes,23 Roberto Romo,11

Matthew Tighe,26 Cristian Torres-Daz,18 James Val,27 Jos P. Veiga,28 Deli Wang,29 Eli Zaad

Experiments suggest that biodiversity enhances the ability of ecosystems to maintain multiplefunctions, such as carbon storage, productivity, and the buildup of nutrient pools (multifunctionalitHowever, the relationship between biodiversity and multifunctionality has never been assessed globain natural ecosystems. We report here on a global empirical study relating plant species richness aabiotic factors to multifunctionality in drylands, which collectively cover 41% of Earth s land surfaand support over 38% of the human population. Multifunctionality was positively and significantlyrelated to species richness. The best-fitting models accounted for over 55% of the variation inmultifunctionality and always included species richness as a predictor variable. Our results suggestthat the preservation of plant biodiversity is crucial to buffer negative effects of climate change andesertification in drylands.

Two decades of research have revealed

causal linkages between biodiversity and

univariate measures of ecosystem func-

tioning, such as primary productivity or nitrogen

accumulation, in many terrestrial and aqua

habitats (14). These relationships suggest t

the loss of biodiversity may impair the functio

ing of natural ecosystems and thus dimini

Fig. 4.(A) Changes in breedingsuccess over thepast 40 years(r2 = 0.30, P = 0.0003). From 1988 to 2009 only, r2 = 0.19, P = 0.048. (B) Changes over the p20 years in the mass of breeding wandering albatrosses in January to February.

13 JANUARY 2012 VOL 335 SCIENCE www.sciencemag.org14

REPORTS


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the number and quality of services they provide

(57). Ecosystems are valued for their ability to

maintain multiple functions and services simul-

taneously [multifunctionality (8)]. If the main-

tenance of biodiversity is to be justified as a

strategy for enhancing ecosystem services (5, 9),

it is essential to understand how biodiversity

affects multifunctionality (810). Existing knowl-

edge comes from controlled small-scale experi-

ments from a limited number of ecosystems,

mainly in North America and Europe (8

12).Furthermore, biodiversity is by no means the only,

or even the primary, driver of ecosystem func-

tioning, which is also influenced by other biotic

andabiotic factors (13, 14). Given this complexity,

a rigorous examination is needed of the role of

biodiversity in maintaining multifunctionality at a

large number of sites that represent a wide range of

spatial variability in resource availability, abiotic

factors, and species richnessand composition(15).

Arid, semi-arid, and dry-subhumidecosystems

(called hereafter drylands) constitute some of

the largest terrestrial biomes, collectively cov-

ering 41% of Earths land surface and supporting

over 38% of the global human population (16).Drylands host many endemic plant and animal

species (5) and include about 20% of the major

centers of global plant diversity and over 30% of

the designated endemic bird areas (17). These

ecosystems are also highly vulnerable to global

environmental change and desertification (16, 18).

Nevertheless, the relationship between biodiver-

sity and ecosystem functioning has seldom been

studied in drylands (19). We evaluated how the

richness of perennial vascular plants (hereafter

species richness) and a range of key abiotic

factors (climate, slope, elevation, and soil texture)

relate to multifunctionality in 224 dryland ecosys-

tems sampled from all continents except Ant-arctica (map S1). We surveyed plots measuring

30 m 30 m, which were large enough to rep-

resent the main ecosystem features at each site,

and assessed 14 ecosystem functions related to

the cycling and storage of carbon (C: organic C,

b-glucosidase, pentoses, hexoses, aromatic com-

pounds, and phenols), nitrogen (N: total N,NO3-N,

NH4+-N, aminoacids, proteins, and potential N

transformation rate), and phosphorus (P: availa-

ble inorganic P and phosphatase). These func-

tions were chosen because they deliver some of

the fundamental supporting and regulating eco-

system services (9, 18, 20) and because they are

used to identify the onset of desertification pro-

cesses (21). Our survey captured a substantialrange of the climaticconditions, ecosystem types,

and soil classes found in drylands worldwide (fig.

S1 and map S1).

We first evaluated the direct relationship be-

tween species richness and multifunctionality at

the global scale using both nonspatial [ordinary

least-squares (OLS)] and spatial [simultaneous

autoregression (SAR)] regression models (20).

Because we did not experimentally control for

other abiotic and biotic factors that are known to

affect ecosystem functioning, significant relation-

ships would indicate potentially strong effects of

richness on multifunctionality. To quantify multi-

functionality, we calculatedZ-scores (standardizeddeviates) of the 14 functions evaluated (20). The

multifunctionality indexMfor each plot was the

averageZ-score for all functions measured within

the plot. This index measures all functions on a

common scale of standard deviation units, has

good statistical properties, and is well correlated

with previously proposed indices for quantifying

multifunctionality (20) (fig. S4). Multifunction-

ality was positively and significantly (P< 0.05)

related to species richness, according to both OLS

and SAR models (Fig. 1A). Separate analyses of

functions related to the C, N, and P cycles ( 20)

also yielded positive and significant relationships

with species richness in all cases when usingOLS regression (Fig. 1, B to D). When SAR re-

gressions were used, significant relationships were

found only for functions related to C cycling

(Fig. 1, B to D).

We then evaluated whether the observ

effects of species richness were important as co

pared to those of abiotic factors, with a mu

model inference approach based on informati

theory and OLS regression (22). We built s

arate models using the multifunctionality ind

Mand functions from the N, C, and P cycles

dependent variables, and seven abiotic variab

[sand content, slope, elevation, and four comp

nents derived from a principal-components an

ysis of 21 available climatic variables (20)] pspecies richness as potential independent var

bles. Among the 255 possible models result

from all possible combinations of these indep

dent variables, we selected the set of best-fitti

models that minimized the second-order Aka

information criterion (AICc). Collinearity amo

independent variables in these models was neg

gible (20) (table S15). Whenever a model includ

species richness as an important predictor,

compared its AICc to that of the correspondi

model without species richness; differences

plant species richness and ecosystem multifunctionality in global drylands

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