Download BIODIVERSITY AND ECOSYSTEM FUNCTION: DO SPECIES

BIODIVERSITY AND ECOSYSTEM
FUNCTION: DO SPECIES MATTER?
Paul S. Giller and Grace O’Donovan
ABSTRACT
Biological communities perform a variety of functions within ecosystems, including regulation of
climatic processes, breakdown of waste, recycling of nutrients, maintenance of soil fertility and
provision of natural resources. Although exact numbers and timescales are difficult to determine, it
is clear that biodiversity (species and habitat richness, genetic diversity and community complexity)
is declining. Studies of biodiversity are thus assuming greater significance as ecologists try
desperately to document global biodiversity in the face of unprecedented perturbations, habitat loss
and extinction rates. How will such decline in biodiversity affect the biosphere and the quality of
human life on the planet? Does biodiversity matter? Internationally, research has begun to
investigate whether the current unprecedented losses in biodiversity will damage the functioning of
ecosystems. This paper reviews this work and highlights the general patterns identified. Scientific
evidence continues to show that, in general, biodiversity does influence the rates or nature of
ecosystem processes, and a majority of studies have found that a reduction in biodiversity does have
a negative effect on ecosystem function. The paper also considers the potential indirect effects of
biodiversity losses on conservation, particularly in relation to fragmentation and critical transition
zones between terrestrial and aquatic habitats.
Paul S. Giller,
Department of Zoology
and Animal Ecology,
University College Cork,
Republic of Ireland
(corresponding author;
e-mail: [email protected]);
Grace O’Donovan,
Department of
Environmental Resource
Management, University
College Dublin, Belfield,
Dublin 4, Republic of
Ireland.
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AND
INTRODUCTION
Currently, there is unprecedented interest in the
earth’s biological diversity, with the year 2001 –2
designated as International Biodiversity Observation Year by a range of international bodies,
including the International Union of Biological
Sciences (IUBS), the Scientific Committee on
Problems of the Environment (SCOPE), Diversitas
and UNESCO among others. At the Earth
Summit in Rio in 1992, more than 150 countries
signed the Convention on Biological Diversity,
which came into force in 1993 and was ratified by
Ireland in 1996. This Convention and a range of
other international conventions and directives
oblige Ireland to work towards establishing legal
and institutional frameworks for the protection and
enhancement of biodiversity and environmental
quality. The state must take measures, by
developing or adapting existing national strategies,
plans and programmes, to ensure the conservation
and sustainable use of biological diversity. In the
Rio Convention, biological diversity is defined as
‘the variability among living organisms from all
sources including, inter alia, terrestrial, marine and
other aquatic ecosystems and the ecological
complexes of which they are part; this includes
diversity within species, between species and of
ecosystems’. Biodiversity must therefore be
considered at three interdependent levels:
ENVIRONMENT: PROCEEDINGS
OF THE
ecosystem diversity, species diversity and genetic
diversity within species.
With advances in science and technology, we
are on the verge of understanding the natural
world while at the same time in real danger of
destroying it. The environment is larger and much
more complex than any man-made machinery, and
the consequences of system failure are thus more
disastrous. Every human activity has some effect on
the natural environment as a whole, and over the
past few decades, there has been a growing
recognition and concern that increasing economic
activity and development carry environmental
costs. Environmental trends such as urban
congestion; increasing waste production and
inadequacies of waste disposal; erosion; global
warming and climate change; and pollution and
ozone depletion —with consequent deterioration
of landscape quality, loss of biodiversity and
habitats and over-exploitation and depletion of
resources —are all symptoms of environmental
deterioration. What we know of past, present and
projected rates of habitat change, species extinction
and human population growth and development
suggests some profoundly disturbing conclusions
about the future of the earth’s biosphere (Gaston
1996).
Environmental policy-making is more or less
genuinely science-based (Porritt 1994) and thus
requires high-quality, objective and informative
ROYAL IRISH ACADEMY, VOL. 102B, NO. 3, 129– 139 (2002). © ROYAL IRISH ACADEMY
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science to underpin it, yet we commonly make
decisions about the management of the
environment with scarcely any adequate
indications regarding environmental trends, the
state of the environment or its response to our
activities. The result is often unforeseen damage,
decreasing productivity and loss of sustainability,
defined as ‘the ability to meet the needs of today
without jeopardising the ability of future
generations to meet their own needs’ (Holdgate
1991). Much more information is required if we
are to optimise responses to the worsening
situation. The development of new technologies
and disciplines, such as GIS and remote sensing,
molecular biology, telemetric remote sampling
equipment, analytical methodologies, controlled
environmental chambers and taxonomic expertise,
has provided many of the necessary tools to make
great strides forward in our understanding of, and
ability to sustainably manage, the natural world.
Never before has ecology been of such critical
importance in tackling the major social and
economic problems that the world faces, and this
role poses challenges to the subject itself as a
scientific discipline. How can we overcome the
bottleneck in our ability to quantify biological
diversity fully? How can we make ecological
predictions at the scale appropriate to the current
and future problems that need to be addressed?
What kind of data do we need to tackle the
problems? What are the important interactions and
ecological processes, and how are they affected by
environmental change and species loss?
Biological communities and their associated
chemical and physical processes are collectively
referred to as ecosystems and perform a variety of
functions, including regulation of climatic
processes, breakdown of waste and recycling of
nutrients, maintenance of soil fertility and
provision of natural resources. These functions in
turn provide to humans, directly or indirectly, a
range of benefits (ecological services) that have
recently been valued at US$33 trillion per year
(Costanza et al. 1997). Living organisms integrate
the effects of many variables within the
environment, and their biological efficiency,
productivity or balance within the ecosystem
indicates the overall health of the system
(Spellerberg 1991). Biodiversity has thus been
promoted to centre stage in national and
international strategies and debates concerning the
environment. Biodiversity studies are increasingly
important at a time when global biodiversity is in
flux, with unprecedented perturbations, habitat loss
and extinction rates. International research efforts
are now focused on answering the question of
whether current unprecedented losses in biodiversity will negatively affect ecosystem functioning (see ‘Nature insight: biodiversity’, Nature 405
(2000), 207–53).
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ENVIRONMENT
Concern has usually been focused on what the
entities of biodiversity are and where they are,
with increasing concentration on the most diverse
and understudied habitats, e.g. tropical rainforests
or deep-sea and hydrothermal vents. The soil, for
example, is perhaps one of the most understudied
of habitats, yet it is probably also one of the most
diverse (Giller 1996) and has only recently received
significant attention (Brussaard et al. 1997; Wall
Freckman et al. 1997; see also BioScience 50 (12)
(2000): special issue on soil and sediment
biodiversity). Ecologists have also been studying
systems for a long time and getting a better idea of
biodiversity levels. For example, the bestdocumented stream system is the Breitenbach
stream near Schlitz in Germany, where Joachim
Illies, Peter Zwick, Rudiger Wagner and others
have been sampling entire animal communities for
over 25 years. Allan (1995) offered a compilation
of the data, showing that 642 insect species
(including 476 dipterans, 70 coleopterans and 57
trichopterans),
and
446
non-insect
taxa
(approximately half of which were nematodes and
rotifers) had been recorded.
Despite the obvious widespread interest in,
and importance of, biodiversity, estimates of the
number of species on earth are vague. Larger
organisms are relatively well studied, but it is
among the invertebrates, particularly insects and
marine invertebrates, that much remains to be
done to develop a more complete systematic
knowledge and to understand the taxonomic
relatedness of species. By the beginning of 1988,
1.82 million species had been named, including
9,020 birds, 18,818 fish, 225,000 plants and
approximately one million insects (Rosenzweig
1995), but estimates of the likely total number
range from 5 million to 30 million. In the 1995
book Global Biodiversity Assessment, Hammond
suggests a conservative estimate of around 14
million species (Hammond 1995). In fact, this
figure represents merely a fraction of all species
that have ever existed. Mass extinctions have
occurred in the past, brought about by natural
catastrophic environmental change, and have
generally been followed by bursts of speciation. In
recent years, however, we have been witnessing
another dramatic drop in biological diversity as a
result of human activity, with both species
extinctions and gene pool declines occurring at
rates unprecedented in the earth’s history
(Spellerberg and Hardes 1992). Recent estimates
put the total number of recorded extinctions
(mostly vertebrates) at around 1,100 species since
1600, but the rate of extinction rose dramatically
over the last century, with global loss estimates
varying between 1% and 11% (Jenkins 1992).
Absolute rates of species loss in rain forests are
1,000 to 10,000 times the level before human
intervention (Vitousek et al. 1997), and it is also
BIODIVERSITY
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estimated that we could lose 50% of total biotic
diversity in the next 100 years (Soule 1991).
DOES BIODIVERSITY MATTER?
Although exact numbers and timescales are
difficult to determine, it is clear that biodiversity
(species and habitat richness, genetic diversity and
community complexity) is declining. How will
such a decline in biodiversity affect the biosphere
and the quality of human life on the planet? Does
biodiversity matter? Despite the conceptual
simplicity of this question, it has been difficult to
study in the real world. There is now general
acceptance that ‘biodiversity per se is a good thing,
that its loss is bad and that something should be
done to preserve it’ (Gaston 1996). This is so for a
number of reasons (Spellerberg and Hardes 1992;
Kunin and Lawton 1996; Oksanen 1997; O’Neill
1997), including the following:
“
“
“
“
“
We have a moral and ethical responsibility to
preserve life on earth.
Biodiversity has aesthetic value.
Biodiversity has monetary and utilitarian value,
through provision of drugs, food, genes,
industrial processes, etc.
Biodiversity provides a useful measure of the
quality of the environment and of the
probability of sustainability.
Biodiversity has ecological value, through
provision of ecosystem services, including
maintenance of atmospheric composition and
biogeochemical cycles, soil binding, soil
fertility, decomposition and disposal of wastes,
production, pest control and water purification.
It is this relationship between biodiversity and
ecosystem functioning that has recently become a
focus of ecological research (Hector 2000), for
three reasons. Firstly, concern is growing that the
high rates of species extinction described earlier
could be detrimental to the ecosystem services.
Secondly, enhancing biodiversity in agricultural
systems may improve their performance and
productivity and decrease inputs of energy,
fertilisers and pesticides. Thirdly, experimental
manipulation of biodiversity is intrinsically valuable
as a means of improving our understanding of
the structure and functioning of ecological
communities.
HYPOTHESES RELATING BIODIVERSITY
TO FUNCTION
A meeting of experts in Germany in the early
1990s resulted in an edited volume of papers on
the nature of the relationship between biodiversity
and ecosystem function (Schultze and Mooney
ECOSYSTEM FUNCTION
1993), and this made it clear that, at that time, we
knew embarrassingly little. Thus, over the last few
years research has focused on the question of
whether the loss of biodiversity will negatively
affect the functioning of ecosystems (Naeem et al.
1996; Tilman et al. 1996; 1997; Grime 1997;
Tilman 1997; Hector et al. 1999; Loreau et al.
2001). Possible interactions of biodiversity with
ecosystem processes include the following:
“
“
“
Biodiversity may support specific processes:
communities with high biodiversity may
contain specialists that are absent in less diverse
ones, e.g. pollinators of certain plants.
Biodiversity may influence rates of ecosystem
processes, with increasing, decreasing or
stabilising rates.
Biodiversity may influence standing stocks,
biomass or production.
A diverse array of hypotheses has been
proposed to predict the effect of species loss on
ecosystem function (Erlich and Erlich 1981;
Lawton 1994; Walker 1992; Naeem et al. 1995 and
others (see also Johnson et al. 1996; Martinez 1996;
Stiling 1999)). Although these hypotheses are not
mutually exclusive, and do overlap to a greater or
lesser extent, the major features can be illustrated
by plots of the predicted relationships between
biodiversity and function rate (Fig. 1). The
following are the major hypotheses:
(i) The null hypothesis suggests that there is no
relationship at all between biodiversity and
ecosystem function.
(ii) The rivet hypothesis suggests that every
species plays a role in ecosystem function
and that all species have an equal and
additive effect on function; hence, all species
matter.
(iii) The modified rivet hypothesis predicts that, as
resources are finite, at some point the
relationship must saturate; hence, the curve
rises asymptotically.
(iv) The redundant species hypothesis predicts a
more strongly saturating relationship
between biodiversity and function. Above
the saturation point, species can be lost
without significant effect on ecosystem
function, i.e. not all species matter, so some
species are redundant. Implicit in this
hypothesis is that other species can take over
the role of, or compensate for, lost species.
(This may be related to the notion of
functional groups, whereby species within a
group may be lost without effect, but loss of
a group itself results in significant loss of
function.)
(v) The keystone species hypothesis holds that
keystone species by definition are not
redundant. These are defined as species
whose effects on the community or
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ecosystem are much larger than expected on
the basis of abundance. If large changes
occur in abundances or composition of a
community when a species is removed, the
species is known as a strong interactor; if
not, it is a weak interactor. As strong
interactors are fewer in number than weak
interactors, biodiversity per se may not be
critical to function, but the presence or
absence of a keystone species is. The
question remains, however, as to whether
keystone species are keystone (strong
interactors) throughout their range.
(vi) The uniqueness hypothesis is related to the
keystone hypothesis. When a species is lost,
a particular function of the ecological system
is also largely eliminated. This hypothesis
relates particularly to ecological engineers,
e.g. beavers.
(vii) The idiosyncratic hypothesis suggests that
changing the number of species influences
ecosystem processes, but no obvious pattern
is evident; hence, the role of biodiversity is
unpredictable.
Some inverse relationships are also possible
between biodiversity and ecosystem function:
(viii) The inverse rivet hypothesis suggests that an
increase in biodiversity leads to a
proportional decrease in function. Examples
include a vegetation effect on water yield
from a catchment, whereby increasing
biodiversity and biomass lead to a decreasing
water yield and a situation in which
production levels of a crop plant in an
agricultural habitat are maintained only by
use of pesticides, herbicides and fungicides
to eliminate consumers, parasites and
competitors.
(ix) The gradual decline parabolic (Type 6 ) curve
describes a relationship whereby an increase
in biodiversity gradually reduces some
processes, e.g. the relationship between
diversity of plants and microbes and
inorganic matter in soil (Martinez 1996).
The relationships are dependant to a large extent
on the process or function in question and on the
target species or set of species. There is still no
consensus on the relative merits or validity of the
relationships between biodiversity and ecosystem
processes, but empirical evidence is growing.
EMPIRICAL EVIDENCE OF
RELATIONSHIPS
What has the scientific evidence shown? In
general, biodiversity influences the rates or nature
of ecosystem processes, and a majority of studies
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Fig. 1 —Pictorial representation of the various
hypotheses linking biodiversity to ecosystem function.
have found that a reduction in biodiversity has a
negative effect on ecosystem function (Schmid et
al. 2000; Bolger 2001; Loreau et al. 2001). A range
of examples are given in Table 1. In particular,
biodiversity has been demonstrated to maintain
and increase predictability (McGrady-Steed et al.
1997), reliability (Naeem and Li 1997), invasibility
(Symstad 2000), process efficiency (Heneghan et al.
1999), productivity (Hector et al. 1999) and
sustainability (Tilman et al. 1996). Most of these
studies were undertaken on terrestrial plant
communities and involved the measurement of
nutrient uptake, changes in carbon dioxide levels
or gain in biomass. A survey of the effect of plant
diversity on productivity (Schläpfer and Schmid
1999) showed positive relationships (log–linear or
linear) in thirteen of seventeen studies. Similarly,
Schwartz et al. (2000) found biodiversity effects on
ecosystem processes in 95% of the manipulation
studies they identified and reviewed; the effects
were predominantly saturating (tending towards
the redundant hypothesis). Both comparative and
experimental studies thus suggest that a large pool
of species is required to sustain the assembly and
functioning of ecosystems in landscapes that are
subject to increasingly intensive land use (Loreau et
al. 2001).
In contrast, few studies on the role of
biodiversity in ecosystem function have been
undertaken among animal communities (Mikola
and Setala 1998; Heneghan et al. 1999; Jonsson and
Malmqvist 2000; Jonsson et al. 2001), but apart
from Mikola and Setala (1998), they seem to show
BIODIVERSITY
AND
ECOSYSTEM FUNCTION
quite strong positive relationships (Table 1). A more
detailed look at a few of these studies can be
instructive. Naeem et al. (1995) published results of
the first experimental study to investigate the
biodiversity – function relationship. The Ecotron is
an elaborate set of fourteen controlled environment
chambers, in which replicated terrestrial
communities of 9, 15 and 31 species were
established across four trophic levels that differed
only in biodiversity. Decomposers included
earthworms and Collembola; primary producers
were annual plants; herbivores included aphids,
white flies, snails and slugs; and parasites that
attacked the insect herbivores represented the top
trophic level. The processes measured included
community respiration, decomposition and nutrient
retention and productivity. The results were clear.
Productivity increased by two to three times as
biodiversity increased (close to the rivet hypothesis).
Other processes indicated idiosyncratic responses or
redundancy at low levels of species richness.
A more recent microbial study in aquatic
microcosms was also carried out by Naeem et al.
(2000). Decomposers transfer organic nutrients into
inorganic forms through mineralisation, which
provides the main pathway of inorganic nutrients to
producers. Decomposers cannot acquire carbon
from organic sources, but they can transform
organic carbon from sources supplied by producers
as exudates or dead organic matter. Laboratory
experiments were based on manipulations of species
richness of unicellular green algae and heterotrophic
bacteria and on measurements of algal production,
decomposer production and carbon-source usage
from 95 different sources. Increasing producer
diversity led to increasing productivity, increasing
bacterial richness led to increased bacterial
production, and increasing both bacterial and algal
richness increased both algal and bacterial
production. The number of carbon sources used
was positively correlated with decomposer diversity,
and algal production was shown to be a joint
function of both algal and bacterial diversity. This
type of study shows the value of laboratory
microcosms in unravelling complex relationships
between biodiversity and function through the kind
of manipulations that are impossible in the field.
However, this approach and that of the
Ecotron have been challenged because they are
solely laboratory-based. One of the first field-based
studies centred on grasslands in Cedar Creek,
Minnesota, USA, where Tilman and co-workers
have been studying relationships between function
and biodiversity since the early 1990s. Earlier studies
suggested that increased biodiversity led to increased
drought resistance and resilience (Tilman and
Downing 1994). Later studies (Tilman et al. 1996)
involved much larger experiments, with 147 plots
sown with 1, 2, 4, 6, 8, 12 or 24 species and 20
replicates per treatment. The species sown were
drawn randomly from the 24-species pool. The
results demonstrated clearly that the more diverse
the community, the greater the productivity and the
more efficient the system was at using nutrients.
These patterns matched those in natural
communities in the area.
Table 1 — Examples of diversity–function relationships.
System
Authors
Ecotron study
Grassland
Mycorrhizal fungi
Naeem et al. 1995
Tilman et al. 1994
van der Heijden et al. 1998
Microbial mesocosms
Naeem and Li 1997
Aquatic microbes
McGrady-Steed et al. 1997
Soil microarthropods
Semi-natural grasslands
Aquatic microbes
Heneghan et al. 1999
Hector et al. 1999
Naeem et al. 2000
Stream detritivores
Jonsson and Malmqvist 2000;
Jonsson et al. 2001
Englehardt and Ritchie 2001
Wetland macrophytes
Effects of increasing diversity
Productivity increased
Drought resistance enhanced
Plant diversity, nutrient capture,
productivity increased
Ecosystem reliability enhanced (and
insurance)
More predictable (less variable)
community, respiration
Decomposition rate increased
Production increased
Increase in productivity and in the
number of carbon and algae sources
utilised
Increased litter decomposition by stream
invertebrates
Algal and total plant biomass increased,
phosphate loss decreased
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One problem to date has been that
experiments such as those at Cedar Creek have
been restricted to single locations or laboratories,
thus limiting the ability of researchers to generalise
and predict. This problem has been overcome to a
great extent by a large-scale experimental study
called BIODEPTH, based on common experiments in semi-natural grassland communities in
eight different locations around Europe (Hector et
al. 1999; 2002). Plant diversity was manipulated
directly in the field by establishing plant
communities of different species richness and of
planned functional diversity from seed. A total of
480 experimental plant communities were
established with three functional groups (grasses,
legumes and herbs), and a range of parameters
were measured, including production, decomposition, invasibility, use of space, associated
insect diversity and nutrient retention.
The general results for production across all
sites (published by Hector et al. 1999) suggest
multiple control of productivity of experimental
plant assemblages by geographical location,
number and type of plant species and number and
type of functional groups. The detailed pattern
differed somewhat among locations: for example,
the Greek site data supported the null hypothesis,
whereas the data from several others supported the
redundant species hypothesis (including the Irish
site at Riverstick, Co. Cork (Fig. 2), and the UK
site at Silwood) or the rivet hypothesis (Portugal,
Switzerland). Overall, however, a similar log–
linear reduction in above-ground production was
seen with loss of species (Hector et al. 1999). For a
given number of species, communities with fewer
functional groups were also less productive. The
number of species and number of functional
groups were roughly similar in the strength of their
effects on production. These patterns occurred
along with differences in geographical location
and differences in species composition, thus
representing a very powerful test of the
biodiversity–function relationship.
Data on the effect of biodiversity on herbivory
were also investigated at the County Cork site.
The expectation is that increasing plant species
richness may lead to a reduction in herbivory of
any particular plant species, owing to greater
heterogeneity of the herbivore’s trophic resources:
the concept of apparency. Indeed, results in our
study support this (Fig. 3a). Similarly, pathogen
infection (Fig. 3b) and invasibility (Fig. 4) both
declined with increasing biodiversity, but the
response for decomposition was idiosyncratic. No
effect of plant species richness on decomposition
was found at other sites (e.g. Hector et al. 2000a).
Caution in interpretation of biodiversity– function
results has been urged by Huston and colleagues
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Fig. 2 —Relationship between species richness and peak
above-ground biomass over the three-year study period
at the BIODEPTH Riverstick study site in Co. Cork,
Ireland (data from J. Finn, R. Harris, P. Giller, G.
O’Donovan and J. Good).
(Huston 1997; Huston et al. 2000), especially with
regard to biodiversity–production relationships.
Plant communities are usually dominated by
individuals of the largest species. Hence, the
likelihood of selecting a species of high growth,
biomass or production in a treatment is likely to
increase with increasing species richness— the
so-called ‘sampling effect’. A pattern of increasing
production with biodiversity may thus be nothing
more than the result of an increasing probability
that the community will include and become
dominated by the most productive species as
biodiversity increases. However, this may be
viewed as the simplest possible mechanism linking
biodiversity with ecosystem functioning.
We can overcome such criticism in number of
ways (Hector 1998; Loreau 1998; Hector et al.
2000b; Loreau and Hector 2001). The relative
yield (RY) of a species is its yield in a mixture
expressed as a proportion of its yield in
monoculture, and the relative yield total (RYT) of
a mixture is simply the sum of the individual
species’ RYs. The sampling effect model assumes
an RY of approximately 1 for the dominant
species and therefore an RYT of 1; if the RYT
significantly exceeds 1, this model can be
dismissed. Similarly, if the total biomass of a
mixture of species exceeds that of the monoculture
biomass of the highest-yielding species in the
mixture (the concept known as ‘over-yielding’),
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AND
Fig. 3— (a) Percentage of leaves of Trifolium repens with
insect herbivore damage in plots of different plant
species richness; (b) percentage of leaves of Trifolium
repens with fungal pathogens in plots of different plant
species richness. In both graphs, mean 9SE included
(data from S. Duggan, J. Finn, P. Giller, G. O’Donovan
and J. Good).
the sampling effect can again be overruled (Hector
et al. 1999). This was found to be true in the
BIODEPTH experiment (Hector et al. 1999;
2002; Caldeira et al. 2001; Loreau and Hector
2001) and is considered to be largely due to
complementarity between species in a mixture,
where interspecific competition is reduced through
resource partitioning. In contrast, high intraspecific
competition is found in monocultures. Studies on
animal communities have reached similar
conclusions (e.g. Jonsson et al. 2001). These results
ECOSYSTEM FUNCTION
do not mean that individual species or functional
groups play no part in controlling ecosystem
function— in the BIODEPTH project, the
presence of the legume Trifolium increased
production by 360g m − 2 on average. However, a
consensus is being reached within the research
community that complementarity does occur in
diverse communities, particularly as the
communities develop over time: thus, species
diversity per se does matter (outcome of
discussions at an NSF/DIVERSITAS/LINKECOL
workshop on biodiversity and ecosystem function
in Paris, December 2000) (Loreau et al. 2002; see
also Loreau et al. 2001).
However, not all studies have been so unequivocal in terms of the biodiversity–ecosystem
function relationship, particularly those based on
terrestrial decomposition processes. The frequently
complex experimental designs and relatively
short-term experiments have sometimes generated
equivocal results, making them difficult to
interpret. Of 21 studies on the effects of plant
diversity on mineralisation/decomposition, 5
produced idiosyncratic responses, 6 negative
relationships (most curvilinear), 3 positive
relationships and 7 no relationships (Schmid et al.
2000). These studies may be, to some extent,
examining the wrong group of organisms, and
perhaps relationships between microbial diversity
and decomposition are more appropriate, although
plant diversity may enhance microbial diversity
(Giller 1996) and would thus be expected to
enhance decomposition rates. The relationship
between
biodiversity
and
invasibility
is
theoretically predicted to be negative, and
empirical studies tracking the assembly of
communities have generally suggested that
communities decline in invasibility over time as
species accumulate (Levine and D’Antonio 1999).
Constructed/experimental community studies,
however, have found both positive and negative
effects in both the field and microcosms (Levine
and D’Antonio 1999; Levine 2000; Hector et al.
2001).
Does this mean that biodiversity does not
matter for certain ecosystem functions or under
certain situations? Other hypotheses relating
biodiversity to stability may help with the answer.
OTHER HYPOTHESES RELATING
BIODIVERSITY AND FUNCTION
An additional value of biodiversity is as an
insurance against future change—the so-called
‘insurance hypothesis’ (Walker 1992; Yatchi and
Loreau 1999) or ‘portfolio effect’ (Tilman 1999).
The well-established biodiversity–stability hypothesis (see McCann 2000) introduced the
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notion that increasing the number of trophically
interacting species in a community should increase
the collective ability of member populations to
maintain their abundances after disturbance (i.e.
high resistance) or to recover quickly from a
disturbance (i.e. high resilience). It is suggested that
more-diverse ecosystems are more likely to contain
some species that can withstand environmental
perturbations and thus compensate for functional
loss of other species that are reduced or eliminated
by the perturbation.
Tilman and Downing (1994) concluded that
primary productivity is more resistant to, and
recovers more quickly from, a drought
perturbation in more-diverse communities. Other
experiments have concluded that the positive
biodiversity– stability correlation is not purely a
species effect but is related more to functional
diversity (McCann 2000). Field tests at the scale of
the food web are also few in number. One
example (McNaughton 1985) tested seven
stability– biodiversity measures in the Serengeti
grazing ecosystem under strong seasonal variations
and found that five of the seven measures were
positively related to biodiversity, but again it
appeared that functional diversity was more
important than species diversity. Microcosm
experiments have also tended to agree that
biodiversity is positively related to ecosystem
stability (McCann 2000). The two main
explanations for these responses are that (a)
increasing biodiversity increases the chances that at
least some species will respond differentially to the
environmental fluctuations and disturbances, and
(b) greater biodiversity increases the chance that
the ecosystem will have some functional
redundancy in the form of species capable of
functionally replacing other important species.
Taken together, these two ideas form the insurance
hypothesis (McCann 2000). Overall, experimental
studies are rare, and the crucial question of how
critical biodiversity is for resilience and resistance
of communities and ecosystem processes remains
largely unanswered at present. This represents a
major area for further research.
CONSERVATION ISSUES
In addition to the purely ecological and theoretical
insights arising from the study of relationships
between biodiversity and ecosystem function and
stability, some pragmatic issues also arise with
direct relevance to conservation. The redundant
species hypothesis has been used to discuss
priorities for species conservation (Gitay et al.
1996). However, as Covich (1996) points out,
establishing habitat protection policies based on
those species that provide the essential ecosystem
136
ENVIRONMENT
Fig. 4 —(a) Invasibility of plant communities of different
species richness; (b) invasibility in relation to the total
percentage plant cover of plots in Fig. 4a. Invasibility
was measured as the number of weed species found
growing in the plots (data from S. Duggan, J. Finn, P.
Giller, G. O’Donovan and J. Good).
functions is complex and very much limited by our
knowledge gaps as well as by our ability to deal
with timescales appropriate to both ecological and
evolutionary processes. Until we have a fuller
appreciation of the different roles that species play
under different environmental conditions, any such
approach will probably fail. However, we are
simply unable to assist all species under threat, so
priorities are essential. One possibility lies in the
identification of ‘biodiversity hotspots’ — areas of
extreme biotic diversity. Recent research has
suggested that up to 44% of all species of vascular
plant and 35% of all species in four major
vertebrate groups (mammals, birds, reptiles and
BIODIVERSITY
AND
amphibians) are confined to 25 hotspots that
occupy only 1.4% of the earth’s land surface
(Myers et al. 2000). Concentration of effort in such
areas may be the most pragmatic way forward at
present, although this approach may be hindered
by the fact that species-rich areas for different types
of taxa frequently do not coincide (Prendergast et
al. 1993; Gaston and Williams 1996). In addition,
in 1995, nearly 20% of the world’s population
were living within an area that covers about 12%
of the earth’s land surface and includes all of these
hotspots (Cincotta et al. 2000).
There are two further conservation-related
research areas that are worth mentioning, in both
of which the biodiversity– ecosystem function
debate is relevant.
FRAGMENTATION
We have seen that biodiversity can have profound
effects on ecosystem processes. We also know that
area plays a major role in controlling species
richness through the species–area relationship.
One of the major conservation concerns at present
is habitat fragmentation, which involves both
reduction in area and increasing isolation of
habitats. The resulting loss of species may therefore
be compounded by subsequent loss of function
within the fragmented system. Fragmentation is
particularly dramatic in forests and can disrupt
biological functions that maintain biodiversity,
such as pollination, seed dispersal and nutrient
recycling mediated largely by insects (Didham et al.
1996). For example, fragmentation of forests in
central Amazonia has led directly to a decline in
the species richness and abundance of pollinators
and indirectly to changes in their behaviour and
flight patterns (Powell and Powell 1987), and in
Sweden, plant reproductive success has declined
with increasing forest fragmentation (Jennersen
1988). Likewise, in dung beetle communities, a
sharp decrease in the rate of dung decomposition
has been reported with increasing fragmentation,
again in central Amazonia (Klein 1989). Similar
changes are likely to be occurring in many other
habitats subjected to fragmentation.
CRITICAL TRANSITION ZONES
The role of biodiversity in the functioning of
critical transition zones (or ecotones) also needs to
be examined. Ecotones are zones that form an
interface between major terrestrial and aquatic
habitats (Wall Freckman et al. 1997), for example
between soils and groundwaters or between land
and freshwater habitats. Many of these zones,
especially riparian zones along rivers, have been
ECOSYSTEM FUNCTION
under significant threat because of changes in
landscape management and intensification of
agriculture and forestry. Natural riparian zones are
among the most diverse and complex of terrestrial
habitats and contain valuable water resources and
biota in their own right (Naiman and Decamps
1997). The linear nature of lotic ecosystems
enhances the importance of riparian zones, which
constitute one of the most dynamic portions of the
landscape, forming mosaics of land forms,
communities and environments (Gregory et al.
1991). These zones play an immensely important
role in the functioning of adjacent ecosystems, but
we know very little about the biodiversity of the
zones or the way in which such biodiversity
influences their role in the movement of energy,
nutrients, particles and organisms from one
ecosystem to another. Again, they represent prime
candidates for future research.
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