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
MPD 1 9.67 3 1011 0.002 0.002 0.97SR 1 9.47 3 1015 19.9 14.77 0.003MPD 3 SR 1 4.31 3 1015 8.7 6.72 0.01Error (residuals) 59 4.97 3 1016
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).
PATRICK A. VENAIL AND MARTHA J. VIVES2532 Ecology, Vol. 94, No. 11
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
MPD 1 1.98 3 1016 0.2 0.11 0.75SR 1 9.57 3 1017 7.8 5.06 0.03MPD 3 SR 1 7.61 3 1017 6.5 4.03 0.046Error (residuals) 59 1.27 3 1019
Complementarity effect
MPD 1 8.1 3 1014 1.1 0.85 0.36SR 1 9.83 3 1015 13.2 10.35 0.002MPD 3 SR 1 1.05 3 1016 14.1 11.05 0.002Error (residuals) 59 7.43 3 1016
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).
November 2013 2533BIODIVERSITY AND ECOSYSTEM FUNCTIONING
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.
PATRICK A. VENAIL AND MARTHA J. VIVES2534 Ecology, Vol. 94, No. 11
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).
PATRICK A. VENAIL AND MARTHA J. VIVES2536 Ecology, Vol. 94, No. 11