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REVIEWS REVIEWS REVIEWS
145
Human-induced changes in large
herbivorous mammal density: the
consequences for decomposers
David A Wardle1,2 and Richard D Bardgett3
Work on the impacts of herbivores on ecosystems has traditionally focused on aboveground effects, but a
growing number of ecologists are beginning to consider how herbivores affect belowground organisms and
processes. Human activity has caused considerable changes in densities of mammalian herbivores throughout the world, through the introduction of herbivores to new regions, the creation of conditions that promote high herbivore densities, and the reduction of their population sizes, sometimes to the point of extinction. These human influences on high mammal densities can have major effects on the decomposer
subsystem. Whether these effects are positive or negative depends on the mechanisms involved: for example, whether the changes are in the quantity or quality of the decomposers’ resources or in the pathway of
vegetation succession. In turn, these belowground effects may influence aboveground biota by altering the
supply of available nutrients from the soil. Changes in large mammal densities through human activity may
represent an important, though frequently underappreciated, element of global change.
Front Ecol Environ 2004; 2(3): 145–153
A
boveground herbivores can consume anywhere from
<1% to >50% of total net primary productivity,
depending on the ecosystem (McNaughton et al. 1989).
Herbivory by large mammals is an important ecological driver in many ecosystems, notably in grasslands and tundra, as
well as in forests with high densities of palatable understory
species. The effects of browsing mammals on aboveground
properties such as ecosystem productivity and vegetation
composition have been studied extensively. However, all
terrestrial ecosystems consist of explicit aboveground and
belowground components, which interact to maintain
long-term ecosystem functioning. In this light, a growing
number of recent investigations have considered the
influences of large herbivores on the decomposer subsystem, and the consequences for ecosystem perform-
In a nutshell:
• There is a growing recognition of the types of effects that herbivores have on the belowground subsystem and the mechanisms involved
• Human-induced changes in large herbivorous mammal density often have important effects on the belowground subsystem
• These effects can be either positive or negative, depending on
the mechanisms involved, and induce feedbacks which may
exert long-term influence on the performance of ecosystems
ance (Bardgett et al. 1998; Bardgett and Wardle 2003).
Human activity has drastically altered the distribution and
abundance of much of the Earth’s biota, resulting in the introduction of organisms to new environments, large increases or
reductions in native populations, and local and global extinctions. There is a growing recognition that such shifts represent
an important element of global change (Pimm et al. 1995;
Vitousek et al. 1997). Given the impact that large mammals
have on ecosystems, the major population shifts that humans
have induced in these mammals probably have important
effects on the performance of the decomposer subsystem.
Here, we briefly describe the mechanisms through which large
mammals indirectly influence the decomposer subsystem and
aboveground–belowground feedbacks. Against this background, we then discuss the consequences of human-induced
shifts in the densities of large herbivorous mammals for the
decomposer subsystem and ecosystem functioning, in natural
and semi-natural environments.
Mechanisms involved
Three main categories of mechanisms exist through
which browsing mammals influence decomposer organisms and processes by altering the nature of resources
entering the belowground subsystem (Bardgett and
Wardle 2003), all of which have been shown to be important in at least some contexts (Figure 1).
1
Department of Forest Vegetation Ecology, Swedish University of
Agricultural Sciences, SE901 83 Umeå, Sweden (david.wardle@
svek.slu.se); 2Landcare Research, PO Box 69, Lincoln, New Zealand;
3
Institute of Environmental and Natural Sciences, Lancaster University, Lancaster LA1 4YQ, UK
© The Ecological Society of America
Changes in resource quantity
In the short-term, defoliation can greatly increase the
amount of carbon allocated belowground and to the rhiwww.frontiersinecology.org
Human-induced changes in large herbivorous mammal density
146
DA Wardle and RD Bardgett
Effects on decomposers
POSITIVE
Effect on
rhizosphere C
exudates
Effects on
resource
quality
FOLIAR
HERBIVORES
Effects on
resource
quality
NEGATIVE
Enhancement of
available C in
rhizosphere
Reduction of NPP
through tissue
removal
Effects on NPP
Grazing
optimization of NPP
Return of fecal
material
Resource return to
soil in labile form
Reduced C to N
ratio of material
Effects on litter
quality through
changes at
whole plant level
Increased nutrients
and reduced
secondary
metabolites
Induced defences,
greater amounts of
secondary
metabolites
Effects on litter
quality through
changes at plant
community level
Grazing optimization
reduces later
successional plants
with poor litter quality
Acceleration of
succession through
replacement by low
litter quality species
Figure 1. Mechanisms through which herbivores can influence decomposers in both the short and long term. (NPP = net primary
production; C = carbon; N = nitrogen.)
zosphere, the soil immediately surrounding plant roots
(Bokhari and Singh 1974; Hamilton and Frank 2001).
This may explain why defoliation of herbaceous plant
species can cause large increases in populations of decomposer organisms, even when net belowground productivity is reduced (Holland 1995; Guitian and Bardgett 2000;
Mikola et al. 2001). In the longer term, foliar herbivory
often substantially alters net primary productivity (NPP),
both aboveground and belowground. Exclusion studies of
large mammals show that aboveground NPP is often negatively affected by grazing in grasslands, but that many
exceptions exist (Milchunas and Lauenroth 1993).
Optimization of aboveground NPP by browsing mammals
can occur in grassland ecosystems (McNaughton 1985),
and there is theoretical evidence that in fertile conditions
promotion of NPP by foliar herbivores may occur at the
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level of the whole plant community (De Mazancourt et
al. 1998). Evidence also suggests that browsing mammals
have both positive and negative effects on belowground
NPP (Milchunas and Lauenroth 1993; McNaughton et
al. 1998; Ruess et al. 1998), and since NPP is an important driver of decomposer organisms (Wardle 2002),
varying effects on the decomposer subsystem may therefore occur.
Changes in resource quality
Browsing or grazing by herbivores at the whole plant
level can increase the concentrations of nutrients in
both leaves (Ruess and McNaughton 1987) and roots
(Seastedt et al. 1988). This may result from plant allocation strategies in response to browsing, or through
© The Ecological Society of America
DA Wardle and RD Bardgett
Human-induced changes in large herbivorous mammal density
147
Plant traits
Plant traits
• high growth rate
• slow growth rate
• short-lived tissue
• long-lived tissue
• high shoot leaf area
• low shoot leaf area
• poorly defended leaves
• well defended leaves
• high leaf nutrient content
Role of herbivory
• low leaf nutrient content
Retardation of
succession
Acceleration of
succession
Role of herbivory
• compensatory plant
growth responses
• non-compensatory plant
growth responses
• high % NPP consumed
• low % NPP consumed
• most OM returned to soil
as fecal material
• most OM returned to soil
as litter
HERBIVORY
Decomposer subsystem
• high litter quality
(Foliar
herbivores)
(Foliar and root
herbivores)
NUTRIENT-REPLETE
NUTRIENT-LIMITED
Reproduced courtesy of EIC of Ecology.
• high rates of decomposition
and mineralization
• low rates of carbon
sequestration in soil
EARLY SUCCESSIONAL
ECOSYSTEMS
Decomposer subsystem
• low litter quality
• low rates of decomposition
and mineralization
High supply
rates of
plant
available
nutrients
low supply
rates of
plant
available
nutrients
Succession
• high rates of carbon
sequestration in soil
LATE SUCCESSIONAL
ECOSYSTEMS
Figure 2. How browsing mammals can alter vegetation succession (Bardgett and Wardle 2003).
improved nutrient availability resulting from
enhanced activity of soil biota in the root zone
(Hamilton and Frank 2001). This may in turn enhance
the quality of litter produced by the plant, and it has
been shown that browsing of deciduous trees can
enhance both the quality of their litter and soil carbon
(C) mineralization rates (Kielland and Bryant 1998).
Conversely, defoliation of some plant species promotes
the production of secondary defense (antiherbivore)
compounds in subsequently produced leaves, adversely
affecting the quality of the resulting litter. This should
have negative consequences for the decomposer subsystem, but to date has only been shown for invertebrate herbivores (Findlay et al. 1996). In highly fertile
ecosystems that support dense mammalian herbivore
populations, a substantial proportion of NPP can be
returned to the soil as dung and urine. This shortcuts
the decomposition pathway, since resources are
returned to the soil in a highly labile form rather than
as relatively recalcitrant plant litter. Return of resources of this type can greatly promote soil organisms
and processes, which ultimately feeds back to influence aboveground biota (Person et al. 2003).
© The Ecological Society of America
Changes in successional trajectory
Over longer time scales, foliar herbivory often operates as
an important determinant of vegetation composition. This
has important implications for the decomposer subsystem,
since those plant species that have the most palatable
foliage are generally the ones that produce the most readily
decomposable litter (Grime et al. 1996). Earlier successional plant species are usually more palatable and produce
better quality litter than species that appear in later stages.
Depending on the situation, browsing mammals can either
accelerate or retard vegetation succession (Figure 2;
Davidson 1993). Acceleration of succession is especially
apparent in forests, where browsing mammals can cause
increasing domination by those plant species that produce
the most recalcitrant litter. This phenomenon is particularly apparent in the “moose, microbes, and boreal forest”
study of Pastor et al. (1998; 1993), where long-term, fenced
exclusion plots on Isle Royle, northern Michigan, were
used to show that moose herbivory allowed spruce to
replace deciduous tree species that produced litter of much
higher quality. This in turn led to a reduction of a whole
range of belowground properties indicative of soil fertility.
Retardation of succession occurs in higher fertility situawww.frontiersinecology.org
Human-induced changes in large herbivorous mammal density
148
DA Wardle and RD Bardgett
Table 1. The effects of browsing mammals on plants and soil organisms in New Zealand rainforests, based on data
from 30 long-term fenced exclosure plots (data presented in Wardle et al. 2001)
Response variable
Overall negative effects
Plant variables
Vegetation density and species
richness in understory
Overall idiosyncratic effects*
Overall neutral effects
Microbial variables
Microbial biomass and respiration
in both humus and litter layers
Microfaunal variables
Densities of microbe feeding and
predatory nematodes, and of rotifers,
copepods, and tardigrades
Mesofaunal variables
Densities of springtails and of
all the main orders of mites
Macrofaunal variables
Densities of all major groups (eg
millipedes, spiders, harvestmen,
gastropods, beetles); diversity
(richness) of gastropods and millipedes
Diversity (richness) of
nematodes
Densities of enchytraeids
Diversity (richness) of
staphylinid beetles and
beetle families
*“Idiosyncratic” means that several exclosures showed both positive and negative effects, indicating that the direction of effect is context-dependent.
tions such as grasslands, where mammalian herbivores
maintain the vigour of existing vegetation, thereby deterring late-successional species that produce poorer quality
litter (Augustine and McNaughton 1998).
Thus, there are a range of mechanisms through which
browsing mammals may influence the decomposer subsystem, and these can have either positive or negative consequences. Different mechanisms may dominate in different
contexts, and for this reason a variety of responses of the
belowground subsystem to browsing mammals has been
reported (Wardle 2002; Bardgett and Wardle 2003). In this
light, we now consider the belowground consequences of
three scenarios of human-induced changes in browsing
mammal densities: invasions, population increases, and
population declines and extinctions.
Browsing mammals as invasive organisms
As humans have colonized new regions of the world, they
have greatly facilitated the spread of organisms to new
areas. Over the past three centuries, considerable numbers
of large herbivorous mammals were introduced to new
regions, including those that already had a native herbivorous mammal fauna (eg the Americas, Australia, Britain)
and those that did not (eg New Zealand, Hawaii). Here
we focus on New Zealand forests as a case study of the ecological impacts of introduced browsing mammals.
Several species of large browsing mammals were introduced to New Zealand between the 1770s and 1920s.
Prior to human settlement, browsing mammals did not
exist in New Zealand, making these islands ideal for investigating the impacts of introducing a whole functional
group of organisms into an ecosystem where they were
previously absent. The most widespread and ecologically
important introduced browsers in New Zealand forests are
the European red deer and feral goats, although there are
substantial localized populations of numerous other
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species, such as sika deer, white-tailed deer, North
American elk (wapiti), fallow deer, sambar deer, feral
horses, and Dama wallabies. Collectively, these mammals
have caused widespread shifts in the forest understory vegetation throughout the country, often reducing or eliminating broad-leaved, fast-growing palatable plant species
and promoting unpalatable fern and monocotyledonous
species (Figure 3a). New Zealand’s native megaherbivores,
the moa birds, were hunted to extinction a few hundred
years ago, and while their past ecological impact is poorly
understood, their effects on vegetation are believed to
have been considerably less than those of introduced
mammals (McGlone and Clarkson 1993).
From the 1950s to the 1980s, the former New Zealand
Forest Service established several hundred fenced exclosure plots (typically 20 m x 20 m) throughout the country’s indigenous forests to assess the effects of introduced
browsing mammals on vegetation. Wardle et al. (2001;
2002) selected 30 of the remaining exclosures, which
included most of New Zealand’s main indigenous forest
types. Measurements inside and outside each exclosure
revealed that browsing mammals had consistent adverse
effects on the density and diversity of vegetation present
in the understory, and promoted unpalatable species with
poor litter quality (typically monocotyledonous, fern, and
small-leaved dicotyledonous species) at the expense of
palatable species with higher litter quality (typically largeleaved dicotyledonous species). Despite the consistency of
these trends, the response of the belowground biota was
far less predictable (Wardle et al. 2001; Table 1). Most
groups of smaller bodied soil organisms (microfauna and
microflora) showed idiosyncratic responses to browsing;
both strong positive and negative effects, depending upon
the site. Ecosystem processes and properties that are driven by soil biota, such as soil carbon mineralization and
soil C and nitrogen (N) sequestration, also showed context-dependent responses. In contrast, browsing mammals
© The Ecological Society of America
DA Wardle and RD Bardgett
Human-induced changes in large herbivorous mammal density
(b)
(c)
(d)
149
© Courtesy of D Marquis
(a)
Figure 3. Effects of browsing mammal densities, as influenced by human activity, on the functional composition of vegetation. (a)
Effects of introduced fallow deer on forest understorey vegetation in Woodhill Forest, New Zealand. Deer have been excluded from
the right-hand side of the fence for 14 years, and a dense understory of shrubs that produce litter of high quality is present. On the lefthand side, where the deer have access, this vegetation is replaced by monocotyledonous species requiring high light, which produce poor
quality litter. (b) Effects of reindeer on reindeer lichens (Cladina spp) in a pine-dominated heathland, near Muonio, Finnish
Lappland. Reindeer have been excluded from the left-hand side of the fence for 30 years, but not from the right-hand side. (c) Effects
of white-tailed deer on regenerating vegetation in a clearcut cherry–maple forest in northwest Pennsylvania, US. Deer have been
excluded for 5 years on the right-hand side of the fence, but not on the left-hand side. (d) Effects of removing grazing ungulates (red
deer and sheep) for 50 years in mountain regions of Britain that have been grazed for centuries. On the inside of the fence the
vegetation is dominated by dwarf shrubs such as Calluna vulgaris and Vaccinium myrtillus, and regenerating trees, which are
eliminated by grazers and replaced by grasses outside the exclosure.
consistently had adverse effects on larger soil animals.
The idiosyncratic responses of smaller soil organisms
and soil processes are probably due to the existence of
several mechanisms through which browsers affect
decomposers and to the dominance of different mechanisms in different locations. Although across the experimental sites browsers had consistent effects on vegetation properties (eg reduced understory density and
promotion of plant species that produce poor quality litter) that might be expected to negatively affect
microbes and microfauna, at several sites, these effects
seemed to be overridden by other mechanisms. Further,
it appears that the body size of soil animals serves as a
determinant of their response to browsers; unlike small
soil animals, large soil animals were often adversely
affected by browsing. The probable reason is that large
© The Ecological Society of America
soil animals are more susceptible than smaller ones to
typical adverse physical disturbances such as trampling
caused by mammalian herbivores. Small-bodied organisms would be in a better position to resist such disturbances, because they are protected within the soil
matrix. In this context, it is relevant that the physical
pressures exerted by the hooves of introduced ungulates
is probably much greater than that of the extinct moas,
despite the fact that moas had a greater individual body
mass (Duncan and Holdaway 1989).
The above example points to important effects of
browsing mammals on the decomposer subsystem, which
in the long term should affect the rates of nutrient supply
from the soil and ultimately the nutrition, productivity,
and composition of the forest. Although the issue of how
alien browsing mammals affect the decomposer subsystem
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Human-induced changes in large herbivorous mammal density
150
DA Wardle and RD Bardgett
Oksanen 2002). Reindeer densities are
very low on the Russian side of the
Russian–Finland border, and the influence of reindeer on vegetation in northeast Finland is great enough that the border is easy to distinguish in satellite
images (Väre et al. 1996).
The aboveground effects of reindeer are
matched belowground. This has been
investigated by long-term fenced reindeer
exclusion plots in several recent studies,
notably in northern Finland. Reduction of
soil microbial biomass C and rates of C
mineralization by reindeer are frequently
Figure 4. Reindeer are native to northern Scandinavia, but during the past century observed, especially in nutrient-poor
domesticated reindeer have reached very high abundances throughout this region, and heathlands (Väre et al. 1996; Stark et al.
recent studies have shown that this has profound effects over large spatial scales on 2000, 2003; Stark and Grellman 2002). In
decomposer organisms and the C and N mineralization processes they regulate.
contrast, microbial biomass N and rates of
N mineralization show varied responses to
has seldom been investigated, several studies worldwide reindeer (Stark et al. 2000, 2003; Stark and Grellman
have documented important effects of introduced mam- 2002), with both increases and decreases in these measures,
mals on vegetation composition (Vazquez 2002). It is suggesting that mineralization of C and N are strongly
likely that there are many situations in which these ani- decoupled when effects of reindeer grazing are considered
mals significantly impact the decomposer subsystem and (Stark et al. 2003). Reindeer grazing also has varied effects
hence the long-term performance of the ecosystem.
on plant litter decomposition rates; while Stark et al. (2000)
found impaired decomposition rates outside of exclosure
plots, Olofsson and Oksanen (2002) found the reverse
Population increases of native browsing
trend. There is also evidence that reindeer grazing can
mammals
induce multitrophic effects in the soil food web. For examHuman activity often causes substantial increases in the ple, Stark et al. (2000) found that reindeer stimulate popudensities of native mammalian herbivores in two main lations of most trophic groups of soil nematodes in the
ways: (1) the reduction or extermination of natural preda- lichen layer and encourage nematode taxonomic diversity.
tors of herbivores, either intentionally or through habitat In contrast, Suominen (1999) found that reindeer consismodification, reduces top-down regulation of herbivores; tently reduce both densities and diversity of soil-associated
(2) human activities that enhance the availability of food gastropods.
resources for herbivores reduce bottom-up regulatory
The varied effects of reindeer on some soil biological
forces; this can occur due to the supplementary feeding of properties may appear because these animals predomiherbivores, or when they have access to agricultural crops nantly affect decomposers by different mechanisms in difand forage at times of the year when food is otherwise lim- ferent situations. Negative effects of reindeer on the
iting. Reindeer are a good example of a herbivore which decomposer subsystem may occur through removal of the
has undergone this kind of large population growth due to protective cover of lichens and exposure of the soil biota
human activity.
to a less favorable microclimate (Stark et al 2000), and
Reindeer (Figure 4) are a native species of Fennoscandia, through reindeer trampling plant roots and reducing carthe peninsular land mass which includes Norway, Sweden, bon inputs to the soil (Stark et al 2003). Positive effects
Finland, and part of north-western Russia, and were might arise through the promotion of plant species that
domesticated by the Sámi people in the 16th century. Over produce better quality litter (Olofsson and Oksanen
the past century their numbers have increased more than 2002), and the return of materials to the soil in the labile
2.5-fold in northern Scandinavia (Väre et al. 1996), due to forms of dung and urine. Further, reindeer waste may creseveral factors, including winter feeding, vaccines, and ate a situation where N becomes less limiting than C,
massive declines in their predators, notably wolves and causing mineralization of soil C, but not soil N, to be
bears (Väre et al. 1996). Reindeer feed predominantly on impaired by grazing (Stark et al. 2000). Therefore, there
reindeer lichens (notably Cladina spp), and heavy grazing are parallels between the influence of reindeer in
can cause important changes in vegetation composition by Scandinavia and deer and goats in New Zealand, in that
severely reducing the lichen ground cover (Figure 3b; den both the magnitude and direction of herbivore effects on
Herder et al. 2003) and ericaceous dwarf shrubs and by the decomposer subsystem are highly dependent on site
encouraging the dominance of grazing-tolerant grass conditions.
species (Bråthens and Oksanen 2001; Olofsson and
Although the belowground impacts of unusually high
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© The Ecological Society of America
DA Wardle and RD Bardgett
native mammal densities have seldom been investigated
elsewhere, there are many other situations where these
might be important. For example, many regions of the
eastern US support densities of white-tailed deer that are
several times greater than those of pre-European times
(Rooney and Waller 2003). A ten-year enclosure study in
forests of northern Pennsylvania (Horsley et al. 2003), in
which white-tailed deer were fenced within large plots at
several densities, revealed that deer adversely affected the
growth and density of palatable deciduous tree species.
Conversely, sedges, grasses, and ferns, which the deer
avoided, or which were resistant to browsing, reached
much higher densities in the presence of deer (Figure 3c).
It is probable that such functional changes in vegetation
would influence the decomposer subsystem and ultimately
create feedbacks affecting the supply of nutrients available
to plants and forest stand properties.
Mammal population reductions and extinctions
Given that large increases in herbivore densities can
greatly influence the decomposer subsystem, large reductions in populations of native herbivores due to human
activity should also have important effects. Investigating
the ecological impacts of reduced animal abundances
poses particular challenges because of the difficulty in
implementing experimental treatments that represent
the higher densities of animals present before human
interference. However, insight can be gained from the
study of species that are severely reduced or absent in
most parts of the landscape, but present in high densities
in some areas, such as protected reserves or sites of reintroduction.
A key example is the North American bison, once the
dominant megaherbivore of the Great Plains, but
reduced by the 1880s to a few thousand individuals.
Recent reintroductions of bison to some tallgrass prairie
sites have offered a glimpse of the influence they would
have exerted throughout their previous range. At the
Konza Prairie in Kansas, where bison were reintroduced
in 1987, fenced exclusion plots provide evidence that
bison promote forbs over grasses, enhance floristic diversity, alter patterns of NPP, increase N concentrations of
foliage, and enhance spatial heterogeneity of vegetation
(Knapp et al. 1999). These effects are matched belowground by changes such as enhanced N mineralization
rates (Johnson and Matchett 2001). Exclosure plot studies in Yellowstone Park, Wyoming, which consider
effects of large mammalian herbivores such as bison and
elk, that have been severely reduced throughout most of
the Great Plains, suggest that these herbivores greatly
enhance N mineralization and ecosystem N retention,
reduce C:N concentrations in plant tissues, and enhance
microbial activity (though not biomass) (Tracy and
Frank 1998; Frank et al. 2000). In the Great Plains system, bison presumably promoted soil processes by returning substantial amounts of nutrients to the soil in labile
© The Ecological Society of America
Human-induced changes in large herbivorous mammal density
forms, as well as encouraging the return of plant residues
of a higher quality to the soil. Furthermore, more complicated effects of bison population changes on ecosystem
structure and function could be expected when their
interactions with coexisting herbivore species (eg pronghorn and prairie dogs) are considered (Coppock et al.
1983; Krueger 1986).
Another example comes from the Scottish Highlands,
UK, where major efforts have been made to reduce the
population sizes of sheep and native red deer to encourage
regeneration of the native birch (Betula pubscens) and
pine forest (Pinus sylvestris). Historically, these mammals
heavily grazed mountain areas of Britain, and consequently the vegetation below the natural tree line is dominated by grassland and heath, with little woodland
regeneration (Rodwell 1992; Figure 3d). In recent years,
conservation bodies have altered land management practices, with the aim of encouraging forest regeneration,
either through fencing to eliminate large grazers or by
intensive culling to reduce populations of red deer
(Ramsey 1996). In certain areas, such as the Creag
Meagaigh National Nature Reserve in the Scottish
Highlands, exclusion of red deer for ten years led not only
to major increases in birch growth, but also to important
changes in belowground properties, most notably a fourfold increase in nitrogen mineralization (Harrison and
Bardgett 2004), which will probably feed back to provide
the trees with an increased nitrogen supply. In other
areas, where sheep grazing was stopped on grasslands that
had been grazed for centuries, there has been no tree
growth even after 50 years of grazer exclusion; here, the
net effect of grazer removal on soil fertility is strongly
negative, due largely to the dominance of dwarf-shrub
plant species that produce poor quality litter (Bardgett et
al. 1997).
In the past, human colonization of new regions often
coincided with extinctions of megaherbivore species,
although in many cases, the extent to which these
extinctions were caused by humans or by other mechanisms, such as climate and vegetation shifts, remains
uncertain (Zimov et al. 1995; Guthrie 2003). Over this
longer timeframe, extinctions of mammal species probably had important, though poorly understood, effects
on the belowground subsystem. For example, it has
been proposed that megaherbivore extinctions in
Alaska and Russia 10 000–12 000 years ago led to the
transformation of vegetation from grazed steppe grassland to wet moss tundra (Zimov et al. 1995). The proliferation of plant species which produce poorer litter
quality, greater waterlogging, and retardation of soil N
mineralization, provided a feedback that maintained
the dominance of the tundra vegetation (Figure 5). In
instances in which human colonization led to extinctions of megaherbivore species, there were probably
major, irreversible consequences for aboveground–belowground linkages and therefore ecosystem
properties.
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151
Human-induced changes in large herbivorous mammal density
152
High evapotranspiration
Dry soils
Reproduced with permission from Princeton University Press
DA Wardle and RD Bardgett
Moist soils
High soil oxygen
Low soil oxygen
High mineralization rates
High
litter
quality
High nutrient
availability
PRODUCTIVE
STEPPE
Low evapotranspiration
Megaherbivores
Feces
urine
Low mineralization rates
MEGA HERBIVORE
EXTINCTION
Surface
disturbance
Low nutrient
availability
Low
litter
quality
UNPRODUCTIVE
TUNDRA
Low surface
disturbance
Figure 5. Effects of megaherbivore extinction in northern Russia and western Alaska in the late Pleistocene on feedbacks between
vegetation and nutrient cycling, as hypothesized by Zimov et al. (1995)(Wardle 2002).
Conclusions
Acknowledgements
The above examples show that human-induced changes
in large mammal densities can exert important influences on decomposer organisms and processes, and that
these effects subsequently influence the supply of nutrients available to plants, and therefore vegetation productivity and composition. A range of mechanisms exist
through which herbivory by large mammals can affect
decomposers (both positively and negatively), and different mechanisms dominate in different situations. This is
especially apparent in the case of invasive deer in New
Zealand and reindeer in Fennoscandia; in both cases
described, animal exclusion was found to either promote
or retard soil organisms and processes, depending on
local conditions.
The way human-induced changes affect native communities and ecosystems is of direct relevance to land
management, which often focuses on restoring animals
to the densities in which they existed in the absence of
human activity – something that is theoretically possible
(although often costly and impracticable) except where
global extinction has occurred. A key component of
management and the setting of conservation priorities is
to determine the ecological impacts of changes in large
mammal densities as a result of human activity.
Traditionally, this has been done by observing the effects
of these mammals on vegetation, often by using exclusion plots. However, this approach is incomplete, especially if we are to adopt a more explicit ecosystem-oriented approach to land management. Any ecosystem
approach requires us to consider both the aboveground
and belowground consequences of changes in animal
populations, as well as the long-term consequences of
these for key ecosystem properties. Human-induced
changes in the densities of large herbivorous mammals
represent a major, but under-appreciated, element of
global change, and consideration of the influence of
these animals in an aboveground–belowground context
will enable us to better understand their substantial ecological impacts.
We thank Rob Allen for helpful comments on the
manuscript, and D Marquis for the photograph shown in
Figure 3c.
www.frontiersinecology.org
References
Augustine DJ and McNaughton SJ. 1998. Ungulate effects on the
functional species composition of plant communities: herbivore selectivity and plant tolerance. J Wildlife Manage 62:
1165–83.
Bardgett RD and Wardle DA. 2003. Herbivore mediated linkages
between aboveground and belowground communities. Ecology
84: 2258–68.
Bardgett RD, Leemans DK, Cook R, and Hobbs PJ. 1997.
Seasonality of soil biota of grazed and ungrazed hill grasslands.
Soil Biol Biochem 29: 1285–94.
Bardgett RD, Wardle DA, and Yeates GW. 1998. Linking aboveground and below-ground interactions: how plant responses to
foliar herbivory influence soil organisms. Soil Biol Biochem 30:
1867–78.
Bokhari UG and Singh JS. 1974. Effects of temperature and clipping on growth, carbohydrate reserves and root exudation of
western wheatgrass in hydroponic culture. Crop Sci 14: 790–94.
Bråthens KA and Oksanen J. 2001. Reindeer reduce biomass of
preferred plant species. J Veg Sci 12: 473–80.
Coppock DL, Detling JK, Ellis JE, and Dyer ME. 1983. Plant–herbivore interactions in a North American mixed-grass prairie.
II. Responses of bison to modification of vegetation by prairie
dogs. Oecologia 56: 10–15.
Davidson DW. 1993. The effect of herbivory and granivory on terrestrial plant succession. Oikos 68: 23–35.
Den Herder M, Kytöviita MM, and Niemelä P. 2003. Growth of
reindeer lichens and effects of reindeer grazing on ground cover
vegetation in a Scots pine forest and a subarctic heathland in
Finnish Lappland. Ecography 26: 3–12.
De Mazancourt C, Loreau M, and Abbadie L. 1998. Grazing optimization and nutrient cycling: when do herbivores enhance
plant production? Ecology 79: 2242–52.
Duncan KW and Holdaway RN. 1989. Footprint pressures and
locomotion of moas and ungulates and their effects in the
indigenous biota by trampling. New Zeal J Ecol 12: 97–101.
Findlay S, Carreiro M, Krischic V, and Jones CJ. 1996. Effects of
damage to living plants of leaf litter quality. Ecol Appl 6: 269–75.
Frank DA, Groffman PM, Evans RD, and Tracy BF. 2000. Ungulate
stimulation of nitrogen cycling and retention in Yellowstone
Park grasslands. Oecologia 123: 116–21.
© The Ecological Society of America
DA Wardle and RD Bardgett
Grime JP, Cornelissen JHC, Thompson K, and Hodgson JG. 1996.
Evidence of a causal connection between anti-herbivore
defense and the decomposition rate of leaves. Oikos 77:
489–94.
Guitian R and Bardgett RD. 2000. Plant and soil microbial
responses to defoliation in temperate semi-natural grassland.
Plant Soil 220: 271–77.
Guthrie RD. 2003. Rapid body size decline in Alaskan Pleistocene
horses before extinction. Nature 426: 169–71.
Hamilton EW and Frank DA. 2001. Can plants stimulate soil
microbes and their own nutrient supply? Evidence from a grazing tolerant grass. Ecology 82: 2397–402.
Harrison KA and Bardgett RD. 2004. Browsing by red deer negatively impacts on soil nitrogen availability in regenerating forest. Soil Biol and Biochem 36: 115–26.
Holland JN. 1995. Effects of above-ground herbivory on soil microbial biomass in conventional and no-tillage agroecosystems.
Appl Soil Ecol 2: 275–79.
Horsley SB, Stout SL, and de Calesta DS. 2003. White-tailed deer
impact on the vegetation dynamics of a northern hardwood
forest. Ecol Appl 13: 98–118.
Johnson LC and Matchett JR. 2001. Fire and grazing regulate
belowground processes in tallgrass prairie. Ecology 82: 3377–89.
Kielland K and Bryant JP. 1998. Moose herbivory in taiga: effects
on biogeochemistry and vegetation dynamics in primary succession. Oikos 82: 377–83.
Knapp AK, Blair JM, Briggs JM, Collins, et al. 1999. The keystone
role of bison in North American tallgrass prairie. Bioscience 49:
39–50.
Krueger K. 1986. Feeding relationships among bison, pronghorn
and prairie dogs: an experimental analysis. Ecology 67: 760–70.
McGlone MS and Clarkson BD. 1993. Ghost stories: moas, plant
defenses and evolution in New Zealand. Tuatara 32: 1–18.
McNaughton SJ. 1985. Ecology of a grazing system: the Serengeti.
Ecol Monogr 55: 259–94.
McNaughton SJ, Osterheld M, Frank DA, and Williams KJ. 1989.
Ecosystem level patterns of primary productivity and herbivory
in terrestrial habitats. Nature 341: 142–44.
McNaughton SJ, Banyiwka K, and McNaughton MM. 1998. Root
biomass and productivity in a grazing system: the Serengeti.
Ecology 79: 587–92.
Mikola J, Yeates GW, Barker GM, et al. 2001. Effects of defoliation
intensity on soil food web properties in an experimental grassland community. Oikos 92: 333–43.
Milchunas DG and Lauenroth WK. 1993. Quantitative effects of
grazing on vegetation and soils over a global range of environments. Ecol Monogr 63: 327–66.
Olofsson J and Oksanen L. 2002. Role of litter decomposition for
the increased primary production in areas heavily grazed by
reindeer: a litterbag experiment. Oikos 96: 507–12.
Pastor J, Naiman RJ, Dewey B, and McInnes P. 1988. Moose,
microbes and the boreal forest. Bioscience 38: 770–77.
Pastor J, Dewey B, Naiman RJ, et al. 1993. Moose browsing and soil
fertility in the boreal forests of Isle Royale National Park.
Ecology 74: 467–80.
Person BB, Herzog MP, Ruess RW, et al. 2003. Feedback dynamics
of grazing lawns: coupling vegetation change with animal
© The Ecological Society of America
Human-induced changes in large herbivorous mammal density
growth. Oecologia 135: 583–92.
Pimm SL, Russell GJ, Gittleman JL, and Brooks TM. 1995. The
future of biodiversity. Science 269: 347–50.
Ramsey P. 1996. Revival of the land: Creagh Meagaidh National
Nature Reserve. Edinburgh, UK: Scottish Natural Heritage.
Rodwell JS. 1992. Grassland and montane communities. British
plant communities. Volume 3. Cambridge, UK: Cambridge
University Press.
Rooney TP and Waller DM. 2003. Direct and indirect effects of
white-tailed deer in forest ecosystems. Forest Ecol Manag 181:
165–76.
Ruess RW and McNaughton SJ. 1987. Grazing and the dynamics
and energy related microbial processes in the Serengeti grassland. Oikos 49: 101–10.
Ruess RW, Hendrick RL, and Bryant JP. 1998. Regulation of fine
root dynamics by mammalian browsers in early successional
Alaskan taiga forests. Ecology 79: 2706–20.
Seastedt TR, Ramundo RA, and Hayes DC. 1988. Maximization of
densities of soil animals by foliage herbivory: empirical evidence, graphical and conceptual models. Oikos 51: 243–48.
Stark S and Grellmann D. 2002. Soil microbial responses to herbivory in an arctic tundra heath at two levels of nutrient availability. Ecology 83: 2736–44.
Stark S, Tuomi J, Strömmer R, and Helle T. 2003. Non-parallel
changes in soil microbial carbon and nitrogen dynamics due to
reindeer grazing in northern boreal forests. Ecography 26:
51–59.
Stark S, Wardle DA, Ohtonen R, et al. 2000. The effect of reindeer
grazing on decomposition, mineralisation and soil biota in a dry
oligotrophic Scots pine forest. Oikos 90: 301–10.
Suominen O. 1999. Impact of cervid browsing and grazing on the
terrestrial gastropod fauna in the boreal forests of
Fennoscandia. Ecography 22: 651–58.
Tracy BF and Frank DA. 1998. Herbivore influence on soil microbial biomass and nitrogen mineralization in a northern grassland ecosystem: Yellowstone National Park. Oecologia 114:
556–62.
Väre H, Ohtonen R, and Mikkola K. 1996. The effect and extent
of heavy grazing by reindeer in oligotrophic pine heaths in
northeastern Fennoscandia. Ecography 19: 245–53.
Vazquez DP. 2002. Multiple effects of introduced mammalian herbivores in a temperate forest. Biol Invasions 4: 175–191.
Vitousek PM, D’Antonio CM, Loope LL, et al. 1997. Introduced
species: a significant agent of global change. New Zeal J Ecol
21: 1–16.
Wardle DA. 2002. Communities and ecosystems: linking the
aboveground and belowground components. Princeton, NJ:
Princeton University Press.
Wardle DA, Barker GM, Yeates GW, et al. 2001. Introduced browsing mammals in natural New Zealand forests: aboveground and
belowground consequences. Ecol Monogr 71: 587–614.
Wardle DA, Bonner KI, and Barker GM. 2002. Linkages between
plant litter decomposition, litter quality, and vegetation
responses to herbivores. Funct Ecol 16: 585–95.
Zimov SA, Chuprynin VI, Oreshko AP, et al. 1995. Steppe–tundra
transition: a herbivore-driven biome shift at the end of the
Pleistocent. Am Nat 146: 765–94.
www.frontiersinecology.org
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