Colonization sequence influences selection andcomplementarity effects on biomass production inexperimental algal microcosms

Quan-Guo Zhang and Da-Yong Zhang

Q.-G. Zhang and D.-Y. Zhang (zhangdy@bnu.edu.cn), State Key Laboratory of Earth Surface Processes and Resource Ecology & MOEKey Laboratory for Biodiversity Science and Ecological Engineering, Beijing Normal Univ., Beijing 100875, PR China. Presentaddress for QGZ: Dept of Zoology, Univ. of Oxford, South Parks Road, Oxford, UK, OX1 3PS.

Species extinction and immigration are both common in natural communities and the sequence with whichspecies are lost from or added to communities may be crucial to community structure. We experimentallyaddressed this issue by growing six green algal species in monocultures and all possible two-species mixtures,with two colonization sequences for each mixture. Both convergence and divergence in community structurewere observed. The compositions containing particularly productive species were more likely to converge, whilethose comprising of species with similar monoculture yields were more likely to diverge. The species mixtureswith high-yielding initial and low-yielding invading species produced more biomass than monocultures, butmixtures with the opposite assembly order produced only the same level of biomass as monocultures did. Toaddress the diversity�ecosystem functioning issue, we estimate complementarity effect by relative yield total(RYT) and selection effect by the correlation between species’ monoculture yields and their relative yields inmixtures, respectively. We found overall negative complementarity and positive selection effect in mixtures withhigh-yielding species as initial colonizers, but positive complementarity and negative selection effect in mixtureswith low-yielding initial species. Nonetheless, because we used only up to two species in each microcosm, ourresults are limited in addressing the relationship between species diversity and ecosystem functioning. Futureresearch should study the effects of immigration history with many more species involved in communityassembly.

Understanding the determinants of community struc-ture has been a long-standing task for ecologists(MacArthur 1972, Tilman 1988, Rosenzweig 1995).One effort is to examine the influence of history onspecies interactions and community structure (Ricklefsand Schluter 1993). History can shape communitieseither by determining which species can be colonizers orwhich species arrive first. The major question is whetherthe initial difference in community structure canpersist; or equally, whether communities from a similarspecies pool converge in appearance over time (Lewon-tin 1969, May 1977).

Simple models of interspecific competition predictthat the outcome of species competition depends oninitial species abundance under certain conditions. In

Lotka�Volterra model, for example, when the twointerspecific competition coefficients are equal andlower than one, two species can coexist regardless ofinitial conditions; when the two coefficients are equaland greater than one, the initially more abundantspecies could competitively exclude the other species(Tilman 1982). In line with theory, empirical testshave found alternative stable states of communitiesunder the influence of a variety of historical factorssuch as perturbations (Morris et al. 2003, Didhamet al. 2005, Fukami and Lee 2006), initial populationdensity (Hu and Zhang 1993), and colonizationsequences (Robinson and Dickerson 1987, Drake1991, Drake et al. 1993, Lawler and Morin 1993,Shorrocks and Bingley 1994). However, there are also

Oikos 116: 1748�1758, 2007

doi: 10.1111/j.2007.0030-1299.15988.x,

Copyright # Oikos 2007, ISSN 0030-1299

Subject Editor: Tadashi Fukami, Accepted 31 May 2007

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many studies that convincingly demonstrate commu-nity convergence, in which outcome of species compe-tition is history free (Tilman and Sterner 1984, Grover1988, 1991, Sommer 1991, Tilman and Wedin 1991).

A question then naturally arises, ‘when shouldhistory matter?’ (Chase 2003). Recently, there hasbeen a heated debate among ecologists about whatabiotic environments allow history to play moreimportant roles (Suding et al. 2004, Didham andWatts 2005, Didham and Norton 2006, Ejrnaes et al.2006, Fukami and Lee 2006, Didham and Norton2007, Mason et al. 2007). Meanwhile, Long andKarel (2002) proposed that history would influencecommunity structure when not all resources areavailable to all species, but would play a far lessimportant role in communities where species competefor the same resources in algal (Tilman and Sterner1984, Sommer 1991), grassland (Tilman and Wedin1991), or forest ecosystems (Pacala et al. 1996).Clearly, many issues in this field are still open andwant for empirical test.

In a similar vein, the consequences of communityassembly history for ecosystem functioning havereceived little attention, although the relationshipbetween biodiversity and ecosystem functioning(BEF) has been studied intensively in the past twodecades (Kinzig et al. 2001, Loreau et al. 2002,Hooper et al. 2005). Both species colonization andextinction are crucial to community structure, andmay shape biodiversity effects on ecosystem processes.The influences of species extinction scenarios oncommunity structure and BEF relationship have beenexplored in both modelling and experimental ap-proaches (Petchey 2000, Jonsson et al. 2002, Ostfeldand LoGiudice 2003, Smith and Knapp 2003,Zavaleta and Hulvey 2004, Gross and Cardinale2005, Larsen et al. 2005, Srinivasan et al. 2007).However, BEF studies have paid much less attentionto species colonization (except Loreau and Mouquet1999, Loreau 2004, France and Duffy 2006, Zobelet al. 2006). A previous study shows that the effect ofhabitat productivity on species diversity is influencedby species colonization history (Fukami and Morin2003). We propose that biodiversity effects onecosystem functioning could also be dependent oncommunity assembly history. The early colonists in ahabitat may either promote or inhibit the establish-ment of the late arrivals (Peterson 1984, Robinson andDickerson 1987, Drake 1991, Drake et al. 1993,Lawler and Morin 1993, Sait et al. 2000, Price andMorin 2004, Fukami et al. 2007), and thus affect thelatter’s contributions to ecosystem function. Forinstance, in poor or stressful environments wherefacilitation among species is found to be important(Callaway 1995, Callaway et al. 2002), early arrival offacilitator species (e.g. legume species in grassland)

could be of great benefit to the subsequent invadingspecies, enhancing biomass production of the entirecommunity. Conversely, a late arriving facilitatorspecies can have very limited benefit to the commu-nity.

Here we report results of an algal microcosmexperiment designed to examine the consequences ofspecies arrival order for community structure anddiversity effect on biomass production. Species diversitycan influence community biomass production bycomplementarity or selection effect, or both (Aarssen1997, Huston 1997, Tilman et al. 1997, Loreau et al.2001). In the present study we use the terms ‘com-plementarity’ and ‘selection’ as in Loreau and Hector(2001); ‘complementarity’ means resource partitioningor positive interactions among species, while ‘selection’indicates the tendency for species interactions in diversecommunities to favour species with higher monocultureyields (but see Hooper et al. 2005). Colonizationhistory may alter species evenness and identity ofdominant species, and change biodiversity effects onecosystem functioning. When high-yielding specieswere added to communities before low-yielding ones,species dominance would be very strong, leading topronounced selection effect (Aarssen et al. 2003);but such an assembly sequence should suppress thecontribution of the invading species, and the particu-larly low evenness among species could limit theopportunity for complementarity effect to enhancecommunity performance. By contrast, an unproduc-tive-productive species arrival order should lead tohigher species evenness, which allows complementarityeffect to be higher and suppresses selection effect (Nijsand Roy 2000, Wilsey and Potvin 2000, Polley et al.2003, 2007, Mattingly et al. 2007).

Methods

Experimental design and microcosm assembly

We used six unicellular green algal species (Table 1), allof which are common species in fresh waters insouthern China (Hu et al. 1980). Six possible mono-cultures and fifteen possible two-species mixtures wereconstructed, with two possible assembly sequences foreach mixture. We constructed four replicates for eachtreatment. This experimental design yielded a total of144 microcosms (6 monocultures �4 replicates �15mixtures �2 assembly sequences �4 replicates). Welimited the level of diversity in the experimentalcommunities in the interest of having a completeexperiment (i.e. all possible pairwise communities andassembly sequences are to be examined).

The communities were assembled in microcosms(covered 50 ml conical flasks), each of which contained

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20 ml initially sterile nutrient medium (freshwatermedium WC; Guillard and Lorenzen 1972). Allmonocultures were inoculated twice with 1000 algalcells, at the start of the experiment and day 2,respectively. The mixtures received their initial speciesat the start and day 2, and the invading species at day12 and 14 (1000-cell inocula at each time). We used asemi-continuous culture method (Tilman and Kilham1976); 5 ml of the medium in each microcosm wasreplaced every other day, resulting a 4/3-fold dilutionevery 48 h. In our chamber the temperature wasmaintained as 258C, and the photosynthetic photonflux density (400�700 nm) was 31 mmol m2 s�1, witha 14:10 h light: dark cycle. The positions of themicrocosms in the chamber were alternated daily tominimize positional effects, and the microcosms weremanually shaken twice a day to keep algal cells insuspension. We terminated the experiment at day 90(78 days after the addition of invading species). Theturnover of cultures imposed by experimental dilution(4/3 per 48 h) allowed the algae to experience at least 16generations within 78 days.

Biomass measurement

Algal biomass was measured at 6-d interval from day 6to 90 for monocultures, from day 18 to 90 for mixtures.At these days, three 0.1-ml samples were collected fromthe 5 ml replaced cultures for each microcosm, and cellnumbers were counted by using microscope andhemacytometers. We calculated biomass of each algalspecies in each microcosm by multiplying the numberof algal cells by their average cell volume, assuming thatalgal cell biomass is equal to mass of an equivalentvolume of water (Wetzel and Likens 2000). Cellvolume was calculated from the critical linear dimen-sions converted to volume using equations that approx-imate cell shapes (Wetzel and Likens 2000). The cellvolume of each individual species was observed to beinvariable across different treatments and over time; theaverage volume of 15 randomly chosen cells was usedfor estimating cell biomass for each species. Contami-nants (unexpected algal species) were observed in two

microcosms until day 18, two at day 36�42, four at day42�48, and one at day 66�72. These microcosms wereexcluded from subsequent analyses.

Data analysis

We looked at how many species-pairs has finalcommunity structure dependent of colonization se-quence and how many did not. (1) Divergence occurs ifone species composition had different dominant speciesunder different colonization sequences; (2) incompleteconvergence occurs when the dominant species wasthe same regardless of the species arrival order, withthe subordinate species performing differently underdifferent colonization sequences (the subordinate spe-cies persisted if they were initial species but went extinctif they were invader); (3) convergence occurs when onecommon dominant was found for both assemblages of aspecies-pair, the subordinate species either persistedunder both colonization scenarios or went extinct underboth colonization scenarios.

We also looked at the effect of colonization orders interms of species coexistence. Again, the 15 species-pairsfell into three categories. (1) coexistence, two speciescoexisted through the experiment regardless of coloni-zation orders; (2) exclusion, species could not coexistunder either colonization order; (3) conditional coex-istence, two species could coexist only under onecolonization scenario.

We then evaluated the effect of historical role (beinginitial or invading species) on the performance of everyspecies. Repeated measures ANOVA was used for theoverall effect across time (with the biomass of eachspecies at day 18�90 as the repeated measured responsevariables and its historical role as a categorical explana-tory variable), and one-way ANOVA was used for theeffect at each point of time. The same analysis methodswere used for the effect of identity of the initial andinvading species on the overall community structure, interms of total biomass of species. We used SPSS ver.10.0 software for the execution of statistical analyses. Inrepeated measures ANOVA, the Huynh-Feldt degreesof freedom adjustment was used when the sphericityassumption was violated (van Ruijven and Berendse

Table 1. Species used in the experiment in descending order of monoculture yield. Estimates of individual cell mass are based oncell volume (Wetzel and Likens 2000). Monoculture yield is the average from day 6 to 90. Initial colonies of the algal species werepurchased from Freshwater Algae Culture Collection (FACHB) of the Chinese Acad. of Sci.

Organism Abbreviation Individual cell mass (mg) Monoculture yield (mg l�1)

Chlamydomonas sajao Cs 3.16�10�7 1174Golenkinia paucispina Gp 1.59�10�7 544Ankistrodesmus falcatus Af 6.42�10�8 288Selenastrum capricornutum Sc 3.19�10�8 239Scenedesmus dimorphus Sd 4.40�10�8 231Chlorella pyrenoidosa Cp 1.31�10�8 205

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2005). The relationship with time was determined byusing linear contrasts in this procedure. Biomass datawere transformed as log10 (mg/l �1) before analyses.

Relative yield analysis (Trenbath 1974, Harper1977, Vandermeer 1989, Hector 1998, Hooper1998) was used for evaluating complementarity effectin mixtures. The relative yield (RY) of a species is itsbiomass in mixture expressed as a proportion of itsyield in monoculture, and the relative yield total(RYT) of a mixture is the sum of the RYs of thecomponent species. Because the invading species wereadded to the microcosms 12 days later than the initialspecies, we calculated RY of invading species at ith dayas (yield of invading species in mixture at day i)/(yieldof invading species in monoculture at day i-12). RYTof mixtures measures overyielding effect. A RYT valueclose to one implies that species in a community areusing the same limiting resource, without any com-plementarity occurring. RYT �1 indicates thatcomplementarity effect leads to overyielding, andRYT B1 demonstrates occurrence of interferenceamong species.

We calculated the correlation between species’ RYand monoculture yields for test of selection effect. Apositive relation between species’ RY and monocultureyields indicates the presence of positive selection effect.The component species of different mixtures hadvarying monoculture yields. To make RY-monocultureyield relations comparable across mixtures, we adjustedfor the among-mixture difference in species’ mono-culture yields, following a methodology used by Austin(1982) and Hector et al. (2002). For each mixture, wedefined normalized monoculture yield of a componentspecies i as Yi/Ym, where Yi is the monoculture yield ofspecies i and Ym is the monoculture yield of thecomponent species with the highest monoculture yield.We used the correlation between RY and normalizedmonoculture yields (calculated by Pearson’s Correlationtest) to indicate selection effect.

We did not use Loreau and Hector’s (2001)‘additive partitioning’ method in our analyses, althoughit has been regarded as the most powerful approach toseparating complementarity and selection effects. Thismethod was designed for substitutive experiments, butnot suitable for invasion experiments. See the onlineappendix for further discussion on this method and itsapplication to our experimental data.

The mixtures were classified into two categories,productive�unproductive (the initial species washigher-yielding than the added species) and un-productive�productive (the initial species was lower-yielding). We tested whether biomass production,complementarity and selection effect showed anydifference between the two types of assemblages.

Results

Community structure

In four out of the fifteen 2-species compositions, Cs/Gp, Cs/Af, Cs/Cp and Gp/Af, colonization sequencehas no effect on the final community structure,classified as convergent category (Fig. 1; see Table 1for species abbreviations). In each of the four composi-tions, assemblages with opposite colonization se-quences converged to the same state (they shareddominant species and the subordinate species eitherpersisted in both assemblages or went extinct in bothassemblages). Divergence was observed in four compo-sitions, Gp/Sc, Gp/Sd, Af/Sc and Sd/Cp, for each ofwhich the two different assemblages were dominatedby their respective initial species (Fig. 1). The remain-ing seven compositions could be categorized as‘‘incompletely convergent’’, among which six (Cs/Sc,Cs/Sd, Af/Sd, Af/Cp, Sc/Sd and Sc/Cp) have the samedominant species in common across the two assemblyorders, with the subordinate species being persistent(when being initial species) or extinct (when beinginvading species). In the composition Gp/Cp, oneassemblage was dominated by the initial species (Cp)and the other was co-dominated by both species at endof the experiment (Fig. 1).

Five pairs of species (Cs/Gp, Cs/Cp, Gp/Af, Gp/Sd,and Gp/Cp) coexisted regardless of species arrivalorder. In one composition (Cs/Af) coexistence didnot occur under either colonization sequence. Theother nine pairs exhibit conditional coexistence (twospecies coexisted only under one of the two coloniza-tion sequences).

Overall, each species had greater biomass when itwas the initial species (repeated measures ANOVA day18�90, pB0.001, for each species). For each of the sixspecies, being initial or invading species made aconsistently significant difference during the experi-ment (one-way ANOVA, pB0.001, at each point oftime), although for the most productive species C.sajao , being the initial species was only marginallydifferent from being the invading species at day 78(F1,37�3.04, p�0.089) and 84 (F1,37�3.04, p�0.107). Community biomass was affected not only bythe identity of the initial species (repeated measuresANOVA day 18�90, F5,106�45.46, pB0.001) butalso by which species is the invader (F5,106�3.21, p�0.010), although with different patterns. The identityof initial species was always a significant predictor (one-way ANOVA, pB0.001, at each point of time),whereas the identity of invading species exerted asignificant influence only at the late stages (day 54�90, pB0.010).

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Fig. 1

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Fig. 1. Population dynamics of each species in each historical treatment. Two panels on each row are for assemblages with thesame constituent species but opposite colonization sequences. The title of each panel indicates the colonization sequence; forexample, Cs-Gp means that Cs is the initial species and Gp is the invading species. The legend on each row shows the category ofthe composition (divergent, convergent, or incompletely convergent), and symbols for species. See Table 1 for speciesabbreviations.

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Biomass production

Overall the mixtures with productive�unproductivespecies assembly sequence yielded more biomass thanthe monocultures, though only marginally significantly(Fig. 2, repeated measures ANOVA day 18�90,F1,77�3.29, p�0.074). However, no difference wasdetected between monocultures and unproductive�productive assemblages (F1,77�0.32, p�0.577).Compared with that of the monocultures, biomassproduction of the productive�unproductive assem-blages was higher at day 30 and 48�66 (independentsamples t-test, pB0.050), marginally higher at day 24(p�0.079), 42 (p�0.053) and 78 (p�0.097), andnon-significantly higher at other times (p�0.100).Biomass of the unproductive�productive assemblageswas lower at day 18 (p�0.027), non-significantlylower at day 24�60 and 72 (p�0.100), and non-significantly higher at day 66, and 78�90 (p�0.100),than that of the monocultures (Fig. 2).

Complementarity

Overall, relative yield total (RYT) of the productive�unproductive assemblages was significantly lower thanthat of the assemblages with the opposite colonizationsequence (Fig. 3, repeated measures ANOVA day 18�90, F1,109�16.78, pB0.001). RYT decreased steadilywith time (F1,109�5.75, p�0.018). The interactiveeffect of time and colonization sequence was alsosignificant (F1,109�20.77, pB0.001), suggesting thatthe difference in RYT between the two types ofassemblages with reciprocal sequences became smallerover time (Fig. 3). RYT of the productive-unproductiveassemblages varied through time, close to one or lessthan one (Fig. 3), with the average (day 18�90) beingless than one (p�0.017). In the unproductive�productive mixtures, RYT ranged from greater thanone to less than one, with the average greater than one(Fig. 3, p�0.001).

Selection effect

The presence of the most productive species, C. sajao ,exhibited significant effect on biomass of the produc-tive-unproductive assemblages (one-way ANOVA,pB0.001 at each point of time), so did it for theunproductive�productive assemblages (pB0.05) ex-cept for at day 18 (p�0.055). The other five speciesdid not have significant effect (p�0.05).

The correlation between RY and normalized mono-culture yields of species was positive in the productive�unproductive assemblages throughout the experiment(Pearson’s correlation test, pB0.001 at any time; andon average over day 18�90, r�0.789, pB0.001, n�116; Fig. 4). The unproductive-productive assemblagessaw a varying relation between RY and monoculture

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Fig. 2. Community biomass over time. (a) biomass ofmonocultures and mixtures with high-yielding species asinitial species. (b) biomass of monocultures and mixtureswith low-yielding species as initial species. Data of mono-cultures biomass in (a) and (b) are the same. Asterisks indicatesignificant difference between monocultures and mixtures(pB0.050, based on independent samples t-test); ms,marginally significant (0.050BpB0.100); ns, non-significant(p�0.100).

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Fig. 3. Relative yield total (RYT) of two types of assemblageswith opposite colonization orders over time. A horizontaldashed line through one shows the null hypothesis that nooveryielding occurs. Asterisks indicate significant departurefrom null hypothesis (pB0.05, based on one-sample t-test).

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yields, from positive (day 18) to neutral (day 78�90) ornegative (day 24�72), being negative on average overdays 18�90 (r��0.316, pB0.001, n�120; Fig. 4).

Discussion

Colonization sequence and community structure

In our experiment, both convergence and divergence incommunity structure were observed (Fig. 1). Thecompositions containing particularly productive specieswere more likely to exhibit convergent communitystructure: three (Cs/Gp, Cs/Af and Cs/Cp) out of thefour convergent compositions contained the mostproductive species C. sajao , with the remaining one(Gp/Af) having the secondly most productive speciesG. paucispina . On the other hand, in each of the fourdivergent compositions (Gp/Sc, Gp/Sd, Af/Sc or Sd/Cp, where two assemblages with different colonizationsequences were dominated by their respective initialspecies), species exhibited relatively small differences inmonoculture yields (see Table 1 for species monocul-ture yields). Four low-yielding species (Af, Sc, Sd andCp) have relatively small difference in monocultureyields among them. Communities comprising ofthese species are more likely to show incompleteconvergence behaviour (four out of six species composi-tions did so). It might take longer time for communitieswith low-yielding species to reach their final equili-brium states.

Whether and when colonization history influencescommunity structure is a long-standing question inecology (Chase 2003, Ejrnaes et al. 2006). Abioticfactors such as disturbance regime are thought toinfluence the importance of history (Suding et al.2004, Didham and Watts 2005). In our experimentall microcosms experienced the same physical environ-

ments; some of them showed community structuredependent of species arrival order but the others didnot. The results suggest that species attributes areimportant for understanding the question of ‘whenhistory matters’.

Long and Karel (2002) proposed that history wouldinfluence community structure when not all resourcesare available to all species, but is not important incommunities where species compete for the sameresources. In our experiment all species are green algae(Chlorophta), probably using the same resources. TheN: P ratio of the medium is 20: 1, larger than Redfieldratio 16: 1 (Redfield 1934); so all algal species usedwere probably limited by phosphorus. However, notonly convergence but also divergence was observed inthe present study. Community divergence was morelikely to occur in the compositions consisting of specieswith relatively small differences in monoculture yield,whereas the compositions containing particularly high-yielding species were more likely to converge. Thedivergence observed in the present study comes outplausibly from symmetrical competition among species,under which initial population density might exert alasting effect on the outcome of interspecific competi-tion (Long and Karel 2002).

Long enough study duration is one necessarycondition for judging alternative states of community(Connell and Sousa 1983), but many previous experi-mental studies providing evidence for divergent com-munity structure were short, rendering their findingssomewhat inconclusive (Schroder et al. 2005). Ourexperiment is quite long, lasting for 78 days afterinvasion of the late arriving species (at least 16generations for each species). However, not all com-munities reached their final equilibriums, as implied bythe seven incompletely convergent compositions (whichcould possibly become convergent had we run theexperiment for an even longer period). The differentialstates in assemblages of the incomplete convergentcompositions could be regarded as long-term transients(Schroder et al. 2005). Some transient phenomena canbe very long-lasting, and hence, have importantecological consequences (Hastings 2004). Furthermore,natural communities are often under various types ofperturbation, and long-term transients might neverreach their presumable stable end-states, and evenbecome ‘‘permanently transients’’ (Schroder et al.2005). Long-term transient phenomena deserve moreattention in future studies.

Colonization sequence and ecosystemfunctioning

In our experiment, biomass production of mixtures wasinfluenced by species arrival order. Overall, mixtures

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with high-yielding initial species and low-yieldinginvaders (productive�unproductive assemblages) weremore productive than monocultures, while mixtureswith the opposite colonization sequence (un-productive�productive assemblages) produced thesame amount of biomass as monocultures did. RYTwas on average less than one in productive�unproduc-tive assemblages, and greater than one in mixtures withthe opposite species arrival order (Fig. 3). The relationbetween species’ RY and normalized monoculture yieldsindicated that the selection effect was positive in theproductive�unproductive assemblages and negative inthe unproductive�productive assemblages (Fig. 4). Thefact that the difference in RYT between the two types ofassemblages became smaller over time (Fig. 3) suggeststhat the influence of colonization on biodiversity effectsmay fade out through time. However, the presentexperiment lasted for 78 days after colonization of thelate arrivals (at least 16 generations), suggesting thatcolonization history can exert impact on BEF relation-ship on an ecologically important time scale. Note thatwe only grew monocultures and two-species mixtures,and this may limit the generality of these findings.

A most recent and extensive literature survey(Cardinale et al. 2006) shows that selection effect is amore general mechanism than complementarity in theexisting BEF studies, suggesting that the identity ofindividual constituent species rather than the interac-tions among species largely determines ecosystemprocess. In this context, a conceptual model originallyproposed to examine the influence of species extinctionorder on biodiversity�ecosystem function relationship(Larsen et al. 2005) could be adapted to illustrate theinfluence of colonization order on BEF relationship.The functional consequences of colonization maydepend on two types of species-specific traits: coloniza-tion traits (which determine the likelihood of a speciesto arrive early at empty habitats) and effect traits (whichdetermine the functional contribution of a species).When colonization traits and effect traits are indepen-dent of each other, the order of species arrival will berandom with respect to functional importance ofspecies. On the other hand, a correlation betweenthem can modify BEF relationship. If all species had thesame access to vacant habitats, and thus equally likely tobe the first species, a linear increase of function throughcolonization process could be expected; the resultingBEF relationship would be linear. A positive relationbetween functional importance and colonization traitscan lead to a rapid increase of function with initialcolonization and result in a saturating form of BEFrelationship. A negative relationship between coloniza-tion and effect traits could cause an accelerating upwardcurve in ecosystem function with increasing speciesnumber. A humped effect�colonization traits relationcould lead to a sigmoid biodiversity�function relation-

ship. Currently, we do not know which of thesescenarios are more realistic; observational studies onspecies diversity and ecosystem processes in commu-nities of early succession stages (where immigration isone of most important determinants of communitystructure) might help answer this question.

Acknowledgements � This work was supported by the State KeyBasic Research and Development Plan (2007 CB106802), theNational Natural Science Foundation of China (30628005)and Beijing Normal Univ. We are grateful to Dr. TadashiFukami for their very useful comments.

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Appendix 1.

Separating complementarity and selection effects by‘additive partitioning’ method. (Available online asAppendix O15988 at www.oikos.lu.se)

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