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Generalities in grazing and browsing ecology
du Toit, Johan T.; Olff, Han
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10.1007/s00442-013-2864-8
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du Toit, J. T., & Olff, H. (2014). Generalities in grazing and browsing ecology: Using across-guild
comparisons to control contingencies. Oecologia, 174(4), 1075-1083. DOI: 10.1007/s00442-013-2864-8
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Oecologia (2014) 174:1075–1083
DOI 10.1007/s00442-013-2864-8
Concepts, Reviews and Syntheses
Generalities in grazing and browsing ecology: using across‑guild
comparisons to control contingencies
Johan T. du Toit · Han Olff Received: 11 June 2013 / Accepted: 11 December 2013 / Published online: 4 January 2014
© Springer-Verlag Berlin Heidelberg 2014
Abstract In community ecology, broad-scale spatial replication can accommodate contingencies in patterns within
species groups, but contingencies in processes across species groups remain problematic. Here, based on a focused
review of grazing and browsing by large mammals, we use
one trophic guild as a “control” for the other to identify
generalities that are not contingent upon specific consumerresource interactions. An example of such a generality is
the Jarman–Bell principle, which explains how allometries
of metabolism and digestion influence dietary tolerance
and thereby enable resource partitioning within both guilds
at multiple scales. By comparing the grazing succession
with browsing stratification we show how competition
from smaller herbivores, rather than facilitation from larger
ones, is the underlying process structuring ungulate assemblages when shared resources become limiting. Also, grazing lawns and browsing hedges are functionally similar.
In each case, plants expressing tolerance traits can withstand chronic grazing or browsing in sites where the nutritive value of the local food resource is enhanced in positive feedback to the actions of its consumers. The debate
over whether ungulates accelerate or decelerate nutrient
cycling can be resolved by comparing grazing and browsing effects in the same ecosystem type. Evidence from
Communicated by Jörg U. Ganzhorn.
J. T. du Toit (*) Department of Wildland Resources, Utah State University,
Logan, UT 84322‑5230, USA
e-mail: [email protected]
H. Olff Center for Ecological and Evolutionary Studies, University
of Groningen, Nijenborgh 7, 9747 AG Groningen,
The Netherlands
African savannas points to the rate of nutrient cycling being
controlled by the mix of tolerance and resistance traits in
plants; not the relative dominance of grazing or browsing
by local herbivores. We recommend this across-guild comparative approach as a novel solution with widespread utility for resolving contingencies in community processes.
Keywords Community ecology · Ungulate ·
Competition · Facilitation · Lawn · Nutrient cycling
Introduction
Finding generalities at the community level is a special
challenge to ecologists because communities are both
complex and idiosyncratic. Any patterns or processes that
might be identified within them are contingent upon the
conditions that define them (Lawton 1999). Therefore, in
the context of community ecology, a contingency is a constraint on a generality and is caused by the observed pattern or process being applicable only within a subset of
potential conditions. Controlling such contingencies can
require large-scale replication using global research networks to standardize multiple local studies for testing postulated generalities in community-level patterns (Adler
et al. 2011). Another approach is to make comparisons
across similar ecosystem types on different continents
(Knapp et al. 2004) or even across marine and terrestrial
ecosystems (Webb 2012), with the one ecosystem serving as the “control” for the other. For example, it has been
found helpful to compare marine and terrestrial predator–
prey systems to identify universal behavioral responses by
which prey animals reduce their risk of predation (Wirsing and Ripple 2011). Here we propose that contingencies can also be controlled within ecosystems by making
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Oecologia (2014) 174:1075–1083
Variation in body size
Guild 1
Guild 2
Guild k
Generality
Variation in resource use
Fig. 1 A conceptual framework for identifying generalities applicable to vertebrates at the community level. Variation in resource use
allows for the functional classification of species into two or more
guilds, within each of which there is variation in body size. Ecological or evolutionary patterns or processes identified within one guild
might be contingent upon the subset of resources defining that guild.
Across-guild comparisons enable the emergence of patterns or processes that apply across all variations in resource use and body size
within the assemblage of interest, and the identification of contingencies in those that do not. A community-level generality is free of contingencies across guilds
comparisons at the community level, between functionally
differentiated species groups.
As a conceptual framework for vertebrates (Fig. 1), body
size and resource use are ecologically important sources of
variation that provide the basis for a functional classification of species within a community of interest. Empirical
patterns within separate functional groups (trophic guilds)
are contingent upon separate resource classes and such patterns are blurred, or “noisy,” if the functional groupings are
ignored. If, however, an ecological or evolutionary process
is explored in each guild and analogous patterns are found,
even despite certain differences (in slope, intercept, scatter, etc.), then a generality has emerged across guilds. For
example, the scaling of space use by individual animals has
long been debated by authors using global meta-analyses in
which the data are grouped by taxonomic class and trophic
level. In mammals the groupings were initially as coarse as
“hunters” and “croppers” (McNab 1963) and over the next
40 years were only minimally refined to carnivores, omnivores, and herbivores (Jetz et al. 2004). But now a focused
meta-analysis of space use by terrestrial and arboreal
primates—essentially an across-guild comparison—has
at least clarified the general determinants of home range
overlap, even if not the individual use of space (Pearce
et al. 2013). Conversely, across-guild comparisons are also
useful for identifying contingencies. The island rule, for
instance, predicts gigantism for small terrestrial vertebrate
species and dwarfism for large ones when insular types are
compared with their mainland ancestors (Lomolino 2005).
In their recent meta-analysis Lomolino et al. (2013) found
the island effect to be strongest in palaeo-insular species
13
(extant species excluded) dependent on terrestrial food
resources (species using aquatic food resources excluded).
Hence, the effect emerges through prolonged isolation and
is contingent upon a relatively restricted resource base;
identifying the contingency delimits the generality of the
rule. Such examples fit within the conceptual framework of
across-guild comparisons (Fig. 1) yet that general approach
has not previously been formalized for controlling the contingency problem in community ecology. Here we demonstrate the utility of the framework for clarifying generalities
in grazing and browsing ecology. Our focus is on animal–
plant and animal–animal interactions in terrestrial communities that include large herbivorous mammals (>5 kg).
Grazers and browsers
Grazers mainly eat the foliage of monocotyledons (such as
grasses and sedges) whereas browsers mainly eat the foliage of dicotyledons (forbs and woody plants). Browsing is
evolutionarily older than grazing, which mostly coevolved
with the radiation of grasses over the past 15 million years
(Janis et al. 2000). Therefore, because the two guilds result
from evolutionary radiation in different episodes with different contingencies, they can be considered a “repeated
experiment” in evolutionary time. Browsers have always
been in a coevolutionary arms race with their woody food
plants, which have a plethora of physical and chemical
defenses against herbivory, towards which grasses are comparatively tolerant (Gordon and Prins 2008). Some mammalian taxa such as bovids, cervids and rhinos are represented in both guilds, and some such as equids (grazers)
and giraffids (browsers) are exclusive to either one. Some
species known as “mixed feeders” switch back and forth
between guilds, mainly grazing when green grass is available and browsing when the grass turns brown or disappears in the winter or dry season. Among species of similar
size and gut morphology, the digestive systems of grazers
and browsers are essentially the same (Gordon and Illius
1994). Nevertheless, the numerous large herbivore species
that are specialized for either grazing or browsing represent
two species groups recognized as being behaviorally and
functionally distinct within their ecosystems (Gordon and
Prins 2008).
The resource base of grazers is distributed across the
landscape in an essentially continuous two-dimensional
grassy carpet while the shrubs and trees fed on by browsers occur as discrete food sources each with its own threedimensional architecture. The economically most important free-ranging livestock species (cattle, sheep, horses)
are grazers, which stay in herds on open plains or pastures
from which excess food can be harvested and stored as hay,
making them generally easier to manage than browsers. As
a result there is a research bias towards grazers and therein
Oecologia (2014) 174:1075–1083
lies an unresolved contingency—grazers use only a subset
(mainly grass) of all the plant types constituting the food
resources of large herbivores. Here we propose, and aim to
demonstrate with examples, that browsing ecology is now
sufficiently developed for us to assume that a meaningful
generality in large herbivore ecology is one that applies to
grazing and browsing guilds alike.
Our conceptual framework (Fig. 1) entails the comparison of guilds in which member species display substantial
variation in body size, which suits large mammalian herbivores because their body masses span three orders of
magnitude. However, the megafaunal extinctions of the late
Quarternary period have, for a variety of possible reasons
of which some are anthropogenic (Brook and Bowman
2004), depauperated the larger mammalian size classes on
all continents other than Africa (Johnson 2002). We thus
draw heavily from the literature on grazing and browsing
ecology in African savannas, where both guilds are represented in the fauna with the highest diversity of extant
ungulate species in the widest body-size range (du Toit and
Cumming 1999).
Generality 1: variations in body size and trophic
morphology underlie resource partitioning at multiple
scales
The across-guild comparative approach was used, apparently inadvertently, by Geist (1974) in his formulation of
the strongest generality in ungulate ecology, the Jarman–
Bell principle. It was based on two independent studies: one of behavioral ecology in grazing and browsing
antelopes (Jarman 1974); the other on feeding ecology in
a grazing guild (Bell 1971). The essential principle, that
larger herbivores can survive on lower quality food that is
more abundant, has been found to rest solidly on allometric scaling laws and empirical evidence (Demment and Van
Soest 1985; Illius and Gordon 1987, 1992). Differences in
body size among sympatric guild members therefore imply
interspecific differences in tolerance for less-digestible
(fibrous) foods during periods of nutritional limitation,
signaling evolutionary pressure for resource partitioning
(du Toit 2011; Kleynhans et al. 2011).
Scaling up from bites of food to the spatial arrangement
of herbaceous plants in a pasture or branches on a tree,
allometries of dietary tolerance and other size-dependent
features (e.g. stride length, bite volume) predict that herbivores of different body size should perceive food patches at
coarser or finer scales of spatial resolution (Cromsigt and
Olff 2006; Laca et al. 2010). Indeed, recent field experiments and simulation models confirm that grazers (sheep,
cattle) and browsers (moose Alces alces) are predictably
sensitive to variation in the fractal dimensions of their
1077
immediate foraging environments (Laca et al. 2010; Pastor and De Jager 2013). Also, at the habitat scale, the wider
dietary tolerances of larger herbivore species should enable
them to occupy a wider range of habitat types. Conversely,
smaller species should each be more specialized for specific habitats that provide higher quality food year-round.
This theoretical prediction has been empirically confirmed
for grazing and browsing guilds (du Toit and Owen-Smith
1989; Redfern et al. 2006) despite differences in digestive
morphology (ruminant vs. non-ruminant) complicating
the pattern among grazers (Cromsigt et al. 2009). Overall,
across multiple scales, body size emerges as the primary
axis along which resources are partitioned among coexisting species in both guilds. Being a contingency-free rule,
the Jarman–Bell principle is of immense heuristic value to
the ecology and management of communities that include
large herbivores. It also reaffirms the importance of metabolic theory as a conceptual pillar of ecology (Brown et al.
2004).
Generality 2: competition exerts a stronger influence
than facilitation on the structure of large herbivore
assemblages when food resources are limiting
Originally described from field observations in East Africa
(Vesey-Fitzgerald 1960), “the grazing succession” refers
to waves of different ungulate species grazing patches of
grassland in a predictable sequence. In his classic analysis
of the phenomenon, Bell (1971) surmised that the “earlier
members of the succession prepare the structure of the
vegetation for the following members,” implying facilitation as the primary interspecific interaction. The particular
grazing succession studied by Bell involved zebra Equus
quagga, wildebeest Connochaetes taurinus, and Thomson’s
gazelle Eudorcas thomsonii feeding from the same sward
but with their peak densities separated by intervals of about
2 months (Fig. 2). With zebras being non-ruminants and
larger (approximate adult female mass = 219 kg) than wildebeest (163 kg) and gazelles (16 kg), the order of succession corresponds with the order of narrowing dietary tolerances; zebras can tolerate ingesting the highest fraction of
fibrous stem from the mix of grass stem, sheath and leaf tissues available in the sward. Bell’s grazing succession, with
partitioned grazing niches and facilitation of the smaller
members by the voluntary actions of the larger members,
is a compelling concept but has become widely questioned
(Illius and Gordon 1987; Arsenault and Owen-Smith 2002,
2008; Kleynhans et al. 2011). We suggest some clarity can
be gained by resolving the contingency inherent in community-level studies that focus on grazers. If communities that
include large herbivorous mammals are primarily structured either by facilitation or competition, then a common
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Oecologia (2014) 174:1075–1083
underlying process should be evident in both grazing and
browsing guilds.
The disproportionately long necks of some terrestrial
herbivores such as giraffes Giraffa camelopardalis, tortoises (e.g. Chelonoidis spp.), and perhaps sauropod dinosaurs, are parsimoniously explained by selection for high
browsing (Wilkinson and Ruxton 2012). Giraffes can feed
up and down a wide height range, but by feeding above
reach of other browsers they derive an advantage in leaf
mass gained per bite from the canopy (Woolnough and du
Toit 2001). An experiment involving fenced and unfenced
trees in the wild showed reduced leaf availability per shoot
in the lower canopies of unfenced trees, caused by selective browsing by various ungulate species shorter than
giraffes (Cameron and du Toit 2007). Those smaller-bodied guild members, having narrower dietary tolerances,
narrower muzzles, and lower intake requirements enabling more time for selective feeding, pick out the most
palatable leaves and shoots from the foliage within their
reach. Giraffes therefore benefit by browsing on leafier
shoots higher in the canopy. The result is browsing stratification, which, we argue, is driven by the same process
as the grazing succession but in a vertical instead of horizontal plane (Fig. 3). The patterns obviously differ in that
the grazing succession involves herbivores of different
size feeding in the same sward at different times, whereas
in browsing stratification the different-sized herbivores
feed at different heights at the same time. Nevertheless,
1.0
Relative density
0.8
Thomson's
gazelle
0.6
0.4
Zebra
0.2
Wildebeest
0.0
0
1
2
3
4
5
6
Month after peak rain
Fig. 2 Grazing succession in which different ungulate population
densities peak on the same patch of grassland in a sequence through
time. Counts of each herbivore species were made by Bell (1971) in
standardized transects in each month over 3 successive years in the
Serengeti ecosystem of East Africa. Here, the counts over all 3 years
are combined for each month following peak rain and expressed as
relative density with 1.0 being the highest population density for that
species. Zebras graze down the tall grass during and soon after the
rainfall peak. They become replaced by wildebeest, which, when the
abundance of the grass resource is declining some 3–4 months after
the rainfall peak, are replaced by Thomson’s gazelles
5
a
b
Giraffe
Kudu
Steenbok
Height (m)
4
3
2
1
0
0.0
0.5
1.0
1.5
2.0
2.5
0.0
Leaf biomass (g)
Fig. 3a, b Browsing stratification in which ungulate species differ
in the heights above ground at which they allocate time to browsing.
Measured in the Kruger ecosystem of South Africa (Cameron and du
Toit 2007), leaf biomass (dry) per standardized Acacia nigrescens
shoot is reduced in the lower canopies of trees exposed to a complete
guild of browsing ungulates (filled symbols; mean ± SE), when compared to neighboring trees excluded by fences 2.2 m high (open sym-
13
0.2
0.4
0.6
0.8
Proportion of feeding time
bols), but not above ~3 m where only giraffes have access (a). In the
same ecosystem, the allocation of feeding time across heights from
the ground (du Toit 1990) shows that giraffes avoid competing with
other guild members, here represented by kudu Tragelaphus strepsiceros and steenbok Raphicerus campestris, that selectively reduce
leaf biomass per shoot at the lower levels of the canopy (b)
Oecologia (2014) 174:1075–1083
the underlying process—smaller species directionally displacing larger species from feeding sites—is the same and
is supported by modeled and observed interactions within
both guilds (Illius and Gordon 1987; Gordon and Illius
1989; Van de Koppel and Prins 1998; Cameron and du
Toit 2007). The emerging generality is that competition
has a stronger influence than facilitation in structuring
large herbivore assemblages under conditions of resource
limitation.
When the food resource is abundant, facilitation can
explain the movement of smaller grazers onto swards
that have been coarsely grazed and trampled by larger
species (Van de Koppel and Prins 1998). Facilitation
can also explain wet season weight gains in cattle grazing together with zebras (Odadi et al. 2011), and impala
Aepyceros melampus population growth in areas where
browsing elephants Loxodonta africana have converted
woodland to shrubland (Rutina et al. 2005; Moe et al.
2009). Nevertheless, reduced patch residence time and/
or locally depressed feeding efficiency are to be expected
for the facilitating species when the abundance of shared
resources declines (Arsenault and Owen-Smith 2002).
That expectation is consistent with Bell’s original data
from the Serengeti grazing succession in which, about
3 months after the rainfall peak in 3 successive years,
wildebeest moved forward each time Thomson’s gazelles
began moving in from behind (Fig. 2). Exceptions apply,
of course, to those large species that are anatomically
specialized for lawn grazing, such as hippos Hippopotamus amphibius and white rhinos Ceratotherium simum
that pluck short grass with their wide lips (Arsenault and
Owen-Smith 2008). The particular niches into which
those species have evolved appear to be virtually immune
from interspecific competition.
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Generality 3: plant‑herbivore feedbacks maintain
grazing lawns and browsing hedges
Lawns form where grazing is chronically concentrated on
localized sites occurring within a lightly grazed matrix of
grassy vegetation (Fig. 4a). They are dominated by grazing-tolerant stoloniferous grasses maintained in early
growth stages within close-cropped patches surrounded by
taller bunchgrasses (McNaughton 1984; Archibald 2008;
Cromsigt and Olff 2008). Typically linked with aggregations of grazers such as herds of ungulates or flocks of
geese, grazing lawns can also be created and maintained
by small groups, or even individuals, of very large grazers such as white rhinos (Waldram et al. 2008). Although
grazing lawns are, by definition, phenomena of the grazing
guild, we are interested in whether the underlying herbivore-plant interactions are contingent upon grazing or can
be generalized across guilds. Indeed, recent comparisons of
grazing lawns and browsing hedges (Fornara and du Toit
2007; Cromsigt and Kuijper 2011) confirm that similar
interactions do occur in both guilds, allowing a generality
to emerge.
There are numerous examples from tropical, temperate,
and boreal ecosystems of increased browsing intensity
on woody plants that respond with tolerance traits (Fornoni 2011) associated with increased palatability, attracting further browsing (Cromsigt and Kuijper 2011). Compensatory growth can be of enhanced nutritional value
to browsers (du Toit et al. 1990; Danell et al. 1994) but
is produced by chronically pruned plants at the expense
of sexual reproduction. Long-term population studies
are needed on the comparative life histories of woody
plants that support browsing hedges and those that do
not, yet some patterns are apparent. For example, in the
Fig. 4a, b A typical grazing lawn (a) maintained by cattle on the island of Schiermonnikoog, the Netherlands, and an A. nigrescens tree pruned
into a characteristically conical browsing hedge (b) by giraffes in the Kruger National Park, South Africa. Photographs: J. T. du Toit
13
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taiga vegetation of northern Scandinavia, winter browsing by moose on willows (Salix phylicifolia) results in
fewer catkins on browsed compared to unbrowsed twigs
within individual plants in the following spring (Stolter
2008). Across gradients of browsing intensity in African
savannas, Acacia stands at the high ends have a lower proportion of trees carrying pods and fewer pods per tree in
comparison with stands at the low ends (Fornara and du
Toit 2007; Goheen et al. 2007). Saplings at the high ends
of browsing gradients also build disproportionately large
root systems, perhaps as “storage” that can be mobilized
for rapid growth in sporadic windows of opportunity when
browser densities are low (Fornara and du Toit 2008a).
Also, in temperate European floodplains where Prunus
spinosa is chronically browsed by large herbivores, this
spinescent shrub propagates through rhizomes to form
thickets in a strategy similar to that of lawn grasses (Bakker et al. 2004).
At the plant community level, grazing lawns are distinct
in both structure and composition, being densely packed
assemblages dominated by prostrate, grazing-tolerant grass
species. Browsing hedges, however, can vary from heavily browsed individual shrubs or trees (Fig. 4b) within
mixed stands that include lightly browsed plants (Bakker
et al. 2004; Fornara and du Toit 2007) to dense multi-species patches of saplings “captured” by browsers in forest
gaps (Cromsigt and Kuijper 2011). The latter case has the
community-level characteristics of a grazing lawn, but is
the lawn analogy being stretched too far when applied to
hedged individual trees and shrubs? We suggest not. When
a patch within a bunchgrass community becomes converted
into a grazing lawn by local interactions of grazing, rainfall and fire (Archibald 2008), some plants grow horizontally by sending out stolons that establish multiple new
tufts within a dense lawn. If all tufts within a grazing lawn
were grouped by their vegetative origins, and each resulting
genet classified as one plant, then the numerical dominance
of the community would change dramatically. Viewed in
this way, each genet of stoloniferous tufts in a grazing lawn
is the prostrate equivalent of a clonal Prunus thicket (Bakker et al. 2004) or a hedged Acacia tree (Fornara and du
Toit 2007).
As a generality, spatial variations in grazing and browsing intensity are associated with variations in the morphophysiological traits of each guild’s food plants. Grazing
lawns and browsing hedges are characterized by herbaceous and woody plants (respectively) with tolerance traits
that allow survival in physiologically young growth stages
under chronic herbivory regimes. In each case, the nutritive value and productivity of the local food resource
is enhanced by plants maintaining younger tissues that
are replaced in positive feedback to the actions of their
consumers.
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Oecologia (2014) 174:1075–1083
Generality 4: nutrient cycling through large herbivores
is controlled by plant defensive traits
Resistance is any plant trait that reduces the preference or
performance of herbivores, whereas tolerance is the relative degree to which a plant’s fitness is affected by herbivores (Strauss and Agrawal 1999). Both traits influence the
effects of herbivores on nutrient cycling and in terrestrial
ecosystems these effects can be either accelerating or decelerating (Ritchie et al. 1998). First described in the savanna
of East Africa’s Serengeti (McNaughton 1976, 1985), the
accelerating effect occurs where grasses with tolerance
traits compensate for grazing by replacing nutrient-rich
above-ground tissues through increased rates of nutrient
uptake and growth. The decelerating effect is best known
from the boreal forest of North America’s Isle Royale (Pastor and Naiman 1992) where long-term selective browsing
by moose exposes the competitive advantages of woody
plants with resistance traits. Such traits include chemically
defended leaves with low nitrogen and high lignin contents,
which decompose slowly. Serengeti and Isle Royale represent ecosystem types with extreme differences in multiple dimensions yet from them a generality has emerged in
the literature: accelerating effects are attributed to grazing
systems; decelerating effects to browsing systems (Pastor
et al. 2006). Here we apply the across-guild comparative
approach to question the generality of this grazer-browser
dichotomy in nutrient cycling.
Chronically intense herbivory by ungulates contributes to the encroachment of woody plants in rangelands
worldwide and even targeted browsing by goats is usually inadequate to reverse the process (Archer 2010). In
African savannas, the encroaching woody plants are commonly shrubs and trees such as various Acacia species and
Dichrostachys cinerea (Roques et al. 2001). These fastgrowing, herbivore-tolerant legumes are physiologically
adapted for fertile soils, with foliage that is highly palatable
to browsing ungulates (Bryant et al. 1989). Plant tolerance
to herbivory can be expressed together with resistance (Fornoni 2011) and in the cases of African Acacia species and
D. cinerea the main resistance trait is spinescence. Uncommon among boreal forest plants, spinescence in African
savanna plants restricts tissue loss sufficiently to allow
palatable species to persist in sites of chronically intense
browsing without any apparent deceleration of nutrient
cycling (Fornara and du Toit 2007, 2008b, c). Furthermore,
post-browsing regrowth on such species is typically characterized by reduced leaf concentrations of carbon-based secondary metabolites (du Toit et al. 1990; Fornara and du Toit
2007) and this even applies to some non-spinescent species
(Rooke and Bergström 2007; Scogings et al. 2011). With
accelerated decomposition of the resulting litter, browsing
can have a positive effect on nutrient cycling in ecosystems
Oecologia (2014) 174:1075–1083
Fig. 5a, b Simplified pathways
of flow among nutrient pools
and the controls exerted upon
them by plant defensive traits in
terrestrial ecosystems. In boreal
forests (a) biomass is dominated
by woody plants that express
strong resistance to herbivory
through plant chemical defense.
Chronic selective browsing
drives a long-term shift in plant
community composition leading
to an accumulation of nutrients in plants and litter, with
decelerated “brown” nutrient
cycling. In African savannas
(b) plants with tolerance traits,
such as compensatory growth,
can withstand chronic grazing
and browsing. Tolerance can be
expressed together with resistance such as spinescence, which
is common in these ecosystems
among woody plants that are
fast growing and produce highly
palatable leaves that decompose
quickly. Here nutrients flow
through an accelerated “green”
cycle (color figure online)
1081
Resistance
a
Tolerance
Litter
Plants
Herbivores
Soil
Urine
Dung
Carrion
Carnivores
Resistance
Resistance
b
Tolerance
Litter
Plants
Herbivores
Soil
Urine
Dung
Carrion
Carnivores
Resistance
as different as Acacia savannas in South Africa (Fornara
and du Toit 2008c) and mountain birch (Betula pubescens
ssp. czerepanovii) forests in northernmost Finland (Stark
et al. 2007).
Accelerating and decelerating effects of herbivores on
nutrient cycling, as postulated by Ritchie et al. (1998), were
not originally ascribed to grazing and browsing guilds,
respectively. Despite compelling evidence linking browsing and decelerated nutrient cycling in the boreal forest of
Isle Royale (Pastor and Naiman 1992), results from exclosure studies in other North American ecosystems remain
equivocal (Singer and Schoenecker 2003; Bressette et al.
2012). Further research is needed on the rates and pathways of nutrient cycling associated with browsing hedges
in multiple ecosystems (Cromsigt and Kuijper 2011) but
we question the generality of the grazer-browser dichotomy
as a controller of nutrient cycling. Rather, we point to factors controlling whether nutrients taken up by plants are
recycled through herbivores (accelerated “green” cycle) or
detritivores (decelerated “brown” cycle), which can also
partly explain “why the ground is more brown than the
world is green” (Allison 2006). In some plant communities, such as in boreal forests where resistance (chemical
defense) is the dominant defensive trait, browsing drives
a long-term shift in woody plant species composition that
results in accumulations of recalcitrant litter decomposing
slowly in the brown cycle (Fig. 5a). In other plant communities, such as in African savannas where tolerance (compensatory growth) and resistance (spinescence) are both
commonly expressed, grazing and browsing together provide a major conduit for nutrients to pass comparatively
rapidly through the green cycle (Fig. 5b). We consequently
propose, as a broad generality, that the influence of large
herbivores—grazers and browsers alike—on the rate of
nutrient cycling is controlled by the mix of tolerance and
resistance traits in the plant community.
Conclusion
In heed of Lawton’s (1999) warning that “community ecology is a mess, with so much contingency that useful generalizations are hard to find,” we encourage enquiry into
methods to control the contingency problem rather than
discourage the search for useful generalizations. For an
approach that is at least applicable to terrestrial vertebrates,
we recommend a conceptual framework in which the species of interest are organized into two or more trophic
guilds. If a candidate generalization is found to hold across
guilds then it is not contingent upon any particular subset
13
1082
of resources. It can thus be accepted as a generalized ecological or evolutionary pattern or process at the community
level. We used large mammalian herbivores to illustrate
this approach because they display wide variation in body
size within two distinct trophic guilds. Each of those guilds
has been extensively studied within the topics we sifted
through for generalities, those being: interspecific competitive displacement from shared feeding sites when resources
are limiting; plant-herbivore feedbacks; the involvement of
large herbivores in nutrient cycling. We chose those wellstudied topics for the very reason that generalities can only
be drawn from an adequate knowledge base. The acrossguild comparative approach, therefore, requires both an
adequate distribution of species across guilds within the
same ecosystem types and an adequate distribution of
research across these guilds. Nevertheless, in addition to
clarifying or rejecting generalities, across-guild comparisons should also be helpful for identifying knowledge gaps
and stimulating new hypothesis-driven research in community ecology.
Acknowledgments We are grateful to Jörg Ganzhorn and two anonymous reviewers for helpful comments on a previous draft. J. T. d. T.
was supported by a visitor’s travel grant from the Nederlandse Organisatie voor Wetenschappelijk Onderzoek. We thank Dick Visser for
help with the figures.
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