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Ecology: Larger islands house more bacterial taxa

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Thomas Bell
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Duane Ager at Oxford Molecular Biosensors
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Ji-Inn Song
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Jonathan A Newman at Wilfrid Laurier University
Jonathan A Newman
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Abstract

The power law that describes the relationship between species richness and area size is one of the few generalizations in ecology, but recent studies show that this relationship differs for microbes. We demonstrate that the natural bacterial communities inhabiting small aquatic islands (treeholes) do indeed follow the species-area law. The result requires a re-evaluation of the current understanding of how natural microbial communities operate and implies that analogous processes structure both microbial communities and communities of larger organisms.
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Larger Islands House More
Bacterial Taxa
Thomas Bell,
1,3
Duane Ager,
2
Ji-Inn Song,
2,4
Jonathan A. Newman,
3
*
Ian P. Thompson,
2
Andrew K. Lilley,
1
Christopher J. van der Gast
2
.
The relationship between species richness and area
size is one of the few generalizations in ecology,
but recent studies show that the slope of the
relationship differs for microbes (1, 2). Here we
show that the slope of the taxa-area relationship
for natural bacterial communities inhabiting small
aquatic islands is comparable to that found for
larger organisms. The result implies that analo-
gous processes structure both microbial commu-
nities and communities of larger organisms.
Several mechanisms explain how the number
of taxa can increase with the size of the area. The
number of taxa in a particular area results from the
balance between the colonization of new taxa and
the extinction of extant taxa. The size of the area
influences the rate of colonization and extinction
and so indirectly influences biodiversity. Alterna-
tively, if taxa are adapted to a particular habitat,
then larger areas likely contain more habitats and
therefore more species. Finally, a taxa-area re-
lationship will appear if more effort is devoted to
sampling larger areas, because the number of taxa
discovered increases with sampling effort (3). The
relationship between diversity and island or
sampling area size is well described by the
equation S 0 cA
z
,whereS is the number of
species, c is an empirically derived taxon- and
location-specific constant, A is the size of the
area, and z is the slope of the line. The value for
z is generally consistent across taxa but differs
between islands (z È 0.3) and areas of con-
tiguous habitat (z È 0.1) (3).
Recent work has suggested that, although there
appears to be a similar relationship between
microbial diversity and area, the slope z for
microbial taxa (z È 0.02 to 0.07) falls well
below that observed for taxonomic groups of
larger organisms (1, 2, 4). Many microbial taxa
appear to be ubiquitous (5), so increasing the area
of a survey results in only a marginal increase in
the species richness of the sample. However,
these studies have investigated the taxa-area re-
lationship only within single contiguous habitats,
where it is plausible that constant colonization
from adjacent areas rapidly homogenizes the
community. The slope of the species-area re-
lationship is expected to be steeper on discrete
islands, partly because they present a partial barrier
to colonization. We predicted that the slope of
species-area relationship for insular bacterial
communities would be similar to that found for
communities of larger organisms.
The Bislands[ that we used are water-filled
treeholes, a common feature of temperate and
tropical forests. Rainwater accumulates in bark-
lined pans formed by the buttressing at the base
of large European beech trees (Fagus sylvatica)
to form small but often permanent bodies of
water. Each of these islands houses a micro-
ecosystem that derives its nutrients and energy
from leaf litter. We measured the water vol-
ume (island size) and the bacterial genetic
diversity (taxon richness) in 29 treehole
islands, using denaturing gradient gel electro-
phoresis (DGGE) (6), a standard molecular
technique in microbial ecology.
Bacterial genetic diversity in this system
increased with increasing island size according
to the familiar species-area power law (Fig.
1A). The slope z of the relationship (z 0 0.26)
is indistinguishable from published values for
larger organisms (Fig. 1B). The data show that
area size strongly influences the diversity of
these microbial communities.
These results have implications for under-
standing how microbial communities operate and
complement recent studies (1, 2) by indicating
the conditions under which high microbial z
values can occur. In relatively large areas of con-
tiguous habitat, the slope of the species-area
relationship appears to be reduced (Fig. 1B). Such
communities might never approach equilibrium,
because environmental conditions change faster
than competitively inferior species become ex-
tinct. We suggest that treeholes and similar
habitat patches are islands of relative stability
where microbial communities can approach
equilibrium. Under such conditions, the patterns
of abundance and diversity of microbial commu-
nities would be similar to those found for larger
organisms. It is possible that other mechanisms
underlie the difference between our result and
those of other microbial studies. Perhaps, for ex-
ample, the treehole habitat is more heterogeneous,
so diversity increases more rapidly with area size.
What is evident is that, as for larger organisms,
comparatively steep microbial taxa-area relation-
ships are possible.
References and Notes
1. J. L. Green et al., Nature 432, 747 (2004).
2. M. C. Horner-Devine, M. Lage, J. B. Hughes, B. J. M.
Bohannan, Nature 432, 750 (2004).
3. M. L. Rosenzweig, Species Diversity in Space and Time
(Cambridge Univ. Press, Cambridge, 1995).
4. B. J. Finlay, Science 296, 1061 (2002).
5. B. J. Finlay, K. J. Clarke, Nature 400, 828 (1999).
6. Materials and methods are available as supporting
material on Science Online.
7. A. Azovsky, Ecography 25, 273 (2002).
8. Supported by the NERC Centre for Ecology and Hy-
drology. T.B. is supported by the Natural Sciences and
Engineering Research Council of Canada, the Formation
Chercheurs et Aide Recherche and the Clarendon Fund.
Supporting Online Material
www.sciencemag.org/cgi/content/full/308/5730/1884/
DC1
Materials and Methods
References and Notes
22 February 2005; accepted 7 April 2005
10.1126/science.1111318
BREVIA
1
Molecular Microbial Ecology Section,
2
Environmental
Biotechnology Section, Natural Environment Research
Council (NERC) Centre for Ecology and Hydrology,
Mansfield Road, Oxford, OX1 3SR, UK.
3
Department of
Zoology, University of Oxford, South Parks Road, Oxford,
OX1 3PS, UK.
4
Department of Engineering Science, Uni-
versity of Oxford, Parks Road, Oxford, OX1 3PJ, UK.
*Present address: Department of Environmental Biolo-
gy, University of Guelph, Guelph, Ontario N1G 2W1,
Canada.
.To whom correspondence should be addressed.
E-mail: cjvdg@ceh.ac.uk
0.26
2
10
plants
plants
Fig. 1. The species-area relationship for microbial
communities. (A) Bacterial genetic diversity (the
number of DGGE bands, S) in water-filled tree-
holes increases with increasing island size (vol-
ume, V) according to the power law S 0
2.11V
0.26
. There is a similar linear relationship
(not shown) between island surface area (A,in
cm
2
) and bacterial genetic diversity (S 0
3.30A
0.28
, R
2
0 0.38, P G 0.001). Treehole volume
and surface area are correlated (r 0 0.71). (B)
Slope of the species-area relationship for marine
benthic ciliates and diatoms, salt marsh bacteria,
and fungi inhabiting arid soil compared with
slope from the current study. Black bars are
microbial studies (1, 2, 7); gray bars are typical
values for studies with larger organisms (3).
24 JUNE 2005 VOL 308 SCIENCE www.sciencemag.org
1884
on December 1, 2013www.sciencemag.orgDownloaded from
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Article
  • May 1995
Why do larger areas have more species? What makes diversity so high near the equator? Has the number of species grown during the past 600 million years? Does habitat diversity support species diversity, or is it the other way around? What reduces diversity in ecologically productive places? At what scales of space and time do diversity patterns hold? Do the mechanisms that produce them vary with scale? This book examines these questions and many others, by employing both theory and data in the search for answers. Surprisingly, many of the questions have reasonably likely answers. By identifying these, attention can be turned toward life's many, still-unexplained diversity patterns. As evolutionary ecologists race to understand biodiversity before it is too late, this book will help set the agenda for diversity research into the next century.
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  • A Azovsky
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M. C. Horner-Devine, M. Lage, J. B. Hughes, B. J. M. Bohannan, Nature 432, 750 (2004).
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  • J L Green
J. L. Green et al., Nature 432, 747 (2004).