2013
Grazing in wetlands:
aboveground and belowground
responses to herbivory
Annelon Bollen
Utrecht University
30-1-2013
Grazing in wetlands: aboveground and belowground responses to herbivory
30 januari 2013
Index
Summary ................................................................................................................................................. 3
Introduction ........................................................................................................................................... 3
1.1 The effect of grazing on biochemical processes ............................................................................ 6
1.1.1 Changes in the microbial community induced by grazing .................................................... 7
1.2 How does grazing affect the phosphorus cycle? ........................................................................... 8
1.2.1 The phosphorus cycle............................................................................................................... 8
1.2.2 Phosphorus in the soil .............................................................................................................. 8
1.2.2.1 Plant-available inorganic P ............................................................................................... 8
1.2.2.2 Organic P ............................................................................................................................ 8
1.2.2.3 Less available inorganic P ................................................................................................. 8
1.2.3 How does grazing affect the movement of phosphorus through a system? ........................ 8
1.3 How does grazing affect the nitrogen cycle? ............................................................................... 10
1.3.1 The nitrogen cycle .................................................................................................................... 10
1.3.2 How does grazing affect the movement of nitrogen through a system? ............................ 10
1.3.3 Processes that enhance the nitrogen cycle ........................................................................... 11
1.3.4 Processes that slow down the nitrogen cycle....................................................................... 12
1.3.5 What determines the effect of grazing on the nitrogen cycle? ............................................ 12
1.4 How does grazing affect the carbon cycle? .................................................................................. 14
1.4.1 The carbon cycle ....................................................................................................................... 14
1.4.2 How does grazing affect the movement of carbon through a system? ............................... 14
1.4.3 Processes that enhance the carbon cycle.............................................................................. 15
1.4.4 Processes that slow down the carbon cycle ......................................................................... 15
1.4.5 Global warming and the influence of grazing ....................................................................... 16
1.4.6 The effect of herbivorous waterfowl on methane emissions .................................................. 18
2.1 Vegetation responses to grazing .................................................................................................. 21
2.1.1 Herbivore selectivity .............................................................................................................. 21
2.1.2 Changes in primary production in response to herbivory........................................................ 23
2.1.2.1 Belowground plant biomass response .............................................................................. 24
2.1.2.2 Aboveground plant responses to grazing ......................................................................... 26
2.2 Do the species richness and composition change in wetlands when grazing takes place? ..... 27
2.2.1 The effect of grazing on species richness and composition ................................................ 27
2.3 Does grazing have any influence on the functioning and structure of wetlands? .................... 30
2.3.1 The influence of grazing on the structure of wetland vegetation ....................................... 30
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Annelon Bollen
Utrecht University
2.3.1.1 Succession ........................................................................................................................ 30
2.3.1.2 Vegetation structure ........................................................................................................ 31
2.3.1.3 The influence of large water birds and muskrats on the vegetation structure ................ 33
2.3.2 The influence of grazing on the functioning of a wetland ................................................... 35
2.3.2.1. Birds ................................................................................................................................. 35
2.3.2.2 Invertebrates.................................................................................................................... 36
2.3.2.3 Soil characteristics ........................................................................................................... 36
Discussion .............................................................................................................................................. 38
Biogeochemical responses ................................................................................................................ 38
Vegetation responses ........................................................................................................................ 38
Grazing as a management tool.......................................................................................................... 39
Future recommendations.................................................................................................................. 39
Conclusion ............................................................................................................................................. 40
References ............................................................................................................................................. 41
Grazing in wetlands: aboveground and belowground responses to herbivory
30 januari 2013
Summary
Wetlands have been grazed for many centuries, however this happened by natural grazers like
deer and elk. In the last couple of decades humans introduced cattle as a management tool on
peat meadows. This change in type of grazer and grazing intensity have a large effect on the
cycling of nutrients in the system and determine for a large part the vegetation response. The
cycling of nutrients is strongly influenced by the activity of the soil microbial community, and
these organisms respond to the soil characteristics and the quality of litter. Herbivores influence
both these factors and are therefore responsible for the acceleration or deceleration of the
nutrient cycles. The vegetation response is largely based on the foraging behaviour of the
herbivore. Differences in foraging behaviour explain for a large part the possible shift in species
richness and composition, however both these things are also dependent on the type of wetland.
Additional to the human-induced grazing by cattle in these systems, wetlands are also
threatened by the grazing of muskrats and several herbivorous water bird species. So far not
much literature is available on the threats these herbivores pose on the environment. However, it
is certain that they have a large negative effect on the structure of the vegetation, and thereby
influence the functioning of wetlands.
Herbivory – Wetlands – Waterfowl – Nutrient cycling – Soil microbial community – Primary
productivity – Species diversity – Succession
Introduction
Wetlands are threatened by intensified land usage and disrupting management practices among
other things. A combination of these threats is present in the form of grazing. Grazing is often
used as a management practice with the goal of maintaining the natural biodiversity and
preventing succession (Bokdam et al. 2002; Oene et al. 1999). However, this is often disruptive
instead of helpful, since the wrong type of herbivores, and in the wrong quantities are allowed to
graze on the wetlands (Bokdam et al. 2002). To understand why grazing is often disruptive
instead of helpful this thesis will focus on the effects of grazing on the biochemical processes that
take place in the soil, and the response of the vegetation to grazing.
The original vegetation that grows in wetlands is negatively influenced by several, human
induced, threats. Grazing, among an increased input of ammonia and the (deliberate)
introduction of exotic species threatens the original species diversity. However, the most
threatening is not human induced but is actually the natural process of succession (Aptroot et al.
2007). The succession that moves the vegetation from a species-poor pioneer vegetation to more
species-rich herb vegetation is ultimately replaced by a more species-poor shrub and tree
vegetation (Smith et al. 2006; Aptroot et al. 2007).
Several studies have shown that grazing in wetlands prevents succession and helps
maintain species diversity (Aptroot et al. 2007). However, this is largely dependent on the type
and amount of grazers that are present. Looking from a historic viewpoint, it can be argued
whether or not grazing in an invasive practice in wetlands. Before livestock farming was widely
used, wetlands were grazed by several large ungulates like Elk and Moose (Alces alces) and Red
deer (Cervus elaphus). It is therefore difficult to determine if grazing has a destructive effect on
vegetation richness and composition or not (Middleton et al. 2006). When grazers are removed
from a system an encroachment by shrubs takes place, this change in environmental conditions
results in species replacement, which effectively lowers the floral diversity of the wetland
(Middleton et al. 2006; Smith et al. 2006). It can therefore be reasoned that, in the past, the
grazing by Elk, Moose and Red deer was not disruptive but actually played a large role in
maintaining the vegetation of a wetland (Middleton et al. 2006). In an attempt to maintain the
original species diversity, grazing in wetlands by species that show the same feeding preferences
as the above mentioned wildlife could have a large impact.
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Annelon Bollen
Utrecht University
Floral diversity and composition are not the only things that are influenced by herbivory. In fact
several aspects are influenced that make it difficult to determine whether or not herbivory is a
threat to an ecosystem. The difficulty in determining the effect of grazing is largely caused by the
fact that not only the plants respond to the process of grazing. Ecosystems are affected by
grazing in several ways (Tanner 1992; Worralll et al. 2012):
- The removal of plant biomass, often through selective grazing on nutrient-rich and easily
accessible tissue, and also through defoliation. Defoliation influences the plants
reproduction, carbon storage, litter accumulation and production
- Trampling of the soil and plants. The trampling of soil reduces soil aeration and water
permeability, therefore strongly influencing microbial activity
- The addition of easily accessible nutrients through faeces and urine
- Through their excrement, herbivores also return easily degradable biomass to the
system. Since this material is easily degradable it lowers the rate of peat formation.
Since the microbial community in the soil is also influenced, grazing therefore causes a shift in
the turnover rate of nutrients that are available to the microbes, but also to the plants (Bakker et
al. 2004; Tanentzap et al. 2012). Another factor that makes it difficult to determine the effects of
grazing on the ecosystem, is the fact that many floral and microbial responses are not directly
caused by grazing, but are secondary responses, as is shown in Figure 1 (Bardgett et al. 1998).
Figure 1. Schematic overview of the plant-microbial responses to herbivory (Bardgett et al. 1998).
In this thesis several of the plant and microbial responses, shown in Figure 1, will be discussed.
The first part of the thesis will focus on the biogeochemical responses of the soil microbial
community, whereas the second part will look at the aboveground responses and the effects on
the ecological functioning of wetlands:
Part I – Biogeochemical cycles
1. How does grazing affect the phosphorus cycle?
2. How does grazing affect the nitrogen cycle?
3. How does grazing affect the carbon cycle?
Grazing in wetlands: aboveground and belowground responses to herbivory
30 januari 2013
Part II – Vegetation
4. How do the species richness and composition change in wetlands when grazing takes
place?
5. Does grazing have any influence on the functioning and structure of wetlands?
The first part will focus on the changes that take place in the microbial community when grazing
takes place and what the cause is of these responses. In these chapters the focus will be placed
on a general response, and will not focus specifically on wetlands, due to the fact that most
ecosystems show the same response and there is little literature focusing on wetlands. However,
references will be made to wetlands when important findings have been made in such an
ecosystem. An introduction will be given that explains how the microbes are influenced and
what their response is to the changes in the soil. In the following chapters an overview will be
given on how two important nutrient cycles are influenced and how the turnover of those
nutrient changes in an ecosystem. The phosphorus and nitrogen cycle will be discussed first
since these nutrients are two of the macronutrients for plants and is therefore a determining
factor in a plant’s response. The final chapter of part I will focus on the carbon cycle since many
wetlands can be seen as carbon sinks. The wetland types that will be discussed in that chapter
are peatlands, these peatlands have large amounts of carbon stored in them and grazing might
turn these peatlands in a carbon source. With the current discussions on climate change it is
important to determine what grazing on peatlands can do to the carbon storing capacity of these
systems (Tanentzap et al. 2012; Worralll et al. 2012).
Part II will focus on the vegetation and structure and function of wetlands. A general
introduction will be given on how grazers select their food, based on nutrient availability as
discussed in Part I, and the physiological responses of the vegetation to grazing. The following
chapters will focus on the vegetation response of different wetland types to grazing and what
that means to the species richness and composition as well as the wetland structure and
function. Species richness and the vegetation composition are discussed in the first chapter of
Part II. Changes in species richness are discussed for several wetland types and will show that
grazing does not always have a positive influence on the species richness and diversity. An
explanation will be given on why the vegetation responds differently to different types and
intensities of grazing. The final chapter will discuss how the wetland responds in terms of
structure and function. The different functions of wetlands will be discussed and how grazing
influences them through changing the structure. Additional to that, this chapter will look at the
influence of grazing on succession and what that means for the structure of the wetland.
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Annelon Bollen
Utrecht University
1.1 The effect of grazing on biochemical processes
Part I will focus on the processes that play a role in the phosphorus, nitrogen and carbon cycles.
These cycles are influenced through several pathways by the grazing of aboveground biomass.
Many studies only look at the vegetation response to grazing, but do not take into account that
soil processes determine (for a large part) the actual response of the vegetation (Tanentzap et al.
2012; Worrall et al. 2012).
Grazing directly affects nutrient cycling, for example through the increased breakdown of
organic material in the herbivores digestive system. Grazing also has indirect effects, for instance
trampling which changes soil characteristics which influences the microbial community (Bakker
et al. 2004).
Figure 2 gives a schematic overview of the nutrient fluxes between the compartments of
the ecosystem. The fluxes are indicated by arrows, and whether or not the nutrient fluxes
accelerate or decelerate is indicated by a + or – sign. The dotted line indicates that the microbial
activity is dependent on soil characteristics like temperature and aeration, and these
characteristics are also influenced by herbivory. For that reason the actual effect of grazing on
the microbial activity is therefore difficult to determine. The figure shows that herbivory
influences the fluxes of carbon, nitrogen and phosphorus through several pathways: in the
remainder of Part I the different fluxes will be discussed and how herbivory influences these
fluxes.
Figure 2. Schematic overview of the compartments and nutrient fluxes within an ecosystem that are influenced by
herbivory. The arrows represent processes that are responsible for the fluxes of carbon (C), nitrogen (N) and phosphorus
(P) between the different compartments. Whether or not these fluxes accelerate or decelerate because of herbivory is
indicated by a + or - sign, the ± sign indicates that herbivory can have an accelerating or decelerating effect but this is
dependent on the foraging behaviour of the herbivore or ecosystem characteristics.
Grazing in wetlands: aboveground and belowground responses to herbivory
30 januari 2013
1.1.1 Changes in the microbial community induced by grazing
The decomposition of dead organic matter by microbial activity can be influenced by herbivory.
The general effect is that grazing increases the rate of decomposition and thus the turnover rate
of nutrients. Several studies showed that grazing influences soil microbial biomass and the
number of soil microorganisms (for instance Bardgett et al. 1998; Bardgett et al. 2001; Bouasria
et al. 2012). Soil microbial biomass increases under a grazing regime, whereas the number of
microorganisms actually decreases (Bouasria et al. 2012).
Research has shown that herbivory has an effect on the microbial community of the soil
with a community that is dominated by bacteria in grazed systems, whereas ungrazed systems
contain a soil microbial community that is dominated by fungi. This has an influence on the
decomposition rate, with grazed systems supporting a faster decomposition cycle compared to
ungrazed systems (Figure 3). Several studies have shown that the ratio of decomposing fungi to
bacteria is negatively correlated with the nitrogen concentration of the soil (Bardgett et al. 1998;
Bardgett et al. 2001; Bouasria et al 2012). The presence of grazers in a system can cause
increased N availability and can therefore be seen as the cause of the shift in microbial
community.
Figure 3. Schematic overview of the shift in microbial
community structure that’s influenced by aboveground
grazing (Bardgett et al. 1998).
This change in microbial community structure is an important factor that is largely responsible
for the changes in nutrient cycling. However, the shift in dominance is not the only change that
takes place in the soil.
Another group of organisms that is influenced by grazing are the soil nematodes. These
organisms are influenced by grazing in several ways and it is largely dependent on the feeding
strategies of the nematodes. Many soil nematodes use bacteria as a food source and since the
biomass of the bacteria increases, the nematodes also flourish, resulting in a higher density of
nematodes in grazed areas compared to ungrazed areas. However, this also appears to be caused
by more favourable abiotic conditions for the nematodes, these abiotic conditions were
positively influenced by the presence of herbivores (Bardgett et al. 1998).
There is also a group of nematodes that feeds on roots instead of bacteria. These
nematodes are also positively influenced by grazing. When grazing takes place, plants that are
subject to nematode presence, allocate large amounts of carbon to their root system. This
response was weaker when nematodes were not present. This way nematodes caused a feedback
mechanism that would force the plant to allocate more C, which would increase the nematode
biomass (Bardgett et al. 1998). Beside increasing the total amount of C in the roots, the leakage
of C to the rhizosphere also increases when grazing takes place (Bardgett et al. 1998; Wang et al.
2006). This increased leakage of C can increase the amount of root-feeding nematodes as well as
other organisms that live in the rhizosphere (Walker et al. 2006; Wang et al. 2006).
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Annelon Bollen
Utrecht University
1.2 How does grazing affect the phosphorus cycle?
1.2.1 The phosphorus cycle
In contrast to the nitrogen and carbon cycle, the phosphorus cycle does not have a major
atmospheric component and moves solely through the terrestrial and aquatic pools (Figure 2).
Phosphorus is present in rock and phosphate deposits, and most terrestrial systems receive their
phosphorus through the weathering of calcium phosphate minerals (Smith et al. 2006).
In the soil, most phosphorus is not directly available to plants, and the phosphorus that
is available primarily comes from the decomposition of dead organic matter and from the faeces
of herbivores. Since herbivore activity influences the amount of faeces input and the rate of
decomposition it has a large potential of influencing the cycling of phosphorus (Smith et al.
2006; Campbell et al. 2005), as is shown in Figure 2.
1.2.2 Phosphorus in the soil
Three phosphorus pools can be identified in soils: 1) plant-available inorganic P (water soluble
P), 2) organic P (present in both living and dead organic material) and 3) less available inorganic
P (poorly soluble P, which is bound to clay particles). Grazing can influence in what direction and
how fast the P moves from one pool to the other (Leech 2009; Rui et al. 2012).
1.2.2.1 Plant-available inorganic P
Inorganic P that is available to plants usually makes up a very small part of the total amount of P
that is found in the soil (around 1%). This inorganic P is present in several forms, ranging from
the more soluble forms that are easily used by plants, to the less soluble forms that are more
difficult for a plant to use. Since plants use this P for their growth, it has to be replenished, if this
does not happen plant growth will become restricted due to P limitation. The inorganic P is
replenished through the release of P by clay minerals or through (organic) fertilizer input (Leech
2009).
1.2.2.2 Organic P
Phosphorus that is chemically bound in organic matter is called organic P. When this organic
matter is broken down, the P is released in a form that is available to plants. Through the
breakdown of plant material by herbivores the P is also released in a for plants available form,
however part of this P is also used by the herbivore and therefore removed from the phosphorus
cycle. The amount of P in a natural system is constant, since no P is removed from the system. P
that is removed through herbivory is returned when the herbivore dies or through its faeces
(Leech 2009).
1.2.2.3 Less available inorganic P
Phosphorus that is not associated with non-living material is often tightly bound to clay or other
soil particles. This P is not available to the plants, and it takes a very long time before it can
become available.
1.2.3 How does grazing affect the movement of phosphorus through a
system?
Grazing effects the rate at which phosphorous moves between the different pools in two ways: 1)
a decelerating effect since they use some of the P from their food for their own maintenance and
2) an accelerating effect by returning some of the P that was stored in plants to the organic and
available inorganic P pool (Figure 4).
Grazing in wetlands: aboveground and belowground responses to herbivory
30 januari 2013
Figure 4. Schematic overview of the cycling of phosphorus in a grazed and fertilized system. Units are kg
P/ha/year (after Leech 2009).
When plant material is broken down by bacteria in the rumen of the herbivore, some of the P will
be turned to the available inorganic P form and a small part of this P is used by the herbivore
itself. However, not all the material is broken down and some will remain in the organic P form,
which eventually will be returned to the soil in the form of faeces. This organic P will be turned
to available inorganic P by the decomposing microbes in the soil, thereby increasing the amount
of P available to plants (Figure 2, Figure 4).
This increase in available P will lead to an increase in amount of plant material, which in
turn increases the carrying capacity for grazers. These grazers will remove more plant material,
but in turn will also produce more faeces, therefore increasing the amount of inorganic and
organic P that is returned to the soil. This increase in organic matter will provide positive
feedback to the microbial community, which will increase in abundance, resulting in a higher
level of microbial activity. A higher microbial activity will increase the input of P to the available
inorganic P pool by increasing the rate of decomposition (Chaneton et al. 1996; Leech 2009).
The increase in available P for the plants is reflected in the amount of P uptake on grazed
grasslands compared to ungrazed grasslands. Nutrient uptake can become 50% higher in grazed
systems, which is related to the increased rate of nutrient mineralization. In these grazed
grasslands, grazing did not increase the total amount of P that was present in the soil, it did
however increase the cycling of P through the system. This was caused by the removal of P by
herbivores, which caused a feedback mechanism that made the plant increase the uptake of P
(Chaneton et al. 1996).
The deceleration effect is only temporary, since the P will be returned to the system when the
herbivore dies and its organic material is decomposed by the microbial community. However,
when the grazing pressure is very high, large amounts of P will be removed from the system.
When this occurs, plant growth will be limited by P (Chaneton et al. 1996; Leech 2009).
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Annelon Bollen
Utrecht University
1.3 How does grazing affect the nitrogen cycle?
1.3.1 The nitrogen cycle
When looking at the nitrogen cycle it is important to note is that to plants nitrogen is generally
available in only two forms, ammonium (NH4+) and nitrate (NO3-). Both ammonium and nitrate
are formed by bacteria living in the soil. Beside these bacteria, certain terrestrial plants like
legumes, live in symbiosis with mycorrhizal fungi, these fungi assist the plant with nutrient
uptake (Campbell et al. 2005; Smith et al. 2006).
Ammonium can be formed in two ways or 'paths', the first pathway starts with the fixation of
atmospheric nitrogen. This nitrogen (N2) splits in 2 atoms that bind with H+ in the soil resulting
in ammonia (NH3) and ammonium (NH4+). The second pathway through which NH4+ becomes
available in the soil is through the decomposition of dead matter by microbial decomposition.
When microbes decompose organic matter, they produce NH3 as a waste product, and this NH3
can be converted to NH4+ (Zak et al. 1991; Campbell et al. 2005; Smith et al. 2006).
The formation of Nitrate (NO3-) is called nitrification (Equation 1). Nitrification takes
place in multiple steps and is done by aerobic bacteria that oxidise NH4+ to NO2- and NO2- to NO3-.
In ecosystems where there is a lack of oxygen, like many wetlands, a group of bacteria
(Pseudomonas) can convert the NO3- to N2O and N2 (as shown in Equation 2), this process is
called denitrification (Zak et al. 1991; Campbell et al. 2005; Smith et al. 2006).
Equation 1
2 NH4+ + 3 O2 →2 NO2- + 2 H2O + 4 H+
2 NO2- + O2 → 2 NO3- + energy
Equation 2
2 NO3- + 10 e- + 12 H+ → N2 + 6 H2O
As shown in Figure 2, the processes that are part of the nitrogen cycle can be influenced by
herbivores. These influences can be direct or indirect and will be discussed in more detail in this
chapter.
1.3.2 How does grazing affect the movement of nitrogen through a system?
In most terrestrial systems, including wetlands, most nitrogen is stored in soil organic matter,
which has a low turnover rate (Figure 5). Plants that are not exposed to grazing eventually die
and the nutrients from the litter become available again in the cycle. When this litter is
decomposed, part of the nutrients become available again, whereas the rest becomes part of the
soil organic matter which has a slow turnover rate. Herbivory leads to a cycle with a much faster
turnover rate. Plant material that has been eaten is broken down by the digestive system of the
herbivore and part of the nutrients return to the cycle in the animal’s faeces. These nutrients are
all available to plants, and none of them become part of the soil organic matter (Bakker et al.
2004). Grazing also has some indirect effects, with the most prominent one being an influence on
the vegetation composition (this will be discussed in part II). Besides that it also influences some
soil characteristics, namely the temperature, moisture content and aeration. The effect of these
factors will be discussed. However these changes appear to be highly dependent on herbivore
size and behaviour. Large herbivores, like cattle, trample the ground, resulting in reduced
aeration and making the soil more compact. Smaller herbivores, like the muskrat (Ondatra
zibethicus), do not have this effect and their creation of burrows can actually make the soil less
compact and increase aeration (Connors et al. 2000; Bakker et al. 2004).
Grazing in wetlands: aboveground and belowground responses to herbivory
30 januari 2013
Figure 5. Schematic overview of the nitrogen cycle that takes place below- and
aboveground. Slow cycle shows the ungrazed pathway and the fast cycle shows
the nitrogen pathway when grazing takes place (Bakker et al. 2004)
1.3.3 Processes that enhance the nitrogen cycle
As mentioned above, grazing has several ways in which it influences the nitrogen cycle. Some of
these effects accelerate the cycle whereas others slow it down. Looking at figure 5 it shows that
the faster cycle is solely based on the digestion of plant material by herbivores. ). The cycle is
enhanced by the digestive system of the herbivore. In the digestive system temperature and
moisture content are higher compared to the soil. These conditions result in a higher rate of
organic breakdown. Additionally the plant material is also fragmented, making breakdown easier
(Bakker et al. 2004; Smith et al. 2006).
The return of N is dependent on the size of the herbivore, smaller herbivores spread the
N to a larger area because they produce small pellets. Whereas large herbivores return the N in
small patches. This difference can result in a difference in N availability with pellets from small
herbivores returning N to the system that is more readily available to plants (Bakker et al. 2004
The grazing of the vegetation has an indirect effect on the soil temperature, through the
removal of coverage. Due to this removal, the soil and the air above the soil, become warmer than
in ungrazed areas (Wan et al. 2002). The increased soil temperatures have a positive effect on
the mineralization of nitrogen (Sierra 1997). The mineralization is enhanced because
decomposition goes faster when the temperature is higher (Smith et al. 2006). As mentioned
before the burrowing that is done by smaller herbivores, like the muskrat and rodents, can result
in a more aerated soil. The increase in aeration makes it possible for nitrification to take place
since it is an aerobic process. This increase in aeration is especially important in wetlands, since
its soil usually lacks large amounts of oxygen due to the high water content (Connors et al 2000;
Bakker et al. 2004; Smith et al. 2006).
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Annelon Bollen
Utrecht University
1.3.4 Processes that slow down the nitrogen cycle
There are several ways in which grazing can actually slow down the nitrogen cycle (Figure 6b).
One of these ways is related to the grazing behaviour of the herbivore. Smaller herbivores are
more selective when it comes to their food than large herbivores, as they tend to feed mostly on
plants that have high tissue N. This selectivity can influence the N cycling in a negative way, as it
can slow down the cycling of N due to the removal of plant species that are rich in N (Ritchie et
al. 1998; Bakker et al 2004). This negative effect becomes even more apparent when the
herbivore selects nitrogen fixers. The return of N to the system through the waste products still
takes place, but it is not enough to offset the deceleration of the cycle that takes place due to a
lowering of the aboveground productivity (as shown in 6b)(Ritchie et al. 1998).
Grazing can also have indirect, but still negative effects, this is caused by the effects of grazing on
soil temperature, aeration and moisture content (Figure 5). As mentioned before an increase in
soil temperature is actually good for the turnover rate of the nitrogen cycle, it has the side effect
of increasing the evaporation rate of water from the soil. This lowering of the soil moisture
content, has actually a negative effect on the turnover rate of nitrogen in the soil. When grazing
in question is done by large herbivores, the effects on moisture content of the soil is increased.
This increase is due to the weight of these animals, as they graze this weight causes the soil to
become more compact, resulting in a loss of porosity, and thus a lowering of the ability of the soil
to take up water (Pietola et al. 2004). This loss of porosity increases the risk of surface runoff,
which can result in the runoff of nutrients that are delivered on top of the surface (faeces, wetfall,
etc.) (Bakker et al. 2004; Pietola et al. 2004). By making the soil more compact, it also becomes
more difficult for the soil to contain oxygen, which will lower the process of nitrification, while
making denitrification more effective (Smith et al. 2005; Campbell et al. 2006).
1.3.5 What determines the effect of grazing on the nitrogen cycle?
Some studies state that the herbivores actually control ecosystem functions, because of how they
influence the feedback mechanisms between (dominant) plant species and nutrient cycles. These
studies focus on two hypotheses (Figure 6). The first of these hypotheses state that grazing has
an accelerating effect on the nutrient cycle (Figure 6a) (Pastor et al. 1997; Ritchie et al. 1998).
The enhancing effect of herbivores on the nitrogen cycle is based on the principle that
plant species that tolerate herbivory lose more nutrient rich tissue because they are being
grazed. However, these plants can compensate this loss of nutrient rich tissue, because they have
a faster nutrient uptake, higher concentrations of nutrients in their tissue and a higher relative
growth rate (Pastor et al. 1997; Ritchie et al. 1998). While this seems counterproductive, the end
result of these changes, is that a higher rate of nutrient turnover and litter decomposition is
reached. This, when combined with the N input through herbivore faeces, means a large N
supply rate is reached. This higher nutrient supply rate is positive for the plants, because it
makes it possible for them to compete with plants that do not tolerate grazing. The feedback
mechanisms that are influenced by grazing are thus positively influenced: higher aboveground
plant productivity and a higher rate of nutrient cycling (Ritchie et al. 1998).
As shown in Figure 6b it can also be argued that grazing negatively influences the feedback
mechanism between plants and the nutrient cycle (Pastor et al. 1997; Ritchie et al. 1998).
This negative effect has the same foundation as the hypothesis that focuses on the positive effect
of grazing. Herbivores are expected to select plants that have a nutrient rich tissue, and this
would result in a loss of these species in the vegetation. The plants that have mechanisms that
prevent grazing, or that have nutrient poor tissue would become more dominant in the
vegetation. Litter that comes from these species are less degradable and will result in a slower
nutrient turnover and lower N availability. This lower availability can be a positive feedback for
the nutrient poor plants, because they are often better nutrient competitors. When following this
hypothesis, herbivores can reduce the aboveground biomass, while at the same time slowing
down nutrient cycling (Pastor et al. 1997; Ritchie et al. 1998).
Grazing in wetlands: aboveground and belowground responses to herbivory
30 januari 2013
Figure 6. Schematic overview of the feedback loops that show the A) accelerating effect and the B)
decelerating effect herbivory can have on the cycling of nutrients in a system. Arrows indicate the effect
herbivory has on the abundance of plants or the rate of processes (Ritchie et al. 1998).
When comparing the above mentioned hypotheses about the effect of grazing on the nitrogen
cycle, it becomes clear that the actual response of plants to herbivory is still unclear. The
hypotheses are both valid, but which one takes place is dependent on the ecosystem, the type of
plants that are present, but the most important factor determining the response is the amount of
available N in the system.
When looking at the different ways on how grazing can affect the nitrogen cycle, it can be
reasoned that the actual response is determined by the resource that limits plant growth.
Systems in which plant productivity is limited due to a low N availability, dominant plants will
contain lower tissue N, grazing will then slow down the nitrogen cycle. This deceleration takes
place because herbivores will remove the species with high tissue N, the remaining plants will
then contain low tissue N, and litter from these plants decompose slowly (Ritchie et al. 1998;
Bakker et al. 2004).
However, In systems where N is not a limiting factor for plant productivity, dominant plants are
expected to have higher tissue N and since N is not limiting in these systems, the plants can
maintain this high concentration of N. This higher concentration of N in the system is maintained
through the decomposition of easily degradable plant litter and the return of N through waste
products. These factors allow a high N mineralization rate, which in turn allows plants to
maintain a high N concentration in their tissue. In some ecosystems (North-American prairie
and grasslands), herbivores stimulate plants that are rich in tissue N to increase their growth
rate, in this way the herbivores provide a positive feedback to the plants to make more tissue
that is rich in N which in turn increases the food availability of the plants. The exact mechanism
of this process is however not clear, and has not been tested in many ecosystems (Ritchie et al.
1998; Tanentzap et al. 2012). The above mentioned hypotheses show that the actual response
of an ecosystem can be predicted based on the factor that limits plant growth, but that the
interaction between herbivore and plant also plays a role in the actual response of the nitrogen
cycle.
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Annelon Bollen
Utrecht University
1.4 How does grazing affect the carbon cycle?
1.4.1 The carbon cycle
In contrast to the nitrogen cycle, there is only one form in which carbon enters an ecosystem.
Carbon enters the ecosystem in the form of carbon dioxide, which is used by plants in the
process of photosynthesis (Equation 3)(Campbell et al. 2005; Smith et al. 2006).
Equation 3
6 CO2 + 12 H2O + light (energy) → C6H12O6 + 6 O2 + 6 H2O
In terrestrial systems most carbon is stored in the soil in the form of dead organic matter and a
small part is stored in living matter like plants and animals. The value of stored carbon in the soil
is largely based on the activity of decomposers. The activity of the decomposers is dependent on
many factors, including moisture content, temperature, aeration and pH. Many wetlands, most
importantly peatlands, have characteristics that strongly inhibit decomposition, resulting in a
buildup of dead organic matter and thus the storage of carbon dioxide (Campbell et al. 2005;
Smith et al. 2006). As mentioned before, these characteristics are influenced by herbivory, and
therefore grazing will have an effect on the carbon cycle (Figure 2).
1.4.2 How does grazing affect the movement of carbon through a system?
In Part II, an overview will be given on how grazing affects aboveground biomass. In this chapter
only the belowground carbon stocks will be taken into account. The understanding of the
influence of herbivores on the belowground carbon stocks is important, since most of the carbon
in terrestrial ecosystems is actually stored belowground. There is, however, a relation between
the above and belowground carbon fluxes and that will be discussed as well).
A much used hypothesis about the effect of grazing on the carbon cycle is that the
consumption of plants by herbivores lowers the aboveground biomass, and since it is correlated
with belowground biomass, that should lower as well (Tanentzap et al. 2012). However, just as
with the nitrogen cycle, grazing also has many direct and indirect effects on the carbon cycle
(Figure 7). These effects can either enhance or slow down the carbon cycle, depending on the
herbivore, vegetation and soil characteristics.
When looking at the entire ecosystem, the indirect effects (C-emission from the soil) can
compensate for the direct effects (increased C-storage in aboveground biomass due to removal of
herbivory), thus no gain or loss in carbon will be reached (Tanentzap et al. 2012).
Figure 7. Schematic overview of the effects herbivory has on the cycling of
carbon in a system. Dark lines indicate fluxes that might increase due to
herbivory, grey lines represent fluxes that can decrease due to herbivory
(Tanentzap et al. 2012).
Grazing in wetlands: aboveground and belowground responses to herbivory
30 januari 2013
1.4.3 Processes that enhance the carbon cycle
There are several pathways through which grazing can accelerate the cycling of carbon in an
ecosystem. These enhancements are correlated to the movement of biomass through the system.
The consumption of plant material by herbivores enhances the carbon cycling in three different
ways, as shown in Figure 7, through respiration and CH4 emissions, excrement and death, and by
indirectly altering the processes of leaching and erosion (Tanentzap et al. 2012).
Herbivores enhance the cycling of carbon through CO2 respiration and the emission of
CH4, which is formed via fermentation. These forms of carbon return to the atmosphere and the
CO2 can be used by plants for photosynthesis. CH4 is a greenhouse gas (GHG) that has a high
warming potential, which will be discussed in detail later (Tanentzap et al. 2012; Worralll et al.
2012).
The excrement of herbivores does not return a lot of carbon to the soil (Tanentzap et al.
2012), however other nutrients, like nitrogen, are returned and can speed up the decomposition
of litter. This increased rate of decomposition would also increase the rate of microbial
respiration, resulting in a faster carbon flux to the atmosphere (Tanentzap et al. 2012; Worralll et
al. 2012). Upon death, the carcass of a herbivore could also increase microbial respiration as it
increases the availability of a large number of nutrients (Tanentzap et al. 2012).
Finally, it is also possible for herbivory to influence the carbon cycle by increasing soil
erosion and leaching. As grazing occurs it alters the amount of plant coverage, and the soil
becomes exposed to precipitation, which can cause soil erosion and carbon leaching (Tanentzap
et al. 2012). Trampling of the ground while grazing has the added effect of soil compaction, as a
result the soil becomes less porous, thus increasing surface runoff. These effects are often very
small, unless measured over extremely large periods of time. However the impact is far greater
in areas that are frequently flooded, such as riparian zones (Tanentzap et al. 2012).
As mentioned in the chapter about the nitrogen cycle, trampling also results in a loss of
soil aeration, this has important consequences for the CH4 emissions. This is especially
important for wetlands, which are often considered as a CH4 source, for they are often poorly
aerated which increases CH4 emissions (Pol et al. 1996; Ward et al. 2007). Through the process
of methanogenesis, degradation of organic matter takes place under anaerobic conditions, when
the only available electron acceptor is CO2. This reaction takes place in many wetlands, especially
on peat soils, since these systems are well hydrated and thus are poorly aerated while at the
same time containing large amounts of organic matter available for breakdown (Pol et al. 1996;
Ward et al. 2007).
Grazing also influences the CO2 fluxes of plants, under a grazing regime plants increase
their rate of photosynthesis. This results in an increase of CO2 storage, but at the same time
increases the respiration of the plants. However, this increase in photosynthesis is not enough to
offset the increase in CO2 emission through the process of respiration, the carbon balance of the
vegetation is therefore negative and the system can be seen as a carbon source (Clay et al. 2009;
Ward et al. 2007).
1.4.4 Processes that slow down the carbon cycle
As shown in Figure 7, herbivory has several ways through which it can slow down the cycling of
carbon. One of those is caused by the effect herbivory has on the vegetation, as the litter quantity
and quality can change due to grazing. The quantity of the litter can be lowered in two ways: (1)
the plant community can shift, resulting in an increase of plant species that produce less
litterfall, slowing down the input of material that can be decomposed and (2) the quantity can
also lower due to herbivores eating plant material, thereby removing potential litter (Pastor et al.
1997).
The effect on litter quality is more difficult to quantify and can actually work two ways.
Carbon stocks in the soil can increase when the vegetation shifts to species that produce litter
that is rich in lignin and other less degradable components. This litter is slowly broken down,
thus successfully increasing the soil carbon stocks. Several studies have shown that many species
that tolerate grazing produce lignified leaves, these leaves decompose very slowly, resulting in
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Annelon Bollen
Utrecht University
even slower breakdown of litter (Pastor et al. 1997; Tanentzap et al. 2012). When grazing takes
place on soils that are nutrient-rich, grazing can actually increase the turnover of carbon in the
system. In these systems carbon and other nutrients are returned to the system in a easily
accessible form (from waste products). This returned carbon is used for regrowth, and can,
together with other nutrients, be stored in aboveground vegetation structures When these
nutrient-rich structures get returned to the soil in the form of litter, it can increase the rate of
decomposition (Tanentzap et al. 2012).
Certain plant species also respond to grazing by increasing root exudation, thus losing
large quantities of carbon, to increase microbial activity. This way plants can increase the
respiration, activity and biomass of microbial organisms. Only plants that are adapted to grazing
show this type of response (Bardgett et al. 1998; Tanentzap et al. 2012). It is reasoned that these
plants increase the amount of root exudation to positively influence bacteria living in the soil. As
mentioned before, grazed areas show a faster decomposition pathway because bacteria are more
active than fungi, this can be caused by the increased root exudation (Bardgett et al. 1998).
1.4.5 Global warming and the influence of grazing
As mentioned before, peatlands contain large amounts of carbon (1 375 t C ha-1), which is stored
in peat (Tanentzap et al. 2012). This CO2 has been stored in the peatlands over long periods of
time: during the Holocene, peatlands of the northern hemisphere stored carbon at an average
rate of 0.96 Mt C/yr (Clay et al. 2009; Worrall et al. 2012). It is therefore clear that peatlands can
function as a carbon sink, but through certain management practices (drainage, burning, etc.) the
peatland can also function as a source since these practices damage the peat. Which function it
takes is dependent on both biotic and abiotic characteristics, and these characteristics can be
influenced by grazing. The presence of herbivores has therefore a large influence on the
functioning of peatlands (Clay et al. 2009; Ward et al. 2007; Worralll et al. 2012).
In 2012, Worralll et al. looked at the influence of sheep grazing on the greenhouse gas balance of
a northern peatland (in the UK). They determined that grazing by sheep influenced the carbon
balance of peatlands in several ways (Figure 8):
- Sheep presence has a direct effect on the emission of greenhouse gasses. Plant material is
converted by sheep in wool, meat and CO2 and CH4. Through the process of fermentation,
CH4 is formed, and this has a very high GHG warming potential (Ward et al. 2007;
Worralll et al. 2012). Beside that some of the excrement of sheep will release nitrous
oxides (N2O) when they are decomposed, N2O has an even higher warming potential than
CH4 (IPCC, 2007; Worrall et al. 2012).
- Trampling results in decreased aeration and therefore lowers the breakdown of organic
matter. This successfully reduces the amount of GHG emissions. At the same time, the
removal of vegetation as a result of trampling, results in runoff events that wash away
particulate organic carbon. Trampling of the soil also results in a rise of the groundwater
table, resulting in a decrease of dissolved organic carbon, while at the same time
lowering CO2 emissions from decomposers (Worralll et al. 2012).
- The turnover of carbon is increased, because sheep convert the vegetation into a form
that is more readily broken down than litter. Due to this, the formation of peat is reduced,
since the plant material that would become part of a new peat layer, is easily
decomposed and thus lost from the ecosystem (Tanentzap et al. 2012; Worralll et al.
2012).
Grazing in wetlands: aboveground and belowground responses to herbivory
30 januari 2013
Figure 8. A conceptual diagram, showing the greenhouse gas balance of sheep grazing.
Red arrows indicate fluxes, processes, flows and transfers that are caused by sheep grazing
(Worralll et al. 2012).
Their study showed that on northern peatlands grazing will result in a net decline of the GHG
flux from the system. 89% of this decline in flux was caused by the sheep itself and not by the
response of the vegetation or soil, it can therefore be concluded that the response of the entire
system is not unique to peatlands, but will be present in other systems that are grazed by sheep
as well. However it is important to note that, sheep are very inefficient when it comes to carbon
assimilation, their efficiency lies around 5%, meaning that for every kilogram of biomass they
create they have to consume 50kg of plant biomass. This way they return 49kg of easily
degradable matter to the system, this results in an increase of CO2 emissions from the system.
The final conclusion of their research was that the amount of sheep per hectare actually
determines if a peatland is a carbon source or sink. They showed that peatlands (UK) have a GHG
carry capacity, which is defined by the grazing intensity at which the flux of GHG emissions is
equal to the sink that the soil represents, and that his carry capacity lies between 0.2 and 1.7
ew/ha (depending on altitude). They compared this carry capacity with the amount of grazers
on the peatland and they found that in most cases too many sheep are present. Due to this
incorrect management of peatlands the GHG emissions of the system are often higher than it
could be (Worralll et al. 2010; Worralll et al. 2012)
In 2011, a similar study was done by Sjogersten et al., in their research they looked at the impact
of grazing by barnacle geese (Branta leucopsis) on two arctic tundra wetland systems. They
found that the removal of geese results in an increase in biomass of vascular plant species and
this caused the ecosystem to change from a carbon source to a carbon sink. This response of the
vegetation was caused by a change in CO2 uptake by the vegetation, whereas the CH4 flux and soil
organic carbon concentration did not change with the removal of the geese.
Besides the reduced amount of carbon uptake due to the presence of barnacle geese, the
presence of pink-footed geese (Anser brachyrhynchus) also lowered the CO2 uptake of the plants
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Annelon Bollen
Utrecht University
and of the soil. In this study it became clear that the removal of herbivores, or a lowering of their
density can be used to increase the net storage of carbon in the vegetation (Figure 9).
The response of the vegetation was relatively quick, the exclosures where grazing would
not take place have been present for 4 years, while these areas were heavily grazed for the past
20 years. When looking for ways to tackle the problem of global warming, the carbon storing
capacity of Arctic tundra should not be underestimated. By removing herbivores, or at least
lowering their density, the system is capable of successfully removing CO2 from the atmosphere
(Sjogersten et al. 2011).
Figure 9. Diurnal variation in net ecosystem exchange of CO2 in a grazed and ungrazed arctic wetland.
Positive values indicate emissions of CO2 whereas negative values represent an uptake of CO2 by the system.
Significant differences where present between 8AM and 8PM, error bars indicate the standard deviation
(taken from Sjogersten et al. 2011).
1.4.6 The effect of herbivorous waterfowl on methane emissions
Cattle, and other large grazers are not the only herbivores that have the potential to influence the
emissions of greenhouse gasses. In contrast to large herbivores, water birds and smaller
mammals lack the weight to significantly alter the soil through trampling. However, their
foraging behaviour is capable of modifying the soil microbial processes, thereby influencing the
emission rates of greenhouse gasses like methane (Figure 10) (Bodelier et al. 2006).
The study by Bodelier et al. (2006) showed that, the grazing of fennel pondweed
(Potamogeton pectinatus) by Bewick’s Swans (Cygnus colombianus bewickii) had an influence on
the production of CH4 in wetlands. The swans caused bioturbation in the soil, which influenced
the cycling of CH4 in the soil and the processes that determine the fate of the CH4. The extraction
of roots and tubers by the swans negatively influenced the activity of methanogenic Archaea,
while at the same time causing an increase in the rate of CH4 oxidation (Bodelier et al. 2006).
Aside from this direct effect on CH4 emission, the swans also had an indirect effect: the
removal of fennel pondweed, which reduces the density of the plants. This reduction in plant
density has negative effects on the CH4 production; removal of roots reduces the rhizosphere
area, and as mentioned in the previous chapter, plants release nutrients into the rhizosphere to
increase microbial activity. This reduction of rhizosphere area, also reduces the amount of
nutrients available to the CH4 consuming and producing microbes , thereby decreasing the
amount of CH4 which is formed in the wetland. However, the actual effect seems to be dependent
on soil type. In clay soils the consumption of CH4 was negatively influenced by grazing, this was
caused by the removal of roots. Plants introduce oxygen into the soil through the loss of radial
oxygen and this oxygen is used by the CH4-oxidizing bacteria. However, with the removal of roots
Grazing in wetlands: aboveground and belowground responses to herbivory
30 januari 2013
and tubers, the amount of oxygen released into the soil is reduced, thereby reducing the
consumption of CH4. This effect is less apparent in sandy soils, since the substrate is more porous
than clayey soil, it can therefore hold more oxygen.
In clayey soils, the production of CH4 increases at first, since the removal of roots and
tubers decreases the amount of oxygen present in the soil. The production of CH4 is an anaerobic
process, therefore the production rate will increase. This is only a short-term effect, since the
continuous grazing by swans will increase the bioturbation, therefore increasing the amount of
oxygen in the soil.
Figure 10. Schematic overview of the effect of swan grazing on the
emission of CH4 from a wetland. Solid lines indicate tested effects,
whereas the broken lines indicate proposed effects (Bodelier et al. 2006).
The effect of grubbing by swans is reasoned to decrease the CH4 emissions from a wetland.
However, not all herbivorous water birds grub, some tend to defoliate the plants instead of
pulling the tubers and rhizomes from the substrate. The defoliation of aquatic macrophytes by
water birds can actually lead to an increase in CH4 emissions (Dingemans et al. 2011).
The emission of methane can take place through the littoral zones, in these zones plants
form a connection between the soil and the atmosphere. Methane can move through intact
emergent macrophytes from the soil towards the atmosphere, and is largely responsible for the
emission of CH4 in these areas. Through diffusion and active transport it is possible for gasses to
be moved from the atmosphere to the soil and vice versa.
In the soil anaerobic bacteria produce CH4, which is absorbed through the roots and
eventually released into the atmosphere (Figure 11a). At the same time oxygen is taken from the
atmosphere by the plant and moved towards the roots. Damage from defoliation will result in an
open pathway between the soil and the atmosphere, therefore increasing the emission of CH4 by
the plants (Figure 11b). Meanwhile, the flux of oxygen to the soil will decrease since the amount
of photosynthesising tissue is lower than in intact plants, thereby slowing the flux of oxygen into
the plant (and the soil). When grazing takes place underwater, the emission of CH4 will happen at
a lower rate, since the diffusion rate of gasses through water is slower than through air (Figure
11c). Therefore the movement of oxygen from the atmosphere to the soil will slow down as well.
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Annelon Bollen
Utrecht University
The decreased flow of oxygen to the soil will result in an increased production of methane, since
this is an anaerobic process (Marlby et al. 2009; Dingemans et al. 2011).
Figure 11. Overview of the movement of gasses between the soil and atmosphere through the vegetation in three
situations. A) an ungrazed plot will show a methane flux from the soil to the atmosphere and an oxygen flux from the
atmosphere to the soil. B) a plot where the emergent parts of the vegetation is grazed, this will result in an increase in the
methane flux and a decrease in the oxygen flux through the damaged material. C) a plot where the vegetation is grazed
underwater will result in a slower flux of oxygen and methane since the movement of gasses through water is slower than
when it moves through air. The reduced flux of oxygen to the soil will result in an increase in methane production by the
anaerobic bacteria (Dingemans et al. 2011).
This study showed that there is a difference in emission rates, dependent on the plant structure
that is eaten. In contrast to Bodelier et al. (2006), this study showed that herbivory by water
birds can actually increase the emission rate of CH4. This makes clear that the type of grazer, and
its food preference will determine for a large part what will happen with the emissions of a
wetland. Animals that feed on emergent macrophyte, like many geese, muskrats, coypu and
certain fish species will likely increase the emissions, whereas herbivores that forage through the
process of grubbing (like many swan species) will actually help reduce the emissions (Bodelier
et al. 2006; Dingemans et al. 2011).
Research that looks at the effect of grazing and grubbing by swans only show an
influence on the methane emissions. Swans appear to have no (significant) effect on other parts
of the carbon cycle, nor do they seem to influence any of the other nutrient cycles in an
important way (Bodelier et al. 2006).
It can be concluded that more research is needed on the effects of grazing on the cycling of
nutrients and how it can influence the process of global warming. The schematic overview in
Figure 2 predict an increase in the rate of decomposition and therefore an increase in the rate of
nutrient cycling. However, as was expected the cycling of nutrient was also influenced by the soil
characteristics, and the type of plants and herbivores. From this we can hypothesize that not all
ecosystems and nutrient cycles will respond in the same way (Clay et al. 2009; Tanentzap et al.
2012; Worrall et al. 2012).
Grazing in wetlands: aboveground and belowground responses to herbivory
30 januari 2013
2.1 Vegetation responses to grazing
The response of the vegetation to grazing is largely determined by the type of herbivore and
which parts of the plants are eaten (Bakker et al. 1985). To predict the effect of grazing on the
vegetation composition and species richness it is important to understand the behaviour of the
herbivores and how they influence the primary production of the vegetation (Gauthier et al.
1995; Bardgett et al. 1998). The type of herbivore determines for a large part which (type of)
plants are removed from the vegetation, and therefore the effects on composition and species
richness of the vegetation.
2.1.1 Herbivore selectivity
In several studies it is assumed that the vegetation can be seen as a homogenous pool and that
herbivores have no preference for certain species or type of plants. However, experiments and
field work have made clear that herbivores do have a preference for certain plants, often because
of their high nutrient content. These plants are selectively taken from the community, resulting
in an increase in the amount of plants that are less attractive to herbivores (Bokdam et al. 2002).
This shift in diversity results in a plant community that is characterized by a low decomposition
rate, low(er) nutrient content and also a lower growth rate. As a side effect this also slows down
the nutrient cycle of the entire system, however this effect is not that straight forward as was
discussed in Part I (Bakker et al. 2004; Pastor et al. 1997; Ritchie et al. 1998).
As mentioned before, grazers prefer plants or the parts of plants, that have a higher
nutrient concentration. In many plants the youngest leaves and structures hold the highest
amount of nutrients and are therefore targeted by grazers. The removal of this young tissue
lowers the plant’s chance of survival and reproduction as it is placed at a disadvantage compared
to plants that are not grazed upon. However, some plant species, for example grasses, actually
take advantage of the presence of herbivores. The meristems, the source of new structures, are
located close to the ground in certain grass species. When these species are subject to grazing,
the oldest leaves are eaten whereas the young, nutrient-rich leaves survive. With the removal of
the old leaves, the younger leaves receive more sunlight, for these species grazing actually
enhances growth (Bokdam et al. 2002; Smith et al. 2006).
The vegetation consists of multiple plant species and not all species experience the same
grazing pressure. The variation in nutrient concentration not only exists in a plant, but also
differs between species, therefore certain plant species are more likely to be eaten. In general
smaller grazers are more capable of selecting plants that contain high amounts of nutrients
compared to large grazers like cattle. Different herbivores will therefore have different impacts
on vegetation composition as shown in Table 3 (Bakker et al. 2004).
The response of the vegetation to grazing is not only dependent on the type and behaviour of the
grazer, but also on the type of ecosystem. There are different types of wetlands and these
wetlands respond differently to grazing. Three different types of wetlands are recognized:
estuarine, riverine and palustrine wetlands. The estuarine wetlands are connected to the sea and
therefore influenced by tidal actions or they experience fluctuations in salinity. Wetlands that are
located in stream or river channels, or who are situated on deltas or near watercourses that are
influenced by flowing water are called riverine wetlands. The wetlands that are not connected or
influenced by sea or freshwater bodies, but are fed by rain, ground or surface waters (which
cannot be considered estuaries, rivers or lakes) are called palustrine wetlands. These different
types of wetlands show some common features in response to grazing, but differences can also
be recognized (Reeves et al. 2004).
Table 2 shows the different vegetation responses of the above mentioned wetlands. It
becomes clear that there are also differences between wetlands that belong to the same type.
The estuarine wetlands that are mentioned show that in the saltmarsh the species richness
increased, whereas the richness decreased in the seashore meadow. This difference in change of
the species richness is also observed when looking at the palustrine wetlands. There seems to be
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Utrecht University
no general response, or at least not one that is related to the type of wetland (Reeves et al. 2004).
Table 1. Overview of the different responses of several wetland types to the presence of herbivores (After
Reeves et al. 2004).
Estuarine wetland
Saltmarsh (Holland)
Delta marsh
(Finland)
Seashore meadow
(Finland)
Riverine wetland
Floodplain meadow
(USA)
Floodplain
Westland (NZ)
Floodplain meadow
(USA)
Palustrine wetland
Sub-alpine tarn (NZ)
Swamp (Denmark)
Grazing regime
Vegetation response
Reference
Cattle
Cattle
Increase in species richness
Increase in rarer species
Bakker 1985
Jutila 2001
Cattle
Decreaes in species richness
Jutila 1999
Decrease in total cover
Jutila 2001
Increase in rarer species
Jutila 2003
Decrease in shrub cover and
spatial heterogeneity
Increase in species richness
Popotnik &
Giuliano 2000
Buxton et al.
2001
Clary & Kinney
2002
Cattle
Cattle and
Sheep
Simulated1
moderate
intensity in
summer
43% less aboveground biomass
No change in root biomass
Simulated1
heavy intensity
season long
87% less aboveground biomass
32.5% decrease in root biomass
Cattle
Sheep
Increase in species richness
Removal of undesirable weeds in
7 years
Species richness decreased,
leaving only grazing tolerant
species
Species richness lower than
under high intensity
Amount of bare ground lower
than under high intensity
Species richness higher under
grazing, but increased when
grazers were removed, dropped
after that due to dominance of
exotic grasses
Species richness decreased with
increasing grazing intensity
Mire (UK)
Cattle (low
intensity)
Ephemeral swamp
(NZ)
Cattle
Praire wetland
(USA)
Cattle
Haines 1995
Anderson &
Calov 1996
Bullock &
Pakeman 1997
Rebergen 2002
Hornung & Rice
2003
simulation of grazing by different clipping intensities, trampling caused by a hoof imitator, and application
of urine and feaces.
1
The vegetation composition is influenced by the same factors that influence the species richness.
The selectivity of herbivores for certain plant species also influences how the species richness
and abundance changes. Different herbivores have different preferences for certain species or
type of plants, but also show different behaviour, as can be seen in Table 3 (Reeves et al. 2004).
Grazing in wetlands: aboveground and belowground responses to herbivory
30 januari 2013
When looking at Table 3 it shows that cattle feeds on non-woody, as well as, woody species, it
shows therefore more resemblance to natural wetland feeders like deer than f.e. horses. Looking
from a management point of view, cattle is therefore more suitable in maintaining wetland
diversity, since it shows the same behaviour and feeding preference as the natural herbivores
(Bokdam et al. 2002; Middleton et al. 2006).
In contrast to natural wetland feeders, cattle also increases the spatial heterogeneity of
wetlands due to their grazing behaviour. Cattle does not feed on the entire wetland, but instead
creates so called ‘lawns’, which consists of regularly grazed sites. In between these lawns are
‘tussocks’, areas which are rarely grazed, and therefore are less influenced by the cattle. In these
tussocks, the dominance between species is not, or is barely, influenced and woody plants are
also capable to grow. This way grazing can actually influence the species richness due to the
creation of a mosaic pattern of grazed and ungrazed patches (Middleton et al. 2006).
Table 3. Summary of feeding preferences and behaviour of different herbivore species (after Reeves et al.
2004).
Herbivore
species
Red deer
(Cerves elaphus)
Fallow deer
(Dama dama)
Goat
(Capra hircus)
Horses
(Equus caballus)
Cattle
(Bos taurus)
Black swans
(Cygnus atratus)
Vegetation preference
Grazing behaviour
Citation
Prefer woody species with
low foliar lignin
Attracted to water
Forsyth et al. 2002
Prefer woody species with
low foliar lignin
Prefer woody species with
low foliar lignin
Prefer monocots
Prefer short grasses (<5cm)
Prefer grasses (9-16cm in
height), but eat most things
including woody species
Prefer to feed on actively
growing parts of
macrophytes
Attracted to water and
will wallow
Avoid water
Forsyth et al. 2002
Will feed in water
Feed low to the ground
Depending on breed,
will feed in water
Menard et al. 2002
Prefer to feed while
swimming on
submerged and
emergent plants
Will feed in water
Smith et al. 2012
Stays near water bodies
(as they are used as
escape routes from
predators)
Hygnstrom et al.
1994
Kadlec et al. 2007
Snow geese
(Chen
caerulescens)
Prefer roots and rhizomes of
graminoid species (dry area)
Prefer the shoots of Carex
aquatilis and other
freshwater sedges (wet area)
Muskrat
(Ondatra
zibethicus)
Prefer cattails (Typha
latifolia), and feed on the
inner part of the plant that
contains little lignin and
moderate levels of cellulose
Forsyth et al. 2002
Menard et al. 2002
Kerbes et al. 1990
2.1.2 Changes in primary production in response to herbivory
The removal of aboveground biomass can result in an increase in primary production through
several pathways: 1) reduced (self-)shading and the removal of less productive and old
structures, 2) an increase in nutrient availability through the input of faeces. When these
changes offset the loss of (photosynthetic) plant material the primary production of the
vegetation can increase. The effect of grazing on the net aboveground primary production
(NAPP) is dependent on the grazing history of the ecosystem and which plant parts are
consumed. Ecosystems that have been used for grazing by livestock in the past show only a small
23
Annelon Bollen
Utrecht University
(negative) response to a reintroduction of grazing livestock, whereas systems that are not used
to extensive grazing respond much stronger (Milchunas et al. 1993)
This response is clear in arctic wetlands where primary production and grazing pressure
are very low. Grazing in these systems by caribous (Rangifer tarandus), lemmings (Lemmus spp.)
or lesser snow geese (Chen caerulescens caerulescens) and greater snow geese (Chen caerulescens
atlantica) had negative impacts on the primary production, this was most likely caused by the
late season grazing, and the low capacity of plants to regrow at that point in the season..
However, this only seems to be the case under a high grazing intensity, when the grazing
intensity is low the primary production is actually increased due to the input of nutrients
through the faeces in these nutrient-poor systems (Milchunas et al. 1993; Gauthier et al. 1995).
Gauthier et al. (1995) looked at the graminoids Eriophorum scheuchzeri and Dupontia
fisheri and how these species responded to grazing by greater snow geese. They both showed a
decrease in primary production, however the decrease was stronger for the less dominant E.
scheuchzeri. This was expected since this species contains less fibres and more nitrogen,
therefore it is more easily digestible. In this study it was shown that more than 65% (for both
species) of the net aboveground primary production was removed by the geese, and this result is
consistent with other studies previously done in subarctic wetlands (Cargill et al. 1984). This
large removal of biomass, and the coupled negative influence on NAPP, gives an indication for
the threat the growing population of geese pose on arctic wetlands (Gauthier et al. 1995).
Studies that look at the effect of grazing on emergent plants also show a decrease in NAPP.
Emergent plants are dependent on their shoots and leaves to catch oxygen and transport it to the
soil, the damage done by defoliation has large effects on the root systems. In several studies it
has been observed that productivity decreases when roots suffer a lack of oxygen, and this was
caused by the fermentation of carboydrates in the roots which formed toxic amounts of ethanol.
Grazing below the water surface is therefore lethal for many emergent plants (van den
Weyngaert et al. 2009).
In most of the cases, grazing in terrestrial systems will lead to a decrease in NAPP, however this
is largely dependent on the timing of grazing, and whether or not the vegetation is capable of
regrowth (Milchunas et al.1993; Gauthier et al. 1995). Aboveground removal of biomass during
spring and summer does not have a large (negative) effect on NAPP, since the plants can often
regrow new tissue, however this is only the case when the oxygen transport to the roots is not
severely disrupted. Removal of belowground structures (for example through grubbing) during
autumn and winter is very likely to have a large negative effect on the NAPP of wetlands and
other terrestrial systems. The belowground structures are often used for the storage of carbon
and other nutrients that the plants use for the production of new tissue at the start of the
growing season. Grubbing in these seasons will therefore have a large effect on the annual
productivity of the vegetation, since is negatively influences the productivity of the plants at the
start of the growing season (Milchunas et al. 1993; van den Weyngaert et al. 2009).
Most wetlands show a decrease in NAPP since the plants cannot offset the loss of material
(undercompensation) or the NAPP will remain the same, (in comparison to an ungrazed plot,)
when the plants can recover from defoliation (compensation). So far, only in two wetland studies
an increase in NAPP was found, and this increase was caused by the increase in nutrient
availability through the input of faeces. This positive effect of grazing on the NAPP was found in
two nutrient poor systems, which shows the impact that grazers have on the cycling of nutrients
in these systems. (Maltby et al. 2009; Gauthier et al. 1995).
2.1.2.1 Belowground plant biomass response
Plants that are subject to grazing often relocate large amounts of carbon and other nutrients to
the root system. By relocating these nutrients to the root system, plants are capable of surviving
herbivory. The C stored in the roots is protected from herbivory and can be used as a resource to
Grazing in wetlands: aboveground and belowground responses to herbivory
30 januari 2013
produce new aboveground biomass (Marlby et al. 2009; Bouasria et al. 2012). When plants are
no longer subject to grazing, the amount of C stored in the roots decreases.
Comparing a grazed system with a previously grazed system, it shows that the previously
grazed system shows a lower root biomass compared to the grazed system. This difference is
also apparent when looking at the shoot-root ratio of both systems, the previously grazed system
has a higher ratio which indicates that the relocation of C to the roots is no longer happening.
once the grazers have been removed. It can therefore be reasoned that plants relocate C stored in
the roots to aboveground biomass when grazing ceases (Bakker et al. 2004).
Another process that influences the belowground biomass is succession of the vegetation, which
is prevented by herbivory. When grazers are removed, the vegetation can be invaded by woody
plants. This results in an increase of aboveground biomass, but at the same time the
belowground biomass will decrease due to a lowering of the groundwater table and an increase
in aeration, which is caused by the removal of large grazers. This will result in the mobilization
and emission of carbon dioxide (Bokdam et al. 2002).
The root system of plants not only responds in terms of biomass, but also in terms of nutrients
that are released to the rhizosphere. Beside the increase in C efflux that caused an increase in
microorganisms living in the rhizosphere (Wang et al. 2006), the efflux of other nutrients also
changes (Table 1)(Bardgett et al. 1998).
Table 2. Summary of below-ground responses to the removal of aboveground biomass (after Bardgett et al.
1998)
Effect tested
clipping of wheatgrass
(Agropyron smithii) in
hydroponics
grazing by grasshoppers on blue
grama grass (Bouteloua gracilis)
grazing by grasshoppers on
African C4 grass (Panicum
coloratum)
clipping of Italian ryegrass
(Lolium multi¯orum) and white
clover (Trifolium repens) in
hydroponics
clipping on 14C transfer between
roots of vesicular-arbuscular
mycorrhizal plants
grazing by grasshoppers on
short-term C allocation in maize
(Zea mays)
Response
increased root respiration and
exudation
Citation
Bokhari et al. 1974
increased efflux of organic acids
from roots
increased translocation of labile C to
roots
Dyer et al. 1976
increased root-efflux of nitrate and
ammonium nitrogen
McDuff et al. 1992
increased root 14C transfer
Waters et al. 1994
increased C allocation to roots and
enhanced root respiration and
exudation
Holland et al. 1996
Dyer et al. 1991
An increase in root exudation takes place when aboveground vegetation is removed (through
grazing). Since the main carbon source of the microbial community is root biomass (Holland et
al. 1996), an increase in soil microbes in the rhizosphere is expected. The increase in soil
microbes is beneficial to the plant since the increase in soil microbes provide food for the
protozoa living in the soil. These protozoa graze the microbes (mostly bacteria), this grazing
results in an increase in the mineralization of nitrogen increasing its availability to plants
(Holland et al. 1996).
However, more research has shown that the relocation of C to the roots is only a temporary
reaction of plants. When grazing takes place over longer periods of time (years), the biomass of
25
Annelon Bollen
Utrecht University
roots actually decreases. Long term grazed vegetation forms a superficial root system with a low
biomass, caused by a reduction in C allocation to the roots (Bardgett et al. 1998). The response of
the vegetation and the microbial community is therefore dependent on the duration of the
grazing regime. The moment at which the vegetation stops relocating C to the root systems is
difficult to determine and for that reason it is challenging to predict the response of the
vegetation and the microbial community over longer periods of time. These differences in
responses of the vegetation to grazing make it difficult to predict the response of the vegetation
and the microbial community.
2.1.2.2 Aboveground plant responses to grazing
Herbivores have a large impact on the vegetation as a whole, but this impact is determined by
the response of each individual plant. Plants that are subject to grazing loose above- and
belowground biomass, and this reduces the chance of survival and ability to compete with other
plants for resources (Campbell et al. 2005; Smith et al. 2006).
Defoliation often results in an increase in the production of new leaves, and for woody
species twigs. The energy and nutrients a plant invests in this new biomass, result in a decrease
of reproductive ability and survival chance in winter. For example, Milkweed plants (Asclepias
spp.) show a reduction in biomass and fruit production by more than 20% when they have been
defoliated by cattle (Campbell et al. 2005; Smith et al. 2005).
Plants contain a large array of secondary compounds, that are not part of the basic
metabolism in their cells. Many of these secondary compounds serve a function in preventing
herbivory or make the plant less attractive to eat for a herbivore.
- Quantitative inhibitors are produced in large amounts. One of the most common
quantitative inhibitors are lignins, these lignins make up 5 to 35 percent of all carbon
present in terrestrial plants. Lignins are complex carbon-based molecules that cannot be
digested by herbivores, therefore the herbivores cannot reach the nitrogen and other
nutrients that are also stored in these structures, making the plant less attractive to feed
on. Other, less common quantitative inhibitors are tannins and resins.
- Qualitative inhibitors are produced in small amounts. These inhibitors are toxic and
therefore very successful in repelling herbivores. The quantitative inhibitors contain
cyanogenic compounds or alkaloids that influence the metabolic processes of herbivores
and are therefore widely used for pesticide production (Campbell et al. 2005; Smith et al.
2005).
In chapter 2.2 the effect of grazing on the species richness will be looked at in more detail. An
explanation will be given for the different responses of the different types of wetland. At the
same time the vegetation composition will be taken into account and how it responds to the
presence of (large) grazers.
Grazing in wetlands: aboveground and belowground responses to herbivory
30 januari 2013
2.2 Do the species richness and composition change in wetlands when
grazing takes place?
2.2.1 The effect of grazing on species richness and composition
Extensive research has shown that grazing either increases or decreases the species richness in
wetlands and this is mostly determined by the characteristics of the vegetation and the type and
amount of grazers (Reeves et al. 2004).
Aside from the vegetation and grazer characteristics, the physical changes caused by
herbivory are also an important factor in shifting the species diversity (Jones et al. 2011). For
example, removal of aboveground biomass and a decrease in litterfall, combined with trampling
caused by cattle results in bare ground. Certain species are more capable of establishing in these
bare areas and gain an advantage due to the increase in light availability (Jones et al. 2011).
Litter creates a physical barrier and reduced the amount of light penetration, a decrease in
litterfall would therefore increase the rate of germination (Jutila 2003; Jones et al. 2011).
Beside the decrease in literfall, and increased light penetration the germination strategy
of the plant also determines whether or not it can successfully establish in a new are. Since
certain plant species are capable of establishing more quickly than others, it is possible these
species can increase in abundance or invade a grazed wetland. For North American fens it has
been shown that P. pratensis is capable of establishing more quickly than C. nebrascensis, thus
becoming the dominant species in the grazed areas. This shift in dominance not only takes place
due to the difference in establishing capability but also due to differences in growth strategy. P.
pratensis has a phalanx strategy where the rhizomes are long-lived and short which form in
dense packs, whereas C. nebrascensis has a guerrilla growth strategy (less dense packs, which
live shorter, while the rhizomes are longer). These differences in growth style make it easier for
P. pratensis to invade an area more quickly, thus quickly increasing its abundance (Martin et al.
2001; Middleton et al. 2006).
The shift in species diversity also takes place because the competition between the plants shifts
in different directions. Table 4 gives an overview of the shifts in species richness that take place
in different wetland types. In these studies the in- or decrease in species richness was caused by
creating competitive (dis)advantages for the dominant species, thus increasing or decreasing
chances for other species (Reeves et al. 2004).
Species that are capable of growing very quickly have a competitive advantage as they
can rapidly outgrow the rest of the vegetation thus winning the competition for light. In this way,
these dominant plant species can exclude less competitive species from the vegetation by
catching away light. Grazing can also increase the species richness by removing large amounts of
the dominant species, therefore giving a competitive advantage to the less competitive species
(Wheeler 1988; Olff et al. 1999; Reeves et al. 2004).
Certain dominant species can prevent this since they are unpalatable or resistant to grazing. In
these situations species richness will actually decrease since grazers will feed on the less
dominant species (Reeves et al. 2004). A decline in species richness often takes place under a
high grazing intensity as over-consumption and trampling will remove more species then are
recruited (Olff et al. 1999; Reeves et al. 2004).
Jones et al. (2011) found that in an intermountain depressional wetland the most
dominant plant species, which belonged to the tall and rhizomatous species, declined when
grazing took place. This reduction made it possible for the less competitive groups (annual and
non-rhizomatous species) to increase with grazing intensity. Their research showed only a small
change in species richness, but a large change in most dominant species. They managed to tie the
shift in dominance not to specific plant species but to functional groups, though more research is
needed to see if the response is the same in other wetlands. This shows that even though species
richness might not change, there is actually a shift in the composition. The fact that the species
composition does change, in contrast to the species richness, shows that just looking at the
richness is not always sufficient to measure changes in the vegetation.
27
Annelon Bollen
Utrecht University
The study of Tanner (1992) showed that the intermediate disturbance theory applies to grazing
in lake shorelines in New Zealand (Table 4). He found that under a high grazing intensity the
vegetation was dominated by a few grazing-tolerant, long-lived and fast-growing species. This
high grazing regime can be seen as a large disturbance, whereas a lower intensity resembles an
intermediate disturbance. When grazing does not take place, the amount of species was also low,
but this was caused by a few very competitive species whose presence excluded the appearance
of less competitive species. From his study he concluded that under a low grazing intensity the
species richness was highest, which was likely caused by a modification of the vegetation
structure. For that reason he argued that grazing could be used as a management tool to increase
the amount of species growing in wetlands, but the effect of the management would be
dependent on the intensity, frequency and scale.
The grazing intensity can be measured in several values, and one of the most common is
the ‘stock unit’ also knows as ‘SU’ that is used in New Zealand and which is calculated as 1 SU is
equal to 1 breeding ewe. This can be converted to other livestock, which gives 1 dairy cow the
value of 7 SU. Unfortunately many studies do not give any information on the intensity of grazing
but only mention intensity as low or high, this makes comparison between different studies
difficult and it is therefore difficult to determine which quantity of livestock is suitable for
successful management of diverse plant communities (Reeves et al. 2004).
Table 4. Summary of studies on different wetland types and the effect of different grazing regimes and
intensities on the species richness. ‘–‘ indicates a decline in species richness, whereas ‘+’ indicates an increase in
species richness (after Reeves et al. 2004).
Wetland type
Saltmarsh (Holland)
Lake shoreline (NZ)
Mire (UK)
Delta meadow
Seashore meadow
(Finland)
Lake turf (NZ)
Riverine floodplain
(France)
- Abandoned grassland
- mowed grassland
Ephemeral swamp (NZ)
Grazing
regime/intensity
Cattle mod-high (1.31.7 animals/ha)
Cattle low
Cattle high
Cattle/high
Cattle
Cattle
Species
richness
+
Citation
Bakker 1985
+
+
+
-
Tanner 1992
Cattle/horses
-
Champion et al. 2001
Touzard et al. 2001
(simulated) herbicide
(simulated) herbicide
Cattle
+
+
Bullock et al. 1997
Jutila 1999
Beadel et al. 2000
Not mentioned in Table 4, but also important to note is that not all herbivores eat the same plant
species. Cattle are considered most effective at maintaining a high species richness in wetlands,
since they are less selective in their food source. However, horses on the other hand are much
more selective and prefer the most productive areas, and they do not feed of woody species. The
fact that they do not feed of woody species like the shrub Phillyrea or Sambucus nigra, causes
wetlands to be rapidly invaded by these species. Cattle grazing, at a high enough density, is
capable of reducing the height and coverage of these species, which helps maintain the wetland
diversity (Menard et al 2002; Reeves et al. 2004).
Red deer (Cerves elaphus) and Fallow deer (Dama dama) are two species of grazers that
can be seen as native grazers of many wetland types like fens. These species foraged mostly on
woody plant species and therefore had the same effect as cattle on the vegetation. For that
reason it can be argued that cattle grazing can be beneficial to the conservation of a rich
Grazing in wetlands: aboveground and belowground responses to herbivory
30 januari 2013
vegetation community (Foryth et al. 2002; Middleton et al. 2006). However, this is also
dependent on the grazing intensity, under a low intensity cattle ignores the saplings of many
unpalatable tree species like Alder (Alnus glutinosa), but when there are more herbivores
present the grazers do eat the saplings, therefore preventing the trees from growing. Herbivory
may result in maintaining a herbaceous vegetation through maintaining the woody species at a
small stature, this way the woody species cannot catch away light from the other species.
Something they would do if they were allowed to grow to full height (Middleton et al. 2006).
More about the prevention of the establishment of woody species will be discussed in chapter
2.3.
A study on a freshwater tidal marsh showed that muskrats had no influence on the
species richness. Muskrats prefer to feed on cattail, and often they pull the rhizomes from the
soil therefore creating open patches. It would be expected that other species would establish
these patches, however this appeared not to be the case. It is likely that these patches, which
were located near the muskrat lodges, did not have favourable conditions for the establishment
of plants (Connors et al. 2000).
It can be concluded that the species richness of a wetland can be influenced by grazing, but that
the direction of the effects (increased or decreased diversity) is largely dependent on the grazing
intensity and the type of grazing. To maintain a high species diversity cattle are more suitable
than horses as a management tool, but the intensity should not be too high (Tanner 1992; Foryth
et al. 2002; Reeves et al. 2004).
When looking at the composition of the vegetation it is clear that the changes in litterfall
and light penetration can have a large impact on the settlement of new species. A system can be
invaded by a new plant when it proves to be more successful in establishing itself in the bare
areas created by herbivores. The type of grazer also influences the composition since certain
plant species are more likely to be targeted than others by different herbivores. Grazing by
horses will result in an increase in woody species since horses avoid these plants. Cattle on the
other hand will feed on woody species, and will therefore maintain a non-woody vegetation
(Reeves et al. 2004).
29
Annelon Bollen
Utrecht University
2.3 Does grazing have any influence on the functioning and structure
of wetlands?
The previous chapter discussed the effect of herbivory on the species composition of wetlands,
the change in vegetation composition influences the structure and functioning of the specific
wetland. Wetlands that are grazed show a more open landscape with less woody species than
ungrazed areas, indicating that grazing can slowdown succession in the system. While slowing
down succession, grazing also influences the functioning of wetlands. Part of the functioning of
wetlands is related to the cycling of nutrients as has been discussed in Part I. Additional to the
nutrient cycling, grazing also influences other functions of a wetland, mainly the provision of
habitats for birds and other animals, hydrologic cycles and peat formation.
2.3.1 The influence of grazing on the structure of wetland vegetation
2.3.1.1 Succession
According to the intermediate disturbance theory, proposed by Joseph Connell in 1978, species
diversity will be highest in habitats that experience a moderate amount of disturbance. The
intermediate disturbance will allow plant species of different successional stages to live in
coexistence (Smith et al. 2006). The first successional stage of most fen and peat meadows
(which are often used for cattle grazing) wetlands consists of a low amount of pioneer species
and after a few years these are replaced by a more species-rich herbaceous vegetation. However,
as succession continuous these species are replaced by a few woody species, resulting in a loss of
species diversity and richness (Aptroot et al. 2007).
Grazing is often used as a management tool in wetlands, to make sure that typical
wetland vegetation remains, while preventing woody species to invade the ecosystem (Ausden et
al. 2005; Bokdam et al. 2002). When looking at the effect of grazing on succession, it becomes
clear that it is highly dependent on the intensity of grazing and time of the growing season
during which grazing takes place (Bokdam et al. 2002; Oene et al. 1999).
A similar study was done by Aptroot et al (2007) on the islands located between the Wadden Sea
and the North Sea. They looked at the effect of grazing on the succession of wet dune valleys.
Wetlands in wet dune valleys are considered species-rich, but over time the vegetation changes
into species-poor dwarf shrub vegetation. In a long term study (over 30 years) they showed that
low density cattle grazing can prevent this succession from taking place.
The greatest threat to the vegetation of these wet dune valleys is the process of
succession. The wet dune valleys start with a species-poor pioneer vegetation, which gets
replaced by a species-rich herb vegetation, which is in turn replaced by a shrub and wood
vegetation which has a low diversity. This process of succession was prevented in the past by
rabbit grazing, however viral outbreaks almost eradicated the rabbits. The lower rabbit density
made the succession of the wet dune valleys speed up significantly and in an attempt to halt this
succession, cattle was introduced with the goal to mimic the effect the rabbits had in the past.
The study showed that cattle can indeed have the same influence the rabbit used to have
on the vegetation, namely the halting of succession. However, this is only achieved when the
structure of the vegetation is taken into account, and the herbivore density must be adjusted
depending on that. When the vegetation has a high spatial variety, grazing can have large
negative effects. When cows graze in the species-poor areas, but deposit their faeces in the
species-rich herb vegetation, the input of nutrients will influence the species diversity in these
areas.
The absence of rabbits had distinct effects on the various vegetation types present in the
wet dune valleys. 1) The lichen-rich dune heathlands were dominated by Ericaceae (Callina
vulgaris, Empetrum nigrum and Erica tetralix), also present were two Red List lichen species
(Cladina ciliate and Cladina portentosa). These Red List species increased in abundance
whenever grazers were present, 2) The species-rich wet dune valleys the vegetation mainly
Grazing in wetlands: aboveground and belowground responses to herbivory
30 januari 2013
consists of Schoenetum and Nanocryperion (plant species considered as pioneer species)
species like Radiola linoides and Pirola minor. In the absence of grazing the nanocryperion
species are readily replaced by (fewer) Schoenetum species, resulting in a decrease in species
diversity. However, when grazing is present the species diversity actually increased due to the
occurrence of characteristic species like Carex oedori and Carex panicea.
Even though grazing seemed to have largely positive effects on the vegetation, more
management showed to be needed for the dune valleys. Since many of the characteristic species
are considered pioneer species, more drastic practices other than grazing are needed. Practices,
like removing the top layer, would provide a suitable place for the establishment of these
pioneers. These drastic measures are needed since the natural grazers (rabbits) are no longer
abundant and can therefore no longer create an optimal environment for these pioneer species.
Through the removal of the top layer the characteristic vegetation of the dune valleys can be
maintained.
Fen formation
The first successional state of certain wetlands starts with the colonization of open waters by
plants, thereby creating floating plant mats. In the Netherlands, research has been done on the
effect of grazing on the colonization of open waters by plants. The colonization of open waters is
important in the process of forming floating peat mats, however the rate at which open waters
are colonized have decreased in the last decades, partially caused by herbivory.
The muskrat (Ondatra zibethicus) is an invasive species in the Netherlands that lives near
freshwater bodies and feeds primarily on plants, including rhizomes. Research indicated that
the colonization of open water was inhibited when muskrats were feeding on the vegetation,
thereby preventing the formation of floating peat mats. While preventing the formation of peat
mats, the species richness was also lower in ponds where the muskrats are present (Sarneel et
al. 2011).
2.3.1.2 Vegetation structure
Preventing succession, through grazing has an effect on the height and structure of the
vegetation. Herbivores prevent the establishment of tall (often woody) species, while defoliation
creates a more open structure.
When grazing takes place during the entire growing season, more than 50% of the
biomass production can be removed, this way a short herbaceous vegetation can be maintained
(Bokdam et al. 2002). Grazing during the start of the growing season can protect the wetlands
from an invasion of tall sedges like Carex elata and Carex appropinquata, due to defoliation of
these species. In peatlands, a low productive vegetation, mostly consisting of sedge-moss and
grasses can be maintained by allowing grazing during the start of the grazing season (Bokdam et
al. 2002).
The effect of grazing on the height of the vegetation over multiple seasons is represented
in Figure 13 (Ausden et al. 2005). Ausden et al. (2005) found in their study that Phragmites
australis became less dominant due to defoliation and trampling, and that it was replaced by the
less dominant species Glyercia maxima. P. australis generally grows taller than G. maxima and the
replacement of P. australis is therefore the cause of the decrease in vegetation height.
In their study, Ausden et al. (2005) found no proof of any influence of herbivory on
succession, even though the study took place over several years. They did notice that the cattle
grazed on Salix bark and leaves in winter, possibly preventing encroachment of Salix shrubs. On
the other hand they found that the removal of vegetation and tramping resulted in open patches
which could be invaded by woody species, therefore making succession possible.
31
Annelon Bollen
Utrecht University
Figure 13. Vegetation height in a tall-herb fen in Broadland, England.
Data comes from grazed (solid line) and ungrazed (broken line) plots,
collected in 2002. Values represent means ± standard error (Ausden et al. 2005).
In 1992, Tanner looked at changes in the vegetation among lake margins in New Zealand, he
found that the height and structure of cattle-grazed areas differed greatly from ungrazed riparian
areas (Figure 14). He found a difference in the vegetation that grew at the water’s edge and
more inshore.
The vegetation at the grazed plots shows a remnant of the sedge community that was still
present at the ungrazed plots. This is shown in Figure 14a, where the sedge community mainly
consists of Baumea juncea and B. huttonii. Large part of the sedge community was replaced by
short shallow-water submerged plants (mostly Juncus spp.) in the grazed areas. Additional to this
shift in inshore species, the ungrazed plots showed a lower diversity in submerged plant species
than the grazed areas and this was likely caused due to the litter accumulation and shading that
was caused by the taller sedge species. The increase in light penetration that was caused by
grazing also made it possible for adventive species, like Axonopsus affinus, Cyperus tenellus,
Isolepis sepulcratis, Juncus articulatus and J.bulbosus, to grow in the grazed plots (species not
shown in Figure 14b).
In this study, Tanner also looked at the effect of different intensities of grazing and he
found that a high intensity can have aversive effects on diversity. He found that a low grazing
intensity could actually have a positive effect on the species diversity and abundance of many
short-water plants like Potamogeton, Juncus and Myriophyllum spp. This increase in diversity and
abundance under a low grazing regime was caused by the small modifications that were made to
the structure of the vegetation. The increase in diversity was caused by an increase in light
penetration. The grazing intensity determines for a large part how the vegetation would
respond, and this in turn would influence several functions of the wetland (most importantly the
provision of habitats for wildlife).
Grazing in wetlands: aboveground and belowground responses to herbivory
30 januari 2013
Figure 14. Schematic overview of the marginal vegetation of Lake Ngatu (NZ).
A) Vegetation profile of an ungrazed (protected by fences) lake margin, B) vegetation
profile of a grazed lake margin. Symbols represent the different plant species found
along the lake margin (not all species present in these profiles)(Tanner, 1992).
2.3.1.3 The influence of large water birds and muskrats on the vegetation structure
In addition to the effects of large herbivores on the vegetation structure, some research has also
been done on the effect of swans. However, there is surprisingly little known about the effect of
these large water birds on the vegetation of wetlands. The birds often live in high abundance and
for that reason can create a high grazing pressure on the system which in turn can have
detrimental effects on the structure of the vegetation (Stafford et al. 2012; Smith et al. 2012).
One of the more recent studies (Stafford et al. 2012) looked at the effect of mute swans (Cygnus
olor) on the structure of the submerged aquatic vegetation (SAV) in North-American wetlands.
The mute swans had detrimental effects on wetlands since their grazing habits degraded
SAV communities. In their study, they noticed little changes in aboveground biomass, but the
swans did have a large effect on belowground biomass and plant structures. While foraging,
mute swans mostly focus on aboveground biomass (72.4% of biomass) of SAV species, the other
part consists of belowground biomass and tubers. Mute swans (and other swan species) dislodge
plants from the substrate and eat only the parts they are interested in, this has detrimental
effects on the vegetation, since the dislodged plants cannot regenerate. Due to this foraging
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Annelon Bollen
Utrecht University
behaviour large parts of many North-American wetlands suffer from localized depletion of
aquatic plant species (Stafford et al. 2012).
The Bewick’s Swans have the same food preference as the mute swans, as they feed mostly on
aboveground biomass but also on tubers. Fennel pondweed (Potamogeton pectinatus) is a plant
that is readily eaten by Bewick’s Swans, as they are known to pull the tubers of this plant from
the sediment (Bodelier et al: 2006; Klaassen et al. 2007; Hidding et al. 2009);.
Hidding et al. (2009) looked at the depth of tuber distribution and how it changes with
differing grazing pressures. They reasoned that tubers that were deeply buried, were less
accessible to the swans, and that would increase the survival rate of the plants. The only
downside for the plants is that the tubers must be bigger because it costs more energy to sprout.
Fennel pondweed is an aquatic macrophyte that survives the winter through
subterranean tubers. Swans trample the sediment, creating small craters, in an attempt to reach
the tubers. With the use of their bills, they filter the tubers from the sediment. Through this
practice the swans can reach around 85cm below the water surface.
In their study, Hidding et al. compared two wetlands (Estonia and France) and one lake
(The Netherlands) and these locations were all located on the migration route of the swans. They
found that the lake, which had the highest grazing pressure, had tubers mostly located in the
deep sediment, whereas the wetlands had tubers located mostly in the shallow sediment. Since
the more heavily grazed location gives deeper tuber depth, they reasoned that plants can show
adaptive, escape strategies to the threat of grazing. The same observation was made in a study
from Klaassen et al. in 2007. Since fennel pondweed shows this behaviour it is possible that
other (aquatic) plants show the same escape strategy, however this strategy is barely studied.
In Australia a similar study was done, the effect of black swans (Cygnus atratus) on marsh
vegetation (emergent and submerged) was studied. Grazing by this swan species appeared to
have a large effect on the structure and biomass of the vegetation, as shown in Figure 15 (Smith
et al. 2012).
The black swans fed on the rush Eleocharis equisetina, which is one of the most dominant
plant species in the Australian wetlands. The black swans prefer to feed while swimming,
however they did not feed on the submerged parts of the plant. This was most likely caused by
the fact that the swan density was low, since foraging with their head underwater only took place
under higher densities.
The removal of the tall rush E. equisetina made it possible for other waterfowl to access
the area, thereby increasing the threat of more grazing by other herbivorous birds. One of the
most interesting changes in waterfowl diversity was the occurrence of Comb-crested Jacana
(Irediparra gallinacea). The removal of E. equisetina by the swans created open areas and the
remaining E. equisetina lodged (bend horizontally) in these parts, creating a floating mat on the
water. Due to the presence of these floating mats the Comb-crested Jacana was capable of moving
into the wetland, showing the significance of the swans in changing the ecosystem (Smith et al.
2012).
Grazing in wetlands: aboveground and belowground responses to herbivory
30 januari 2013
Figure 15. The effect of grazing by black swans on Eleocharis equisetina in
Little Broadwater (Australia). Overview to show the difference between the
exclosed plot and the surrounding grazed area (Smith et al. 2012).
Additional to the swans, the muskrat (Ondatra zibethicus) also has an effect on wetland
vegetation, but like the swans not much research is done on its effect on wetland vegetation. The
muskrat is an invasive North-American species that was introduced in Central-Europe (Prague)
at the start of the 20th century. In the following years the species rapidly expanded to other parts
of Europe and readily moved into wetland areas. When looking at the effect on wetlands, the
muskrat has a high potential of removing large parts of the vegetation (Hygnstrom 1994;
Connors et al. 2000).
Muskrats create ‘houses’ from mud and plant materials, and often create multiple houses
in their territory. These houses are created in patches were little, to no vegetation grows, since
they remove plant material to build the houses. These houses are connected by ‘channels’, and
these channels and patches create a mosaic pattern in the wetland vegetation, resulting in
fluctuating light and temperature conditions within the wetland (Danell 1996; Connors et al.
2000).
The threat of muskrats and water birds to a wetland are also present in the form of so called
“eatouts”. An eatout is an area where the emergent plants part have been removed by herbivores.
These eatouts are common in areas where muskrats or herbivorous water birds forage. With the
creation of these eatouts, the herbivores create a more open landscape that makes it possible for
waterfowl to feed on the small or emergent plants (Kadlec et al. 2007; Maltby et al. 2009; Smith
et al. 2012). While it is known these herbivores can have a large effect on the structure of the
vegetation, little research has been done on this subject.
2.3.2 The influence of grazing on the functioning of a wetland
Since the consumption and trampling of vegetation in wetland has the potential to change the
structure of the vegetation, a change in functioning of the wetland is expected. The functioning of
the wetland is largely dependent on the structure of the vegetation and the above mentioned
changes in structure are therefore likely to change some of the functions, especially the provision
of habitats to the different wildlife can change in both type and quality (Reeves et al. 2004;
Tanner 1992; Allen-Diaz et al. 2004).
2.3.2.1. Birds
wetlands from which peat has been extracted are often suitable for many bird species, due to the
open landscape that was created during the time of peat extraction. These areas contain reed
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Utrecht University
beds, meadows and other suitable habitats for birds. The landscape shows a mosaic pattern that
attracts breeding and foraging waterfowl, marsh birds and waders. The foraging of these birds
has little effect on the structure of the wetland and therefore the habitat of the birds remains
largely intact. (Tanner 1992; Bokdam et al. 2002). Peat pits, canals and ditches are also favoured
by large water birds like swans (Bokdam et al. 2002).
Grazing by large vertebrates had one obvious negative effect on birdlife, namely the
trampling of nests by large grazers. Additionally, the removal of high vegetation structures makes
the area more open, therefore decreasing the habitat, and more importantly, the nesting quality
of the area (Popotnik et al. 2000; Bokdam et al. 2002; Reeves et al. 2004).
Beside this negative effect, grazing also has positive effects that are caused by the
prevention of the establishment of large (woody) species. In the Biebrza National Park (Poland),
wetlands were invaded by large reeds and tall sedges, which negatively impacted the density of
breeding water birds (Bokdam et al. 2002). Grazers reduced the tall vegetation, recovering
favourable conditions for birds. This positive effect is also found in many other bird species and
in different wetlands (Jutila 1999).
2.3.2.2 Invertebrates
Additional to studies that focus on the response of birds to grazing, there are also studies that
focus on the response of invertebrates (Bullock et al. 1997; Reeves et al. 2004; Ausden et al.
2005). The response of the invertebrates was largely caused by the same changes that also
influenced the response of bird species; the change in vegetation structure caused by grazing.
In a tall-herb fen wetland, the species richness and densities of molluscs was lower in
grazed areas than in ungrazed areas. Especially snails were negatively influenced by grazing, and
this was likely caused by the removal of Carex species like C. riparia, C. acutiformis and C.
paniculata. Defoliation of these plants resulted in a less dense vegetation, which in turn
decreased the humidity. This had a negative effect on the snails since they prefer a humid
environment. The defoliation also resulted in less litter formation, this reduced the survival rate
of the snails since they hibernate in the litter (Ausden et al. 2005).
Invertebrates living on a lowland heath showed more positive responses to grazing. The
southern damselfly (Coenagrion mecuriale), which is a threatened species in the UK, showed a
strong increase in abundance under a heavy grazing regime. Additional to the positive response
of this dragonfly, several insects like burrowing wasps (Ammophila spp.) and tiger beetles
(Cicindela spp.) also increased in density (Bullock et al. 1997).
2.3.2.3 Soil characteristics
As mentioned in Part I, the soil characteristics change and this has an effect on the cycling of
nutrients in the system. The compaction of the soil has already been discussed, however that is
not the only thing that changes. Grazing also influences the pH and salinity of the soil and this
can have an effect on the survival and growth of the vegetation (Reeves et al. 2004).
Trampling by large herbivores changed the structure of the soil in salt marshes. Due to
the change in soil structure, the infiltration of water was reduced and that prevented the
leaching of salt. However, after removal of the herbivores, it took less than 5 years for the soil
salinity to decrease (Amiaud et al. 1998).
Grazing in a calcareous wetlands on mineral soil showed a decrease in pH and an
increase in NO3- which was caused by the nitrification of manure. Since nitrification is inhibited
when pH drops below 6.0, the decrease in pH would most likely be slowed down or stopped
since it is caused by the process of nitrification. Therefore nitrification can be seen as a negative
feedback for the decreasing pH. As mentioned before, the vegetation response on changes in the
N availability are difficult to predict. In this study the change in pH and N availability did not
seem to have a large effect on the vegetation, however it is possible that these changes positively
influence the herbaceous vegetation of calcareous wetlands (Van Hoewyck et al. 2000).
In coastal marshes in the Gulf of Mexico, grazing has an effect on soil elevation. The marshes in
this region are subject to a high subsidence rate (>1.0 cm/year), due to deep subsidence
Grazing in wetlands: aboveground and belowground responses to herbivory
30 januari 2013
processes like tectonic plate movement, but also due to shallow subsidence processes that can be
connected to grazing. The shallow subsidence is caused by a reduction of soil volume due to
mechanic loading (like trampling by large herbivores), degassing and dewatering, but also
through the decomposition of organic matter (Ford et al. 1998).
These coastal marshes have to accrete more than 1 cm/year of sediment to make sure
they stay emergent. This sediment is formed from above- and belowground biomass and the
deposition and retention of sediment. However, an increase in grazing pressure threatens the
coastal marshes since it causes soil subsidence (Figure 12).
Figure 12. Schematic representation of the change in soil elevation, surface accretion
and shallow subsidence for both a grazed and an ungrazed coastal marsh (Ford et al. 1998).
As shown in Figure 12, the grazed coastal marshes show a lower increase in elevation, even
though the surface accretion was higher than in the ungrazed plots. The increase in accretion
was likely caused by the destructive feeding habits of the studied herbivores (nutria and wild
boar), while their feeding habits resulted in a large input of organic matter. However, the root
biomass in the grazed systems was greatly reduced, which resulted in an increase of soil
subsidence, indicating that herbivory can have a large influence on soil subsidence (Bakker et al.
2004; Ford et al. 1998).
The change in vegetation structure has a large effect on the functioning of the wetland. Through
the removal of biomass, the structure becomes more open and, dependent on the type of
herbivore, succession can be prevented. Changes in the vegetation structure have a large impact
on the capability of the wetland to provide habitat for different animals. As with the species
richness and vegetation composition this is largely dependent on the type of herbivore and the
grazing intensity.
37
Annelon Bollen
Utrecht University
Discussion
Biogeochemical responses
The response of the cycling of phosphorous, nitrogen and carbon is mainly dependent on the
type of grazers that inhabit the ecosystem. However, it can be reasoned that the response is also
dependent on the particular characteristics of the ecosystem. The possible responses have been
seen in a number of different ecosystems, however due to lack of research little is known about
the responses in wetlands. Since the cycling of nutrients can accelerate or decelerate, and this is
dependent on several biotic and abiotic factors, the actual response that takes place in a wetland
is difficult to determine and since there are multiple types of wetlands, the logical conclusion is
that responses would differ depending on the type of wetland.
When grazing takes place, the cycling of phosphorous in a grassland first decelerates,
then over time the cycle accelerates (Leech 2009). While this acceleration can lead to increased
plant growth, it is unclear what this means for the vegetation composition. Plants that are very
successful in competing for phosphorous, are likely to decrease when it is no longer limited.
Additionally, phosphorous is often a limiting factor for plant growth, it can therefore be reasoned
that an increase in availability will make it possible for other plants to invade the system.
The hypotheses that explains the response of the nitrogen cycle to grazing (Figure 6),
and how the response is determined by the N availability in the system (Ritchie et al. 1998) has
not been tested for wetlands. It is possible that these hypotheses can be used to determine how a
wetland will respond, or possibly explain already observed responses in different type of
wetlands. This however cannot be done without further research, and as mentioned before, the
response must be studied in relation to the other nutrients.
The response of the carbon cycle has been studied more extensively in wetlands, most
likely due to the large amounts of carbon stored in peatland. In contrast to the phosphorous and
nitrogen cycle, the carbon cycle is also one of the processes that has been proven to be
influenced by the grazing of herbivorous waterfowl. The actual effect of these birds seems to be
largely dependent on their foraging behaviour (Bodelier et al. 2006; Dingemans et al. 2011). To
predict the threat these animals may pose to the storage of greenhouse gasses in wetlands it is
important to determine the type of waterfowl and on which vegetation structure they graze.
One of the most challenging aspects of these biogeochemical cycles is that most literature only
looks at the belowground response without linking it to the response of the vegetation and vice
versa. It therefore ignores the feedback mechanisms between the soil microbial community and
the vegetation. Only the research by Bardgett et al. (1998) looks at the interactions between the
soil microbial community and the vegetation. The low amount of literature dealing with these
interactions, makes it very difficult to connect the changes in biogeochemical cycling, discussed
in Part I, to the vegetation responses in Part II.
Vegetation responses
In contrast to the biogeochemical responses, the response of the vegetation has been researched
for several wetland types (Table 2, Table 4). It is clear that different wetlands show different
responses and that this response is largely dependent on the grazing intensity. Most wetlands
show an increase in species richness under a low grazing regime, whereas a drop in species
richness is seen when the grazing intensity becomes too high (Reeves et al. 2004).
The most common explanation for these shifts in species richness and composition, are
connected to the dominance of the plant species and whether or not these species are targeted
by the herbivores. Whether these dominant species are targeted depends largely on their ability
to defend themselves from herbivory (Smith et al. 2006). Unfortunately, many studies only look
at the shifts in species richness and composition, but do not look at the individual plants species
involved. It is therefore difficult to determine the actual reason for the shifts in vegetation
composition, and if this is caused by the defensive mechanisms of the plants or the preference of
the herbivore for nutrient-rich tissue.
Grazing in wetlands: aboveground and belowground responses to herbivory
30 januari 2013
When looking at the function and structure of a wetland, it shows that grazing can have a
variety of effects, and that the function of the wetland is largely dependent on the vegetation
structure. Changes in vegetation structure influence the capability of a wetland to shelter birds
and other species. Soil characteristics also change in response to herbivory, and this can have a
major impact on the cycling of nutrients as discussed. Aside from the cycling of nutrients,
herbivores also have an effect on soil elevation, and in areas where the accretion of soil sediment
is offset by herbivorous impact, soil subsidence is expected. This process can cause loss of
coastal wetlands, and since these wetlands are also exposed to increases in the global sea level,
herbivory is a major threat to these systems (Ford et al. 1998).
One very important aspect that has to be taken into account is that wetlands are not only
influenced by herbivores that have been introduced by humans, but also by wild herbivores that
forage in the wetlands. Especially waterfowl and muskrats have a large impact on the vegetation
(structure), however research on the effect of these herbivores is limited. Muskrats and
waterfowl are capable of destroying large parts of the aboveground biomass, thereby creating
eatouts, which result in a mosaic vegetation pattern. This (more open) pattern makes it easier
for waterfowl to forage in the wetland, thereby increasing the grazing pressure (Smith et al.
2012; Stafford et al. 2012).
Grazing as a management tool
As mentioned in the introduction, grazing has become a very popular management tool in
wetlands. However, grazing only seems to be effective at maintaining the original (and often
desired) vegetation when the type of herbivore and intensity of grazing are taken into account
(Bokdam et al. 2002; Reeves et al. 2004).
At a low grazing pressure a high plant species richness can be acquired and maintained,
while at the same time the low amount of herbivores prevents extensive trampling or disruption
of the vegetation structure. When this is taken into account, grazing can be successfully used as a
management tool, however the required grazing pressure and type of herbivore may differ
between wetlands and is therefore often difficult to determine (Reeves et al. 2004).
Future recommendations
Since different types of wetlands appear to have different sensitivities to grazing (Table 2, Table
3), it is advisable to also look at what happens with the cycling of nutrients in these systems
under herbivore presence. Most studies on the effects of herbivory on nutrient cycling have been
done on other ecosystems like shrub- and grasslands and forests (Milchunas et al. 1993).
However, even though a lot is known about the cycling of nutrients in wetlands, little is known
about the actual effect(s) of grazing on that cycling.
Little is also known about the effects of grazing by large herbivorous birds on the vegetation of
wetlands, and even less is known about how these herbivores influence the cycling of nutrients
(other than carbon) in these systems (Smith et al. 2012; Stafford et al. 2012). The same holds
true for the impact of muskrats, additional to the obvious visual effects in the form of eatouts
(Kadlec et al. 2007). With the increasing populations of (migratory) birds the grazing by these
animals is becoming more and more of an important factor that influences the vegetation of
wetlands, and possibly the cycling of nutrients.
39
Annelon Bollen
Utrecht University
Conclusion
It can be concluded that grazing has large effects on the biogeochemical cycles and vegetation of
wetlands, however the actual effects are difficult to predict since it is dependent on the type of
grazer and wetland, and intensity of grazing. Literature on the response of nutrient cycling and
vegetation to grazing in wetlands is limited compared to other terrestrial systems. Therefore it is
difficult to determine whether or not wetlands respond the same way as other ecosystems, for
that reason more research should be done to see if wetlands show the same response, and
whether or not this response is the same for all type of wetlands.
Grazing in wetlands: aboveground and belowground responses to herbivory
30 januari 2013
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43
Annelon Bollen
Utrecht University
Books
Campbell N.A., Reece J.B. (2005) Biology. Place of publication: San Franscisco, Publisher: Benjamin
Cummings
Hygnstrom S.E., Timm R.M., Larson G.E., (1994) Prevention and Control of Wildlife Damage. Place of
publication: University of Nebraska-Lincoln. 2 vols: Paper 15 ‘Muskrats’
Maltby E., Barker T. (2009) The wetlands handbook. Place of publication: Oxford, Publisher: Black-Wiley
Olff. H., Brown V.K., Drent R.H. (1999) Herbivores: between plants and predators. Place of publication:
Oxford, Publisher: Blackwell Science
Smith T.M., Smith R.L. (2006) Elements of ecology. Place of publication: San Franscisco, Publisher:
Benjamin Cummings
Reports
Beadel S., Perfect A., Rebergen A., Sawyer J. (2000) Wairarapa Plains Ecological District // Survey
report for the Protected Natural Areas Programme
Bokdam J., Braeckel A. van, Werpachowski C., Znaniecka M. (2002) Grazing as a conservation
management tool in peatland
Champion P.D., Beadel S.M., Dugdale T.M. (2001) Turf communities of Lake Whangape and some
potential management techniques // Science for Conservation 186
Leech F. (2009) Cycling of phosphorus in grazing systems // primefacts – profitable & sustainable primary
industries // primefact 921
Reeves P.N., Champion P.D. (2004) Effects of livestock grazing on wetlands: literature review // NIWA
Client report: HAM2004-059