Phylogenetic distance and species richness interactively affect the productivity of bacterial communities

Ecology, 94(11), 2013, pp. 2529–2536� 2013 by the Ecological Society of America

Phylogenetic distance and species richness interactively affect theproductivity of bacterial communities

PATRICK A. VENAIL1

AND MARTHA J. VIVES

Centro de Investigaciones Microbiologicas (CIMIC), Universidad de los Andes, Carrera 1 No 18A-10, Bogota, Colombia

Abstract. Our understanding of how biodiversity influences ecosystem functioning isentering a new stage of its development through the incorporation of information about theevolutionary relatedness of species. Bacteria are prime providers of essential ecosystemservices, representing an excellent model system to perform biodiversity–ecosystem functionresearch. By using bacteria isolated from petroleum-contaminated sites, we show thatcommunities composed of poorly related species were more productive than those containinghighly related species. The nature of the forces controlling this positive effect of phylogeneticdiversity on community productivity depended on the number of species in culture. Incommunities of two species the positive effect of phylogenetic diversity on productivity wasdriven by changes in the selection effect. Communities of two distantly related species weredominated by the most productive species in monoculture, whereas communities of twoclosely related species were dominated by the less productive species in monoculture. Incommunities of four species the positive effect of phylogenetic diversity on productivity wasdriven by changes in the complementarity effect. In communities composed of four distantlyrelated species the influence of positive interactions such as facilitation, cross-feeding, andniche partitioning seemed to outweigh the influence of negative interactions such asinterference. As a consequence the proportion of species favored by the presence of otherspecies increased as they became less related. Multiple facets of biodiversity may influenceecosystem functioning. Here, we present evidence of an interaction between phylogenetic andtaxonomic diversity on community productivity, underlining the importance of consideringmultiple aspects of biodiversity when studying its impact on ecosystem functioning.

Key words: bacteria; complementarity effect; ecosystem functioning; phylogenetic distance; selectioneffect; species interactions; taxonomic richness.

INTRODUCTION

Over the last two decades, great efforts have been

focused in understanding the relationship between

biodiversity and ecosystem functioning (BEF; Cardinale

et al. 2012). The study of this relationship has been

dominated by the use of species richness as a measure of

biodiversity (Cardinale et al. 2012). Recently, motivated

by the influence of evolution in determining species

ecological traits and the impact this may have on the

structure of ecological communities (Webb et al. 2002,

Wiens et al. 2010), BEF research has started to

incorporate information about the evolutionary rela-

tionships among species (Cadotte et al. 2008, Srivastava

et al. 2012). Under this perspective biodiversity is no

longer measured as species richness only; instead it is

quantified as phylogenetic diversity, which also consid-

ers the amount of evolutionary differentiation among

species in a community (Srivastava et al. 2012).

Phylogenetic diversity is used as a proxy for ecological

differentiation that otherwise may be very difficult to

assess through measuring functional traits. The incor-

poration of a phylogenetic perspective into the study of

the relationship between diversity and ecosystem func-

tioning may be highly beneficial for BEF research,

especially in prokaryotic systems, as it represents a more

reliable quantification of diversity than species richness

(Rossello-Mora and Amann 2001, Vos 2011). The

empirical evidence on the effect of phylogenetic diversity

on ecosystem functioning is mounting (Maherali and

Klironomos 2007, Cadotte et al. 2008, Cavender-Bares

et al. 2009, Flynn et al. 2011, Jousset et al. 2011, Cadotte

et al. 2012), but its potential interactive effects with

other facets of diversity remain unexplored.

Bacteria are essential for many ecological systems.

They control fundamental processes such as nutrient

cycling (Falkowski et al. 2008) and human digestion

(Walter and Ley 2011). They also provide important

ecosystem services such as waste degradation (Bell et al.

2005, van der Heijden et al. 2008), and their inherent

capacity to break down pollutants makes them a major

contributor to the recovery of contaminated environ-

ments (Swannell et al. 1996, Boopathy 2000). For

instance, bioremediation using bacteria has been pro-

Manuscript received 14 November 2012; revised 20 February2013; accepted 8 May 2013. Corresponding Editor: M. C.Rillig.

1 Present address: Institut F.A. Forel, Universite deGeneve, 10 Route de Suisse, CP 416, 1290, Versoix,Switzerland. E-mail: [email protected]

2529

posed as a strategy for treating petroleum contamina-

tion (Boopathy 2000). Thus, given their importance as

ecosystem drivers, bacteria represent an excellent model

system for studying the influence of biodiversity on

ecosystem functioning (Bell et al. 2005, Venail et al.

2008, Jousset et al. 2011).

Here, we experimentally explore the influence of

phylogenetic and taxonomic diversity on the productiv-

ity of bacterial communities isolated from petroleum-

contaminated sites. For this, we isolated and identified a

total of 12 bacterial strains from two petroleum-

contaminated sites in eastern Colombia (Cravo Sur

and Gloria Norte) for which we developed a molecular

phylogeny. Our experimental design allowed us to

manipulate the evolutionary relatedness of bacteria

independently from taxonomic richness and measure

the relative influence of these two facets of biodiversity

on community productivity. We also established at

which extent the effect of biodiversity on productivity

was driven by selection or complementarity effects

(Loreau and Hector 2001). These two major forces are

recognized to control the impact of diversity on

ecosystem functioning (Cardinale et al. 2011). The

selection effect suggests that the performance of a

diverse system is driven by shifts in the dominance of

individual species and their relative contributions to

ecosystem functioning. The complementarity effect

suggests that diversity influences ecosystem functioning

above the expected performance of individual species

through mechanisms such as facilitation and niche

differentiation, underlining the importance of havingmultiple species to ensure ecosystem functioning. Given

the contrasting implications of the selection andcomplementarity effects for ecosystem management,

evaluating their relative contribution to the impact ofbiodiversity on ecosystem functioning is crucial.

METHODS

Isolation of microorganisms

We collected samples of crude oil- (petroleum)

contaminated aquifers from two different explorationsites in eastern Colombia (Cravo Sur and Gloria Norte).

From each site, ;1 L of crude oil and water wassampled and kept in the dark at room temperature

(;158C). After enrichment for 10 days at 308C in M9Minimal Medium (80 g of Na2HPO4-7H2O, 20 g of

KH2PO4, 3 g of NaCl, and 6 g of NH4Cl in 1 L ofdistilled water), bacterial communities were plated in LB

agar plates (10 g of tryptone, 5 g of yeast extract, and 10g of NaCl in 1 L of distilled water). Based on distinct

colonial morphology (see Appendix and Plate 1), sixbacterial strains (hereafter species) were isolated fromeach site. The 12 bacterial species were kept in�808C in

a 10% glycerol solution.

Identification and phylogenetic relationship

The 12 isolated bacterial species were identified by

means of 16S r-RNA sequencing. For this, single-colony16S r-RNA amplification was performed with a PCR

System Icycler, BioRad thermocycler (Biorad Labora-tories, Hercules, California, USA) using primers 27F (50-

AGAGTTTGATCCTGGCTCAG-3 0) and 1492R (50-GGTTACCTTGTTACGACTT-3 0) specific for bacteria,

yielding a fragment of about 1465 bp. Purification,concentration, and sequencing of PCR products were

performed by Macrogen Korea, Inc. (Seoul, Korea)using the same primer pair. Sequences obtained were

compared to database sequences using BLAST (Altschulet al. 1997) and the genus name with higher maximal

identity percentage was retained (Fig. 1). The 12sequences obtained and two outgroups (Deinococcus,Deinococci; Holorubrum, Archaea) were aligned using

Muscle version 3.8.31 (Edgar 2004) to build a smoothedMaximum Likelihood phylogeny using RAxML version

7.2.8 (Fig. 1).

Experimental design

For bacteria isolated from each site (Cravo Sur and

Gloria Norte) we assembled communities of two or fourspecies and cultured all possible species combinations

for a total of 15 different community compositions perrichness level (30 in total per site). Monocultures from

each of the 12 species were also established. Forpolycultures each species composition was replicated

twice and each monoculture was replicated three times.Prior to inoculation, we controlled initial cell abun-

dances by measuring light absorbance at 650 nm and

FIG. 1. Phylogenetic relationships of the 12 bacterial speciesidentified by means of 16S r-DNA sequencing (see Methods:Experimental design for details). Numbers in parenthesesrepresent the order of sequencing. The reference bar at topright represents a 5% gene sequence divergence among strains.Shading represents different major groups of bacteria. Daggers(�) indicate that the bacteria originated at the Cravo Sur site.

PATRICK A. VENAIL AND MARTHA J. VIVES2530 Ecology, Vol. 94, No. 11

properly diluting using sterile media. We inoculated 100

lL of bacterial culture in a substitutive design. Bacteria

were allowed to grow for 10 days at 308C in 15-mL

Falcon tubes (BD Biosciences, San Jose, California,

USA) containing 10 mL of M9 minimal media and 1 g

of UV-sterilized petroleum as the only carbon source.

Pilot experiments revealed that all cultures reached

stationary phases after 10 days. Productivity was

estimated as the number of colony-forming units

(CFU) per milliliter after 10 days. Control tubes

containing no carbon sources (petroleum) revealed

absence of bacteria after 10 days of incubation for all

mono- and polycultures.

Phylogenetic distance

Using the phylogenetic tree generated (Fig. 1) we

calculated the phylogenetic distance between each pair

of species as the sum of tree branch lengths connecting

them (Cadotte et al. 2008). As a measure of phylogenetic

distance independent from species richness we calculated

the mean pairwise distance (MPD) as the average

phylogenetic distance connecting the species in a

community (Webb et al. 2002).

Data analysis

The capacity of visual differentiation among species

based on their colonial morphology (Appendix: Fig. A1)

allowed us to estimate their individual contributions to

community productivity. Thus, we performed the

additive partitioning of diversity effects proposed by

Loreau and Hector (2001). For this, we estimated the

differences in yield between polycultures and monocul-

tures DY as

DY ¼ Y0 � YE ¼ NDRYMþ ½N covðDRY;MÞ�: ð1Þ

The parameter Y0 is the observed yield of a

polyculture, and YE is the expected yield of a polyculture

based on the productivity of species when grown in

monoculture. N is the number of species in the

polyculture; M is the yield of a monoculture; and

DRY is the difference between the observed yield of a

species when in polyculture and its expected yield based

on its performance in monoculture. This means that if a

species performs better in polyculture than would be

expected from its performance in monoculture, its DRY

will be positive. M and DRY represent averaged values

for a community with multiple species. The first term on

the right of Eq. 1, NDRYM refers to the complementar-

ity effect of diversity. It represents the net balance

between any sort of biological processes (either negative

or positive) among species in a polyculture (e.g.,

interference, facilitation, cross-feeding or niche parti-

tioning). A positive complementarity effect suggests a

higher productivity of polycultures relative to values

expected from monocultures. This results because the

relative influence of positive interactions among species

is higher than the relative influence of negative

interactions. A negative complementarity effect suggests

a lower productivity of polycultures relative to values

expected from monocultures. This results because the

relative influence of negative interactions among species

is higher than the relative influence of positive interac-

tions. The second term on the right of Eq. 1, N

cov(DRY, M ) refers to the selection effect of diversity.

It includes a covariance term between the change in

species’ yields (observed minus expected) when grown in

polyculture (DRY) and the yield in monoculture, M. A

negative selection effect indicates that the yield of a

polyculture is dominated by the less productive species

in monoculture. A positive selection effect indicates that

the yield of a polyculture is dominated by the more

productive species in monoculture. When the selection

effect increases, it indicates that species with higher yield

in monoculture are also more favored by the presence of

other species in the polyculture, whereas the less

productive species in monoculture were the less favored

in polyculture.

As a measure of the strength of competition among

species we estimated for each of them its relative yield

(hereafter competition yield, to avoid confusion with

relative yield from Eq. 1), defined as the ratio of species

productivity when cultured alone and when cultured in

the presence of a competitor (Austin et al. 1988):

Competition yieldx ¼Yx monoculture

Yx polyculture: ð2Þ

This is a standard metric used to quantify the strength

of competition among species for which a value above 1

suggests the species performed better in polyculture than

in monoculture. For each polyculture we established the

frequency of finding a species with competition yield

higher than 1.

For each site (Cravo Sur and Gloria Norte) we tested

the effect of phylogenetic distance (mean pairwise

distance, MPD) and number of species (taxonomic

richness) on community productivity (log [CFU] per

milliliter), the selection effect and the complementarity

effect by performing an ANCOVA. We correlated MPD

with the frequency of finding competition yields higher

than 1.

RESULTS

Regardless of the number of species in the culture,

community productivity increased with phylogenetic

distance, either for communities from Cravo Sur (Table

1, Fig. 2a; r2 ¼ 0.29, P ¼ 0.002) or from Gloria Norte

(Table 2, Fig. 2b; r2 ¼ 0.2, P ¼ 0.01). In other words,

communities composed of less related species performed

better than communities of closely related species. MPD

explained 9% and 8.5% of total variation in community

productivity for Cravo Sur and Gloria Norte, respec-

tively, whereas species richness explained 0.07% and 6%of variation in productivity in Cravo Sur and Gloria

Norte, respectively.

When communities with two and four species were

analyzed together, neither the selection nor the comple-

November 2013 2531BIODIVERSITY AND ECOSYSTEM FUNCTIONING

mentarity effects were influenced by phylogenetic

distance (Fig. 3, Tables 1 and 2). However, in both sites

the interaction effect of phylogenetic distance and

species richness on selection and complementarity effects

were significant (Fig. 3, Tables 1 and 2). In communities

with two species the relationship between phylogenetic

distance and selection effect was positive (Fig. 3a; r2 ¼0.3, P¼ 0.03, and Fig. 3b; r2¼ 0.44, P¼ 0.01), whereas

the relationships between phylogenetic distance and

complementarity effect were null (Fig. 3c, d). For

communities with four species the relationships between

phylogenetic distance and complementarity effect were

positive (Fig. 3c; r2 ¼ 0.33, P ¼ 0.03, and Fig. 3d; r2 ¼0.22, P ¼ 0.05), whereas the relationships between

phylogenetic distance and selection effect were null (Fig.

3a, b).

In both sampled sites the proportion of species being

favored by the presence of other species (frequency

competition yield .1) was positively related to phylo-

genetic distance when four species were present in the

communities (Fig. 4a; r2¼ 0.46, P¼ 0.004, and Fig. 4d;

r2¼ 0.28, P¼ 0.03), but was null when only two species

were present.

DISCUSSION

Instead of considering taxonomic richness as the only

facet of diversity influencing ecosystem processes, BEF

studies are now including information on the common

ancestry relationships of species. The rationale is that

phylogenetic diversity, which can be considered a proxy

for ecological differentiation (but see Gravel et al. 2012),

influences the structure and composition of ecological

communities and thus may describe better than taxo-

nomic richness the functioning of an ecosystem. In this

experimental study, we assessed the importance of

phylogenetic distance (measured as mean pairwise

distance) and taxonomic richness (measured as species

TABLE 1. Summary of the ANCOVA results on the effects of phylogenetic distance (MPD) andspecies richness (SR) on community productivity, selection, and complementarity effects ofdiversity for bacteria isolated in Cravo Sur site.

Parameters and effects df SS Percentage explained F P

Productivity

MPD 1 1.06 9 5.58 0.02SR 1 0.01 0.07 0.04 0.84MPD 3 SR 1 0.39 3.3 2.07 0.16Error (residuals) 59 12.08

Selection effect

MPD 1 5.08 3 1014 1.6 1.11 0.3SR 1 1.18 3 1015 3.8 2.58 0.11MPD 3 SR 1 3.57 3 1015 11.6 7.81 0.009Error (residuals) 59 3.09 3 1016

Complementarity effect


Notes: SS is sum of squares; percentage explained is the amount of variation explained.

FIG. 2. The effect of phylogenetic distance (mean pairwisedistance) on bacterial productivity (log [CFU/mL]) for bacterialcommunities, either (a) from Cravo Sur or (b) from GloriaNorte. CFU stands for colony-forming units. Each circlerepresents a polyculture with a different species composition.Solid circles represent communities with two species, and opencircles represent communities with four species. Lines representsignificant correlations (P , 0.05) between phylogeneticdiversity and productivity for communities with two speciesonly (dotted line), with four species only (dashed line), andcombined data sets (solid line).


richness) on the productivity of petroleum-degrading

bacterial communities.

Our results suggest that bacterial communities com-

posed of closely related species were on average less

productive than those with less closely related species.

This is in accordance with previous studies using either

grassland plants (reviewed by Cadotte et al. 2008, Flynn

et al. 2011) or bacteria (Jousset et al. 2011), where a

positive effect of phylogenetic diversity on ecosystem

functioning was observed. Also in accordance with

previous studies, phylogenetic diversity predicted better

ecosystem functioning than taxonomic richness (Cadotte

et al. 2008, Flynn et al. 2011). However, because in those

studies phylogenetic diversity was not manipulated

TABLE 2. Summary of the ANCOVA results on the effects of phylogenetic distance (MPD) andspecies richness (SR) on community productivity, selection, and complementarity effects ofdiversity for bacteria isolated in Gloria Norte site.

Parameters and effects df SS Percentage explained F P

Productivity

MPD 1 0.98 8.5 5.54 0.03SR 1 0.69 6 3.92 0.05MPD 3 SR 1 0.0005 0.004 0.003 0.96Error (residuals) 59 11.6

Selection effect


Complementarity effect


Notes: SS is sum of squares; percentage explained is the amount of variation explained.

FIG. 3. The effect of phylogenetic distance (mean pairwise distance) on the selection (top panels) and complementarity effect(bottom panels) of diversity for bacterial communities, either (a, c) from Cravo Sur or (b, d) from Gloria Norte. Each circlerepresents a polyculture with a different species composition. Solid circles represent communities with two species, and open circlesrepresent communities with four species. Lines represent significant correlations (P , 0.05) between phylogenetic diversity and theselection or complementarity effects for communities with two species only (dotted line) and with four species only (dashed line).


independently from species richness, it was difficult to

establish their relative impacts on ecosystem function-

ing. In a post hoc attempt to separate out the relative

influence of species richness from the influence of

phylogenetic distance on ecosystem functioning, Flynn

and colleagues (Flynn et al. 2011) found that the

observed positive relationship between phylogenetic

diversity and biomass production resulted primarily

from the influence of species richness and its strong

correlation with phylogenetic diversity, not from the

phylogenetic relatedness of species themselves. Thus, the

evolutionary relatedness of grassland species had

actually no effect on community performance. In a

study with bacteria, also based on a post hoc statistical

analysis, Jousset and colleagues (Jousset et al. 2011)

found that the functioning of microbial ecosystems

increased as bacteria were more dissimilar from an

evolutionary standpoint, independently of genotypic

richness. In this case, however, the positive effect of

phylogenetic relatedness on ecosystem function relied on

a higher functional dissimilarity of bacterial genotypes

that resulted in a more efficient use of resources.

Interestingly, the impact of diversity was completely

the opposite when using richness as a measure of

biodiversity. In contrast to these previous studies, our

experiment was deliberately designed to test the influ-

ence of phylogenetic distance per se, independently from

the number of species, providing direct evidence of the

effect of the evolutionary relatedness of species on

ecosystem functioning.

Interestingly, we found that the nature of the forces

underlying the effect of phylogenetic distance on

productivity depended on the number of species present

in a community. When only two species were present,

the positive effect of phylogenetic distance on produc-

tivity relied on an increase of the selection effect. At high

phylogenetic distance (high MPD, i.e., communities

composed of poorly related taxa), species with the

highest performance in monoculture dominated the

polyculture (i.e., positive and high selection effects),

increasing community productivity. In communities of

closely related taxa (low MPD), species with the lowest

performance in monoculture dominated the polyculture

(i.e., negative selection effects), reducing community

productivity. The complementarity effect of diversity did

not respond to evolutionary relatedness when only two

species were present. In communities with four species

the influence of phylogenetic diversity on the selection

effect disappeared. It is possible that competition for

shared resources got stronger when increasing the

number of species, making species equally productive.

Instead, the positive relationship between phylogenetic

distance and community productivity was driven by the

complementarity effect of diversity. In communities

composed of poorly related taxa (high MPD), the

complementarity effect was often positive and the rare

cases of negative complementarity effects were observed

at low to intermediate MPD values. This suggests that as

species were less related, the influence of positive

interactions such as facilitation increased and/or that

the influence of negative interactions such as interference

decreased. This hypothesis was supported by the fact

that phylogenetic distance was positively related to the

frequency of finding species with positive competition

yields, suggesting that as species get less related, the

presence of other species was beneficial for their

productivity. Unfortunately, our study did not include

any direct measurement of positive interactions such as

facilitation or cross-feeding. We strongly believe that the

next generation of BEF experimental studies should

quantify more accurately the relative importance of

these biological mechanisms.

Recent attempts to increase our explanatory power on

the influence of biological diversity on ecosystem

functioning explored the impact of more than one facet

of biodiversity (Cadotte et al. 2008, Flynn et al. 2011,

Jousset et al. 2011, Eisenhauer et al. 2012). So far, the

evidence suggests that different aspects of diversity have

different influences on ecosystem functioning. Our

results present evidence of the complex outcomes that

can be obtained when more than one facet of diversity is

FIG. 4. The effect of phylogenetic distance (mean pairwisedistance) on the proportion of species being favored by thepresence of competitors (frequency competition yield .1),either (a) for bacteria from Cravo Sur or (b) for bacteria fromGloria Norte. Each circle represents a polyculture with adifferent species composition. Solid circles represent communi-ties with two species, and open circles represent communitieswith four species. The dashed lines represent significantcorrelations (P , 0.05) between phylogenetic diversity andthe frequency competition yield .1 for communities with fourspecies only.


incorporated as predictor of ecosystem functioning.

Because there is no reason to believe a priori that all

the facets of diversity may influence ecosystem processes

in the same way, and because we still do not understand

their multiple interactions, it is important for new BEF

research studies to independently manipulate different

aspects of biodiversity. Recently developed consensus

indices or metrics embracing multiple facets of diversity

have been generated (Cadotte et al. 2009, Scheiner

2012). While this may be valuable under specific

circumstances, the complex interactions between species

richness and phylogenetic distance observed here may

serve as an example of its limitations when trying to

understand ecosystem function.

Our study joins previous efforts to understand the

impact of bacterial biodiversity on ecosystem function-

ing (Naeem et al. 2000, Wohl et al. 2004, Bell et al. 2005,

Jiang 2007, Venail et al. 2008, Salles et al. 2009,

Langenheder et al. 2010, Gravel et al. 2011, Jousset et

al. 2011, Becker et al. 2012). However, ours is the first

study to directly manipulate the phylogenetic relatedness

of bacteria, and shows how communities of less related

species reached higher levels of productivity than

communities of closely related species. From a bio-

remediation perspective, the relationship between diver-

sity and petroleum degradation success still needs to be

established. Our results may help in designing more

effective microbial consortia for the recovery of petro-

leum-contaminated sites (Thompson et al. 2005). From

a more broad perspective, this result may be used as an

example of how important it may be to include

information on the evolutionary relationships of species

into the study of ecosystem functioning, with important

implications for management and conservation pro-

grams (Srivastava and Vellend 2005, Balvanera et al.

2006, Chan et al. 2006). Because a frequent goal of

management programs is to increase ecosystem func-

tioning, the shift on the influence of the selection and

complementarity effects on productivity, depending on

the number of species, has major implications for

management purposes. In communities with low taxo-

nomic richness (two species), productivity would be

increased by assembling communities of poorly related

species and through the dominance of the most

productive species in monoculture. In communities with

higher taxonomic richness (four species), productivity

would also be increased by assembling communities of

poorly related species, but through the influence of

positive interactions among species. Our study is a good

example of how the incorporation of multiple facets of

diversity and their potential interactions need to be

considered when debating the importance of BEF

research for conservation purposes.

ACKNOWLEDGMENTS

We thank Maria Camila Orozco and Angela Holguın fortechnical support during the experiment. We also thankVladimir Ramirez from Biomtec for providing samples andthe Facultad de Ciencias for partially funding this project.

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SUPPLEMENTAL MATERIAL

Appendix

Examples of five different colonial morphologies observed (Ecological Archives E094-232-A1).


http://www.esapubs.org/archive/ecol/E094/232/

Documents

Phylogenetic distance and species richness interactively affect the productivity of bacterial communities