Review
TRENDS in Ecology and Evolution
Vol.20 No.11 November 2005
Linking aboveground and
belowground diversity
Gerlinde B. De Deyn1,2 and Wim H. Van der Putten2,3
1
Department of Integrative Biology, University of Guelph, Guelph, On, Canada, N1G 2W1
Netherlands institute of Ecology, PO Box 40, 6666 GA Heteren, the Netherlands
3
Laboratory of Nematology, Wageningen University and Research Centre, PO Box 8123, 6700 ES Wageningen, the Netherlands
2
Aboveground and belowground species interactions
drive ecosystem properties at the local scale, but it is
unclear how these relationships scale-up to regional and
global scales. Here, we discuss our current knowledge of
aboveground and belowground diversity links from a
global to a local scale. Global diversity peaks towards
the Equator for large, aboveground organisms, but not
for small (mainly belowground) organisms, suggesting
that there are size-related biodiversity gradients in
global aboveground–belowground linkages. The generalization of aboveground–belowground diversity relationships, and their role in ecosystem functioning, requires
surveys at scales that are relevant to the organisms and
ecosystem properties. Habitat sizes and diversity gradients can differ significantly between aboveground and
belowground organisms and between ecosystems.
These gradients in biodiversity and plant community
trait perception need to be acknowledged when studying aboveground–belowground biodiversity linkages.
Introduction
The concept of Von Humboldt, that species diversity
declines with increasing latitude, is considered to be one
of the oldest concepts in ecology [1]. Despite this, the
quantification and interpretation of diversity distribution
patterns for many macroscopic species [2] still causes
debate, and there is only fragmentary information about
the global diversity patterns of microscopic organisms,
many of which live hidden in the soil. Given that soils
sustain life aboveground, a better understanding of the
interactions between aboveground and belowground
biodiversity is needed to predict the potential consequences of biodiversity change for the maintenance of
ecosystem properties [3].
On a global scale, climatic conditions constrain aboveground and belowground biodiversity [2]. Latitudinal
diversity gradients, however, differ for aboveground and
belowground species [4–6] and, therefore, the number of
species interacting aboveground and belowground will
change with global position. Given that aboveground and
belowground subsystems are linked, consequences of
biodiversity loss for ecosystem functioning might depend
on the global position of that ecosystem.
Corresponding author: De Deyn, G.B. ([email protected]).
Available online 8 September 2005
At the local scale, aboveground and belowground subsystems are linked mainly via plants [6]. The number of
species interacting, and their interdependency, will
depend strongly on the spatial and temporal scale considered. For example, a single plant might interact locally
with more species belowground than it does aboveground;
however, the increase in diversity of aboveground organisms interacting with a single plant species throughout its
entire spatial and temporal range might be steeper than
the increase in diversity of belowground species if the
diversity of belowground organisms saturates at smaller
spatial scales [7].
Here, we investigate our current knowledge of aboveground and belowground diversity distribution and the
mechanisms by which they are linked. To frame the
relevance of the study, we explore the consequences of
diversity linkages for ecosystem functioning and discuss
global patterns in aboveground–belowground diversity
distributions. We review the mechanisms of aboveground–
belowground linkages at local scale and discuss how these
might scale up. Finally, we point out some challenges in
the subject of aboveground–belowground diversity linkages and their consequences for the sustainable functioning of terrestrial ecosystems.
Ecosystem functioning and aboveground–belowground
diversity links
Diversity has been thought to be a prerequisite for the
maintenance of stability, resistance and resilience of ecosystem properties [3]. Many empirical studies investigated this hypothesis by studying the effects of changes
in plant diversity on primary production, nutrient retention, invasibility of exotic species, disease outbreaks, or
recovery from abiotic stress [8]. Positive effects of plant
species number on the maintenance of ecosystem properties were merely attributed to complementing abiotic
factors (but see for example [9,10]). Plant characteristics
might be strongly influenced by interactions with aboveground and belowground higher trophic-level organisms
(see [11] in this themed issue of TREE), and these plant
responses can feedback to alter aboveground and belowground trophic interactions. For example, root herbivores
and decomposers can alter plant biomass production and
chemical composition, thereby stimulating herbivore and
parasitoid densities aboveground, as well as flower
visitation and seed production [12]. Complementarity in
www.sciencedirect.com 0169-5347/$ - see front matter Q 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2005.08.009
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Glossary
Arbuscule: complex hyphal branched structure of vesicular arbuscular
mycorrhizal fungus inside plant cells.
Bacterivores: organisms (e.g. nematodes) feeding on bacteria.
Bottom-up: regulation of abundances or biomass by resources.
Complementarity: an interaction whereby a species supplements another
species; for example, complementarity in resource use by a tap-rooted plant
species and a superficially rooted plant species.
Detritivores: organisms feeding on detritus; that is, bacteria, fungi, most
oribatid soil mites, earthworms and many more.
Diversity: a-diversity: species richness within a single community, b-diversity:
change in species composition among different communities in a landscape or
along an environmental gradient, g-diversity: species richness of a landscape
that comprises different communities.
Endophytes: fungi that live inside the plant; often used for fungi inhabiting
aboveground plant parts (although also found in roots), sometimes producing
secondary (anti-herbivore) compounds.
Heterotroph: organism requiring organic compounds as a carbon source.
Microbivorous: feeding on microorganisms.
Mycorrhiza: symbiotic association between roots and mycorrhizal fungi,
exchanging nutrients with plants via arbuscules.
Phoresy: a symbiotic relationship in which one organism transports another
organism of a different species.
Rhizodeposition: the total input of (organic) carbon compounds from the plant
roots into the soil.
Rhizosphere: area immediately surrounding the roots of plants in which their
exudations affect the surrounding microbial flora.
Rhizoplane: part of the rhizosphere comprising root surfaces.
Saprophagous: living on decaying organic matter.
Top-down: regulation of abundances or biomass by antagonists or predators.
plant species traits might be influenced by interactions
with heterotrophic organisms, and might depend on their
diversity, as well as on their trophic complexity [13].
Theoretical studies of how biodiversity might relate to
ecosystem stability are embedded in food-web modelling,
but the approaches differ according to an aboveground or
belowground focus. For soils, detritus-based models focus
on nutrient and energy flow, whereas primary productivity-driven ‘aboveground’ models concentrate on
bottom-up and top-down control effects in aboveground
food chains. These two approaches have now become
merged in a more realistic dynamic food-web approach
that indicates that within-trophic level diversity can
stabilize productivity by enhancing resource use complementarity and by reducing fluctuations in top-down
control of the community as a whole [14,15].
Biodiversity loss aboveground can hamper the topdown control of herbivores and plants, depending on
which species is lost [16], whereas, in soil, many different
organisms are thought to be able to perform similar
functions [17]. However, functional redundancy seems
inversely related to functional dissimilarity of component
species [18]. Therefore, when species diversity declines, it
is likely that species-poor systems will suffer disproportionately when compared with species-rich systems.
Although the soil is extremely species rich, this is not
the case within all functional groups, for example root
symbionts and specific root feeders and root pathogens.
The consequences for ecosystem functioning of species lost
from functional groups that are relatively species poor
might appear faster than when species are lost from
species-rich functional groups such as that of omnivorous
decomposer organisms.
Aboveground–belowground interactions can significantly alter plant productivity and diversity, but little is
known about the consequences of biodiversity for
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Vol.20 No.11 November 2005
community dynamics in aboveground and belowground
food webs and ecosystem properties.
Global and regional aboveground and belowground
diversity patterns
The decrease of terrestrial aboveground biodiversity from
the Equator to the poles [2] has been well established for
larger organisms, such as mammals, birds, amphibians,
plants [2,4] and termites [19]. However, the species
richness of small aboveground invertebrates, including
aphids, bees, sawflies and parasitic wasps [20], and
belowground invertebrate taxa, such as nematodes [5,21]
and earthworms [22], peaks at mid- or high latitudes. Soil
microorganisms (soil bacteria and fungi, of which most
taxa are involved in decomposition and mineralization) for
many years were believed to be omnipresent, leaving local
environmental conditions to determine which taxa are
active (Beyerincks’ law; [23]). This might be true for freeliving microorganisms that are not limited in their
dispersal [24], but it remains doubtful for species
depending on a host or vector for dispersal. Moreover,
recent studies investigating global microbial diversity at a
molecular level suggest that free-living microorganism
taxa are less omnipresent than was previously supposed
[25]. These global biodiversity patterns of species-rich
groups, such as bacteria, fungi and invertebrates, suggest
that the diversity of species involved in aboveground–
belowground diversity linkages is higher in temperate
regions than near the Equator (Table 1). However, the
smaller the organisms, the less data are available on their
diversity and distribution patterns, and the higher the
chance of record bias towards areas with high taxonomist
activity. More global surveys and accurate determinations
are needed to assess global patterns in aboveground–
belowground biodiversity links.
Drivers of global and regional biodiversity patterns
Energy and water
The peak in aboveground biodiversity at the Equator has
been attributed to a corresponding peak in solar energy
and primary productivity [2]. Diversity within [26] and
across trophic levels [13] is strongly correlated with
productivity, but the relationship between diversity and
productivity also depends on spatial scale and on the
trophic level(s) under consideration [27]. At a regional
scale, plant diversity is generally highest at intermediate
productivity [28], but linear positive and negative
productivity–diversity relations have been observed
across geographical scales for aboveground fauna, for
example for birds [29,30], amphibians, reptiles, mammals
and insects [30]. Belowground productivity is strongly
related to the availability of dead organic matter
(detritus), but quality, rather than total biomass of the
detritus, controls the diversity of higher trophic levels [6].
Diversity of competing microorganisms is expected to peak
at ‘intermediate’ abundance or productivity, given lognormal relationships between species number and total
abundance of individuals [31,32]. However, competitive
exclusion might be driving biodiversity aboveground more
than that of microbial diversity belowground, because of
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TRENDS in Ecology and Evolution
Vol.20 No.11 November 2005
627
Table 1. Global diversity (species richness) and distribution patterns of groups of aboveground and belowground organismsa,b
Taxonomic
level
Kingdom
Kingdom
Kingdom
Domain
Organism group
Plantae
Animalia
- Vertebrates
- Insects and myriapods
- Collembola
- Mites
- Earthworms
- Nematodes
Fungi
Bacteria
Global no. of
described
species
270 000
358 800
52 500
963 000
7617
45 231
3500
25 000
72 000
10 000
% known
of expected
Diversity peak
at low latitude
Area surveyed
for gradient
No. of
studies
Refs
84
27
95
1
15
4
50
6
5
1
Yes
Global
Many
Yes
Yes and no
No
Yes or no?
Slightly
No or yes?
Global
Global
Climate
Climate
Climate
Climate
Many
Many to few
Few
Few
Few
Several
No
Global
[2,4,77]
[77]
[2,4,77]
[77]
[34,79]c
[7,34,80]
[22]d
[5,7,21,77]
[23,77]
[24,25,77]
zones
zones
zones
zones
Few
a
Global no. of described species and expected numbers from [77] include terrestrial, fresh water and marine species. Diversity gradients derived from studies in terrestrial
habitats.
b
For a more-detailed table, see Online Supplementary Material. Empty cells indicate that the information is either unknown or not in the public domain.
c
http://www.collembola.org.
d
P. Lavelle, personal communication.
spatial isolation and the dormancy strategies of many soil
organisms [6].
Latitudinal aboveground diversity gradients are asymmetric between the northern and southern hemispheres
[33]. In most of the northern hemisphere and at high
latitudes in the southern hemisphere, ambient energy
restricts plant productivity and plant and bird diversity,
whereas in the southern hemisphere and in low latitude–
high-energy regions in the northern hemisphere water
availability constrains productivity and diversity [4,29].
Whether a similar asymmetry is present in belowground
diversity is not know.
Belowground organism diversity and abundance is also
strongly dependent on water and energy, at least in
extreme environments, such as the poles, where low
carbon input and the restricted availability of liquid water,
and high salinity limit the abundance and diversity of
nematodes and microarthropods [5,34]. However, the
strength and slope of biodiversity correlation with solar
energy and water availability might differ between aboveground and belowground systems when measured over
the same spatial range, given differences in average
energy requirements and tolerance to drought [7,35].
Many soil organisms live in water films, feed on detritus
and have high energetic efficiency owing to their ectothermic physiology [14]. Therefore, life belowground
might relate relatively more to water than does that
aboveground, whereas the opposite can be expected for
solar energy. These ideas, however, need to be more
rigorously tested across latitudinal gradients.
Biogeographical history
Biogeographical history is an important driver of global
patterns in species richness, because it underlies current
environmental heterogeneity [36]. Tectonic drift might
have isolated species, enhancing their speciation and
global diversity. Glaciations, however, might have reduced
the evolution rate of most organisms at higher latitudes
compared with more Equatorial latitudes [36], but little is
known about rates of evolution, centre(s) of origin and
subsequent distribution trajectories of belowground
organisms. Coevolution in aboveground–belowground
species communities occurs in a multitrophic selection
setting of plants, herbivores and antagonists, where
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drivers and passengers can change seats regularly [37].
Some plant adaptations indicating coevolution with
specialist herbivores, pathogens [38], soil bacteria [39]
and pollinators [40] suggest that plants can coevolve with
aboveground and belowground organisms.
Local aboveground and belowground diversity patterns
Aboveground plant and animal diversity generally
increases according to a power function with area [41],
and a similar relationship was recently also found for
bacteria [42,43]; thus, the local diversity of macro- and
microorganisms reflects only a subset of the regional
species pool. Species–area relationships for soil organisms
have been little explored. However, the available data
suggest differential effects of area on different components
of decomposer communities. For example, the linear
increase in species number of earthworms with area size
in Europe compares with those of plants and aboveground
animals [44]. However, in a study of spatially separated
epiphytic islands in the crowns of canopy trees in New
Zealand, the diversity of macrofauna and microarthropods
increased with ‘island’ size, whereas microbial diversity
decreased [45].
Several studies have focused on the effects of plant
species diversity on aboveground or belowground biodiversity, revealing positive [46], neutral or idiosyncratic
patterns [9], or predominantly species-specific relations
[47,48]. Plant species diversity, in turn, can be promoted
by aboveground herbivores [49] as well as by soil organisms [50,51]. However, the effects have rarely been linked
directly to the diversity of heterotrophic organisms, but
rather to the traits of the interacting plants, such as
mycorrhizal dependency and grazing tolerance, and herbivore selectivity. There are only a few examples of how the
diversity of aboveground or belowground organisms can
influence plant diversity and how this, over time, feeds
back to alter diversity above and beneath the soil surface.
In nutrient-poor environments, the diversity of arbuscular
mycorrhizal fungi can stimulate plant diversity and
productivity [52], which could eventually result in the
enhanced diversity of aboveground invertebrate herbivores, or aboveground trophic complexity [10]. Diversity of
aboveground herbivores might affect soil community composition by altering plant community composition and
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TRENDS in Ecology and Evolution
productivity, owing to herbivore selectivity. Therefore,
herbivore selectivity might affect the activity and structure of the soil food web even more than do changes in
plant biomass production [53]. Overall, the number of
studies of local aboveground and belowground biodiversity
are still too limited to reveal any general patterns.
Drivers of local aboveground and belowground
biodiversity links
Productivity distribution
Local biodiversity within a trophic level is driven by
bottom-up (competition for resources) and top-down
(control by predators or pathogens) factors (Box 1). The
strength and overall direction of these control factors
depends on the type of interaction among trophic groups,
both aboveground and belowground [54]. Bottom-up
control of plant species diversity can be strongly
influenced by decomposers and symbionts that influence
mineral nutrient availability and primary productivity
[14,17,51]. The bottom-up control of plant diversity and
productivity via nutrient cycling will depend on the traits
of the plant species pool with respect to complementarity
in nutrient supply to the soil and the acquisition of
minerals and water from the soil [55]. Similarly, the
response of diversity of higher trophic levels aboveground
Box 1. Links between aboveground and belowground
biodiversity and ecosystem functioning: a matter of
functional groups
Understanding relationships between biodiversity and ecosystem
functioning in terrestrial ecosystems requires the coupling of
aboveground and belowground (functional) biodiversity. A possible
approach is the integration of aboveground and belowground
interaction webs and the study of the consequences of diversity
within and between functional groups for ecosystem properties
(Figure 1, main text).
The abundance, activity and diversity of decomposers and
ecosystem engineers are determined predominantly by detritus
quality and soil heterogeneity [6], whereas decomposition rate
depends on functionally complementary decomposer species [18].
Symbionts provide mineral nutrients to plants in exchange for
carbon and, although positive relationships between arbuscular
mycorrhizal fungal diversity and plant diversity have been shown
[52], diverse plant communities, in turn, do not necessarily support
diverse arbuscular mycorrhizal fungi communities [47].
Given their role in plant nutrient availability and thus plant growth,
decomposers and root symbionts can indirectly affect herbivore,
pollinator, fruit and seed-eater abundances aboveground [12,68].
Increases in the diversity of these aboveground functional groups
might also occur, for example when the period of flowering and seed
production is prolonged or shifted. Mycorrhizal fungi might also
stimulate shoot-sucking and -chewing insects, as well as reduce
shoot-chewing insect performance. This stimulation effect aboveground might result from the increased nutritional quality of the host
plant, whereas shoot-chewing reduction might be due to increased
concentrations of plant defensive compounds [11,69].
Herbivores of shoots and roots can stimulate plant growth,
rhizodeposition, soil microbial biomass and decomposition [70–72],
as well as change plant tissue nutrient and defensive compound
concentrations [11]. In addition to the effects of belowground
organisms on plant functioning and aboveground plant-associated
organisms, aboveground herbivores can strongly alter belowground
biota and processes [70]. However, the studies discussed here rarely
report the importance of diversity within and across functional
groups for ecosystem processes that are dependent on aboveground–belowground linkages [17].
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Vol.20 No.11 November 2005
and belowground to increased plant diversity and productivity will, in turn, depend on how the changes in
resource availability and complementarity in their consumption in a lower trophic level are perceived by the next
trophic level. If differences in the degree of specialization
of aboveground and belowground consumers (e.g. shoot
herbivores versus decomposers) and symbionts (e.g. pollinators versus mycorrhizal fungi) are common, responses
of aboveground heterotroph diversity to increased plant
diversity might be stronger than that belowground.
Top-down control of plant diversity is exerted by
herbivores or pathogens, aboveground and belowground,
and the outcome depends on plant traits such as
resistance and tolerance. Top-down and bottom-up mechanisms interact, because decomposers and symbionts can
suppress herbivore and pathogen densities, as well as
enhance plant tolerance to herbivory and diseases [14,51].
However, aboveground and belowground herbivores can
also enhance decomposer activity and, consequently,
nutrient availability to the plants [56]; thus, these
complex aboveground and belowground interactions contribute to the temporal dynamics in abundance and
diversity patterns that are characteristic of natural
communities.
Species pools, assembly history
Local diversity is strongly influenced by local abiotic
conditions and biotic interactions that can act as a filter
for species from the regional pool [57]. These filters might
affect aboveground and belowground diversity differentially, directly and independent or via feedback effects,
which suggest an interdependency of aboveground and
belowground community assemblages [58]. Interdependency might be related to alterations in profiles and
concentrations of plant primary and secondary metabolites. In this way, organisms on one side of the soil surface
can cause shifts in species abundances, trophic interactions and food-web complexity on the opposite side of the
soil surface [11,37]. For example, nematode addition to
plant species-rich microcosms reduced aphid abundances
on grass leaves, but increased body size and parasitization
rates of the remaining aphids [59]. Another example is
plant grazing by aboveground vertebrate herbivores,
which can enhance carbon exudation into the soil,
substrate availability for decomposer organisms and,
consequently, nutrient supply for the plants, resulting in
enhanced plant growth [6].
Resource heterogeneity
Spatial and temporal resource heterogeneity, as perceived
by the organisms, can have major effects on local diversity.
For example, heterogeneity in plant quality [10] and
diversity in habitat structure [60] might affect the
diversity of local aboveground arthropod communities
more than via primary productivity. Belowground local
biodiversity relates to the quantity of living and dead
organic matter, but even more so to the heterogeneity in
the chemical composition of the resources and to the
diversity of soil microhabitats [6,46,61] (Figure 1).
Disturbances that increase environmental heterogeneity enhance biodiversity. For example, soil burrowing
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TRENDS in Ecology and Evolution
1
Secondary
consumers
Predators,
parasitoids
Vol.20 No.11 November 2005
Primary
producers
Biomass,
chemistry,
structures
Symbionts
Primary
consumers
6
7
629
Pollinators
13
8
Seed dispersers
Seed eaters
15
Active dispersal
4
5
Endophytes
Shoot feeders
Chewers
Suckers
16
Miners
Phoresy
Pathogens
14
Passive dispersal
3
Predators,
parasites of
root feeders
Detritus
Symbionts
Root feeders
AM fungi
5
10
N fixers
Chewers
11
Ectoparasites
Nutrients
9
12
Endoparasites,
pathogens
Decomposers
2
15
Active dispersal
Chemistry
Engineers
Soil structure
TRENDS in Ecology & Evolution
Figure 1. Interdependency of aboveground and belowground biodiversity. Aboveground plant community biomass and chemical and structural composition (1) drive the
abundance and diversity of aboveground higher trophic levels, although these aboveground plant characteristics depend upon the net activity of soil functional groups, such
as decomposers and symbionts (5), which make nutrients available (2), and on aboveground and belowground herbivores and pathogens (3,4), which reduce plant growth
[17]. Heterotrophic organisms that interact with plants affect plant metabolism, potentially altering litter, shoot and root biomass production, distribution and chemical
composition by feeding on roots (3) or shoots (4) or living symbiotically in shoots, leaves or roots (5). In the longer term, pollinators (6) as well as seed eaters (7) and seed
dispersers (8) affect the persistence of the plant species and, thus, the specialist organisms associated with it. Soil organisms are constrained in their mobility and, as a result,
organisms interacting with a single plant root system are subsets of the total species pool present in the direct surrounding soil (9). Depending on their size and mobility,
these organisms occupy microhabitats of different sizes and might have different effects on plant growth. Although active roots have high turnover rates and are distributed
throughout the soil, root herbivores and pathogens (3) can account for this ‘unstable food’ source by being relatively mobile generalist feeders (10,11), similar to many
aboveground chewing insects and free-living suckers, by adapting a specialized endoparasitic plant association (12) or by having an aboveground life phase enabling
targeted active dispersal (15). Aboveground plant structures might be easier to find than are roots, and although the availability of more-specific aboveground plant tissues
[e.g. buds, flowers, fruits or seeds (13)] is often brief, these can still affect the aboveground diversity of plant-associated organisms owing to the large active range sizes of
aboveground organisms. Large aboveground and belowground organisms might disperse actively in a directional way (15), by flying, walking, crawling or borrowing,
whereas smaller organisms (or small structures of larger organisms, such as seeds) disperse more randomly via passive dispersal (14) by air, water or via phoresy (16)
(i.e. using other organisms as transport vectors). Abbreviations: AM fungi, arbuscular mycorrhizal fungi; N-fixers, nitrogen-fixing microorganisms.
creates patches of bare soil, where plant competition is
temporarily reduced, or even absent. However, the
relationship between disturbance intensity and organism
diversity is dependent on the nature of the generated
stress (i.e. water, oxygen and nutrient availability, soil
perturbation and xenobiotic compounds), taxon plasticity
and the matrix structure of the environment. The
response of soil biodiversity to disturbance might be
harder to predict and more variable at small observational
scales than it is for aboveground organisms, given that
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soils are spatially heterogeneous in biotic, physical and
chemical properties and all these factors interact with the
imposed disturbance [62]. Response of aboveground
organisms could be derived more directly from changes
in the plant community, but might be more variable in
time than belowground, for example owing to the limited
time that flowers and fruits are present. Heterogeneity
perceived by aboveground and belowground organisms
can thus differ to a great extent because of different
habitat dimensions of the various organisms (Box 2).
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Vol.20 No.11 November 2005
Box 2. Links between aboveground and belowground biodiversity and ecosystem functioning: a matter of scale
A soil volume of !1 m2 of temperate grassland hosts O10 000 species
of microbes and invertebrates that interact in complex food webs, thus
exceeding aboveground diversity at a similar spatial scale by
hundredfold or more [17]. Although this suggests that there are
considerable differences between aboveground and belowground
species pool sizes, it is questionable to what extent 1 m2 represents a
local scale of aboveground–belowground interactions. A local plant
population might be as large as a region for many belowground
species, whereas aboveground migratory vertebrate herbivores might
consider a plant region as a local scale. Therefore, when considering
aboveground–belowground diversity linkages, it is important to
standardize aboveground and belowground scales according to the
habitat characteristics of the interacting organisms (Table I; Figure 1,
main text).
Different resources, combined with high mobility, enables considerable spatial and temporal plant trait-driven niche differentiation of
aboveground organisms. For example, aboveground herbivores and
parasitoids select their hosts based on visual and chemical aboveground plant traits and can respond to changes in these, some of
which might result from belowground interactions [11]. Niche
differentiation belowground is less obvious, given the apparent high
levels of omnivory [6]. However, niche differentiation might occur in
space, via soil microhabitats (e.g. rhizoplane, rhizosphere and soil
pore size classes), and in time (e.g. detritus supply and decomposition
stage) [14,67]. Aboveground organisms altering the availability of
such niches, for example soil pore size distribution resulting from
trampling, can potentially drive selection of belowground species.
Linkages between aboveground and belowground diversity can
thus occur through plant morphology, chemistry and physiology.
Response rates can vary from almost immediately (e.g. for induced
defences), to a lag time of many years (e.g. for interactions via changes
in soil organic matter and soil structure). Such time lags in responses
need to be considered when explaining changes in above or
belowground communities in the field [67].
Table I. Characteristics of local aboveground and belowground habitat, main heterotroph trophic groups and their links via
plants
Characteristic
Habitat size
Aboveground
Large, but small when sedentary
Belowground
Small, but intermediate–large when with aboveground phase (e.g. insects) or
continuous growth (e.g. fungi)
Soil structure, pH, water availability
Dominant habitat abiotic
characteristics
Dominant heterotrophic
groups
Ambient climate
Herbivores, pathogens
Pollinators, endophytic
fungi
Decomposers
Herbivores, pathogens
Active range size of
heterotrophic groups
Form of passive
dispersal
Number of species per
plant (a-diversity)
Main factor affecting
short-term temporal
dynamics
Number of species in
common on two plant
species (b-diversity)
Plant link and specificity
Large to intermediate
Large to small
Small
Small
Mycorrhizal fungi,
growth-promoting
microorganisms
Small to large
Plant traits involved
Aboveground–belowground diversity link
between heterotrophs
Wind, phoresy, plant parts
Wind, plant parts
Wind, phoresy, water
Low to high
Low to high
High
Plant parts, soil, water,
wind
Low
Plant parts, soil, water,
wind
Low
Shoot physiology
Flower physiology
Ambient climate
Root physiology
Root physiology
Low to high
Low to high
High
Low to high
High
Direct, specific to general
Direct, specific to general
Indirect, general
Direct, specific to general
Shoot quantity, quality
K or C, plant trait and
heterotroph specificity
dependenta
Flower quality, quantity?
C via plant species
persistance
Litter quality
C via plant quantity and
qualitya
Root quality
K or C, plant trait and
heterotroph specificity
dependenta
Direct, ‘semi’-specific to
general
Root quality
C via plant quantity, C
or K via plant quality
(e.g. chemical defences)a
a
K indicating a negative and C a positive relationship.
Challenges and further directions
Over the past few years, the exploration of aboveground–
belowground interactions and their potential consequences for ecosystem properties have progressed as a
result of the use of new approaches. The generalization of
our mechanistic understanding of the results across
spatial and temporal scales is, however, still limited,
because most experiments have used individual species in
low-diversity settings over short time spans, focusing
mainly on temperate grassland systems or sub-boreal
forests [6]. Moreover, aboveground–belowground biodiversity links appear to be highly context dependent (Box 3).
Long-term experiments in which aboveground and belowground biodiversity is manipulated through the assemblage of communities, functional, or taxonomic groups
aboveground and belowground, and with factorial designs
in (semi) natural conditions are needed to follow up
removal experiments with selective aboveground and
belowground biocides [63–65].
Hypotheses derived from small-scale aboveground–
belowground biodiversity experiments in controlled conditions need to be tested in larger scale field studies across
geographical latitudes [9]. Other future challenges will
www.sciencedirect.com
involve the integration of aboveground–belowground food
webs in dynamic models [14,15], taking many organism or
community traits with their plasticity and feedbacks of
responses into account. To find traits that underlie
aboveground–belowground biodiversity-related interactions, a metabolomics approach appears promising
[11,66]. Recognition of biochemical profiles of primary and
secondary compounds associated with aboveground and
belowground interactions might enable the identification
of associated organism traits and their role in specific
interactions and food-web processes. A trait- and tradeoffbased approach, from genes to functions, will enable
researchers to elucidate the mechanisms of non-additive
effects of aboveground and belowground biodiversity on
ecosystem properties [17] and might also result in more
function-based categorizations of ‘functional groups’.
Future studies need to be performed at spatial and
temporal scales (see [67] in this themed issue of TREE)
that are relevant to the organisms and processes under
study to further enhance the predictive capacity of
ecological studies. Only accurate predictions will enable us
to prevent, or counteract the disadvantageous consequences
of human-induced and natural global environmental
Review
TRENDS in Ecology and Evolution
Vol.20 No.11 November 2005
631
Box 3. Context dependency: interacting factors and measures of diversity
The interactions between species across trophic levels might depend
on those within trophic levels. For example, exposure of plants to
aboveground and belowground herbivores might interact with the
species diversity of the local plant community [58]. In addition, the
outcome of many aboveground and belowground biotic interactions
for primary productivity, plant species composition and their
feedbacks to higher trophic-level organisms can depend on
resource (i.e. nutrients, water and light) availability and herbivore
or pathogen pressure. These factors direct the balance of costs and
benefits to the plant of symbiotic interactions, the production of
defensive compounds and tolerance to herbivory and diseases
[11,73,74]. Plant species in communities often exhibit different
strategies when dealing with multiple interactors for example,
although all are related to altering the distribution of resources
among leaves and roots, as well as of metabolites within plant
tissues [11]. It is thus likely that not one, but a series of interacting
biotic and abiotic factors determines the pattern of aboveground
and belowground diversity linkages.
In addition, generalization of aboveground and belowground
biodiversity links is complicated by inconsistent biodiversity
measures, such as differences in the taxonomic level of identification,
functional grouping and diversity measures (i.e. a-, b-, g-diversity and
diversity indices). In surveys of diversity distributions, many aboveground organisms have been identified to species level, whereas this is
not the case for most soil organisms. Not only is identification and
classification hampered by the collection process (i.e. isolation from
the soil as opposed to non-destructive observations), but also by the
lack of information about the life cycle of the organism and thus
‘species’ status, distribution and functional classification. For example,
global diversity patterns of arbuscular mycorrhizal fungi correlate
poorly with those of plants, which could be due to limited identification
capacity [75] as well as to high intraspecific diversity [76].
Environmental gradients in diversity are dependent on organism
size [7] and dispersal-related traits, which might differ considerably
between aboveground and belowground organisms (Table I). However, the body and range sizes of aboveground and belowground
organisms might depend on the latitudinal position or the habitat
structure (e.g. prairie versus temperate forest, or Equator versus
poles), adding to the context dependency of aboveground and
belowground diversity linkages.
Table I. Body size and selectivity as determinants of linked above-belowground diversity at a fixed level of productivitya
Body sizeb
/
Abundance
Aboveground
(O1 m3 to !1 mm3)
Large
Low
Small
High
Belowground
3
(!1 m , most !1 dm3)
Small
High
/
Dispersal mode
/
Range size
/
/
Species pool size
Selection active
species
/
Active
Passive
Large, directional
Large, random
Area dependent
Vector dependent
Vegetation structure
Host chemistry
Passive
Active
Large, random
Small, directional
Vector dependent
Local area dependent
Soil physics and chemistry
Detritus quality, host
quality
Diversity (inter) active
species
Y
Spatiotemporal scale
x
Habitat heterogeneity
a
Selectivity drives directional movement and resource (food, shelter) use.
Individual body size relates to an array of organism traits, of high relevance to their role in ecosystem processes [78], and is related to the trophic position and nutrient
turnover rate in food webs.
b
changes for aboveground and belowground biodiversity,
ecosystem properties and the sustainable delivery of
ecosystem goods and services [3].
Acknowledgements
We thank Martijn Bezemer, Stuart Campbell, Jeff Harvey, Jeff Powell,
Jessica Wells, Richard Bardgett and the anonymous reviewers for their
comments on this article, Ian Smith for help with Figure 1 and David
Bignell, Valerie Behan-Pelletier, Paul Eggleton, Colin Favret, Frans
Janssens, Patrick Lavelle, Charles Michener and David Pearson for their
help on the species diversity estimates. We thank the Netherlands
Organization for Scientific Research (NWO) for funding, Talent Postdoctoral Scholarship nr. S86–196.
Supplementary data
Supplementary data associated with this article can be
found at doi:10.1016/j.tree.2005.08.009
References
1 Hawkins, B.A. (2001) Ecology’s oldest pattern? Trends Ecol. Evol. 16,
470
2 Willig, M.R. et al. (2003) Latitudinal gradients of biodiversity: pattern,
process, scale and synthesis. Annu. Rev. Ecol. Evol. 34, 273–309
3 Wall, D.A. (2004) Sustaining Biodiversity and Ecosystem Services in
Soils and Sediments, Island Press
4 Hawkins, B.A. et al. (2003) Energy, water, and broad-scale geographic
patterns of species richness. Ecology 84, 3105–3117
5 Procter, D.L.C. (1984) Towards a biogeography of free-living soil
nematodes. I. Changing species richness, diversity and densities with
changing latitude. J. Biogeogr. 11, 103–117
6 Wardle, D.A. (2002) Communities and Ecosystems, Princeton University Press
www.sciencedirect.com
7 Hillebrand, H. (2004) On the generality of the latitudinal diversity
gradient. Am. Nat. 163, 192–211
8 Symstad, A.J. et al. (2003) Long-term and large-scale perspectives on
the relationship between biodiversity and ecosystem functioning.
Bioscience 53, 89–98
9 Hedlund, K. et al. (2003) Plant species diversity, plant biomass and
responses of the soil community on abandoned land across Europe:
idiosyncrasy or above-belowground time lags. Oikos 103, 45–58
10 Siemann, E. et al. (1998) Experimental tests of the dependence of
arthropod diversity on plant diversity. Am. Nat. 152, 738–750
11 Bezemer, T.M. and van Dam, N. (2005) Linking aboveground and
belowground interactions via induced plant defenses. Trends Ecol.
Evol. doi: 10.1016/j.tree.2005.08.006
12 Poveda, K. et al. (2005) Effects of decomposers and herbivores on plant
performance and above plant–insect interactions. Oikos 108, 503–510
13 Cardinale, B.J. et al. (2003) Biodiversity and biocontrol: emergent
impacts of a multi-enemy assemblage on pest suppression and crop
yield in an agroecosystem. Ecol. Lett. 6, 857–865
14 Moore, J.C. et al. (2004) Detritus, trophic dynamics and biodiversity.
Ecol. Lett. 7, 584–600
15 De Ruiter, P.C. et al. (2005) Food web ecology: playing Jenga and
beyond. Science 309, 68–71
16 Tscharntke, T. and Brandl, R. (2004) Plant–insect interactions in
fragmented landscape. Annu. Rev. Entomol. 49, 405–430
17 Wardle, D.A. et al. (2004) Ecological linkages between aboveground
and belowground biota. Science 304, 1629–1633
18 Heemsbergen, D.A. et al. (2004) Biodiversity effects on soil processes
explained by interspecific functional dissimilarity. Science 306,
1019–1020
19 Eggleton, P. and Bignell, D.E. (1995) Monitoring the response of
tropical insects to changes in the environment: troubles with termites.
In Insects in a Changing Environment (Harrington, R. and Stork,
N.E., eds), pp. 434–497, Academic Press
20 Gaston, K.J. and Williams, P.H. (1996) A biology of numbers and
difference. In Biodiversity (Gaston, K.J., ed.), pp. 202–229, Blackwell
Science
632
Review
TRENDS in Ecology and Evolution
21 Boag, B. and Yeates, G.W. (1998) Soil nematode biodiversity in
terrestrial ecosystems. Biodiv. Conserv. 7, 617–630
22 Lavelle, P. et al. (1995) Mutualism and biodiversity in soils. Plant Soil
170, 23–33
23 Finlay, B.J. (2002) Global dispersal of free-living microbial eukaryote
species. Science 296, 1061–1063
24 Finlay, B.J. and Clarke, K.J. (1999) Ubiquitous dispersal of microbial
species. Nature 400, 828
25 Horner-Devine, M.C. et al. (2004) An ecological perspective on
bacterial biodiversity. Proc. Biol. Sci. 271, 113–122
26 Olff, H. et al. (2002) Global environmental controls of diversity in large
herbivores. Nature 415, 901–904
27 Willis, K.J. and Whittaker, R.J. (2002) Species diversity-scale matters.
Science 295, 1245–1248
28 Grime, J.P. (1973) Control of species density in herbaceous vegetation.
J. Environ. Manage. 1, 151–167
29 Hawkins, B.A. et al. (2003) Productivity and history as predictors of
the latitudinal diversity gradient of terrestrial birds. Ecology 84,
1608–1623
30 Mittelbach, G.G. et al. (2001) What is the observed relationship
between species richness and productivity? Ecology 82, 2381–2396
31 Curtis, T.P. et al. (2002) Estimating prokaryotic diversity and its
limits. Proc. Natl. Acad. Sci. U. S. A. 99, 10494–10499
32 Kassen, R. et al. (2000) Diversity peaks at intermediate productivity
in a laboratory microcosm. Nature 406, 508–512
33 Chown, S.L. et al. (2004) Hemispheric asymmetries in biodiversity – a
serious matter for ecology. PLoS Biol. 2, 1701–1707
34 Courtright, E.M. et al. (2001) Determining habitat suitability for soil
invertebrates in an extreme environment: the McMurdo Dry Valleys,
Antarctica. Antarct. Sci. 13, 9–17
35 Evans, K.L. et al. (2005) Species-energy relationships at the
macroecological scale: a review of the mechanisms. Biol. Rev. Camb.
Philos. Soc. 80, 1–25
36 Wiens, J.J. and Donoghue, M.J. (2004) Historical biogeography,
ecology and species richness. Trends Ecol. Evol. 19, 639–644
37 Van der Putten, W.H. et al. (2001) Linking above- and belowground
multitrophic interactions of plants, herbivores, pathogens, and their
antagonists. Trends Ecol. Evol. 16, 547–554
38 Jimenez-Gasco, M.M. et al. (2004) The Fusarium oxysporum f. sp.
Ciceris/Cicer arietinum pathosystem: a case study of the evolution of
plant-pathogenic fungi into races and pathotypes. Int. Microbiol. 7,
95–104
39 Parker, M.A. and Spoerke, J.M. (1998) Geographic structure of
lineage associations in a plant-bacterial mutualism. J. Evol. Biol.
11, 549–562
40 Kessler, M. and Kromer, T. (2000) Patterns and ecological correlates of
pollination modes among bromeliad communities of Andean forest in
Bolivia. Plant Biol. 2, 659–669
41 Godfray, H.C.J. and Lawton, J.H. (2001) Scale and species numbers.
Trends Ecol. Evol. 16, 400–404
42 Horner-Devine, M.C. et al. (2004) A taxa–area relationship for
bacteria. Nature 432, 750–753
43 Bell, T. et al. (2005) Large islands house more bacterial taxa. Science
308, 1884
44 Judas, M. (1988) The species-area relationship of European Lumbricidae (Annelida, Oligochaeta). Oecologia 76, 593–607
45 Wardle, D.A. et al. (2003) Island biography and ecosystem functioning
in epiphytic soil communities. Science 301, 1717–1720
46 Stephan, A. et al. (2000) Plant diversity affects culturable soil bacteria
in experimental grassland communities. J. Ecol. 88, 988–998
47 Johnson, D. et al. (2004) Plant communities affect arbuscular
mycorrhizal fungal diversity and community composition in grassland
microcosms. New Phytol. 161, 503–515
48 De Deyn, G.B. et al. (2004) Plant species identity and diversity effects
on different trophic levels of nematodes in the soil food web. Oikos 106,
576–586
49 Olff, H. and Ritchie, M.E. (1998) Effects of herbivores on grassland
plant diversity. Trends Ecol. Evol. 13, 261–265
50 De Deyn, G.B. et al. (2003) Soil invertebrate fauna enhances grassland
succession and diversity. Nature 422, 711–713
51 Hart, M. and Klironomos, J.N. (2002) Diversity of arbuscular
www.sciencedirect.com
52
53
54
55
56
57
58
59
60
61
62
63
64
65
66
67
68
69
70
71
72
73
74
75
Vol.20 No.11 November 2005
mycorrhizal fungi and ecosystem functioning. In Mycorrhizal Ecology
(Van der Heijde, M.G.A. and Sanders, I.R., eds), pp. 225–239,
Springer-Verlag
Van der Heijden, M.G.A. et al. (1998) Mycorrhizal fungal diversity
determines plant biodiversity, ecosystem variability and productivity.
Nature 396, 69–72
Wardle, D.A. et al. (2004) Linking aboveground and belowground
communities: the direct and indirect influence of aphid species
identity and diversity on a three trophic level soil food web. Oikos
107, 283–294
Moore, J.C. et al. (2003) Top-down is bottom-up: does predation in the
rhizosphere regulate aboveground dynamics? Ecology 84, 846–857
Eviner, V.T. (2004) Plant traits that influence ecosystem processes
vary independently among species. Ecology 85, 2215–2229
Bardgett, R.D. et al. (1999) Belowground herbivory promotes soil
nutrient transfer and root growth in grassland. Ecol. Lett. 2,
357–360
Lavorel, S. and Garnier, E. (2002) Predicting changes in community
composition and ecosystem functioning from plant traits: revisiting
the Holy Grail. Func. Ecol. 16, 545–556
Bezemer, T.M. et al. (2004) Above- and belowground trophic
interactions on creeping thistle (Cirsium arvense) in high- and lowdiversity plant communities: potential for biotic resistance? Plant
Biol. 6, 231–238
Bezemer, T.M. et al. (2005) Soil faunal community composition drives
aboveground plant-herbivore-parasitoid interactions. Ecol. Lett. 8,
652–661
Southwood, T.R.E. et al. (1979) The relationships of plant and insect
diversities in succession. Biol. J. Linn. Soc. 12, 327–348
Spehn, E.M. et al. (2000) Plant diversity effects on soil heterotrophic
activity in experimental grassland ecosystems. Plant Soil 224,
217–230
Ettema, C.H. and Wardle, D.A. (2002) Spatial soil ecology. Trends
Ecol. Evol. 17, 177–179
Brown, V.K. and Gange, A.C. (1989) Differential-effects of aboveground and below-ground insect herbivory during early plant
succession. Oikos 54, 67–76
Wardle, D.A. et al. (1999) Plant removals in perennial grassland:
vegetation dynamics, decomposers, soil biodiversity and ecosystem
properties. Ecol. Monogr. 69, 535–568
Van Ruijven, J. et al. (2005) Interactions between above- and
belowground herbivores indirectly alters plant diversity. Ecol. Lett.
8, 30–37
Bino, R.J. et al. (2004) Potential of metabolomics as a functional
genomics tool. Trends Plant Sci. 9, 418–425
Bardgett, R.D. et al. (2005) Linking aboveground and belowground ecology: a temporal approach. Trends Ecol. Evol. doi: 10.
1016/j.tree.2005.08.005
Bonkowski, M. (2004) Protozoa and plant growth: the microbial loop in
soil revisited. New Phytol. 162, 617–631
Gange, A.C. (2001) Species-specific responses of a root- and shootfeeding insect to arbuscular mycorrhizal colonisation of its host plant.
New Phytol. 150, 611–618
Bardgett, R.D. et al. (1998) Linking aboveground and belowground
interactions: how plant responses to foliar herbivory influence soil
organisms. Soil Biol. Biochem. 30, 1867–1878
Bardgett, R.D. and Chan, K.F. (1999) Experimental evidence that
soil fauna enhance nutrient mineralization and plant nutrient
uptake in montane grassland ecosystems. Soil Biol. Biochem. 31,
1007–1014
Belovsky, G.E. and Slade, J.B. (2000) Insect herbivory accelerates
nutrient cycling and increases plant production. Proc. Natl. Acad. Sci.
U. S. A. 97, 14412–14417
Johnson, N.C. et al. (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol. 135,
575–585
Scheu, S. (2001) Plants and generalist predators as links between
the below-ground and above-ground system. Basic Appl. Ecol. 2,
3–13
Allen, E.B. et al. (1995) Patterns and regulation of mycorrhizal plant
and fungal diversity. Plant Soil 170, 47–62
Review
TRENDS in Ecology and Evolution
76 Hijri, M. and Sanders, I.R. (2005) Low gene copy numbers shows that
arbuscular mycorrhizal fungi inherit genetically different nuclei.
Nature 433, 160–163
77 Groombridge, B. and Jenkins, M.D. (2002) World Atlas of Biodiversity:
Earths Living Resources in the 21st Century, University of California
Press
Vol.20 No.11 November 2005
78 Woodward, G. et al. (2005) Body size in ecological networks. Trends
Ecol. Evol. 20, 402–409
79 Hopkin, S.P. (1998) Collembola: the most abundant insects on earth.
Antenna 22, 117–121
80 Walter, D.E. and Procter, H.C., eds (1999) Evolution and Behaviour,
CABI Publishing
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