Nontrophic Interactions, Biodiversity, and Ecosystem Functioning: An Interaction Web Model Author(s): Alexandra Goudard and Michel Loreau

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VOL. 171, NO. 1

THE AMERICAN

NATURALIST

JANUARY 2008

Nontrophic Interactions, Biodiversity,and Ecosystem Functioning:An Interaction Web Model

and Alexandra Goudard12',* MichelLoreau3lt

et Unite 1. Biogeochimie Ecologiedes MilieuxContinentaux, 46 Mixtede Recherche 7618, EcoleNormaleSuperieure, rue d'Ulm,F-75230Pariscedex 05, France; Pierreet MarieCurie,4 place Jussieu,75252 Paris 2. Universite cedex05, France; of 1205 avenueDocteur 3. Department Biology,McGillUniversity, Penfield,Montreal, QuebecH3A 1B1,Canada December 2006;Accepted Submitted 19, August20, 2007; November 2007 12, Electronically published Onlineenhancements: appendixes, figure.

ABSTRACT:

into and between Research therelationship biodiversity

ecosystemfunctioninghas mainlyfocusedon the effectsof species in on diversity ecosystemproperties plant communitiesand, more of in recently, food webs.Althoughthereis growingrecognition the in of significance nontrophicinteractions ecology,theseinteractions and arestillpoorlystudiedtheoretically, theirimpacton biodiversity and ecosystemfunctioningis largelyunknown.Existingmodels of and mutualism usuallyconsideronly one type of speciesinteraction do not satisfymass balanceconstraints. Here, we presenta model of an interactionweb that includesboth trophic and nontrophic interactions and that respectsthe principleof mass conservation. are in Nontrophicinteractions represented the form of interaction We between modifications. use this model to studythe relationship andecosystem thatemerges fromtheassembly properties biodiversity webs. We show that ecosystemproperties such of entireinteraction but as biomassand productiondependnot only on speciesdiversity on also on speciesinteractions,in particular the connectanceand and magnitudeof nontrophicinteractions, that the nature,prevain lence,and strengthof speciesinteractions turn dependon species interactions alterthe shapeof the relationship diversity. Nontrophic ecoand influence betweenbiodiversity biomassandcan profoundly systemprocesses. biodiversity, ecosystemfunctioning,nontrophicinteracKeywords: massbalance,model. modifications, tions, interaction
* E-mail:alexandra.goudard@ac-paris.fr. author;e-mail:michel.loreau@mcgill.ca. Corresponding Am. Nat. 2008. Vol. 171, pp. 91-106. c 2007 by The University Chicago. of All 0003-0147/2008/17101-42291$15.00. rightsreserved. DOI: 10.1086/523945

Therelationship funcbetween and biodiversity ecosystem in ecologyin the tioninghas emergedas a centralissue last decade.Human activitiescontribute speciesexto loss tinction,andbiodiversity can causeloss of ecological services(Pimmet al. 1995;Vitouseket al. 1997;Salaet al. 2000; Loreauet al. 2001, 2002; Kinziget al. 2002; a of Hooperet al. 2005).Therefore, betterunderstanding the effectsof biodiversity ecosystem is on properties criticallyneeded. The relationship and betweenbiodiversity ecosystem and hasmostlybeenstudied processes experimentally thein modelsusuTheoretical oretically plantcommunities. with thatprimary increases plant allypredict productivity at et richness saturates high diversity but (Tilman species conal. 1997; Loreau 1998,2000).Controlled experiments ductedin different localities (Hectoret al. 1999;Spehnet al. 2005) or over several years(Tilmanet al. 2001) often The effects species of exhibit predicted the pattern. positive have been explained on ecosystem functioning diversity and Loreau Hec1999; (Tilman by two mainmechanisms from tor 2001):a complementarity effect,whichemerges and facilitation nichedifferentiation, a selectioneffect or arisingfrom the dominanceof specieswith particular Thesemodels,whichfocuson a singletrophic traits. level, for are basedon niche theoryand plant competition a trophic limitingnutrient.Foodweb modelswith several that doesnot always levels,however, predict plantbiomass in withplantdiversity thatchanges diversity and increase can lead to complexchangesin ecosystemfunctioning and 2003;Iveset al. 2005). Recentex(Th6bault Loreau and Malmqvist 2000; Downingand periments(Jonsson Leibold 2002;Duffy2002;Paine2002;Duffyet al. 2003, can 2005) have showedthat trophicinteractions indeed and affect relationship the between biodiversity profoundly functioning. ecosystem and between Thus,the relationship biodiversity biomass or productivity been mostly studiedin plant comhas munitiesor in food webs.The only formof directspecies in interaction considered these studiesis the trophicin-

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The AmericanNaturalist

teraction for resource studythe structural functional and of (exploitation competition a shared properties interacis an indirect effectof the consumer-resource in- tion websandhencethe relationships between trophic biodiversity Someexperiments, that that in however, teraction). suggest non- and ecosystem properties emerge complexecosyssuchas facilitation, playan im- tems. trophicinteractions, may rolein ecosystem et Weneedtheories modelsto provide and (Mulder al. 2001; portant functioning generalizations Cardinale al. 2002; Rixenand Mulder2005). For in- on the roleof nontrophic et interactions ecosystem in functo stance,Rixenand Mulder(2005) showedthat waterre- tioning. It is therefore necessary constructthe most tentionincreases with speciesdiversity through increasing generalpossiblemodelof an ecosystem-a model of an facilitation leads to increased and in web bothtrophic nontrophic and productivity arctic interaction thatincludes tundramoss communities. that dif- interactions that respects principle mass conand the of Experiments suggest ferentkindsof speciesinteractions not act in isolation servation. do we present theoretical a modelthatmeets Here, fromeachotherin naturebut co-occurwithinthe same this need.Despite generality, modelis too complex its our and for tractable. we 1997).Evidence the to be analytically Therefore, studyit using community (Callaway Walker of is simulations mimica community that importance indirectinteractions also accumulating. numerical assembly Habitatmodification one type of indirectinteraction process. is Thisallowsus to investigate relationship the bethathasbeenstudiedexperimentally et al. 1999; tweenbiodiversity ecosystem and undermore (Bertness functioning Mulder al.2001;Cardinale al.2002;Rixen Mulder realistic et et and constraints thanwouldan analytical equilibrium Bertness al. (1999)haveshownthat study of specialcases,in agreement et with Loreau al.'s et 2005).Forinstance, to between algalcanopyreducesphysicalstresssuch as temperature (2001)recommendation studythe relationship or waterevaporation thus has positiveeffectson or- biodiversity ecosystemfunctioning and and with a dynamic in this assembly model,we studythe relaganismrecruitment, growth,and survival rockyinter- approach. Using tidalcommunities, habitatmodification algalcan- tionshipbetweenbiodiversity ecosystem but and by properties, can alsohavenegative effects increasing consumer suchasthebiomass productivity thevarious and of opy by trophic web with a food pressure. levels,in an interaction in comparison of allowsus to examine effectsof the Althoughthere is growingrecognition the signifi- web. Thiscomparison canceof nontrophic in interactions communities eco- nontrophicinteractionson the biodiversity-ecosystem and are web Thus,ourinteraction model systems,these interactions still poorlystudiedtheo- functioning relationship. and we still know little about generalpatterns provides usefulbasisfor reaching a reretically, greater generality and mechanisms. an important currentchal- garding impactof speciesdiversity speciesinterthe and Therefore, how interactions affect actionson the functional of lengeis to understand nontrophic properties complexecosysthe relationship between and func- tems. biodiversity ecosystem thereis an urgent needto include tioning.Moregenerally, in interactions ecological nontrophic theory(Boreret al. 2002;Brunoet al. 2003). Thereare some modelsof muModeland Methods tualism(Goh 1979;Heithauset al. 1980;Addicott1981; Ringelet al. 1996;Hollandet al. 2002),but thesemodels TheInteraction Model Web are specific,as they consideronly one kind of species interactions. lackgeneralmodelsof interaction We webs The modelis an extension a modeldeveloped Th&of by that includeall typesof directspeciesinteractions baultand Loreau for a nutrient-limited (inter(2003) ecosystem ferencecompetition,mutualism, commen- with threetrophiclevelscontaining arbitrary an number exploitation, aswellastheirindirect effects. of plants, andcarnivores. take Plants up a limsalism, amensalism) Simple herbivores, modelsof mutualism basedon Lotka-Volterra thus equations iting nutrientin theirrhizosphere, creating speciesalso have the unrealisticproperty of leading to explosive systems because they do not respectthe physicalprinciple of mass conservation (Ringel et al. 1996). Mass balance is crucial for understandingthe functional processesof natural ecosystems. Thus, it is necessary to construct interaction web models that satisfy mass balance constraints. Arditi et al. (2005) recently made a first step in that direction by adding interactionmodificationsto a food web model; they showed an increasing proportion of superefficient systems as the magnitude of interaction modifications was increased. Here, we expand this approachto specific resource depletion zones and allowing plant coexistence under some conditions (Loreau 1996, 1998). These species-specific resource depletion zones may be viewed as physical soil volumes, but they may also be viewed in a more abstractway as different niche spaces availableto differentspecies. Here, we add nontrophic interactionsto this food web to construct an interactionweb model that satisfiesmass balance constraints.Nontrophic interactionsare included in the form of interactionmodifications:each species can modify the trophic interaction between any two species.

and NontrophicInteractions, Biodiversity, Ecosystem Functioning 93

The modelis described the followingdynamicequaby tions and figure1:

dC dC dt
qcaHiCHHiC-

Carnivores
efficiency

Ci

\death Cx ux non-recycled a% nutrient

,x
7n

uCci,
a
j=i

(I-q)
Herbivores
Hy

recycling(1- Ax) Hz

dH l- = dt

PH.

dt =

j= 1

, CHHi acCHi - UHH

Plants
Nutrient

Pi

P.

apPiLiPPiLiLiFP

Iinput

iffusion
Li 7 IL
R

loss AR

in Nutrient species-specific Soilnutrient

resource zone depletion

pool

dL

dt
dRs

k VR

PiLPiLi, dt dR - XRR+

R-VR

L.i
XHi)UHH,

i=l

(1(1 -

Xpi)UPi

3 E(1
i=1

+ 3
+

i=l1

Xc)uc,Ci

flows. web nutrient represent Figure1: Interaction model.Solidarrows Forclarity the figure, of nutrient returned the to flowsof nonassimilated and are soil nutrient pool during consumption carnivores herbivores by either chain,andflowsof nutrient represented on the left trophic only or deatharerepresented recycled lost fromthe ecosystem only following on the righttrophicchain.Dottedlinesrepresent interaction modifications. Only five examples interaction of modifications represented are herefor the sakeof clarity. instance, For herbivore speciesH, modifies thetrophic interaction between herbivore species andcarnivore species H, of modification m,,. Themodification of C,,witha magnitude interaction of the nutrientflow betweenplant speciesPj and its species-specific to resource zone L,corresponds intraspecific or depletion competition facilitation.

3
3(1
i=1 i j=1

(1 qc)aCHiL
CiHJjCi qH)aHAiPiHPjH,.,

(1)

where
x
= (1 + mxyzlog Xz)

ez= 1

H(1 + X)"xz.
z=

(2)

Here, S is the number of species per trophic level, n = 3S is the total number of species, and Pi, Hi, and C; are the nutrient stocks of plant, herbivore,and carnivorespecies i, respectively. We assume the stoichiometriccomposition of each species to be constant;hence, its nutrientstock is proportional to its biomass. Parameteraxyis a per capitapotential consumption rate, that is, the intensity of the trophic interaction between predator species x and prey species y in the absence of interaction modification 0). Param(axy> 0 or X, the nutrient uptakerate of plant species i. Each eter aPiLi 0, then (1 Xz)mxyz = 1, and species is mxyr betweenspecies herbivoreor carnivorespeciesx may be more or less spe- z does not affectthe trophicinteraction

rates is cialist(if one of its potential consumption axy much than the others)or generalist all its potential (if higher rates are of similarmagnitude), with a consumption ax, for preference certainpreyspecies.The constants and q, efficiencies herbivores carof and qc are the conversion nivores,respectively app.A in the online editionof (see the American Naturalist parameter for values). are into interactions introduced the model Nontrophic modifications trophicinteracof by addingnontrophic to tions:eachspeciesz is allowed modifythe trophicinteraction betweenspeciesx and y with an effectthat depends on both its biomass Xz and a magnitudeof interaction modification of (fig. Parameter is mxY, 1). Ixy the nontrophic it is the totalnontrophic coefficient: effect of all speciesof the community the trophicinteraction on x between x species andy. Thus,species consumes species rate The consumption axyAxy. function y with a realized thatdescribes effects(eq. [2]) waschosensuch nontrophic inthat it satisfies several conditions. First,it is a strictly functionof both the magnitudeof interaction creasing modification and biomass Second, if either Xz. mxY, = = +

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The AmericanNaturalist

x and y. Thus, in the absenceof interactionmodifications, nutrient input in the soil nutrient pool per unit time, and is tx, = 1, and the realizedconsumption rate axYxY equal XRis the rate of nutrient loss from the soil nutrientpool. to its potential value ax,. Third, the function for nontrophic effects is strictly positive, so that the sign of the CommunityAssembly realized consumption rate does not change. The axyxy can magnitudeof interactionmodificationmxyz be positive We constrainedour interactionweb model as little as posor negative without changing the sign of Whatever sible in orderto exploreits generalproperties. Accordingly, axyxY. the nontrophic effects of other species, the nutrient flow we randomly assigned the various biological parameters between species x and y is never reversed.Fourth, while (potential consumption rates, intensities of interaction death rates,nonrecycledproportionsof nuthe magnitude of interaction modification mxyz comes as modifications, trient) to a regional pool of species from a uniform disthe exponent of a power function to keep the function tributionwithin appropriate intervalsand let the local ecopositive, we chose a linear dependence on biomass X,: assemble spontaneously. The establishment of a preliminaryresults showed that a power dependence on system valbiomass is strongly destabilizing.A positive myz leads to species depends on both its intrinsictraits (parameter ues) and its interactions with the other species already multiplication of the potential consumption rate a,y by a in the ecosystem. factor (1 + Xz) mxyzl, whereas a negative leads to di- present The model was simulatednumericallyusing C+ + promxyz vision of by this factor. and numerical integration of the dynamic axy In the presence of interaction modifications, each spe- gramming, was performedwith a Runge-Kuttamethod of cies can affect any other species x by modifying one or equations order 4 and a time step of 0.01 during 1,000 iterations, several trophic interactions that involve species x and that is, 100,000 time steps (100,000 numerical integrahence increasingor decreasingthe population growthrate tions). The local ecosystemresults from an assemblyprodXx/dtof species x. In the absence of interaction modi- cess that involves species' successive introductions and fications, the only direct species interaction is predation, eliminations. Species were introduced with a biomass and our model web reduces to a food web. When interto 0.01 that was subtractedfrom the soil nutrient equal action modifications are added, each species can have a pool, and they were considered extinct if their biomass positive (facilitation), negative (inhibition), or null effect was smaller than 0.005, in which case this biomass was on the population growth rate of any other species, and returned to the soil nutrient pool. Specieswere picked at thus all types of species interactions are possible (com- random from a regionalspecies pool with speciesrichness petition, mutualism, exploitation, commensalism, amen- n = 3S (S species at each trophic level) and introduced salism), including intraspecific (negative or positive) ef- regularlyto the community. Each successiveintroduction fects # 0 for species z). Our model web is then a occurred after a constant period irrespectiveof whethera (mrxz full interaction web that includes both trophic and non- new equilibrium was reached (thus, if the introduction trophic interactions. period was 100 time steps, there were 1,000 introduction Our interaction web model respects the principle of events during a simulation). mass conservation:a nontrophic interaction,such as muLocal species richnessis the total number of species in tualism or competition, does not affect the total quantity the locally assembledecosystem (to be distinguishedfrom of matter in the ecosystem as a whole. Interactionmod- regionalspecies richness).The total volume of the soil was ificationschange the materialflow between a resourceand kept constant irrespective of local species richness: a consumer by multiplying it by some factor,but there is = VR+ .1 V, where Vi= 0 if species i was not Voi mass conservation overall. in the community. Thus, when a plant species present The model also includes nutrient cycling. The constant became extinct, the volume of its species-specific resource is the loss or death rate of species x, and is the depletion zones was set to 0 and added to the volume of ux x nonrecycled (lost) proportion of nutrient coming from the soil nutrient pool. When a plant species was introspecies x. The variable R is the nutrient mass in the soil duced, the volume of its species-specificresourcedepletion nutrient pool with volume V,; Li is the nutrient mass in zones was createdand subtractedfrom the volume of the the set of species-specificresource depletion zones, with soil nutrientpool. This volume allocationrule respectsthe total volume X, of plants from species i. Nutrient is trans- conservation of total soil volume while at the same time ported between species-specificresource depletion zones allowing differentplant species to occupy complementary and the soil nutrient pool at a diffusion rate 7 per unit resourcedepletion zones in the soil. Complementarity betime. In our simulations, y was quite high (y = 10) to tween plant species has both theoreticaland empiricaljusallow rapid soil homogenization and strong indirectplant tifications (Loreau 1998; Loreauand Hector 2001). To be competition for the limiting nutrient. ParameterI is the consistent, however, this allocation rule requiresthat the

and Functioning 95 NontrophicInteractions, Biodiversity, Ecosystem total soil volume be greaterthan the sum of the volumes of the depletion zones of all possible plant species, which was the case in our simulations (app. A). Mass conservation was also satisfiedupon extinction of a plant species by adding the nutrient stocks in its residualbiomass and in its resourcedepletion zone to the soil nutrientpool and, conversely,upon introduction of a plant species by subtracting these nutrient stocks from the soil nutrient pool (app. B in the online edition of the AmericanNaturalist). Communityand Ecosystem Properties We examined the relationshipbetween the structureand functioning of interaction webs and the impact of nontrophic interactions by analyzing the effects of regional species richness, nontrophic connectance, and maximal nontrophicmagnitude (independentparametersof the regional species pool) on variouspropertiesof the local ecosystems, that is, local species richness, species richness at each trophic level, proportionsof the varioustypes of species effects and species interactions,interactionweb connectance,total biomass (total biomass of all species in the local ecosystem), biomass of each trophic level, and production of each trophic level. When we varied regional species richness,we kept equal numbers of species (S) at all trophic levels in the regionalspecies pool. Food web connectance of the regional species pool was defined as the number of realizedtrophic interactionsdivided by the number of possible trophic interactionsand was kept constant in all simulations. Its value was close to 1 because consumers were assumed to be more or less generalist, with potential consumption rates randomly drawn from a uniform distribution between 0 and 0.01 (and hence with a very small probabilityof being exactly 0). Note that our definition differsfrom the conventional definition of food web connectancebecause feeding links within trophic levels and between plants and carnivores were not allowed in our model. Interaction modifications were assigned in two steps: (1) there was a certain probabilitythat mxz # 0; (2) if # 0, the magnitude of the interaction modification mxYz was chosen in a uniform distribution.We call the probability that mxz 0 the nontrophic connectance of the regionalspeciespool, which is the probabilitythat a species modifies the trophic interactionbetween any two species: regional species pool is equal to the number of species mutiplied by the number of possible trophic interactions between species at adjacenttrophic levels in the pool, that
is, 3S(S2 + S2 + S).

We also varied the range of values of the magnitude of was randomly interaction modification. Parameter mxyz taken between a maximum value called "maximal nontrophic magnitude"and a symmetricalminimum equal to minus the maximal nontrophic magnitude. The maximal nontrophic magnitude was then allowed to take on differentvalues.Thus, we exploredthe impactsof nontrophic interactions by manipulating both the nontrophic connectance and the maximal nontrophic magnitude of the regional species pool. We analyzedthe community and ecosystem properties in the local ecosystems that resulted from the assembly process. We measured the proportions of species effects (facilitation, inhibition, or no effect) and species interactions (mutualism, competition, exploitation, commensalism, amensalism, or neutral interaction) based on the sign of the net species effects. The net species effect Ei (including trophic and nontrophic effects) of species g on species i was measured by the partial derivative of the growth rate dXIdt of species i with respectto the biomass Xg of species g:

E, a a7

a(dXI/dt)

(4)

If Eig 0, the effectof species on speciesi is a facilitation. > g If Eg< 0, it is an inhibition.If Eg> 0 and Egi 0, the > If interaction betweenspecies i and g is a mutualism. If < 0 and Eg< 0, speciesi and g are in competition. Ei, > 0 andEgi 0, the species < interaction anexploitation is Eg If formsof exploitation). Eig= 0 nontrophic (including and E, > 0, it is a commensalism. Ei = 0 and Eg< 0, If it is anamensalism. indirect interactions Density-mediated nutrient (Abrams 1995),suchas exploitative competition, do not enter into the calculation Eig. of The speciesinteractions thus definedare phenomenological internet in ecology. A as theyaredefined actions, just traditionally ratherthan a mechanistic definition phenomenological was necessary accountfor the wide varietyof trophic to in This andnontrophic effects a simple unified framework. allowedus to investigate effectsof regionalspecies the richness,nontrophicconnectance,and maximal nonof on and trophicmagnitude the prevalence strength spenontrophic connectance = cies effectsand speciesinteractions. number of realized interaction modifications Interaction web connectance the local community of (3) was measured the proportion nonneutral of number of possible interaction modifications" species by all possiblespeciesinteractions, that interactions among in of The number of possible interaction modifications in the is, by the proportion speciesinteractions which at

96

The AmericanNaturalist

A
(I (.)

40

30
20

Local species richness

Q, 0 C) 0 _J
o

Plant species richness

10
0 0 2 4 6 8 10

Herbivore species richness Carnivore species richness

B 2000
1500

Nutrient mass in the soil nutrient pool Total biomass Plant biomass

E 1000
0
ca[

500 0
Herbivore biomass Carnivore biomass

10

Time (x104)
Figure 2: Temporalchanges in local species richness (A) and biomass (B) during the ecosystemassemblyprocess. Biomassand local speciesrichness are shown for the community as a whole (black dotted lines), all plants (black solid lines), all herbivores (black dashed lines), and all carnivores (gray solid lines). The gray dashed line represents the nutrient mass in the soil nutrient pool. Regional species richness = 45, nontrophic connectance = 0.2, maximal nontrophic magnitude = 0.2.

least one of the two net species effects (Eigor Egi)is nonzero: interaction web connectance = number of nonneutral species interactions local species richness (local species richness- 1)/2
=

The production of each trophic level was measuredby its nutrient inflow (nutrient mass per unit time):
s s

carnivore production =

i=1 s

j=1 s

qcacyHjACHHjCi,

1 - proportion of neutral species interactions. (5)

herbivore production = 1:
i=1 j=1

(6)
qHaHPjAHpjPjHi,

primary production =

i=1

aiLi~PiLiLii.

We call "meanvalue of facilitation"the mean value of all positive net species effects, and we call "mean value of inhibition" the mean value of all negative net species effects. We calculatedthe proportions, mean values, and standard deviations of species effects and the proportions of species interactionsboth in the community as a whole and within each trophic level. We then consideredonly interspecificspecies effectsand interactionswithout takinginto account the effect of a species on itself (Ei).

We measured all these community and ecosystem properties during the course of community assembly.After a transition phase, however, the ecosystem systematically reacheda quasi-stationaryregime (fig. 2), that is, a phase where aggregatedvariablessuch as local species richness and biomass showed small variations around a constant temporal mean value. Therefore,we compared the community and ecosystem properties in the quasi-stationary regime by calculatingthe temporal mean during the last

and NontrophicInteractions, Biodiversity, Ecosystem Functioning 97

of 10% thesimulation iterations. eachvalueof regional For or richness,nontrophicconnectance, maximal species we performed nontrophic magnitude, eight simulations withdifferent random of theregional compositions species pool, as is often done in experiments(Hooper and Vitousek1997;Hectoret al. 1999;Knopset al. 1999;Tilmanet al.2001),andwe calculated meanandstandard the of for deviation the measured properties theseeightrepfor licates.We presentbelow figures a relatively high rerichness(45 species,i.e., 15 speciesper gional species are similar whatlevel),buttheresults qualitatively trophic belowthatdeeverthe numberof species.In the figures both nonscribethe effectsof regional speciesrichness, and connectance maximal nontrophic magnitude trophic wereset to 0.2. Results and at richness species richness eachtrophic Localspecies increased regional with levelin thequasi-stationary regime in webs richness both food websand interaction species the results obtained functions as (fig. 3A, 3B).Therefore, or were of regional speciesrichness localspeciesrichness verysimilar. Richness on Interactions Species and of Impact Nontrophic and Interactions thePrevalence Strength Species of in Webs.NonInteractions Interaction Diversity Species of has effectnot onlyon connectance an important trophic but ecosystemproperties also on the natureof species Whennontrophic connectance the interactions. increased, of 0 specieseffectsdecreased, whilethe proproportion

and portionsof facilitation inhibitionincreased to a up 4A). In a food web, the only directspecies plateau(fig. interaction exploitation is between trophiclevels(fig.4B, = when nontrophic connectance 0, and fig. 4F). In an interaction the proportion neutral deof interactions web, creasedto 0 as nontrophicconnectance and increased, henceinteraction connectance web increased 100%. to The of and first inproportions commensalism amensalism creased thendecreased 0 asnontrophic and to connectance whilethe proportions mutualism, of increased, competiandexploitation increased nontrophic as connectance tion, increased 4B).Thus,interaction modifications created (fig. betweenspecies(such as mutunontrophicinteractions alismor competition). on and Impact Interaction of Modifications thePrevalence As eithernontrophic connectof Species Strength Effects. ance(fig.4A) or maximal nontrophic magnitude 4E) (fig. the increased the and increased, meanvalueof facilitation meanvalueof inhibition thatis, the meanabdecreased; solutevaluesof specieseffects and increased, the standard As nondeviation species of effects increased. maximal also the of increased, proportion 0 species trophicmagnitude effectsfirstfluctuated eventually and increased 4E). (fig. both nontrophicconnectance maximalnonand Thus, trophic magnitudehad an impact on the prevalence, and of strength, variability specieseffects. The increase the meanvalueof specieseffectswith in connectance a consequence the assumpis of nontrophic tion that nontrophic effectsact multiplicatively conon rates. Since the magnitude of interaction sumption modification is randomly takenfroma uniformdismxYz it has the sameprobability beingpositiveor of tribution,

A
50
U)

FOODWEB

B
50
40 30 20

WEB INTERACTION

40
0)

30
20

.0. _)

-J

10

10 20 40 60 80 100 0 0 20 40 60 80 100

00

Regionalspecies richness

Regionalspecies richness

regimeas a functionof regionalspeciesrichnessin food webs (A; nontrophic Figure 3: Local species richnessin the quasi-stationary = = = webs (B; nontrophicconnectance 0.2, maximalnontrophic connectance 0, maximalnontrophic magnitude 0) and in interaction = 0.2). We presentthe meanand standard deviation local speciesrichness for circles), plantspeciesrichness (unfilled (filledcircles), magnitude and richness richness herbivore (triangles), carnivore species (squares). species

Proportions (%)and strength (xl00) of species effects A

100 80 6

Proportions (%) of species interactions

50

O-5 40
-50 0 0.2 0.4 0.6 0.8 1 20

od 0 D
100 80

Non-trophic connectance

0.2 0.4 0.6 0.8 Non-trophic connectance

C
50 0 -50 -100 0

60 40 20

20 40 60 80 100 Regional species richness

0 0

20

40

60

80

100

Regional species richness

E
80 4A 0)1 -4 -80 -120 0 0.5 1 1.5 2

F
100 80 60 40 20 0 0 20 40 60 80 100

Maximal non-trophic magnitude

Regional species richness

Figure 4: Proportions and strength of species effects (A, C, E) and proportions of species interactions (B, D, F) in the community as a whole in the quasi-stationaryregime as functions of nontrophic connectance (A, B; regional species richness = 45, maximal nontrophic magnitude = 0.2) and regional species richness in interaction webs (C, D; nontrophic connectance = 0.2, maximal nontrophic magnitude = 0.2). E shows the proportions and strength of species effects as functions of maximal nontrophic magnitude (regional species richness = 45, nontrophic connectance = 0.2). F shows the proportions of species interactions as functions of regional species richness in food webs (nontrophic connectance = 0, maximal nontrophic magnitude = 0). A, C, and E show the mean and standarddeviation for the proportions of neutral effects (gray diamonds,gray lines, x 100), facilitation (filled circles, x 100) and inhibition (filled triangles,x 100), the mean and standarddeviation for the mean value of facilitation (unfilled circles, x 100), the mean value of inhibition (unfilled triangles, x 100), and the standarddeviation of species effects (unfilledsquares,x 10). B, D, and F show the mean and standarddeviation for the proportionsof mutualism (filledcircles,x 100), competition (filled triangles,x 100), exploitation (filledsquares,x 100), commensalism(unfilledcircles,x 100), amensalism(unfilledtriangles,x 100), and neutral interactions (gray diamonds,gray lines, x 100). Dashed lines (gray-filledoutlineddiamonds, x 100) representinteractionweb connectance.

and NontrophicInteractions, Functioning 99 Biodiversity, Ecosystem

rate thus,thepotential negative; consumption thatit modifies has the same probability being multiplied a of by or factor divided the samefactor [2]). Ontheother by (eq. of hand,the net specieseffectEig a speciesg on another of to speciesi is proportional the magnitude the realized thatareaffected species The rates,ajltij, consumption by g. betweenthe multiplicative difference effectof interaction on modifications the magnitude realized of consumption rates effectof realized ratesandthe additive consumption effectE,g on average, nonon the net species explains why, On interactions to increase species tend effects. net trophic 50%of the x,,will be in the range0-1 and 50% average, nonwill be in the range1-oc.Therefore, increasing with the meanof the realized trophicconnectance, arithmetic rates willincreasingly exceed leadconsumption a,,, a,,x, of both inhibition to an increasing average strength ing and facilitation. This property might be viewedas a limitationof the formulation our model,whichinvolves of mathematical and effectswhilethereis no both multiplicative additive and in of distribution numbers whichboth theirproduct because theirsumareequalto 1. Butit mightbe realistic, ratesdo havea lowerboundof 0 andno upper biological so that nontrophic interactions be expected bound, may this to havethe effects predicted ourmodel.Ultimately, by data on issue will have to be resolvedusing empirical effectsin naturalecosystems, these data but nontrophic are currently sorelylacking.

whichincreases probability thisspecies the for to cialists), haveatleastone trophic modified anyotherspecies link by in the web. The fact that interaction web connectance tends to 100%,however, due to the assumption is that consumers generalists our model.Otherfood web in are configurations leadto smaller may upperlimits. TheStrength Species Decreases Species with Richof Effects ness. As regional increased 4C), the speciesrichness (fig. mean valueof facilitation decreased the meanvalue and of inhibition that values increased; is, the meanabsolute of specieseffectsdecreased. Thus,specieseffectstended to be denser, is, proportionally that morenumerous, and weaker regional as in richness increased interaction species webs(fig.4C).Weak interaction average strength probably buffersthe destabilizing effectsof interaction web connectanceand speciesrichness. Note thataverage interaction strength decreased regional also with richness species in food webs (the meanabsolute valueof inhibitionderesultsnot shown). creased;

and Interactions withinthe Various Species Effects Species Levels. Patterns withinthe various Trophic trophiclevels were very similarto those reported figure4 for the in as concerned the community a whole.Theonlydifference of facilitation inhibition, henceof inand and prevalence and terspecific competition cooperation, amongplantsas connectance increased C1 in the online nontrophic (fig. In edition of the American Naturalist). plants,the proThe Interaction Web ConnectanceIncreaseswith Species increased morerapidly thanthatof portionof inhibition Richness.As regionalspeciesrichness(and hence also whereas the community a whole(fig.4A) in as facilitation, of the localspeciesrichness) increased, proportion 0 spe- or in other trophiclevels (resultsnot shown),the proof cieseffects whilethe proportions facilitation decreased, of inhibitionand facilitation variedin the same the and inhibitionincreased 4C). Accordingly, pro- portions (fig. In the samemanner, proportion interspecific the of to decreased very way. portionof neutralspeciesinteractions increased more rapidlythan that of mutuof low values (fig. 4D), whereas proportions com- competition the theseproportions variedin the alism in plants,whereas mensalism and amensalism first increased and then desame way in other trophic levels or in the whole comof and competition the creased, proportions mutualism was un- munity (fig. 4B). and the proportionof exploitation increased, increased changed.Thus, interactionweb connectance to the with speciesrichness nearly100%: morenumerous Interactions Biodiversity on Impacts Nontrophic of with otherspecies. speciesare,the morethey interact and Ecosystem Properties
In food webs, the proportion of neutral species interactions increased with regional species richness (fig. 4F) whereas the proportion of exploitation decreased.Thus, the increase in interaction web connectance with species richnessin interactionwebs (fig. 4D) is due to the presence of nontrophic links between species. The increase in interactionweb connectance with species richnessis a generalpropertyof interactionwebs that can be explainedintuitively as follows: as regionalspecies richness increases,the number of trophic links of a given species increases (as long as consumers are not strict speNontrophicInteractionsand EcosystemProperties. Nontrophic connectance and maximal nontrophic magnitude had an important effect on ecosystem properties. Local species richness decreasedas either nontrophic connectance (fig. 5A) or maximalnontrophic magnitude (fig. 5B) increased,except at a low level of nontrophic parameters. Plant species richnessdecreasedas either nontrophic connectance (fig. 5A) or maximal nontrophic magnitude (fig. 5B) increased.In contrast,consumer species richnesswas less affected by variations in nontrophic connectance; it

100 The AmericanNaturalist

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in and of as connectance C,E;regional biomass, production the quasi-stationary (A, regime functions nontrophic Figure5: Localspeciesrichness, = = = richness 45, non(B, speciesrichness 45, maximal nontrophic magnitude 0.2) andmaximal nontrophic magnitude D, F;regional species = the connectance 0.2).Wepresent meanandstandard deviation total(filled for local richness biomass plant(unfilled and and circles) species trophic and localspeciesrichness, herbivore and the biomass, production unit time).Dottedlines represent circles), (triangles), carnivore (squares) (per nutrient massin the soil (diamonds).

as decreased maximalnontrophicmagnitude increased, nontrophic exceptat a low levelof maximal magnitude. The biomassand production eachtrophiclevel deof as eithernontrophic connectance 5C, creased (fig. sharply or maximalnontrophic 5E) magnitude (fig. 5D, 5F) increased. Interaction webswith high levelsof eithernonconnectance maximalnontrophic or trophic magnitude were systemsin which the biologicalprocessesof pro-

ductionand recycling wereverylow and inorganic flows Suchhighlevelsof nontrophic connectance and prevailed. arepresumably absentin natural magnitude ecosystems. TheImpacts Nontrophic Interactions Ecosystem on Proof AreMediated Changes Realized in cesses by Consumption Ratesand Species Interactions. The decrease biomass in and production all trophiclevelsas nontrophic at con-

and NontrophicInteractions, Biodiversity, Ecosystem Functioning 101

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Figure 6: Biomass and production in the quasi-stationaryregime as functions of regional species richness in food webs (A, C; nontrophic connectance = 0, maximal nontrophic magnitude = 0) and in interaction webs (B, D; nontrophic connectance = 0.2, maximal nontrophic total herbivore(triangles), total plant (unfilledcircles), magnitude = 0.2). We presentthe mean and standarddeviationfor total biomass (filledcircles), and total carnivore(squares)biomass and production (per unit time). Dotted lines representthe nutrient mass in the soil (diamonds).

nectance or maximal nontrophic magnitudeincreasescan be explainedby the impacts of nontrophic interactionson realized consumption rates and species interactions (fig. 4). First, mean realized consumption rates increase with nontrophic connectance,as mentioned above, which contributes to a decrease in the biomass and production at the next lower trophic level. These declines in the biomass and productionof lower trophic levels cascadeup the food web and lead indirectly to decreased carnivore biomass and production. Increasingnontrophic connectance also leads to more intense competition between consumersfor their resourceand a smallerresource-usecomplementarity, which contributesto a decreasein herbivoreand carnivore biomass and production. Second, the proportions of inhibition and competition increasemore than those of facilitationand mutualism in plantswhen nontrophicconnectanceincreases.Thus, nontrophic interactions tend to make competition between plant species stronger,which may also partly explain the decrease in primary production and plant biomass and hence indirectlyin consumer production and biomass.

The Biodiversity-Ecosystem FunctioningRelationships in Food Websand InteractionWebs Processesin Food Effectsof SpeciesRichnesson Ecosystem Websand InteractionWebs. In both food webs and interactionwebs, total biomass increasedwith regionalspecies richnessand hence with local speciesrichness (fig. 6A, 6B). Plant and carnivorebiomasses increasedin parallel, which suggests a bottom-up control of plants on carnivores. In contrast, herbivorebiomass was less affectedby species richness, which suggests a top-down control of carnivoreson herbivores.The soil nutrient concentration decreased as species richness increased, which shows a better exploitation of the limiting nutrient by plants. Production at all trophic levels increasedwith regional species richness (fig. 6C, 6D). Primary production increased with species richness because of the better exploitation of the limiting nutrient by plants; as a result, the increase in plant biomass was much higher than the decreasein the soil nutrientstock, and primaryproduction increased (eq. [6]; fig. 6A, 6B). Herbivoreproduction depends on plant biomass and herbivorebiomass (eq. [6]),

102 TheAmericanNaturalist and herbivore biomass was top-down controlled; therefore, herbivore production showed the same pattern as plant biomass (cf. fig. 6A, 6C and 6B, 6D). In the same manner, carnivoreproduction depends on herbivoreand carnivorebiomasses (eq. [6]), but herbivorebiomass was top-down controlled;therefore,carnivoreproduction followed carnivorebiomass. Production (especiallyin plants and herbivores) was generally high compared with the inorganic nutrient input, L This results from the high recycling efficiency of ecosystems in the quasi-stationary regime, after a long assemblyprocess. This high recycling efficiencyalso explainswhy the amount of nutrient in the soil often remained relativelyhigh. Differences between food webs and interaction webs highlightthe role of nontrophicinteractionsin ecosystems. The increasein biomass and productionwith regional(fig. 6) and local (fig. 7) species richness was less rapid in interaction webs than in food webs. Differencesbetween food webs and interaction webs were greater at higher levels of regionalspeciesrichness(fig. 6A, 6B). The positive effect of nontrophic interactions on the averagerealized consumption rate as species richness increases explains why nontrophic effects are more importantin species-rich ecosystemsthan in species-poorecosystemsin our model. Higher realizedconsumption rates make species more efficient but also more competitive. Biodiversity-Ecosystem Functioning Relationships. We studied the relationshipbetween total biomass and local species richness at the quasi-stationary regime that emerged from variationsin one of the parametersof the regional species pool, that is, regional species richness, nontrophic connectance, or maximal nontrophic magnitude (fig. 7). Whatever the parameterdriving variations in local species richness, there was a positive relationship between total biomass and local speciesrichness.However, the shape of this relationship differed. The relationship was roughlylinear in both food webs and interactionwebs when regionalspecies richnessvaried,but it was nonlinear and concave-upwhen nontrophicconnectanceor maximal nontrophic magnitude varied in interaction webs. This concave-uprelationshipbetweenlocal speciesrichnessand total biomass is explained by the greater effect of nontrophic interactions on biomass than on species richness (fig. 5). Thus, our model predicts a positive relationship between species richness and biomass in naturallyassembled ecosystems, but with a strong impact of nontrophic interactions on the shape of the diversity-biomassrelationship. Specifically, nontrophicinteractionsare expected to decreasethe magnitudeof biomass and production,but changes in their frequency or strength are expected to increase the dependency of biomass and production on local species richness.

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Figure 7: Relationshipsbetween local species richnessand total biomass driven by variations of differentpropertiesof the regional species pool: regional species richness in food webs (filled circles; nontrophic connectance = 0, maximal nontrophic magnitude = 0), regional species richness in interaction webs (unfilled circles; nontrophic connectance = 0.2, maximal nontrophic magnitude = 0.2), nontrophic connectance in interaction webs (triangles;regional species richness = 45, maximal nontrophic magnitude = 0.2), and maximal nontrophic magnitude in interactionwebs (squares; regional species richness = 45, nontrophic connectance = 0.2).

Discussion Our theoretical model shows that species diversity and nontrophic interactionsaffect stronglyand nonintuitively the community and ecosystem propertiesin communities that have assembledthrough repeatedcolonizationevents. Our main results can be summarizedas follows. First, increasing regional species richness leads to increased species richness, biomass, production, and interaction web connectancebut decreasedaverageinteraction strength in local communities. Thus, species-rich interaction webs are expected to be more productiveand more connected but to have weaker species interactionson average. Their lower interaction strength is probablywhat allows them to maintain a high diversityand connectance, in agreementwith previous theory (May 1973; Kokkoris et al. 1999, 2002). Their high diversityin turn allowsthem to use the limiting nutrient more efficiently and hence have a higher production and biomass, as predicted by existing theory (Tilman et al. 1997; Loreau 1998, 2000; Tilman 1999). Second, increasingthe frequencyand magnitudeof nontrophic interactions in the regional species pool leads to decreasedlocal species richness,biomass, and production. These counterintuitiveeffectsresultfrom the fact that nontrophic connectance and maximal nontrophic magnitude contributeto an increasein the magnitudeof trophic con-

and Biodiversity, Ecosystem Functioning 103 NontrophicInteractions, sumption fluxes, and hence the strength of species interactions, on average.Increasedaverageinteractionstrength allows fewer species to coexist and imposes a higher mortality on lower trophic levels,which eventuallydeteriorates the functioning of the whole ecosystem. Third, as a consequence, interactionwebs that include trophic and nontrophic interactionsare expected to have a lower local richness,biomass, and production than food webs that include only trophic interactions, all else (in particular,regional species richness) being equal. A positive diversity-biomassrelationshipemerges from the assembly of both food webs and interactionswebs, but nontrophic interactionsare expectedto affectthe shape of this relationship. Thus, our results emphasize the need to take into account nontrophic interactionsin theoreticalecology. Our simple, general model allows all types of species interactions to be incorporatedby adding interaction modifications to a food web. This mass-balanceconstrainedmodel of an interactionweb provides a useful tool for studying the impact of diversity on the functional properties of complex ecosystemswith more realism. The Biodiversity-Ecosystem Functioning Relationshipin InteractionWebs community have higher realized consumption rates on average,which makes them more efficient but also more competitive. Therefore, the probability of observing extreme resource exploitation and negative effects on ecosystem propertiesis higher. SpeciesDiversity,SpeciesInteractions, Processes and Ecosystem Our work shows that species interactionsdepend on species richness:both the strengthand the prevalenceof these interactions are diversity dependent. In particular, the mean absolute values of interspecificfacilitation and inhibition effects are expected to decrease with increasing species richness. These results agree with existing theory (Kokkoriset al. 1999, 2002). The analysisof naturalfood webs (Neutel et al. 2002) suggeststhat naturalecosystems are characterizedby a majority of weak interactions and a minority of strong interactions. Our model also predicts that interactionweb connectance increaseswith species richness and that the proportions of the various types of species effects and species interactions depend on species richness.A higher species diversity increases the probabilityfor each species to interact with any other species. Although the relationship betweentrophic connectanceand species richnesshas been well studied in food webs (Martinez 1992; Montoya and Sole 2003), we lack knowledge concerning nontrophic connectance and interaction web connectance in ecosystems. Speciesdiversityis known to affect ecosystem functioning through functional complementaritybetween species that use different resources (Tilman et al. 1997; Loreau 1998; Loreauand Hector 2001). Our model further suggests that it can affectecosystemfunctioning in more subtle ways by changing the nature, prevalence,and strength of species interactions. For instance, it can enhance ecosystem processes by increasingthe probabilityof facilitation (Cardinale et al. 2002). Recent experiments have shown that a form of facilitation,whereby a species enhances the access of other species to resources through biophysicalmodifications,affectsthe productivityand the relationshipin bryophyte commudiversity-productivity nities (Mulder et al. 2001; Rixen and Mulder 2005). Thus, species interactions,in particularnontrophic interactions, should be given more attention in studying the relationship between biodiversityand ecosystem properties.

Totalbiomass increaseswith regionalspecies richness,and hence also with local species richness, in both food webs and interactionwebs. In both types of web, carnivorebiomass is bottom-up controlledby plants,herbivorebiomass is top-down controlled by carnivores,and total biomass depends mostly on plant biomass. These control mechanisms arethe same as in classicalfood webs, and our results concerning food webs are in qualitative agreement with previous theoretical studies (Thdbaultand Loreau 2003; Ives et al. 2005). Thebault and Loreau (2003), however, showed that in a two-level food web with generalistherbivores, plant biomass and herbivore biomass increase nonlinearly with regional species richness and can even decreaseat a high level of species richness,whereasin our food web model, biomass does not decreaseat a high level of species richness. This differenceis probably explained by the presence of a third trophic level in our work and by the fact that, contrary to recent theoretical (Th6bault and Loreau 2003; Ives et al. 2005) and experimental (Downing and Leibold 2002; Duffy et al. 2003) studies in which species richness is controlled, our work provides a dynamic approach to biodiversity and ecosystem functioning in which both factors result from an assembly NontrophicInteractions Incorporating process. Our model predictsthat biomass and production into Theoretical Ecology are generallylower in interactionwebs than in food webs. Nontrophic interactionsare likely to generatestrong con- Our work provides a consistent ecosystem model that instraints on species coexistence. The species present in the corporates nontrophic interactions in the form of inter-

104 The AmericanNaturalist action modifications. Although interactionmodifications were regardedby Wootton (1994) as a class of indirect effects, they may be viewed as either direct or indirect trait-mediatedinteractions (Abrams 1995), depending on the context. The interactionmay be directif, for instance, the interactionmodifier directlyaffectsthe behaviorof the two species whose trophic interaction is affected. But it may also be indirect if, for instance, the interactionmodification occurs through habitat modification, which in turn affects the ability of the predatorto detect or catch its prey.Also, the director indirectnatureof trait-mediated interactions is not necessarilyreflectedin a model's structure (Abrams 1995). Therefore, our measure of the net species effect, Eg, of species g on species i includes both trophic and nontrophic directeffectsas well as, potentially, trait-mediated indirect effects. The ambiguity of current terminologysuggeststhat a reexaminationof the concepts, definitions, and measures of direct and indirect effects might be useful. Ecosystemengineers (Jones et al. 1994) are strong drivers of interactionmodifications:by modifying their physical environment,they createmany nontrophicspecies interactions.Autogenic or allogenic engineerscan modulate resource flows or abiotic parametersthat influences resource flows. Therefore, our modeling frameworkcould be applied to the study of ecosystem engineers through specific nontrophic modifications of trophic interactions or through modifications of abiotic parameterssuch as those that govern the input, recycling,and loss of nutrients. Experimentalstudies show that ecosystem engineering can induce changes in community structuralproperties, such as species richness (Zhu et al. 2006), species composition (Badanoet al. 2006), and species interactions (Collen and Gibson 2001), and ecosystemfunctional processes such as primaryproduction (Zhu et al. 2006). Our model shows that interaction modifications of all kinds can profoundly affect ecosystem properties such as biomass and production at all trophic levels. We view our interactionweb model as a promisingtool for merging the community and ecosystem perspectives in theoreticalecology. By incorporatingnontrophic interactions in the form of modifications of trophic interactions, our model describes material flows in a consistent way and hence allows analysisof ecosystemproperties.At the same time, it is a flexible and dynamic model that allows all kinds of species interactionsto occur,and hence, it allows analysisof community propertiessuch as species diversityand the connectance,prevalence,and strengthof species interactions. form of modificationsof trophic interactions,but it would also be possible to introduce them in the form of modifications of nontrophic parameterssuch as intrinsic death rates and recyclingrates.We assumed that nontrophic effects act multiplicativelyon potential consumption rates because this led to the simplest functional form for interaction modificationsthat respectsthe direction of consumption fluxes between trophic levels. This assumption makes sense mathematically because biological rates have a lower bound of 0 and no upper bound; nontrophic modifications of these rates may have asymmetriceffects, depending on whether they are positive or negative. But this assumption indirectly drives many of the observed effects of nontrophic interactionsin our model, and empirical data to assess its validity are unfortunatelysorely lacking. We also assumed that the various modifications of a given trophic interaction by differentspecies are additive, but interaction modifications might interferewith each other and generatenonadditive effects. For instance, there could be a hierarchyof effects (one effect dominates over the others) or a synergy of effects (the effect of one species can only be expressed in, or is modified by, the presence of another species). Our linear approximation, however,is in line with the simplicityrequiredfor a general ecosystem model. We assumed that there is a single limiting nutrient and that the stoichiometriccomposition of each speciesis constant, although the stoichiometric composition of plants is known to depend on factors such as environmental conditions and the presence of consumers. This simplification was made to avoid unnecessarycomplicationsin a model designed to explore the role of nontrophic interactions. In our model, the soil is compartmentalized, each plant taking up nutrient in its species-specific resource depletionzone. This assumptionwas meantto favor plant species resource-use complementarity and coexistence to some extent, although strong nontrophic interactions led to species-poor communities despite this asrobust sumption. We expect our resultsto be qualitatively to relaxationof this assumption, as suggestedby preliminary simulation results. A decomposer compartment could be added, but it is unlikely to change the results because we have alreadyincluded nutrient cycling in our model without detailing its mechanisms. Lastly,our current model considersan interactionweb with threetrophic levels. It would definitely be interestingto model an interaction web with a more realistic and flexible trophic structureby allowingconsumersto feed on severaltrophic levels and blurringthe separationbetween distincttrophic levels. Model Limitations Our theoretical study suggests several hypotheses that It Despite its strengths and generality,our model also has deserve to be tested experimentally. would be useful to limitations. We representednontrophic interactionsin the study the influence of species richness on species inter-

and NontrophicInteractions, Biodiversity, Ecosystem Functioning 105

in communities. actions:does the strengthof specieseffects(facilitation, and negativeinteractions rockyintertidal Ecology 80:2711-2726. inhibition)dependon speciesrichnessin experimental C. B. S. Does theirconnectance withspecies Borer,E.T.,K.Anderson, A. Blanchette, Broitman, D. Cooper, increase ecosystems? B. S. Halpern, W. Seabloom, J. B. Shurin.2002.Topological E. and richness? would also be usefulto test the impactsof It to a approaches food webanalyses: fewmodifications improve may interactions ecosystem on and nontrophic processes their our insights.Oikos 99:397-401. mechanisms: whatis the influence the connectance Bruno,J. E, J.J. Stachowicz, M. D. Bertness.2003.Inclusionof of or and of nontrophic interactions biomass proon and facilitation into ecologicaltheory.Trendsin Ecology& Evolution magnitude 18:119-125. ductionat varioustrophiclevels?Do nontrophic interR. 1997. and actionsgenerally increase resource consumption, possibly Callaway, M., andL.R.Walker. 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