Pasture Ecology Meeting Plant-Herbivore Relationships · ty, biogeochemical cycles and landscapes....
Transcript of Pasture Ecology Meeting Plant-Herbivore Relationships · ty, biogeochemical cycles and landscapes....
Pasture Ecology Meeting
Plant-Herbivore Relationships
Clermont-Ferrand / Theix, 31 May and 1 June 2002
Conference organized by
P. Carrère and J.F. Soussana
(INRA Agronomy Unit)
R. Baumont
(INRA Herbivore Research Unit)
Published in:
ANIMAL RESEARCH - Volume 52 - Number 2 - 2003 - pp. 141 - 190http://www.edpsciences.org/animres/
Foreword
The Pasture Ecology meeting was organized in Clermont-Ferrand/Theix on 31May and 1st June as a satellite meeting of the 19th congress of the EuropeanGrassland Federation held in La Rochelle (France) in May 2002. Eighty-eightscientists from seventeen countries joined this meeting and had deep and stimu-lating scientific exchanges on vegetation dynamics, plant-herbivore interactionsand management in grassland ecosystems. We are pleased to publish here thethree main papers that were given in the session focussed on plant-herbivorerelationships.
Grazing is one of the major processes that affect grassland ecosystem dynamics.Grasslands are no longer seen only as a feeding resource for domestic herbivo-res, but also as an environmental resource through its contribution to biodiversi-ty, biogeochemical cycles and landscapes. Thus, there is a considerable need toimprove scientific knowledge by including a comprehensive view of how gra-zing can contribute to the multi-functionality of grasslands. Grazing results fromcomplex interactions between animals and vegetation. These interactions occurat different spatio-temporal scales from the smallest that is the prehension ofbites to the largest at the plot level. On all of these scales, animals create andrespond to heterogeneity of the vegetation. The creation and maintenance ofheterogeneity at different scales can be analysed in terms of constraints or bene-fits for grazing animals' diets and for grassland management for environmentalpurposes, biodiversity for example. The three papers gathered here bring anoverview of recent scientific advances in the comprehension of the grazing pro-cess from small to large scales and give some prospects in the development ofgrazing management for a multi-purpose use of grasslands.
R. BaumontGuest Editor
Review article
Sward structural resistance and biting effort
in grazing ruminants
Wendy M. GRIFFITHS*, Iain J. GORDON
Macaulay Institute, Craigiebuckler, Aberdeen AB15 8QH, Scotland, UK
(Received 5 September 2002; accepted 25 February 2003)
Abstract — Grazing ruminants face complex decisions in searching for and harvesting adequate for-
age to meet their requirements in the face of heterogeneity in the abundance, nutritive value and distri-
bution of resources. Some of the major decisions which affect the bite mass and therefore, forage
intake adjustments in bite depth, bite area and exerted bite force, are made in relation to heterogeneity
in sward structure. A number of relationships have been established linking the adjustment of bite
mechanics in response to variations in sward height and bulk density on temperate forages for animals
of a range of body sizes. However, there is less consistency in the response of the bite mechanics to the
greater variations in structural resistance that arise from the vertical and horizontal arrangements of
the plant morphological organs of leaf, pseudostem and stem. Furthermore, only limited progress has
been made in quantifying the biting forces involved in grazing, the linkages between the plant mor-
phological organs and their effect on bite force and, the interaction with body mass. In this paper, we
discuss the different hypotheses that have been proposed to explain the regulation of bite depth and
provide evidence for their acceptance or rejection. We comment on the knowledge gap in understand-
ing biting force mechanisms across animal species of contrasting body mass, and stress the need for
differentiation between the concepts of biting force and biting effort.
bite / effort / force / ruminants / structure
Résumé — Résistance de structure du couvert végétal et effort de prélèvement des bouchées
chez les ruminants au pâturage. Face à l’hétérogénéité de la ressource en abondance, en valeur nu-
tritive et en répartition, les ruminants au pâturage doivent prendre des décisions complexes pour re-
chercher et récolter les fourrages nécessaires à leurs besoins. Certaines de ces décisions affectent la
masse de la bouchée et donc, l’ajustement de l’ingestion en terme de profondeur et de surface de la
bouchée, ainsi que de force de prélèvement. Ces décisions sont prises en relation avec l’hétérogénéité
de la structure du couvert végétal. Nombre de relations ont été mises en évidence liant l’adaptation de
la mécanique de la bouchée aux variations de la hauteur et de la densité du couvert végétal de fourra-
ges tempérés pour des animaux de différentes tailles corporelles. En revanche, les grandes variations
145
Anim. Res. 52 (2003) 145–160
INRA, EDP Sciences, 2003
DOI: 10.1051/animres:2003012
* Correspondence and reprints
Tel.: + 44 (0) 1224 498200; fax: + 44 (0) 1224 311566; e-mail: [email protected]
de résistance des végétaux, qui résultent des arrangements verticaux et horizontaux des organes mor-
phologiques de la plante (feuille, gaine et tige), ont des effets variables sur la mécanique de la
bouchée. De plus, seuls des progrès limités ont été accomplis pour quantifier les forces de prélève-
ment des bouchées impliquées au pâturage, les liens entre les organes morphologiques de la plante et
leurs effets sur les forces de prélèvement, ainsi que l’interaction avec le format des animaux. Dans cet
article, nous discutons les différentes hypothèses qui ont été proposées pour expliquer la régulation de
la profondeur des bouchées, et nous proposons des éléments pour leur acceptation ou leur rejet. Nous
exposons les lacunes qui subsistent pour comprendre les mécanismes des forces de prélèvement à tra-
vers différentes espèces animales de formats distincts et nous soulignons le besoin de différencier
deux concepts : la force de prélèvement et l’effort de prélèvement.
bouchée / effort / force / ruminants / structure
1. INTRODUCTION
The harvesting of forage is a particularly
time-consuming exercise for ruminants; a
large number of bites, of a relatively small
bite mass, are required to meet the nutrient
intake requirements for maintenance,
growth and reproduction. A number of re-
views have discussed the mechanisms of
foraging behaviour [7, 9, 45, 50, 59, 60], in-
cluding the considerable advances that
have been made in understanding the influ-
ence of the independent effects of sward
height and sward bulk density on the com-
ponents (e.g. bite mass and bite rate) of
daily herbage intake [19, 30, 38, 59]. How-
ever, despite the comprehensive informa-
tion available, researchers are still unable to
predict the intake responses of grazing ani-
mals to changes in the vegetation structure
and morphology of more complex swards.
Illius and Hodgson [41] suggested that this
lack of predictive power emphasised the
abundance of descriptive studies, and
called for studies to actively seek a mecha-
nistic explanation of sward-bite interac-
tions. Descriptive and mechanistic approaches
are, however, essentially intertwined due to the
difficulty of clarifying the many confounding,
and indeed complex sward-bite interac-
tions.
Our aim is to focus attention on the im-
portance of the interaction between the
morphological plant organs encompassed
within the bite, and biting effort, an area
that has received considerably less atten-
tion, even though the effects of the distribu-
tion of plant morphological organs on the
feeding strategy in ruminant species has re-
cently been stressed [59]. The principles
should have direct relevance to ruminants
foraging in both temperate and tropical eco-
systems.
In this paper we define sward structure
and the terminology associated with the
study of bite mechanics, describe the anat-
omy of the grass leaf with respect to sever-
ance, and highlight the potential contrasts
in severance action across animals of differ-
ent body mass. The inconsistency in termi-
nology, the methodologies and their
suitability for assessing bite force are iden-
tified. Evidence of the hypothesised link-
age between bite depth, bite area and bite
force is discussed, and lastly the idea of as-
sessing biting effort is introduced.
2. SWARD STRUCTURE AND
BITING FORCE TERMINOLOGY
Studies investigating the linkages be-
tween the structural organs and food
comminution in the mouth have been re-
viewed [56], but there is comparatively less
information on the linkages between sward
structure and biting effort. Further progress
146 W.M. Griffiths, I.J. Gordon
within this field calls for a review of the def-
initions of the terminology used in this area.
Morphological changes that occur with
plant maturation lead to different propor-
tions, and relative age, of leaf, pseudostem,
stem, and inflorescence in the vertical di-
mension of the sward [13]. The architecture
of these organs within the sward canopy is
termed sward structure. Sward bulk den-
sity; the weight of herbage per unit volume,
increases with increasing sward depth. This
pattern is more pronounced for tropical pas-
tures than for temperate pastures [28, 67],
and the slope of the relationship can also
vary markedly across swards of different
structure within temperate pastures [see
25]. The volume of a bite is the major con-
tributor of intake rate, and comprises bite
depth, which is the vertical distance that an-
imals insert their muzzle into the sward,
and measured as the difference between
sward surface height and the residual height
post-grazing, and bite area, which is the
horizontal area of herbage encompassed
within a single bite [38, 48]. Evidence from
temperate swards shows that bite area ex-
hibits less sensitivity to sward variation
than does bite depth [12, 48, 53], although
Wade and Carvalho [74] suggest that bite
area is the primary parameter that animals
adjust to increase bite mass.
In linking the disciplines of plant me-
chanics with foraging behaviour we define
five plant-based terms: (i) fracture force in
tension, which is a measure of herbage
strength and is estimated from the maxi-
mum force that produces fracture of the
plant organ/s [80]; (ii) tensile strength,
which is the fracture force in tension per
unit cross-sectional area of the plant speci-
men [80, 81]; (iii) maximum force in shear,
also a measure of herbage strength and is
the maximum force required to fracture the
plant organ/s, and is determined from the
height of the highest peak on the force dis-
placement curve (N.B.: it does not repre-
sent the force to fracture the whole plant
organ) [80]; (iv) specific work to fracture,
equally known as toughness as it is mea-
sured by the energy required to shear the
test specimen per unit cross-sectional area
of the plant specimen [18, 80] and (v) resis-
tance, which is the theoretical, accumu-
lated force required for severing all of the
plant organs encompassed within a bite.
Two important animal-based terms are: (i)
bite force, which represents the three-dimen-
sional force applied in severing a bite (N.B.:
this term does not represent the force exerted
during chewing as given by Pérez-Barbería
and Gordon [57]) and (ii) biting effort, which
represents the power applied by the animal
to sever a bite and includes components of
resistance, bite force and head acceleration
(N.B.: the importance of the individual com-
ponents may interact with species body
mass and species differences in severance
action, see below SEVERANCE ACTION).
3. GRASS LEAF ANATOMY
Plants are the primary producers in most
food chains, and animal subsistence and
production is dependent upon them. For-
ages, like all plants, however, have evolved
structures that resist ingestion by grazing
animals (grazing resistance; [11]), as a
means of ensuring their own continued ex-
istence within ecosystems.
The grass leaf anatomy responsible for
protection against herbivory can be mod-
elled as a three component system [71],
consisting of sclerenchyma tissue, vascular
bundles and epidermal cells covered by a
protective cuticle. These components com-
prise the ‘fibre’ fraction, along with a ma-
trix consisting of thin-walled parenchyma
cells found in the leaf mesophyll. However,
these thick-walled cells that are heavily lig-
nified, and hence confer mechanical
strength to the plant by way of attachment
to chained bundles of vascular tissue only
account for a small proportion of leaf
cross-sectional area. Despite this, the fibre
Sward structure and biting effort 147
component accounts for 90–95% of the
longitudinal stiffness of grass leaves [71].
The critical disparity between the leaf
anatomy of grasses from the C3 and C4
photosynthetic pathways lies in the greater
number of veins, and smaller interveinal
distance [62, 78], and a higher proportion of
sclerenchyma [1, 78] in C4 species. These
structural characteristics strengthen plant
tissues [72]. In tropical ecosystems, envi-
ronmental temperature increases the rate of
plant growth, which increases plant
strength [72], and also reduces the moisture
content between the sclerenchyma fibres
[72], which leads to increased herbage
strength [34, 36]. Nevertheless, despite
possible categorical groupings of plants,
plant anatomy will vary between plant
groups, genera, species and even lines
within a species [77], but while some plants
may be stronger in tension, fracture proper-
ties will be more dependent on the organi-
sation of the bundles of sclerenchyma
which determines brittleness [73].
Wright and Vincent [81], in their review
of the mechanics of fracture in plants, dis-
cussed the three modes of crack propaga-
tion in a leaf; shear, tension and torsion, and
it is the modes of shear and tension that
have attracted interest from plant and ani-
mal scientists alike. Assessment of the me-
chanical properties of grass leaves is far
from new. It has provided information for
the design and improvement of the cutting
mechanisms in forage harvesting machines
[34, 51], and for plant breeding programmes
where the primary objective is to increase
forage intake [20, 36, 52], through increas-
ing the forage’s feeding value [70]. These
studies have focussed primarily on the
properties of fracture in shear. The interest
in relating the tensile properties of plants to
aspects of foraging behaviour, particularly
prehension, is of more recent origin [42, 68,
80], and has led to a clearer definition and
use of tensile strength to quantify fracture
properties in tension and the specific
work to fracture (i.e. toughness) in shear
for determining properties such as those as-
sociated with food comminution in the
mouth. Henry et al. [35] contended, how-
ever, that there was a lack of evidence to
support the partitioning of the fracture me-
chanics between prehension and chewing.
The sclerenchyma tissue content is often
reported in biomechanical studies where
the structural and fracture properties of
plants have been extensively evaluated [73,
80]. Fracture force in tension is well correlated
with the volume-fraction of sclerenchyma tis-
sue [80] when the sclerenchyma tissue is be-
low 15% of the volume-fraction of the leaf,
and the fibres are laterally separated [71,
73]. Above 15%, the fibres can be continu-
ous across the leaf, rendering the leaf brittle
[81], and thus more susceptible to fracture
since the leaf will lose a large proportion of
its strength with only a very small applied
force [72]. The plant properties that in-
crease mechanical resistance, chiefly the fi-
bre component, are essentially the same as
those that reduce plant digestibility [66,
80]. However, to rely on the nutritional in-
dices of Neutral Detergent Fibre (NDF) or
Acid Detergent Fibre (ADF) to provide
measures of herbage strength and resis-
tance would be inappropriate since fracture
force in tension (the maximum force that
produces fracture) is poorly correlated with
both NDF and ADF [80], whereas, for ex-
ample, the work to fracture in shear (the
area under the displacement curve) is well
correlated with both NDF and ADF, as well
as the lignin content of the leaf [80].
4. SEVERANCE ACTION
All ruminant species have a common
dental structure that consists of four paired
incisors set on the lower jaw, with a thick
pad of connective tissue, also known as the
dental pad, positioned on the upper jaw.
The act of severance entails the incisors
closing against the dental pad to grip each
mouthful of herbage before fracture of
148 W.M. Griffiths, I.J. Gordon
plant tissue occurs, although cattle have
been observed to grip herbage against the
incisors using the tongue [16].
The structural arrangement of parallel
venation in grass leaves, ensures that leaves
exhibit little fracture sensitivity, thus the
damage at the point of incisor insertion
does little to act as a concentrator of stress
[72]. Wright and Vincent [81] commented
that unlike small herbivores which can
avoid the problems of indigestible fibres in
plant tissues, by eating around them (e.g.
larvae of the gum-leaf skeletoniser moth,
Uraba lugens) or cutting the lamina with
their mandibles or incisors (e.g. rabbits
have upper and lower incisors), ruminants
must use their strength. If strength scales
with body mass [42], then how do small-
bodied ruminants cope with the same con-
straints as large-bodied ruminants? Vincent
[72] suggested that sheep (Ovis aries), like
geese, probably use a strategy that involves
creating a crease on the lamina, through
pulling the lamina at an angle across the in-
cisors, and thereby reducing the force re-
quired to create fracture. There is no known
quantitative evidence for this severance ac-
tion in sheep, and there is the puzzling con-
cern, as Vincent noted, that it is difficult to
create creases across multiple lamina. Cat-
tle (Bos taurus), sheep and goats (Capra
hircus) foraging on a range of swards have
been observed to insert and/or move their
mouth sideways into swards to gather herb-
age [21, 28, 61]. In these examples it is
likely that animals were making use of the
shearing cusps on the molars to grip and
sever plant tissue [see also 63], thereby ob-
taining a bite mass above what would other-
wise be possible.
5. QUANTIFYING BITE FORCE
The idea of measuring the mechanical
resistance of plants is far from new, but the
motivation, approach and reporting have
varied considerably [5, 18, 22, 32, 35, 51,
52, 73, 80]. One consequence has been the
number of different descriptive terms that
have surfaced and these are often used in-
terchangeably. ‘Strength’ and ‘toughness’
are both biological terms that have been
adopted in quantifying plant mechanical re-
sistance [e.g. 17, 22], possibly since they
represent a physical attribute that is easily
understood. There is, however, some confu-
sion since toughness commonly implies
strength. Correctly defined, toughness is a
measure of the energy required to propa-
gate a crack, and not a measure of the force
involved in fracturing material [81]. This
definition is crucial since it implies that
toughness is an important mechanical pa-
rameter for the chewing dynamics, but not
for the process of severance of plant mate-
rial.
Other inconsistencies have emerged in
the definition of tensile strength and the use
of the term shear strength, which has no
clear definition in its own right, and, there-
fore, varies in terms of its units of expres-
sion [e.g. 23, 69, 80 for tensile and 20,
43 for shear]. According to Wright and
Vincent [81] tensile strength should be re-
ported as the force for crack propagation
per unit cross-sectional area of plant mate-
rial, and consistent expression of tensile
strength would greatly facilitate across-
study comparisons. However, it is not al-
ways a feasible use of resources to conduct
laborious estimates of tensile strength
within the context of animal-based studies.
Fracture force is a measure of the maximum
force required to fracture a test specimen
[80]. It takes no account of cross-sectional
area of the plant material [80], and so has
less acceptability for comparison across
different plant species with contrasting
tiller size-density relationships, and thus
potentially contrasting lamina cross-sec-
tional area. Fracture force measurements,
however, can be carried out more quickly
since they omit the additional laborious cross-
sectional area measurement, and thus can
provide objective information on herbage
Sward structure and biting effort 149
strength, as long as the above constraints
are borne in mind.
When answering questions on the causal
relationship between bite force and bite me-
chanics, an area of concern lies with the es-
timates on single, whole or separated
fractions of plant organs and their relation
with clumped plant material encompassed
within a bite. For single tests to have direct
relevance, one question of particular impor-
tance, and that does not appear to have been
answered, is the potential error associated
with estimates using a constant multiplier
[e.g. 42]. In practical terms, it is unlikely
that the bite force required for the severance
of 10 leaves together will be the summation
of the strength of 10 single leaves, unless a
correction for the packing effect of leaves
encompassed within the bite is applied. The
absence of a constant multiplier would have
implications for the scaling of bite force
with modulations in bite area [e.g. 42, 68].
Other factors worthy of consideration are
that the number of leaves able to be creased
i.e. running at an angle over the incisors,
would be of a magnitude lower than the to-
tal number grasped. This is of particular im-
portance for the severance action in small
ruminants [see 72]. Furthermore, it is diffi-
cult to conceive that integrating the esti-
mates of fracture force in tension from
single, separate tests of leaf, pseudostem
and stem can model the predicted force for
a bite encompassing two or more morpho-
logical components, unless measurements
are made at a very fine level of precision
(i.e. 1 cm strata), forming serious con-
straints for swards more applicable for test-
ing with large-bodied animals.
Indirect assessments of bite force [42,
68] are derived from estimates of the force
required to fracture plant organs in the ver-
tical dimension. Although the contribution
from Illius et al. [42] predicted bite forces
indirectly from regressions based on a sepa-
rate set of swards, they amassed their data
from three studies, which may not be possi-
ble where time is a major constraint. Small-
scale apparatus’ that provide direct, quick
and reliable estimates from field conditions
would aid progress. There has been some
recognition of the need for the development
of portable field operated devices that mea-
sure fracture force in tension [68] and ten-
sile strength [76] in situ, providing an
estimate of the magnitude of the contrast in
resistance, for a given bite volume. Prog-
ress has nonetheless been slow and fraught
with difficulties; Westfall et al. [76] in a
short communication described a portable
tensilmeter with hand-operated modified
pliers and an electronic recording system,
and Tharmaraj [68] discussed a portable le-
ver operated clamping apparatus mounted
on a tripod frame, which expressed the peak
fracture force reading (Fig. 1). However,
for neither apparatus was it clear how the
rate of acceleration during fracture was
controlled.
Furthermore, an indirect estimate of bite
force from fracturing plant organs in ten-
sion does not fully mimic the mode of the
characteristic jerk action in the horizontal
plane during severance. By comparison, di-
rect quantification of the forces involved in
severing herbage in grazing animals yields
potentially more valuable information as
biomechanical force plates [75], such as
those used by Hughes et al. [40] and Laca
et al. [47] record three dimensional forces
(Figs. 2 and 3). Consequently, some dispar-
ity between values obtained from indirect
estimates as compared with direct method-
ology must be expected (Griffiths and
Gordon, in preparation). In the foreseeable
future, such technical difficulties will be-
come inconsequential if effort is made to
partition and present the force according to
the Cartesian coordinates. This is also a
critical point of evaluation as animal spe-
cies of contrasting body mass may allocate
the force between the Cartesian coordinates
differently. It is important to recognise that
bite force predicted indirectly from esti-
mates of fracture force and tensile strength,
provide only a theoretical framework for
150 W.M. Griffiths, I.J. Gordon
comparative purposes. These predictions
also leave many unanswered questions as to
the effort exerted, particularly as evidence
does not suggest a 1:1 response in bite ge-
ometry with plant resistance (see below
SUMMIT FORCE HYPOTHESIS).
6. BITE DEPTH AND THE LINKAGE
WITH BITE AREA AND BITE
FORCE
An increasing number of studies have
focussed on the responses of the bite me-
chanics to the structural complexity and the
rigidity of plant organs, but can we draw
any consistency between studies and quan-
titatively relate the response patterns to bite
force? Three hypotheses have been pro-
posed for the regulation of bite depth pene-
tration:
– Summit Force (6.1).
– Balancing reward against cost of bite
procurement (6.2).
– Marginal Revenue (6.3).
In discussing the available evidence to
support or reject the above three hypotheses
we pull together studies which have pro-
vided supporting data on fracture force in
tension, tensile strength and leaf toughness
and/or bite force when examining the pa-
rameters of bite volume. There are rela-
tively few studies that meet this criterion,
and all of these come from the vegetative
temperate forages. Only a few studies [e.g.
54, 69] have assessed tensile strength on
forages in more extensive grassland envi-
ronments, but these studies have not pro-
vided parallel data on bite volume. There is a
need to evaluate the hypotheses for swards
displaying greater structural complexity
Sward structure and biting effort 151
Figure 1. Tensile bite fracture force apparatus (from Tharmaraj [68]).
including those present in extensive grass-
land environments.
6.1. Summit force
The Summit Force hypothesis [37] was
originally offered as an explanation for the
association between bite depth and
pseudostem height [8, see also 2, 3] with the
rational response being one of animals being
constrained by the effort required to sever
pseudostem within the lower stratum. The
estimated fracture force of pseudostem was
later quantified [80] as approximately three
times that measured for a single leaf, and
arose from the complex arrangement of
concentric sheaths around the immature
leaves and growing points. In order to main-
tain consistency in bite force, the Summit
Force hypothesis implied that once the limit
in force had been reached, that animals
152 W.M. Griffiths, I.J. Gordon
Base frame bolted to thefloor
Force plate transducers
Sward
Threaded holes for securingtop plate and sward to forceplate
Boards protecting theforce plate
Force plate
Figure 2. Exploded view of a force plate apparatus (adapted from Webb and Clark [75] and Griffiths
and Gordon, unpublished).
Sward structure and biting effort 153
-30
-20
-10
0
10
20
30
40
Tugging the bite to the left
Tugging the bite to the right
Late
ralf
orce
(N)
5 10 15 20 25 30
-200
-150
-100
-50
0
50
Tugging the bite vertically
Pushing the herbage around during the grasping of the bite
Ver
tical
forc
e(N
)
Time (sec)
-60
-40
-20
0
20
40
60
Exclusive chewing jaw movement
Tugging the bite backwards
Tugging the bite forwards
Long
itudi
nalf
orce
(N)
Figure 3. An example of the output from a force plate apparatus for a series of 15 bites (from Griffiths
and Gordon, unpublished).
would adjust bite area to maintain a con-
stant bite force in the face of increasing
strength or tiller density.
There are comparatively few reports
documenting tiller, or leaf and stem
strength, and tiller density on bite area. De-
spite this, there appears to be general con-
sistency across studies in that the rate of
reduction in bite area is much lower than the
rate of increase in tiller density or tiller
strength [39, 48, 53, 68]. This suggests that
there is only a partial adjustment in bite area
in relation to sward structure, and further-
more, the adjustment has little effect in re-
ducing the energy required to sever a bite
[79]. This partial compensation in bite area
also explains, at least in part, the absence of
significant patterns in sweeping tongue
movements in cattle in response to decreased
lamina length across swards of different
structure [25]. Mitchell [53] demonstrated,
using pooled data from sheep and red deer
(Cervus elaphus), that bite area was only
35% greater on wheat (Triticum aestivum)
swards than ryegrass (Lolium perenne)
swards of identical height, despite the
ryegrass swards exhibiting 110% stronger
tissues (measured by shear). The reduction
of bite area in an attempt to maintain the bit-
ing force momentum can thus be consid-
ered to be a small effect. This inference is
supported by the few direct evaluations of
biting force. Hughes and colleagues [39,
40], using boxed swards anchored to a force
plate, found no supporting evidence for a
maximum force that goats or sheep exerted
across a range of sward arrangements
within immature swards and across sward
species. Similarly, cattle grazing from
hand-constructed swards mounted on a
force plate were not observed to exhibit a
maximum force per bite [46]. Furthermore,
Illius et al. [42], in a study with goats, found
appreciable variation in the indirect esti-
mates of bite force, derived by substituting
the grazed heights into polynomial regres-
sion equations summarising force-canopy
structure relationships, across broad- and
fine-leaved plant species. More recently,
Tharmaraj [68] indirectly estimated bite
forces using a field-operated bite force me-
ter and found no indication of a maximum
force that cattle exerted across a range of
plant species and tiller densities. The ab-
sence of a maximum bite force that animals
exert, irrespective of how the bite dimen-
sions are balanced in the face of tiller struc-
tural rigidity and bulk density constraints,
does not, therefore, lend support to the
Summit Force hypothesis. This is also
consistent with the fact that not all leaves
within the bite are severed simulta-
neously but rather in close succession
(W.M. Griffiths and I.J. Gordon, unpub-
lished data). In practical terms obtaining a
measure of the peak bite fracture force is of
little importance, and it is the average force
applied for a given bite that needs to be as-
sessed. Furthermore, rejection of the Sum-
mit Force hypothesis is supported by the
consistent findings that, across a wide
range of body sizes, animals do not always
fully exploit the available depth of regrowth
[sheep and guanacos (Lama guanicoe) [6],
bison (Bison bison) [10], cattle [27, 33]].
6.2. Balancing reward against cost
of bite procurement
A second hypothesis utilising economic
principles described an efficient forager as
one that forages to maximise, or at the very
least, balance the reward against the cost of
bite procurement i.e. force per bite [40].
However, as with the Summit Force hy-
pothesis there does not appear to be any
constancy in the force per bite. Hughes [39]
found that sheep were more willing to in-
crease the force exerted if the force was
compensated by a greater reward, while
Illius et al. [42] found that the expendi-
ture:reward ratio for goats was not consistent
across a range of plant species. More re-
cently, Tharmaraj [68] found a fluctuating
154 W.M. Griffiths, I.J. Gordon
expenditure: reward ratio across short and
tall swards, but a constant ratio when
swards varied in tiller density only. The cal-
culation that the energy gain from increased
penetration will always exceed the energy
cost [42], implies that the greatest gain will
be achieved from severance of material en-
compassed within the buccal cavity at the
base of the sward, in the absence of uproot-
ing. Why then, do cattle and other species,
restrict their grazing depth to some fraction
of sward height, even when the sward is
composed solely of lamina [48]? Further-
more, goats have been found to be insensi-
tive to the differential costs in penetration
depth for broad-leaved and fine-leaved spe-
cies, with the ratio between pseudostem
height and grazed height changing little
across the sward species [42]. It, therefore,
seems likely that the avoidance of a lower
stratum may be unrelated to the greater ef-
fort required by the animal to detach plant
organs relative to bite reward. Rather, it
may reflect the fact that encompassing
pseudostem within the bite slows down bite
formation, and would require additional
jaw movements to chew the more fibrous
material. Therefore, the animal strikes a
balance between severance and chewing
constraints, as discussed in the model of
Spalinger and Hobbs [65] and further eval-
uated by Shipley and Spalinger [63]. The
relationship between bite mass and chew-
ing behaviour has also been ascribed to the
need to strike a balance in the maintenance
of a grazing momentum [49]. However, the
importance attached to striking a balance
between severance and processing may be
over-emphasised since cattle are able to
prehend, and manipulate the contents of ex-
isting bites, within the same jaw movement
[49], effects that were assumed to be mutu-
ally exclusive in Spalinger and Hobbs’model
[65]. The overlap between prehension and
chewing can be, however, incorporated into
models, as shown by Farnsworth and Illius
[24].
6.3. Marginal revenue
Delving deeper into the application of
economic principles, a study by Illius et al.
[42] marked a further attempt to understand
the conceptual basis of bite depth. These
authors demonstrated, using goats and a
group of fine- and broad-leaved grasses,
that depth of penetration into a sward could
be predicted when account was taken of the
marginal revenue i.e. the differential in-
crease in bite force relative to the differen-
tial increase in energy intake rate. Despite
the variation in the predicted bite forces (by
indirect measures) and contrasting grazing
depths, the goats grazed to a common mar-
ginal revenue, although the value of mar-
ginal revenue differed between the fine-
and broad-leaved species. This hypothesis
is both puzzling and plausible. Among the
three fine-leaved species, there was a clear
linkage between the mass of material re-
moved and the force involved in severing
those bites, but the reason for differing
common marginal revenue between the
fine- and broad-leaved species remains un-
clear. It is worth noting that had these au-
thors examined only one plant species from
each of the fine- and broad-leaved catego-
ries, an approach that would have been rea-
sonable, their conclusion would not have
held, emphasising that the marginal reve-
nue hypothesis may not explain penetration
responses across swards of greater structural
complexity. Critical evaluation of the hy-
pothesis across swards of contrasting struc-
ture and animals of different body size
awaits.
To summarise, the evidence to support
the three current hypotheses is weak and
new initiatives are required to shed light on
the determinants of bite mechanics.
7. EFFORT VS. FORCE
Increasingly it has become obvious that
there is no conclusive evidence to support
Sward structure and biting effort 155
any of the three key hypotheses that have
been put forward as mechanisms for ob-
served bite depth penetration responses. It
may not be that we need to put forward new
hypotheses, rather we need to discover new
approaches of thinking the problem. Cen-
tral to our understanding of biting force has
been the assumption that the force applied
in severance will be proportional to the
strength of individual plant components, al-
though Illius et al. [42] argued that the
structural arrangement of the plant compo-
nents has the greater bearing on the force
exerted. Nevertheless, the implication is
that severance occurs as a result of muscle
moving against a fixed anchor of body
mass, and the costs of severance for a given
force are then lower for species of greater
body mass, owing to the allometric scaling
of force with body mass (W0.67 [58]; W0.69
[42] using the assumption that the force
generated by muscle is proportional to
muscular cross-sectional area [14]). Leaf
tensile strength has been found to be of
greater importance in determining plant ac-
ceptability for sheep than for cattle [54], a
finding that more likely reflects the con-
straints imposed on the smaller body mass
and thus smaller potential muscular effort,
rather than the suggested shorter retention
time and lower digestive ability of small ru-
minants [54]. An intra-specific allometric
relationship between body mass and graz-
ing depth (M–0.15) has been reported [31,
42], although the relationship was only
present on the tall swards in the study by
Gordon et al. [31]. By contrast Canigano
et al. [15] did not find evidence for an intra-
specific relationship between body mass
and grazing depth in cattle, despite a wide
contrast in body mass (256–608 kg). Fur-
thermore, there has been consistency in bite
depth for inter-species variation in body
mass; cattle vs. sheep [55], sheep vs.
guanacos (Lama guanicoe) [6]. Given these
inconsistencies in the literature on intra-
and inter-specific species depth of penetra-
tion responses we are left wondering about
the real costs involved in grazing [42]. It
might then be helpful to begin by thinking
of the act of severing plant material as a
two-step process; (i) ‘head’ resistance,
which is the force required to accelerate the
mass of the head in a steady momentum and
(ii) ‘herbage’ resistance, the strength and
architectural arrangement of the plant or-
gans in 3D-space, with the summation of
these two resistances shaping the biting ef-
fort ([53], J. Hodgson personal communi-
cation). This provides a clear distinction
between biting effort and biting force.
Further, the laws of motion state that for
a given force, the rate of acceleration will
be greater for a small object than for a large
object. Chambers et al. [16] reported the
rate of head acceleration as some 65%
greater for sheep than for cattle grazing the
same sward. There is little quantification of
the effort and associated costs incurred in
upholding the tension in the muscles of the
neck to maintain the head momentum, al-
though Illius et al. [42] comment that it
must be considerable. The contribution of
the ‘head’ resistance to maintain a cyclic
momentum for the applied effort can be
predicted to be of some significance. This is
despite the relatively small energy cost as-
sociated with bite severance as a result of
the small displacement, although the dis-
placement will increase with increasing
number, and height, of tillers captured
within the bite. If tiller length is viewed as a
moment arm, the distance and angle per-
pendicular to the tiller, from the tiller’s
rooted position to that at severance will in-
crease with sward height and/or tensile
strength, implying that displacement and
acceleration are important components of
biting effort. In support, Chambers et al.
[16] found that the rate of head acceleration
of sheep decreased with increasing sward
height. However, these authors did not ob-
serve a similar pattern for cattle.
The allometric relationship between
force and body mass would provide the
generality that researchers seek, but as biol-
ogists and ecologists we need to recognise
156 W.M. Griffiths, I.J. Gordon
the existence of many exceptions. In the
only known evaluation of biting force
across species body mass, Hughes [39]
showed that goats (23.5 kg W) did not fully
utilise their body mass (W0.37, estimated
from Tab. 5.12 and text from p. 82 [39]) to
sever bites from 15 cm perennial ryegrass
swards, with bite depth substantially
smaller than that recorded for sheep (64 kg W)
(W0.64, estimated from Tab. 5.12 and text
from p. 82 [39]). Other studies have also ob-
served goats to exhibit a shallow penetra-
tion depth on vegetative swards [26],
suggesting that goats may not exploit the
force stored in their muscles for
prehension. This suggests that constraints
imposed by mandibular length may be a
further critical parameter that needs to be
corrected for in assessing biting effort.
There is ample evidence that incisor
breadth scales with body mass [e.g. 29, 31],
and that total masseter weight, which re-
flects masseter tissue size, is correlated
with body mass [4]. However, whilst man-
dibular length does scale with body mass,
there appears to be no compensation be-
tween mandibular length and masseter
muscle mass in ruminants, unlike in some
carnivores [44]. By inference a lack of cor-
relation between mandibular length and
masseter muscle mass implies a weaker
gripping force at the incisors (see also [64])
leading to increased tiller slippage during
initial clamping of herbage as well as dur-
ing the jerking motion of the head. This im-
plies that, irrespective of body mass,
animals with longer mandibles are likely to
incur substantially reduced bite masses for
the applied bite effort with increasing
canopy depth. Placing this into perspec-
tive, goats have a higher mandibular
length:body mass ratio than sheep (F.J.
Pérez-Barbería and I.J. Gordon, unpub-
lished data), and this may account for the
observed responses by goats in the study by
Hughes [39]. These additional animal-
based constraints strengthen the argument
that it is biting effort rather than biting force
that needs to be evaluated, and therefore
providing a ‘real’ measure of the con-
straints in handling forages rather than just
a measure of the force required to fracture a
given plant organ.
8. CONCLUSION
Given the importance of bite depth as a
contributor to bite volume and intake rate,
there remains considerable scope for un-
derstanding the mechanistic basis for bite
depth regulation. Increasing evidence
points towards responses in bite depth to
the vertical positioning, and maturation, of
the morphological organs within the sward
canopy. Assessment of biting effort would
represent a more holistic approach to un-
derstanding the animal’s response to sward
structural complexity, and might explain
why the adjustments in bite geometry have
been of a smaller magnitude than the
change in herbage resistance. More explicit
arguments have been hampered by the lim-
ited available bite force data, much of
which has been collected from swards ex-
hibiting relatively limited variation in
structural strength, and from comparisons
across plant species where other physical
and chemical characteristics may also vary
[40, 42, 46, 68]. Despite the obvious tech-
nological difficulties in quantifying the var-
ious components of biting effort that have
been described in this paper, progress on
this front will remain essential to aid the de-
velopment of predictive foraging models.
ACKNOWLEDGMENTS
We thank two anonymous referees for
comments on the manuscript. This contribu-
tion was funded by a Foundation for Research
Science and Technology New Zealand, Grant
no: MLUR001 to WMG, and funding from the
Macaulay Development Trust and the Scottish
Executive Environment and Rural Affairs De-
partment.
Sward structure and biting effort 157
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160 W.M. Griffiths, I.J. Gordon
Review article
Spatial heterogeneity and grazing processes
Anthony J. PARSONSa*, Bertrand DUMONTb
aAgResearch Grasslands, Private Bag 11008, Palmerston North, New ZealandbINRA, Unité de Recherches sur les Herbivores, Theix, France
(Received 19 September 2002; accepted 25 February 2003)
Abstract — Large-scale spatial patterns, whether in the height, density, or species composition of
vegetation, are one of the most demonstrable and widely recognised features of heterogeneity in large
herbivore grazing systems. But to understand how their existence relates to grazing processes, and
what the implications of the patterns are for plants, animals, and for land users, requires adding spatial
concepts, and dynamics to our knowledge of the interactions between plants and animals. Neither ap-
proach has been traditional in agricultural research. In this paper, we provide an overview of what we
propose are some of the key topics and questions that arise in attempts to understand spatial aspects of
the interaction between plant growth (food resources) and animals’behaviour. Rather than review ad-
vances in any one area in detail, we look at some basic principles of the fundamentally different ways
in which animals eating from vegetation (with or without selectivity) affect the components of plant
regrowth; the variance about these; the way this ‘seeds’ the creation and maintenance of heterogene-
ity, and most important the outcome (intake) for the animals. Likewise we outline some basic features
of animals’ behaviour, given heterogeneous and so spatially distributed food, which includes the ex-
pected rates of encounter; learning and memory; and both the benefits and costs of social interactions
when foraging as a group. In this way we combine knowledge from several disciplines (plant physiol-
ogy; animal science; behavioural ecology and not least from practical agriculture) with a goal of pro-
viding a basis for the development of simple pragmatic means for manipulating a grazed but multi-
purpose landscape to balance diversity, heterogeneity and agricultural performance.
cognitive abilities / foraging costs / optimal grazing / rate of encounter / social behaviour
Résumé — Pâturage et hétérogénéité spatiale. Les motifs d’hétérogénéité à large échelle, en terme
de variabilité de hauteur, de densité ou de composition botanique du couvert, sont l’un des aspects les
plus reconnus de l’hétérogénéité spatiale dans les systèmes pâturés. Afin de comprendre en quoi ils
résultent du processus de pâturage, et ce qu’ils induisent pour l’évolution des couverts, les perfor-
mances animales et les décisions des gestionnaires, il est indispensable de prendre en compte la com-
posante spatiale des dynamiques de végétation et du comportement animal, ce qui représente en soi
une approche innovante. Dans cet article, nous donnons une vue d’ensemble de ce que nous pensons
161
Anim. Res. 52 (2003) 161–179
INRA, EDP Sciences, 2003
DOI: 10.1051/animres:2003013
* Correspondence and reprints
E-mail: [email protected]
être les éléments clés des interactions spatiales entre les herbivores et les couverts pâturés. Nous dé-
clinons comment différents modes de prélèvement de la végétation (sélectifs ou non) affectent la
croissance des repousses, leur variabilité spatiale, les motifs d’hétérogénéité à large échelle, et les
performances des animaux qui exploitent ces couverts. Ce faisant, nous soulignons les processus mis
en jeu lorsque des herbivores exploitent l’hétérogénéité spatiale des couverts, en particulier le rôle
des probabilités de rencontre avec les items alimentaires préférés, les mécanismes comportementaux
d’apprentissage et de mémorisation, ainsi que les coûts et les bénéfices de la sociabilité sur les choix
individuels. Ceci nous amène à faire appel à des compétences disciplinaires variées, relevant de l’éco-
physiologie végétale, de la nutrition et du comportement animal, et de l’écologie comportementale,
ainsi qu’à des compétences appliquées en agronomie et élevage, afin de proposer des règles de ges-
tion des couverts prairiaux dans un contexte de multifonctionnalité de leurs usages.
aptitudes cognitives / comportement social / coût de sélection / pâturage optimal / probabilité de
rencontre
1. INTRODUCTION
There are numerous sources of hetero-
geneity in vegetation, to the extent it is
probably more difficult to explain how veg-
etation can ever be homogeneous, than it is
to accept its spatial complexity [27]. There
may, for example, be an intrinsic heteroge-
neity in the soil or other resources and this
may or may not interact with the distribu-
tion and propagation of plant species, and
the re-distribution of resources by animals
[32]. Each of these topics deserves ongoing
review. But what we address here are some
specific features of the creation and mainte-
nance of heterogeneity – those induced by
decisions made by herbivores about where
and when to place their bites.
Even within these confines, a study of
grazing is unavoidably a study of a complex
system. It is spatially heterogeneous as ani-
mals both create, and respond to, variations
in vegetation state. Most important, it is a
dynamic system, as defoliation impacts on
the rate of replacement of the vegetation. At
least one of the major processes, biting, is
discrete (rather than continuous) and sto-
chastic (as there is uncertainty as to where
and when animals may place their bites)
[44]. There are numerous non-linearities in
the biological responses. It is recognized
that such features generate spatial and tem-
poral complexity at a number of scales, and
that such a system would be expected to ex-
hibit a potentially bewildering array of phe-
nomena, even without the vagaries of
animal behaviour [33]. In physical sci-
ences, one approach to understanding such
a system would be to develop a body of the-
ory – a framework – for how we would
expect the system to behave under a suc-
cession of carefully defined circumstances,
against which we could overlay the poten-
tially complex phenomena observed in
experiments and in practice, in which nu-
merous factors may interact, and so allude
to interpretations of how these phenomena
arise. This is what we attempt here. In all
cases we work with grazing seen as a spatial
and dynamic system, but we start with some
conceptually simple examples and system-
atically add in factors, notably those for
which information from controlled experi-
ments is available.
Complex phenomena can arise in part
from simple rules operating locally and at a
fine scale. We look first at what is known
about the processes operating at the fine
(bite) scale and consider how far we can go
in explaining the origin of phenomena at
larger scales, without at this stage evoking
any larger scale behaviours.
162 A.J. Parsons, B. Dumont
Next, we review evidence for larger
scale (e.g. social, flock/herd) foraging be-
haviours, and then discuss how these may
add three major aspects to the overall un-
derstanding. First we consider information
gathering (sensory knowledge and spatial
memory) and discuss its adaptive value ac-
cording to environment complexity. Sec-
ond we consider social behaviours and how
these may both help and hinder foraging
success in individuals. Here we explore the
probability that the very ‘rules’for foraging
(notably preference) which are the driving
processes for the fine patch scale impacts,
may change at different scales as animals
are seen to respond to the allocation of
space, and/or their proximity to group
members. Third, we consider the way ani-
mals moving around the resources as an ag-
gregated group, might alter their success in
approaching the maximum marginal value
for the rate of supply of resources by modi-
fying where and when they distribute their
defoliations. We parallel this with accounts
derived from different rotational grazing
scenarios in agriculture.
While we recognise the continuum of
these impacts across the scales, we proceed
systematically in an attempt to unravel the
complexity of the phenomena that emerge
in grazing systems. Our aim is to focus at-
tention on those aspects of heterogeneity
that might be manipulated or controlled
with a view to increasing the sustainability
of grasslands for alternative goals.
2. HOW FAR CAN FINE SCALE
INTERACTIONS EXPLAIN
THE ORIGIN OF PHENOMENA
AT LARGER SCALES?
2.1. Sequential (deterministic)
vs. random biting
First we use a previously published
model [39, 44] to consider the impact of some
fundamentally different ways in which animals
might place their bites in space and time. In
the first case we consider what would be the
outcome if animals were to take bites in a
strict sequence such that no bite sized
‘patch’ was revisited before all other
patches had been eaten from. Note this
would give rise to the situation where ani-
mals were at all times eating from the next
largest patch in the vegetation. We contrast
this with the case where we imagine ani-
mals may take bites totally at random. In all
cases, we perform a full mechanistic analy-
sis of the constraints to searching for and
handling food [37, 46], such that the state of
each vegetation patch determines bite
mass, and the animals face the time costs of
prehending and masticating each bite,
which in turn affects the rate at which ani-
mals progress through the array of patches.
But in these first ‘simplest’ cases, we can
consider foraging with the minimal in-
volvement of any costs of searching, as if
the next bite were adjacent to the last.
The outcome of even these simple forag-
ing examples (Fig. 1a) is revealing, as it
emphasises the importance of the dynamics
of vegetation (resource replacement) and
the impact of foraging on the components
of this. At low stocking rates, intake would
be seen to be unaffected by grazing method,
as intake is not constrained by vegetation
state and each animal eats its ‘fill’. But at
high stocking rates, animals (each and all)
would appear to do better grazing spatially
and temporally at random. The explanation
is that stochasticity gives the vegetation a
chance. Where the animals graze patches in
strict sequence, each patch suffers the same
defoliation (which becomes severe at high
stocking rates as animals progressively re-
duce the overall vegetation state), and each
patch is defoliated at the same (frequent)
deterministic interval [38]. There is spatial
heterogeneity in vegetation state, simply
because animals can only bite from a small
proportion of the total available patches in
any one day, but there is no variance about
the determinants of regrowth – the residual
Spatial heterogeneity and grazing processes 163
patch state or regrowth duration. Even
though animals would always be eating the
next largest patch in the sward, a situation
some have proposed as being optimal for
intake [51], intake is low as there is little
vegetation, so patches and bites are small.
By contrast, under random grazing, some
patches would escape grazing by sheer
chance (there is now not only spatial heter-
ogeneity but also variance in residual patch
states and in regrowth duration). This gives
the opportunity for more growth in those
patches. Intake is greater purely because
the system comes to equilibrium with a
greater mean vegetation state (and so bites
are larger).
Both these simple systems generate spa-
tial heterogeneity in the sense that there
would be a frequency distribution of patch
states at the fine (bite) scale [38]. Spatially
explicit accounts of these methods for plac-
ing bites in space and time reveal that larger
scale patterns can arise purely by chance
under even spatially random grazing,
whether it is portrayed as a Poisson process
or if the animals are constrained to walking
a random path. Such larger scale patterns
are only transient however. But as we shall
see later, these can become the focus for
subsequent larger scale animal behaviours,
and so could contribute to sustained vegeta-
tion patterns.
2.2. Adding preference at the fine scale
We now add to this framework what
would be the effects of grazing with prefer-
ence. Here we still consider the case where
animals might encounter potential bites
spatially and temporally at random, but
now make local, state-dependent decisions
whether to eat from the bite sized patches
they encounter. There are numerous criteria
by which animals might prefer one vegeta-
tion patch over another, but here we focus
on size (density, mass or height). This high-
lights how, although preference is simple to
conceive in a static system, it is more difficult
164 A.J. Parsons, B. Dumont
cons
umpt
ion
(kg/
ha/d
)
0
10
20
30
40
50
60
70
2 4 6 8 10 12 140
stocking rate
cons
umpt
ion
(kg/
ha/d
)
0
10
20
30
40
50
60
70
2 4 6 8 10 12 140 2 4 6 8 10 12 140 2 4 6 8 10 12 140
stocking rate
2 4 6 8 10 12 140 2 4 6 8 10 12 140
(a) (b)
optimal solution
Figure 1. The effect of some fundamentally contrasting ways of placing bites in space and time on
the yield (intake per ha) of the grazed system across a wide range of stocking rates. In (a) bites were
grazed at random (solid line); in strict sequence (dashed line), or encountered at random but grazed
preferentially with an 80% or 95% (lower line) partial rejection of tall patches (dotted lines). In (b)
animals grazed as an enforced group (a 30 day regrowth: 1 day grazing rotation) which suppressed
preference at high stocking rates (solid line), as compared with continuous grazing (dotted line).
According to [44].
to conceive dynamically. We have seen how
grazing animals create a frequency distri-
bution of patch states. All patches in this
size-structured population will endeavour
to regrow (move to the right in Fig. 2a). But
preference rules filter this flow. Patches that
are eaten will in effect be ‘thrown back’
down the size structure, to contribute to the
small categories of the frequency distribu-
tion (Fig. 2b). Of the many simple state-
based preference rules we tested [38], one
in particular was seen to have a very delete-
rious impact – a partial rejection of ‘tall’
(relative preference for short). It was shown
[44] with a simple dynamic model of this
mechanism, that where there is a high prob-
ability of tall patches being eaten, a skewed
but unimodal frequency distribution of
patch states results (Fig. 2c). However,
where there is a low probability of tall
patches being eaten (a stronger stochastic
rejection of tall) a bimodal frequency distri-
bution of patch states emerges (Fig. 2d).
This form of patch selection can lead dy-
namically to considerable reductions in in-
take, and so foraging success (dotted lines
Fig. 1a). When animals partially reject tall,
the mean state of the vegetation (even at
high stocking rates) is larger, but intake by
animals is reduced as they eat preferentially
from the population of smaller patches. In-
take is therefore reduced even at low stock-
ing rates, where it would otherwise not have
been constrained by vegetation. Bi-modal
frequency distributions have been widely
reported in field experiments [23].
Spatial heterogeneity and grazing processes 165
increasing patch size (height)
(d) low probability of defoliation of tall patches
increasing patch size (height)
(c) high probability of defoliation of tall patches
increasing patch size (height) increasing patch size (height)
(b) but preference ‘rules’ filter this flow(a) all patches attempt to grow
Figure 2. Diagram to convey the impact in a dynamic context of stochastic preference ‘rules’(here a
partial rejection of tall) on the frequency distribution of patch states, and the possibility of the emer-
gence of sustained markedly bi-modal distributions that could ‘seed’larger scale patterns in heteroge-
neity. According to [38], using the same spatial model [44] as in Figure 1.
A bimodal frequency distribution of bite
scale patch states will clearly be a powerful
force to ‘seed’ spatial patterns at larger
scales should there be other state-depend-
ent processes that cause the subsets (e.g. tall
and short) of the frequency distribution to
become aggregated in space [5, 32].
2.3. Moving up a scale: adding foraging
(search) costs
So far, we have considered the dynamic
consequences of how animals place their
bites in space and time, without considering
the additional time costs of searching (to be
precise, where search costs are less than
handling costs and these are deemed to
overlap, so there are no additional search
costs for foraging) [37, 44].
Grazing selectively can, however, sub-
stantially increase the costs of foraging ([48]
and Fig. 3). Costs increase as animals pass
by less desirable items (‘lost opportunity’),
in effect travelling further per unit preferred
food. Grazing selectively is shown in Fig-
ure 3 to increase foraging costs in two ways.
First, costs increase substantially with the
degree of selectivity, and second, costs in-
crease substantially if the preferred food is
less abundant in the vegetation. Both are in-
tuitive, though the scale of the increase is
perhaps surprising. Grazing selectively
may clearly create spatial heterogeneity,
both at a fine scale and as a larger scale pat-
tern, but it is important to consider next how
the potential size of foraging costs might
limit animals desire to graze selectively in
the first place.
We can consider the expected feedback
of search costs on animals desire to forage
selectively by modelling the optimal solu-
tions for trading off the benefits of eating a
given diet component, against the costs of
selecting for it, under different circum-
stances (for details see [48]). Optimising
the cost-benefits of foraging, and a desire
166 A.J. Parsons, B. Dumont
Rel
ativ
ein
crea
sein
spec
ific
cost
s
Grass acceptance coeff., Clover acceptance coeff.,
Clover preference coefficient,
Grass rejected Clover rejected
10
5
0
10
5
0
10:90
20:80
50:50
100:0
90:10
80:20
50:50
0:100
0 0.5 1
0.5
0
10 5 2 1 0.8
0.5
0.2 0
�c : g
ac = 1 ag = 1
ag ac
ac / ag
c : g� � �
Figure 3. The calculated relative increase in specific foraging costs (i.e. per unit mass eaten) in a
2 species mixture as affected by the acceptance coefficients (ac, ag) and the relative abundance (λc: λg)
of the two species (assumed here to be clover and grass). From [48].
for a mixed diet [36, 41] predict complex
selective foraging phenomena. Figure 4a
describes how the optimal proportion of
preferred food in the diet should vary with
the proportion (abundance by cover) of the
preferred food in the vegetation. The model
suggests that, if the searching costs are neg-
ligible, the animal would be expected to ex-
tract always its preferred diet (in this case
presumed to be 70% of the preferred food).
If search costs were very high, the animal
would be expected to eat whatever was in
front of it. With intermediate costs, seem-
ingly complex behaviours would be antici-
pated, with animals sustaining their
preferred diet while the composition of the
vegetation is close to that mixture, but in sit-
uations where the abundance of the pre-
ferred food in the vegetation is lower,
animals would be expected to progressively
forego preference. In some cases, e.g. when
the cost structure is very high, then at low
abundance of preferred food, animals
should resort again to eating whatever was
in front of them. Experimental studies of
the effects of the relative abundance of al-
ternative foods, on selectivity, confirm
these predictions in grassland [17].
3. INFORMATION GATHERING:
ANIMAL RESPONSES
TO POTENTIALLY PROHIBITIVE
COSTS
Foraging (search) costs are modified by
the way food is distributed (dispersed or ag-
gregated) and the extent to which animals
are able to exploit this opportunity spa-
tially. It is well established that animals (in-
cluding domestic herbivores) can use
sensory cues (sight or smell) to detect food
items at a distance; can form flexible, even
abstract, associations between food appear-
ance and its value [6, 19] and so learn, and
use spatial memory [15, 18] to aid foraging.
This, clearly and intuitively, can help them
reduce foraging costs, though it is not a
simple task to analyse to what extent, and
under what circumstances, the benefits pre-
vail.
3.1. ‘Theory’ for how spatial
distribution per se affects rate
of encounter
We can argue from the basis of probabil-
ities alone that, if the distribution of pre-
ferred food is approaching random at a fine
scale (or the distribution is for any reason
cryptic), then for any level of abundance,
the potential search costs for grazing selec-
tively would be greatest. There would be
little animals could do other than to re-
spond, as in the examples above, by making
very local decisions, trading off the benefits
of being selective against the potentially
high costs.
However, food may be distributed in
patches (aggregated). To consider how this
would intrinsically affect animals’expecta-
tion of finding the preferred food, we can
start by imagining a situation where the
same amount of food is distributed in one
case in a large number of small patches,
whereas in a second case, it is distributed in
a small number of correspondingly larger
ones. Let us assume the density of food
within the patches is the same and that there
is therefore the same abundance (by cover)
in the area to be searched. We can consider
what problems the animals face, and their
expected encounter with preferred food,
from the well-established theory behind
vegetation sampling techniques [29].
Totally random point sampling would
clearly give an identical level of success in
finding preferred food in both cases. But
this is not the way ground-based animals
can sample as they are constrained to walk-
ing a path. If animals were to sample only
locally along a path (e.g. as with random
line transects, or a random walk), then
when food is distributed patchily, the ex-
pected rate of encounter with the patches is
far greater where there are more smaller
patches than with fewer larger ones. However,
Spatial heterogeneity and grazing processes 167
this would be compensated for in that more
food is found in each larger patch and so the
expected rate of encounter with preferred
food (as opposed to with patches) could be
the same (though patch shape has some im-
pact). There would however be greater vari-
ance about the rate of encounter with food
when it is in fewer larger patches, with lon-
ger periods with no preferred food followed
by longer periods with preferred food.
If animals were to search along a path
but with a wider field of view, and were
drawn toward any preferred food item
within that, they would be sampling in ef-
fect, as if using contiguous ‘quadrats’ and
their success would relate more to the ‘fre-
quency’ and not the ‘cover’ of preferred
items [29]. This sampling approach implies
that for any given level of abundance (by
cover), the probability of encountering a
patch will depend on the size of the field of
view relative to the ‘grain’ of the pattern of
aggregation. There would be an optimal
size field of view (cf. ‘quadrat’ size) which
maximizes the rate of encounter with
patches for each level of aggregation [29].
The probability of encountering patches
would be far greater (in some cases ap-
proaching certainty) where the same
amount of food is distributed in many small
patches.
3.2. Learning and spatial memory
Where the distribution of food items is
not detectable at a distance (e.g. when no
visual or olfactory cues are available for lo-
cating them), learning and spatial memory
become potentially more valuable. To study
the use of learning and spatial memory by
herbivores, and so the impact on animals of
aggregated patterns of food distribution,
experiments and models have been used in
which preferred food is for example offered
168 A.J. Parsons, B. Dumont
prop
ortio
nin
diet
0
0.2
0.4
0.6
0.8
1
0.2
proportion on offer
0
00.2 0.4 0.6 0.8 10.40.6 0.8 1
(a) (b)
low
medium
preferred diet
v.high
t
Figure 4. (a) The complex effects of partial preference, and of low, medium, and high (specific) for-
aging costs on the proportion of preferred food in the diet, in relation to its abundance in the vegeta-
tion, as predicted by a model that seeks the optimal trade-off between the benefits and costs of
foraging selectively [48]. (b) Data from a range of sources show the effect of aggregated (solid sym-
bol) and dispersed (open symbol) spatial distributions of food are consistent with differences in for-
aging costs [17]. It is assumed that the preferred diet is a mixture in (a) of 70% and in (b) of 76% of the
preferred species.
in bowls in an arena [18] or hidden within a
pasture [15 ], or herbage species are planted
in patches mown to look like surrounding
vegetation [16]. The layout of one such ex-
periment is shown in Figure 5a. When naïve
animals are released into this arena, the re-
sults show a marked increase over time in
the success of the animals in finding the
preferred (pellet) food (Fig. 5b), typically
demonstrating the capacity for learning and
spatial memory, as the animals subse-
quently move more directly to and between
the aggregated preferred areas [15]. It is no-
table animals did better, both initially, and
even after learning, when the area to be
exploited was smaller (as in this design, the
overall density of the preferred food was si-
multaneously greater).
Independently manipulating the many
aspects of the complexity of the environ-
ment in which animals forage, in experi-
ments, would be prohibitively exhaustive.
But following this experiment, Dumont and
Hill [14] constructed an individual-based
model to explore the adaptive value of spa-
tial memory in relation to environmental
complexity (e.g. plot size, and consequent
overall density of the preferred food) using
experimental data to calibrate the parameters
of sheep searching behaviour. Comparison of
Spatial heterogeneity and grazing processes 169
0
20
40
60
80
100
M-1
00%
M-8
0%
M-6
0%
M-4
0%
M-2
0%M
odel
M+2
0%
M+4
0%
M+6
0%
M+8
0%
M+1
00%
Nb
bow
lsvi
site
dby
each
ewe
in30
'on
day
12
40 x 40m
80 x 80m
120 x 120m
160 x 160m
200 x 200m
240 x 240m
0
10
20
30
40
50
60
70
80
90
1 2 3 4 5 6 7 8 9 10 11 12
Day
Nb.
bow
lsvi
site
dby
each
ewe
in30
'
80 x 80 m
160 x 160 m
large plot small plot
80m
(a) (b)
(c)
Figure 5. (a) Layout of experimental plots with individual bowls shown as dots [15], (b) the increase
in the number of bowls visited by each ewe in 30 min as animals learn the location of bowls, shown
for different plot sizes [15], (c) simulation of the number of bowls visited by each ewe in 30 min after
12 tests according to the animals’memory capacity and plot size [14]. Model outputs were similar to
that of the ewes in (b) (‘Model’), and the predicted effects of increasing (or decreasing) memory size
and memory persistence by 20%, 40%, 60%, 80% and 100% are shown.
the real system behaviour and of model pre-
dictions was successful for both the visual
features of animal movement paths and for
the main model outputs, i.e. the simulated
data were within the 95% confidence inter-
val of real data. Some examples are shown
in Figure 5c, which portrays the effects of
manipulating the memory capacity of the
animals (reducing or increasing by 20%,
40%, 60%, 80% and 100% the memory size
and memory persistence parameters in the
model) within a range of plot sizes.
This confirms, first, that when the area to
be searched is small, animals should be
more successful (both initially and after
several days learning) in finding the pre-
ferred food, but adds that variations in
memory capacity will have relatively small
effect (the number of bowls visited in
30 minutes, after several days learning, dif-
fered little with major changes in memory
capacity). Second, the benefits of spatial
memory were greatest in intermediate-
sized plots, foraging success increasing by
22–25 bowls with memory capacity. In the
largest plot size considered, increasing
memory capacity had less effect (only
11 extra bowls found) suggesting there is an
upper limit to the benefits of using spatial
memory in herbivores.
3.3. Area-concentrated searching
within patches
Whatever means animals use to increase
their chances of finding a food patch, or
even if they encounter one by pure chance,
it is recognized that animals can concen-
trate foraging within a preferred food patch,
once any part of that patch has been found.
This is achieved by increasing the rate of
turning, to remain within the locality [16,
50, 53]. It can be shown easily (e.g. by tak-
ing simple transects across patches drawn
on graph paper), that area-concentrated for-
aging should increase foraging success
many-fold, compared to where the foraging
path within a patch is not altered. More
elegantly, Benhamou [8] determined the
theoretical efficiency of area-concentrated
searching using computer simulation. The
model simulated searching with high sinu-
osity and low speed within high resource
density areas, but low sinuosity and high
speed between these areas. Tested in habi-
tats having the same mean overall density,
the efficiency of this movement control was
higher in coarse-grained (a few large
patches) than in fine-grained habitats (more
smaller patches) and increased also with
intra-patch resource density. Depending on
the habitat, an animal exhibiting optimal
spatial memory-based area-concentrated
searching behaviour was able to harvest
three to five times more food items than if it
did not exhibit any area-concentrated
searching behaviour but moved in a straight
line with an optimal constant speed [9].
3.4. How well do animals exploit
these abilities?
We can now return to the issue of hetero-
geneity and the prospects offered by these
sensory behaviours to reduce foraging
costs. Data from a range of studies, in
which food was distributed in different
ways, and at different abundances, are plot-
ted together in Figure 4b, which shows ani-
mals (large herbivores grazing a range of
vegetations) are more successful in select-
ing preferred food where it is more aggre-
gated [17]. Relating this to the theoretical
responses to different overall costs of forag-
ing (Fig. 4a), the data suggest this is consis-
tent with the aggregated food leading to
lower foraging costs. But the benefits of
foraging in patchy environments seen in
such studies are not always as great, per-
haps, as would be expected. In this context,
we feel it would be of value if more studies
of the foraging success of herbivores in dif-
ferent (patchy) environments, compared
the observed results with some expectation
of success (e.g. the expected encounter
with patches if animals foraged without
170 A.J. Parsons, B. Dumont
knowledge; if they foraged close to ran-
dom; or assessed how the outcome would
be expected to increase from area concen-
trated foraging). Below, we discuss some
possible reasons why, despite proven abili-
ties in learning and spatial memory, ani-
mals may yet, in some cases, exhibit a
foraging success closer to that expected by
random.
Any increase in knowledge about food
distribution offers animals the opportunity
to devise travelling strategies to minimize
the searching time costs of moving between
patches of preferred food. But, even with
total knowledge of the area to be grazed and
of the location of all preferred food patches,
it becomes progressively more difficult to
exploit this knowledge as the number of
these increases. Seeking minimum distance
travel paths between patches poses com-
plex ‘travelling salesman’ problems. De-
tailed analyses of the search paths observed
in experiments are necessary to confirm if
animals are responding to heterogeneity in
an intelligent fashion, or opting to graze
closer to at random.
Another reason for the distribution of
animals eating not matching the distribu-
tion of food at any instant is that in situa-
tions where animals revisit areas of
vegetation frequently, they may instead be
responding more to the spatial patterns in
the rate of replacement of resources. Spa-
tially this alludes to there being an ‘ideal
free distribution’ [22]. Some notable forag-
ing experiments and models test ‘against’
some of the theories for the expected distri-
bution of animals in a dynamic resource en-
vironment [20, 21]. Several of these
emphasise how the expected outcome of
foraging, in a dynamic system, is distinctly
different from that in a static one, and how
foraging may match, or both increase and
decrease, heterogeneity in the vegetation
[1]. But, a third explanation is that social in-
teractions between animals can create moti-
vation conflicts that can reduce (as well as
enhance) foraging success.
4. FORAGING AS A GROUP
AND ITS EFFECTS ON THE
FORAGING OF INDIVIDUALS
Many large herbivore species forage in
groups (flocks or herds), itself a recogni-
tion, in part, of the impacts of aggregating
the distribution of food (themselves, as
prey) on the expectations and foraging
costs of their predators [28]. Herbivores
have been domesticated more to enhance,
rather than remove, the evolved flocking
and associated anti-predatory (e.g. vigi-
lance) behaviours, many being managed
using wolf-like predators. When sheep are
made to graze in only small groups (e.g. be-
low five) grazing time per day decreases
[40] and vigilance postures increase [13].
4.1. Costs and benefits of foraging
within a group
Social behaviours can be both beneficial
and detrimental to individual (and arguably
even group) foraging success. Animals for-
aging within a group benefit from the feed-
ing sites (e.g. preferred patches) discovered
by other members of the group and from
shared vigilance, but they can face the nega-
tive effects of intra-specific competition for
food within the food patches. Even with
perfect knowledge about food distribution,
herbivores always run the risk of returning
to a patch that has been largely depleted by
other animals of the group. Sociability thus
adds uncertainty in animal’s expectations
of patch value and potentially increases for-
aging costs [25]. The way animals would be
expected to optimise the trade-offs between
‘cooperation’ and competition has been
considered for a number of species, using
game theory [34], and social foraging the-
ory has been established around this [24].
Several models have looked at the impact of
these interactions on the expected distribu-
tion of grazing herbivores [7, 14].
Hence, group behaviour can impose mo-
tivation conflicts, as animals from socially
Spatial heterogeneity and grazing processes 171
stable groups are very reluctant to graze
away from their peers. This has been shown
in intensive grasslands. Sheep were al-
lowed to forage in a long narrow grass field
which contained an area of preferred food
(taller patch) at a distance of either 15 or
50 m from where, at the end of the field,
there was a small sealed paddock contain-
ing a group of their social peers [13]. At
15 m, the tendency to eat from the preferred
patch was unaffected whether animals
grazed alone or in small groups. But their
results suggest that a sheep is very reluctant
to graze the preferred patch when it is lo-
cated further away (50 m in their experi-
ment, this critical distance varying with
sheep breed) unless it is accompanied by
several other peers, and even then (in
groups as great as 7) time spent grazing the
preferred patch was depressed.
Dumont and Hill [14] modelled that in
an unfamiliar and complex environment,
where the cost of finding preferred food
items is high, the foraging success of an ani-
mal decreased together with the increase in
conspecific attraction within the group, and
this was for two reasons. First, ewes were
frequently attracted by peers feeding on
previously discovered sites and therefore
missed the opportunity to discover new
feeding sites. Second, animals faced the ef-
fects of feeding competition for a preferred
and rare resource on sites. Their efficiency
(in g of pellets consumed per minute of
searching) therefore decreased with in-
creasing social attraction index, while in
the same time the number of bowls visited
per minute increased.
Conversely, when animals are aware of
food location and when food is not limiting,
social bonds within a group can favour
patch and habitat selection. Boissy and
Dumont [11] observed the behaviour of
ewes in their motivation conflict procedure
with animals being familiar (reared to-
gether from the young age) or non familiar to
them. The ewes with familiar companions
more easily split from the paddock contain-
ing a group of peers to graze the preferred
patch located away, vocalised less and were
less vigilant than those with unfamiliar ani-
mals. Differences in the strength of social
bonds within a flock are thus likely to affect
the formation of subgroups and the way
herbivores forage in patchy grasslands.
Similarly, under more extensive conditions,
cattle from the same herd share the use of a
common home range, which is very similar
to that of their mothers [26].
A third way in which social interactions
may reduce foraging success is that compe-
tition with peers can encourage animals to
leave a current patch prematurely. Like-
wise, a remaining animal may leave a re-
warding patch to follow its group mates. It
is well recognized that herbivores should
leave patches before exploiting all the food
these patches contain (this is a central tenet
of the Marginal Value Theorem [12] dis-
cussed later) and there is a theoretical opti-
mal time to leave a patch, which is modified
by the time spent reaching the patch [47].
Social factors also alter patch residence
times [24]. It has been proposed that, ac-
cording to the departure criterion (intake
rate falling below a threshold value or dura-
tion without finding a food item) and to the
number of foragers that are likely to take
this patch leaving decision (anyone or only
a leader decides), living in a group can be
either beneficial, neutral or detrimental to
individual foraging success in this regard
[42]. If grazing herbivores use a departure
criterion based on an intake rate threshold,
it has been proposed that foraging for
patchily distributed food, as a group, would
cause a reduction in food intake rate com-
pared to as a solitary forager [52]. Any ten-
dency for group foragers to leave rewarding
patches prematurely would readily explain
why the foraging success of herbivores
in patchy environments falls short of
what would be expected if they fully ex-
ploited their abilities in area-concentrated
foraging.
172 A.J. Parsons, B. Dumont
4.2. Scaling issues: preferences may
change with scale due to social
interaction
One problem in interpreting the behav-
iour of animals foraging as a group, as a
means to understanding how animal behav-
iour interacts with the vegetation, is that the
phenomena may be dependent on scale
(Fig. 6). At small scales (relative to natural
range and herd size), animals may be com-
fortable and sense their preferred inter-animal
distances are satisfied, while distributing
themselves even randomly across the entire
vegetation area, with consequently widely
distributed impacts on the vegetation pat-
tern. That is, at small scales, the desire for
grouping may have no different impact on
foraging success and vegetation dynamics
than if animals forage independently. At
larger scales, animals satisfying a desire for
the same inter-animal distances would ap-
pear to be aggregated in their distribution
(Fig. 6a). On a homogeneous sward,
Sibbald et al. [45] measured the effects of
space allowance on the grazing behaviour
and spacing of groups of ten Scottish
Blackface ewes. At space allowance from
50 to 133 m2 per head, there were no signifi-
cant differences between mean observed
inter-animal distances and those expected
by chance (i.e. there was no grouping pat-
tern), but observed values were lower than
expected values at 200 m2 per head. In very
heterogeneous environments, herds [30]
and flocks [4] may split into subgroups, ac-
cording to the size and distribution of vege-
tation patches.
What matters more, for the interaction
of animals and vegetation, is whether the
act of forming a group, or questions of
space allocation, alter the very rules, at the
fine scale, by which animals graze. The fact
that animals might move around an area,
foraging as a group, should not be seen as
synonymous with them having an obvious
Spatial heterogeneity and grazing processes 173
effic
ienc
y:%
pref
erre
dite
ms
eate
n
‘space allocation’ prompting social behaviours
enforced grouping
social grouping
. .
.
... ..
..
..
.
.
.
.
..
..
..
..
enforced grouping
..
.
.social grouping
..
.
.
....
..
..social grouping
(a) (b)
Figure 6. A speculative graph (b) on how fine scale foraging rules might be anticipated to change
with scale by evoking social foraging behaviours. Preference may be constrained when animals
graze as an enforced group (dotted line), or when grazing as a social group (fall-off at large scales), as
shown in (a).
effect on the large scale spatial heterogene-
ity in the vegetation, nor on the fine scale
heterogeneity. If the group of say 5 moves
at random, and revisits areas on a fairly
short time scale (e.g. where stocking rate is
high), it is unlikely their impacts would be
distinguishable from that of 5 individuals
eachmoving at random. The group may act
like a ‘meta-animal’. If the group grazed
with the same fine scale rules as individu-
als, the outcome would be the same, and as
seen in Figure 1.
But fine scale foraging rules might be
anticipated to change with scale as indi-
cated in Figure 6b. Such a graph is, we feel,
an essential component for a foraging
model (either as an input or preferably an
emergent property) that aims to analyse
heterogeneity and its impacts across a range
of scales. But such an analysis is rarely pre-
sented, and is largely speculative here. The
axis of ‘space allocation’ should be seen
perhaps only as a surrogate for the extent to
which various social behaviours are
evoked. We propose that foraging effi-
ciency (the apparent selection of preferred
items) might decline at large spatial scales
as a combination of environmental com-
plexity and the constraints of group forag-
ing limit the foraging success of individuals
(as we have discussed earlier). What we add
is that individuals’ foraging success might
also be expected to decline when animals
are forced into groups at very small spatial
allocations. Consistently, increasing the in-
stantaneous stocking rate from 50 to
150 ewes per ha and per day in an oak cop-
pice where the availability of the preferred
herbaceous layer was low resulted (for a
same overall high stocking rate) in an in-
crease of browse consumption by the ewes
[31]. What is critical here is that not all ani-
mals are equal. Social groups impose con-
straints on subordinate individuals. In
grazing red deer, for example, the subordi-
nates do not have access to preferred
patches [2] are less synchronised with the
dominants [10] and have a lower biting rate
when near the dominants [49]. Similar
hierarchical social relationships may, for
example, be expected to reduce the forag-
ing efficiency of subordinate members of
groups of domestic herbivores at the high
stocking densities in each successive pad-
dock in a rotational grazing system.
5. TO WHAT EXTENT DO ANIMALS
COME CLOSE TO ACHIEVING
THE OPTIMAL SOLUTION?
One final consideration about the conse-
quences of how animals place their bites in
space and time, is to ask to what extent ani-
mals moving as individuals, or as a group,
come close to achieving the optimal solu-
tion for repeatedly harvesting the vegeta-
tion.
5.1. Optimal foraging modelled
at the bite scale
Although the Marginal Value Theorem
[12] elegantly describes the optimal means
to exploit a succession of patches of vegeta-
tion, it is very difficult to conceive and ap-
ply in grazing systems where the vegetation
is spatially more continuous (albeit hetero-
geneous), where grazing and regrowth are
at a field scale simultaneous, and where
patches may be frequently revisited, so that
the rate of replacement of resources be-
comes paramount [3]. However, the opti-
mal solutions can be perceived readily, even
under continuous grazing, again by work-
ing at the fine (bite) scale [35]. Using the
same, previously published models of bite
scale foraging [39, 44], we can recognise
that individual bites are discrete, assumed
instantaneous, events and so generate a
regrowth pattern specific to each and every
bite taken. Just two of numerous possible
examples are shown in Figure 7. The shape
of the regrowth curve, and the amount that
may be harvested subsequently, depends
uniquely on the initial patch state (residual
174 A.J. Parsons, B. Dumont
after the previous bite), and the duration of
regrowth in each case [35]. These are then
two fundamental determinants of the rate of
replacement of resources. For any initial
patch state, (and any ensuing growth curve)
we can identify an optimum timing for har-
vest, which will achieve the maximum av-
erage rate of yield. This (the maximal
marginal value) is shown as the tangents
from Wi to the growth curves in Figure 7. In
Figure 8 (solid lines) we plot the optimal
solutions for all possible initial (residual)
patch states (x axis), in terms of the optimal
defoliation interval that is required and the
maximum sustainable yield that each com-
bination of residual patch states, and defoli-
ation intervals would achieve (for full
details see [35, 39]).
To understand the impact of the funda-
mentally different ways in which animals
may place their bites in space and time, we
can now translate the contrasting animal
foraging behaviours into the components of
regrowth (the residual patch states and de-
foliation intervals) that these would gives
rise to (the emergent properties), and we
can relate these to what would be the opti-
mal solutions. Most important, we consider
not just the mean values but the variance
about these because achieving the optimal
solutions would require that all patches are
defoliated identically – a deterministic so-
lution which is achievable only by uniform
cutting [38].
5.2. Model outputs in the different
grazing scenarios
The modelling predicts that grazing se-
quentially or at random, whether as individ-
uals or a group, would lead to combinations
of residual patch states and defoliation in-
tervals that are clearly suboptimal (Fig. 8a).
At low stocking rates, patches are grazed
too leniently, and defoliation intervals are
too long to approach optimal regrowth
Spatial heterogeneity and grazing processes 175
optimal defoliation interval time
biom
ass
-W
(kg/
ha)
max marginal value
Wi
Wmax
Figure 7. The theoretical basis for seeking optimal solutions for a sustainable harvesting of a hetero-
geneous and regrowing resource is simple only at a bite-sized patch scale where defoliation is instan-
taneous. Unique regrowth curves (only two shown here, one from a low residual state, one from a
greater residual state) depend on the initial state of each patch, Wi , and there is an optimal time of har-
vest for that patch [35]. At even greater residual patch states, regrowth is monotonic, implying the
patch should be regrazed immediately. Foraging rules affect both these components and generate
unique growth curves, but with simple to derive optimal solutions.
rates. At higher stocking rates, although re-
sidual patch states decline, so too do defoli-
ation intervals. The sustainable yields fall
short of the optimum possible, not only be-
cause the combinations of the components
of regrowth are inappropriate, but also be-
cause under random grazing, there is vari-
ance about these components. Note that in
the examples so far, the animals are at all
times free to move around the whole area at
will, motivated by attempting to meet in-
take demand.
Next, we consider the case where ani-
mals move around the area as a group, but
where their rate of movement is regulated
(e.g. by management with subdivision or
fencing). In this way we impishly relate the
expectations for social foraging behaviour
to what is more widely observed in agricul-
ture – rotational grazing. Grazing as a rota-
tion, the models propose, comes considerably
closer to the optimal solutions for exploiting
resource replacement (Fig. 8b). This is be-
cause constraining the movement of the
animals allows control over at least one of
the two major components of regrowth. This
means that it is now possible, e.g. at high
stocking rates, to combine low residual
176 A.J. Parsons, B. Dumont
20
40
60
0
20
30
40
50
60
70
80
residual(initial) patch state (m)
increase instock rate
increase instock rate
sequentialrandom
20
40
60
0
10
20
30
40
50
60
70
80
residual(initial) patch state (m)
increase instock rate
increase instock rate
(a) (b)op
timal
def
.int
erva
l (d)
0 0.05 0.1 0.15 0.2 0.25
10
0 0.05 0.1 0.15 0.2 0.25
0 0max
.sus
tain
able
yie
ld (
kg h
a d)
Figure 8. The effect of residual patch state on the maximum sustainable yield that may be achieved
and the defoliation interval required to achieve this (solid lines) as predicted by a model that seeks op-
timal solution for all combination of residual patch state and the timing of harvest. In (a) we show the
combinations of residual patch state and defoliation intervals that emerge (separate point for each of a
range of stocking rates) when animals are assumed to graze patches either at random (solid dots), or
in strict sequence (open circles) and in (b) the same for rotational grazing (open symbols, 30 days
with animals not present: 1 day grazing) compared to continuous grazing (solid symbols), all as in
Figure 1. Arrows show the direction of increasing stocking rate. According to [35].
patch states (severe defoliation) with long
intervals between defoliation. Note, many
defoliation intervals in a rotation are less
than one day. What matters more to plant
regrowth, however, is there is one interval
(e.g. here 30 days) that has been imposed,
which allows close to optimal resource re-
placement.
Finally, we combine all the impacts,
some probable social changes in foraging
rules with scale, and the concepts of ex-
ploiting the rate of replacement of re-
sources, in a dynamic context, using the
same models, in Figure 1b. Where animals
graze as an enforced group, and where so-
cial behaviours modify their capability to
graze selectively (e.g. at high stock densi-
ties in a rotation, selectivity is depressed in
some if not all animals), foraging success
per ha (and clearly per animal) is greatest
and close to the maximum sustainable. The
model runs, here, clearly demonstrate there
is an optimal time to leave a patch (this is a
simple extension of the MVT which in-
cludes resource replacement). However an
animal moving through the vegetation in-
tent on meeting its daily demand for intake,
may fail to realise the maximum sustain-
able rate of yield. In this analysis, each and
every animal would do better, in the longer
term, to constrain its movements to opti-
mise resource replacement. Presumably in-
dividual animals do not do this for fear their
longer-term vision would be exploited by
those who are more opportunists [24].
Clearly animals are not motivated by feed-
ing alone and the social interactions neces-
sary to ensure fitness and survival of
individuals might mitigate against achiev-
ing the optimal solution for the whole
group.
6. CONCLUSION
Although one of the most notable fea-
tures of heterogeneity is what we regard (as
humans) as large scale pattern, the challenge
for us is to understand how such pattern
could arise in the first place, and in any
case, what heterogeneity means to foraging
success and vegetation dynamics. The most
satisfying explanations, we propose, are
those that can generate pattern from an ini-
tially homogeneous state. The grazing pro-
cesses described here will achieve this,
though some spatially localising behav-
iours are necessary to aggregate the (e.g.
tall or short, or species) components of the
frequency distributions into large patches
in space. As a final note, we cannot overem-
phasise how many sources of heterogeneity
may yet be pre-determined e.g. by varia-
tions in soil quality; dung or urine return, or
due to the nature of the mechanism of dis-
persal of plant species and their biotic inter-
action with soil [32]. Complex spatial and
temporal phenomena can certainly arise
from such vegetation interactions alone
[43].
Given this complexity it is probable that
only by combining models with carefully
focussed experimentation, will we satisfy
the desire to understand the role of hetero-
geneity and grazing processes in ecosystem
function. Such work would need foremost
to address issues of spatial scale. Analyses
of the growth of vegetation resources in
grassland are soundly based in the physiol-
ogy and morphology of individual plants
but have tended to be modelled as a contin-
uous, deterministic process, as if homoge-
neous, at the field scale. This is in marked
contrast to advances in animal foraging sci-
ence and behavioural ecology which are
predominantly individual based, where for-
aging is perceived at the bite (prey or patch)
scale and considers the (stochastic) expec-
tation of success of finding food. This dis-
parity in scales can lead to substantial
imbalance in models and discrete, stochas-
tic, spatial accounts can give critically dif-
ferent predictions, e.g. of carrying capacity
and stability, from conventional continuous,
deterministic, homogeneous ones [39].
But we propose it is not only important to
Spatial heterogeneity and grazing processes 177
address plant animal interactions at the
same scale, but to seek ‘rules’ across a
range of scales (e.g. in Fig. 6). Emphasis on
individual based concepts must not, of
course, overlook group foraging theory
[24].
Major advances in combining vegeta-
tion and animal behaviour have been made
recently, but one component of the system
is substantially overlooked – that of human
intervention in response to risk and uncer-
tainty, and a confusion of regulatory, emo-
tive and socio-economic goals. The models
above are essential for understanding the
biophysical system, but the challenge is
then to capture these insights and rational-
ise them to a scale and level of detail that is
more appropriate for tools for managing the
complexity of grassland ecosystems, and
sufficiently balanced to be able to seek opti-
mal solutions for achieving the human, as
much as the animals, multiple goals.
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Spatial heterogeneity and grazing processes 179
Review article
Grazing and pasture management
for biodiversity benefit
Andrew J. ROOK*, Jeremy R.B. TALLOWIN
Soils, Environmental and Ecological Science Department, Institute of Grassland
and Environmental Research, North Wyke, Okehampton, Devon EX20 2SB, UK
(Received 19 August 2002; accepted 25 February 2003)
Abstract — The primary role of grazing animals in grassland biodiversity management is mainte-
nance and enhancement of sward structural heterogeneity, and thus botanical and faunal diversity, by
selective defoliation due to dietary choices, treading, nutrient cycling and propagule dispersal. Most
research on dietary choices uses model systems that require considerable extrapolation to more com-
plex communities. Grazing animals’ diets are constrained by temporal and spatial changes in sward
structure, plant defence mechanisms, herbage availability, plant phenology and animal physiological
state. Potentially, these could be exploited to manipulate choice in diverse communities. Dietary
choice differs between animal species, driven by factors such as body size, digestive physiology and
dental anatomy. There is anecdotal evidence for breed differences but little experimentation, with ge-
netic effects often confounded with background experience. There is information about landscape-
scale breed and background effects but little about parameters such as bite and feeding station areas
that allow reconstruction of the development of small-scale sward patchiness. An experiment at five
European sites is examining breed effects on grazing behaviour, structural, floral and faunal diversity,
animal production and economic impacts. In another project, calves are being reared by their own
mothers or by cows of another breed allowing genetic effects on grazing behaviour to be separated
from effects of early experience. ‘Designer animals’may be needed to deliver desired grazing behav-
iour and biodiversity outcomes, either by breeding or by the use of training and previous experience to
manipulate choices. Application of research results requires consideration of conservation goals,
whether at landscape, habitat, plant community or plant species level. There is a need to replace
stocking rate prescriptions with sward-based methods and to integrate biodiversity goals into inten-
sive systems. Major gaps in our knowledge of grazing behaviour and its impact on biodiversity re-
main, necessitating greater integration of plant ecophysiology, plant community ecology and animal
behavioural ecology research.
grazing / biodiversity / pasture management / dietary choices / animal type
181
Anim. Res. 52 (2003) 181–189
INRA, EDP Sciences, 2003
DOI: 10.1051/animres:2003014
* Correspondence and reprints
Tel.: +44 1837 883548; fax: +44 1837 82139; e-mail: [email protected]
Résumé — Pâturage et gestion des prairies pour davantage de biodiversité. Le rôle majeur des
animaux au pâturage dans la conservation de la biodiversité des prairies permanentes est de maintenir
et de développer l’hétérogénéité du couvert végétal par la défoliation sélective, selon les choix ali-
mentaires, par le piétinement, le recyclage des éléments nutritifs et la dispersion des graines. Ainsi le
pâturage favorise la diversité floristique de la prairie et la diversité faunistique associée. La plupart
des recherches sur les choix alimentaires utilisent des situations modèles qui exigent des extrapola-
tions considérables pour des communautés végétales plus complexes. En effet, le régime alimentaire
des animaux au pâturage dépend des changements spatio-temporels de la structure du couvert végé-
tal, des mécanismes de défense des plantes, de la disponibilité en herbe, de la phénologie des plantes
et de l’état physiologique des animaux. Potentiellement, ces facteurs peuvent être exploités pour
orienter les choix alimentaires dans diverses communautés végétales. Les choix alimentaires diffè-
rent entre les espèces animales, selon des facteurs comme la taille de l’animal, la physiologie de la di-
gestion et l’anatomie dentaire. Des différences entre races ont été mises en évidence sur la base d’une
démarche plus empirique qu’expérimentale, les effets génétiques étant souvent confondus avec les
effets de l’environnement et de l’expérience alimentaire des animaux. Il existe également des don-
nées sur l’effet de la race et du milieu dans lequel évolue l’animal à l’échelle large du paysage, mais
peu au sujet de paramètres tels que la surface des bouchées et des stations alimentaires qui permettent
la restauration de l’hétérogénéité du pâturage à une échelle plus petite. Un essai conduit actuellement
sur cinq sites européens a pour but d’étudier l’influence de la race sur le comportement au pâturage, la
diversité de la structure et de la flore de la prairie ainsi que celle de la faune associée, la production
animale et l’impact économique. Dans une autre étude, des veaux sont élevés soit par leur mère soit
par des vaches d’une autre race afin de séparer sur le comportement au pâturage les effets liés aux fac-
teurs génétiques de ceux liés à l’apprentissage dans le jeune âge. En orientant les choix alimentaires
des animaux, par la sélection génétique ou bien par l’expérience dans le jeune âge et l’apprentissage,
on pourrait utiliser des animaux ‘modèles’ pour favoriser des comportements de pâturage désirés, et
par voie de conséquence la biodiversité de la prairie. La mise en application des résultats de la re-
cherche doit prendre en compte les objectifs de conservation des espaces pastoraux aussi bien à
l’échelle du paysage, que de l’habitat, de la communauté ou de l’espèce végétale. Il devient alors fon-
damental de remplacer les méthodes traditionnelles de conduite du pâturage, faisant appel à la notion
de chargement, par des méthodes basées sur l’état du couvert végétal, et aussi d’intégrer des objectifs
de biodiversité dans les systèmes d’élevage intensif. De nombreuses lacunes dans notre connaissance
du comportement de pâturage et de son impact sur la biodiversité demeurent. Il est nécessaire de
mieux intégrer les recherches menées en écophysiologie des plantes, en écologie des communautés
végétales et écologie comportementale des animaux.
pâturage / biodiversité / conduite de la prairie / choix alimentaires / type d’animal
1. INTRODUCTION
In this paper, we review the role of the
grazing animal in the management of grass-
lands for biodiversity, and the mechanisms
by which this role occurs. We identify some
of the gaps in our knowledge and describe
experiments at the Institute of Grassland
and Environmental Research, North Wyke
(UK) that are attempting to fill some of
these gaps. We consider the goals of
biodiversity management and some of the
important current issues. In the light of
these goals, we consider some of the poten-
tial management tools that may assist graz-
ing managers to enhance biodiversity.
If we are to exploit current knowledge
and to take sensible directions in applied re-
search, it is necessary to consider the goals
of our conservation management. To some
extent, this is an issue of scale. The goal
might be to manage for a cultural land-
scape, that is not just the physical features
of the landscape but also the human aspects.
182 A.J. Rook, J.R.B. Tallowin
For example, the species and breed of ani-
mal employed might be chosen to reflect
traditional local practices. The possibility
that this might compromise biodiversity
outcomes per se need to be considered. An-
other goal might be to manage at the habitat
level over several different plant communi-
ties or at the community level. Alterna-
tively, interest may centre on rare or
emblematic species or on the fauna rather
than the flora. These scenarios may require
very different grazing management prac-
tices.
Having established the goals, there is
also a need to consider some of the current
issues in the management of grasslands for
biodiversity. One of these is the need to
move away from crude, though easily im-
plemented, management methods such as
stocking rates prescriptions on which many
current agri-environment schemes are
based, to sward based management guide-
lines such as sward height or sward height
distribution [5]. Another pressing issue is to
obtain reliable evidence about animal breed
and background effects as many current
management prescriptions rely heavily on
anecdotal evidence. There is also a need to
integrate biodiversity goals into intensive
systems. Currently, many of our agri-envi-
ronment schemes are aimed at farmers in
marginal areas rather than at, for example
the intensive dairy farmer.
2. THE ROLE OF THE GRAZING
ANIMAL
Most temperate grasslands require peri-
odic defoliation to control succession, if
they are not to succeed to scrub and ulti-
mately woodland. Except on very steep or
uneven ground, it is usually possible to
achieve this defoliation by mechanical har-
vesting of the herbage. Indeed some com-
munities such as hay meadows have
evolved in response to such management.
However, the grazing animal has a unique
role to play. This is to maintain and enhance
structural heterogeneity of the sward can-
opy, which in turn has a vital influence on
floral and faunal diversity.
3. MECHANISMS FOR CREATING
HETEROGENEITY IN GRAZED
SWARDS
Probably the most important mecha-
nism by which grazing animals create
sward heterogeneity is selective defoliation
as a result of dietary choices both between
species and between plant parts within spe-
cies. This alters the competitive advantage
between plant species both by direct re-
moval of phytomass and by altering the
light environment and competition for soil
nutrients [3]. A second mechanism is tread-
ing which opens up regeneration niches for
gap-colonising species. A third mechanism
is nutrient cycling. This has the effect of
concentrating nutrients into ‘hot spots’ at
dung and urine patches and again may alter
the competitive advantage between species,
both directly and by feedback effects on di-
etary choice and thus on heterogeneity, as
cattle in particular will not graze near dung
patches. Grazing animals also have a role in
propagule dispersal. This may be either
endozoochorous (i.e. by seeds passing
through the animal’s digestive system) or
exozoochorous (i.e. by seeds attaching to
the animal’s coat) dispersal but we particu-
larly stress the role of the endozoochorous
route as the mower can also effectively dis-
tribute many exozoochorous species. For a
more comprehensive review of plant re-
sponses to grazing see [2].
The direct effects of grazing on sward
canopy structure and the plant community
lead to secondary effects on faunal diversity
both by changing the abundance of food
plants and by providing breeding sites. The
direct effects on invertebrate diversity feed
through to vertebrate diversity (e.g. [20]).
Another secondary effect of the changes in
Grazing management for biodiversity 183
structure and community brought about by
grazing is the feedback on the grazing be-
haviour of the animals by changing the
choices available to them.
4. DIETARY CHOICES
Since much of the system is driven by
the animal’s dietary choices (both between
species and between potential feeding sta-
tions), it is important to understand the
mechanisms driving these choices. It
should be stressed that most of our knowl-
edge is derived from simple model systems,
such as perennial ryegrass-white clover and
that there has been relatively little detailed
work in more complex communities, at
least in temperate lowland environments.
Generally, behavioural ecologists have
assumed that the animal is striving to opti-
mise its evolutionary fitness. In the context
of foraging, rate of energy intake has usu-
ally been taken as a surrogate measure for
evolutionary fitness [18]. However, in
many situations animals appear to behave
sub-optimally. For example, grazed grass
has a carbon/nitrogen ratio too low to be op-
timal for the animal’s requirements but both
cattle and sheep offered a free choice with
minimal physical constraints consistently
chose a diet containing around 70% clover,
with an even lower C/N ratio [17]. Further-
more, the mixed diet is not due to intake rate
maximisation since in this case animals
would choose 100% clover as this species
can be eaten faster [17]. This suggests that
rate of energy intake is not the currency that
the animal is optimising, and that the true
currency remains to be identified. To opti-
mise fitness the animal has to trade-off
many currencies, for example nutrient in-
take with predation risk and these trade-offs
are not fully understood [17]. These limita-
tions to our knowledge make it difficult to
extrapolate from our simple model systems
to the more complex swards of interest to
biodiversity managers.
In discussing dietary choices, many peo-
ple, particularly those working in conserva-
tion management use the term ‘palatability’
as a plant descriptor. Unfortunately, the
term has been so misused as to have become
almost meaningless. Palatability refers to
the acceptability to an animal of a food
based purely upon organoleptic properties
independent of post-ingestive conse-
quences. Animals can learn to associate
post-ingestive consequences (for example
toxicity) with the taste of a food and subse-
quently use taste as a cue to avoid this food
but there are relatively few examples of
choices being made solely on organoleptic
grounds. Palatability is primarily an animal
not a food characteristic as there are many
situations in which an animal’s food choice
is altered even though the foods themselves
remain unchanged. We therefore recom-
mend that the term is not used as a food
descriptor and suggest that it is of little use
in understanding the basis of dietary
choices (for a fuller discussion see [14]).
It is more useful when describing food
choices to regard the animal as having a po-
tential intake but being constrained by vari-
ous factors, including those inherent to the
food. When grazing there are important
physical constraints on intake and therefore
on the choices between plants with differ-
ent levels of these constraints. These con-
straints include sward structure (sward
height, leafiness, tiller density and horizon-
tal patchiness) and plant physical defence
mechanisms (for review see [15]). This
latter may be a driving force in patch
formation in some situations, for example,
the animals may avoid an area around
Cirsium sp.
Dietary choice changes over time at all
scales. This is due to the availability of
herbage, phenology of the plant and the
physiological state of the animal. An exam-
ple of a relatively short-term temporal ef-
fect is the change in preference between
grass and clover that has been observed over
the day. Both dairy cows and sheep include
184 A.J. Rook, J.R.B. Tallowin
more clover in the diet in the morning and
more grass in the evening [16]. It has been
speculated that this might be either due to
higher sugar levels in the grass at this time
[11] and hence higher digestibility or, alter-
natively, it may be because the animal fills
its rumen with relatively slowly digesting
material (compared to clover) in order to
maintain rumen microflora populations
during the overnight fast. At present, it is
not possible to offer a definitive answer. If a
similar circadian effect was to be seen in
choices between elements of plant commu-
nities of interest for biodiversity, it might be
possible to exploit the effect to manipulate
overall choice and hence effect on sward
structure and diversity.
There are also spatial effects at many
scales. Most animals in lowland systems in
Europe have no opportunity to make
choices at the landscape scale and hence
much of our research in these systems re-
lates to choice at the bite or feeding station
(i.e. without moving the legs) scale. In hill
and upland systems (and range systems in
other countries), we know that animals es-
tablish home ranges within which they
move on daily and longer time scales.
Choice of location may be driven by other
factors than food, such as water, shelter and
social cohesion (itself an anti-predation
strategy) (e.g. [6]).
5. ANIMAL TYPE
Animal type has a major effect on di-
etary choice. The most fundamental effect
is that of body size. Because larger animals
have relatively large gut capacity in relation
to their metabolic requirements, they can
retain digesta in the tract for longer and thus
digest it more thoroughly. This means that
they can deal with a lower digestibility diet
and hence can forage less selectively than
smaller animals which must of necessity
select higher quality items [10]. The ani-
mal’s physiological state will also affect its
selection. For example, hungry animals are
less selective [12].
Species effects are of great importance.
Some of these are driven by body size, for
example, sheep are more selective than cat-
tle. Digestive physiology is also important,
for example, ruminants such as cattle have
more efficient digestion than hind-gut
fermenters such as horses [10]. The latter
therefore rely on high throughput and this
can necessitate long grazing times of up to
19 hours per day (e.g. [4]). Dental anatomy
is also important; horses, with both top and
bottom incisors can graze much closer to
the ground than cattle and appear to con-
centrate their grazing in short areas that rep-
resent only a small proportion of the
available area and thus produce a quite dif-
ferent sward structure [7]. The extent to
which grazing by horses results in a differ-
ent plant community to grazing by cattle is
still the subject of some debate. Many horse
grazed pastures are overstocked, leading to
poor structure and loss of diversity [1]. This
has probably resulted in an unjust, negative
perception of grazing by horses as a tool for
conservation management.
There is much anecdotal evidence (e.g.
[19]) for breed differences in diet selection
and hence in impact on sward structure and
composition but little experimental evi-
dence. In these anecdotal reports, true ge-
netic differences between breeds are often
confounded with the environmental effects,
particularly prior experience of biodiverse
pastures during early life that may affect
subsequent selection.
Secondary evidence on breed effects is
also patchy. There is some good informa-
tion about breed and background effects on
animal movements at a landscape scale. For
example in an experiment in which Scottish
Blackface or Suffolk ewes raised either
lambs of their own breed or of the other
breed [8], the distances between Blackface
ewes was greater than between Suffolks but
Blackfaces kept their lambs much closer to
them, whatever the breed of the lamb. The
Grazing management for biodiversity 185
ewes had a choice of using upland or low-
land pasture; the Blackface ewes made
much more use of upland and this persisted
in the lambs that they had reared whatever
the lamb breed, although some effect of
lamb breed was also evident (Tab. I).
While we have reasonable information
on breed effects on movement at a landscape
scale in heterogeneous environments, we
know very little about differences at the
scale of the grazing bout or feeding patch.
There is information from single breeds
grazing homogeneous pastures (e.g. [9,
13]); these provide information on parame-
ters such those shown in Table II that allow
the development of patchiness in the grazed
sward to be reconstructed [2]. However, we
have no idea if and how breeds differ in
these parameters, how any such effects
would be modified in heterogeneous pas-
tures or how they would interact with the
background of the animals, either immedi-
ately prior to moving to the target area or
during early life. It is also possible that
small-scale selection and the heterogeneity
this creates will differ depending on the
scale of enclosure in which the animal is al-
lowed to make its choices. Some of the
main gaps in our knowledge are summa-
rised in Table III. Because of these gaps, we
are currently ill-placed to predict effects of
different grazing managements and breed
on biodiversity.
6. CURRENT EXPERIMENTS
In this section, we describe two recently
initiated experiments which illustrate re-
search approaches to some current issues in
biodiversity management. In an EU pro-
ject (FORBIOBEN), we are comparing
North Devon (a traditional breed) with
Charolais × Holstein-Frieisan (a commer-
cial breed) yearling steers. The aim of this
project is to test if there are any breed differ-
ences in grazing behaviour and impact on
biodiversity. With the commercial breed,
we will also look at grazing intensity. The
animals are grazing agriculturally semi-im-
proved grassland and rush pasture contain-
ing 5–10 species per m2. We have chosen
the North Devon as it was originally devel-
oped on this type of grassland, particularly
rush pastures. We are monitoring botanical
structure and flora and faunal diversity,
herbage and animal production and eco-
nomic outputs. Similar trials are taking
place at 4 other sites across Europe
(Tab. III).
In a second project (BEFORBIO),
funded by the UK Department for the Envi-
ronment, Food and Rural Affairs, we are at-
tempting to separate true breed (genetic)
effects from the effects of early experience.
North Devon or Hereford-Friesian suckler
cows have been mated to North Devon and
Charolais bulls, respectively. At birth we
186 A.J. Rook, J.R.B. Tallowin
Table I. Inter-animal distance and percentage of time spent on upland pasture by Scottish Blackface
and Suffolk ewes rearing lambs either of their own, or of the other breed (according to Dwyer and
Lawrence [8]).
Ewe
Lamb
Blackface
Blackface
Suffolk
Blackface
Blackface
Suffolk
Suffolk
Suffolk
Ewe-ewe distance (m) 12.77 5.30 12.01 3.84
Ewe-lamb distance (m) 6.03 11.64 5.45 10.88
% upland use (ewes) 78 10 82 2
% upland use (lambs) 82 28 55 4
will cross-foster half the calves onto cows
of the other breed. Devon cows with their
own or fostered calves will graze a fen
meadow/rush pasture while Hereford-
Friesian cows + calves will graze a ferti-
lised ryegrass sward. In their second year,
all the calves will graze on fen meadow/
rush pasture and we will compare behav-
iour and impact on the sward of the differ-
ent breeds and backgrounds.
7. MANAGEMENT OPTIONS
In this section, we consider some of op-
tions for biodiversity management that we
believe current research findings in grazing
behaviour make possible. We believe there
is a need for ‘designer animals’that are cho-
sen to deliver desired grazing behaviour
and hence biodiversity goals. This might be
achieved by exploiting the animal’s genet-
ics. We do not believe that genetically mod-
ified animals per se will be acceptable to
European consumers in the foreseeable fu-
ture, particularly in a conservation context.
However, the new insights provided by
genomic technologies open up opportuni-
ties for greater understanding of the genetic
basis of behaviour and the use of marker
Grazing management for biodiversity 187
Table II. Examples of small scale (within head
down grazing bout) movement parameters for
heifers and ewes. According to Harvey et al. [9].
Heifers Ewes
Bout duration (s) 180 51
Distance moved during
bout (m)
7.3 1.8
Bites per m 32.3 37.4
Bites per bout 244 67
Bites per min 80 79
Bite area (cm3) 36.4 16.7
Table III. Gaps in current knowledge on the ef-
fects of grazing on biodiversity.
Dietary choices of animals in temperate
multi-species swards
Small scale animal movements in
heterogeneous swards
Relative importance of genetics
and environment
Effects of spatial scale at which grazing
management is applied
40
20
0
20
40
7 9 11 13 15 17 19 21 23 1 3 5Hour
clover
grass
Min.
Figure 1. Minutes grazing clover or grass by dairy cows in each hour of the day (according to Rutter
et al. [18]).
assisted selection to obtain animals with
desirable traits. In the short term, we be-
lieve there is opportunity to better exploit
the background of animals and to train them
to produce the biodiversity outcomes that
we desire. There is also much scope for ex-
ploiting temporal behaviour patterns to ma-
nipulate dietary choices so as to ensure that,
whilst animals are productive and provide
the farmer with an acceptable economic re-
turn, they also make the desired choices
when grazing biodiverse pastures. An ex-
treme example of this might be the use of
folding systems (such as practised in the
past in many chalk downland systems) in
which animals are removed to fallow arable
land for part of the day as a means of export-
ing nutrients.
8. CONCLUSIONS
In conclusion, grazing animals have a
vital role to play in the management of
biodiverse pastures. However, major gaps
in our knowledge of grazing behaviour in
such pastures and its impact on biodiversity
remain. We believe that there is a need for
stronger integration between research on
plant ecophysiology and plant community
ecology and the behavioural ecology of for-
aging herbivores in order to address these
knowledge gaps.
ACKNOWLEDGEMENTS
We thank the organisers of the Pasture Ecol-
ogy Group Meeting for inviting us to prepare
this paper and INRA for funding attendance at
the Meeting. We acknowledge funding from the
EU Commission Framework 5 programme
(FORBIOBEN – QLK5-2001-00130) and from
the UK Department for the Environment, Food
and Rural Affairs. We also acknowledge the
contribution of our partners to the setting up of
the FORBIOBEN project – M. Petit, B. Dumont,
J. Isselstein, M. Hofmann, K. Osoro, M.F. Wallis
de Vries, G. Parente, S. Venerus, M. Scimone, P.
Gaskell and J. Mills. Animal Research at IGER
is carried out in accordance with the welfare
standards approved by IGER’s Ethical Review
Procedure.
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