Hierarchical foraging in northern ungulates Anna Skarin Introductory research essay Uppsala 2004 Hierarchical foraging in northern ungulates Anna Skarin Introductory research essay
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Institutionen för husdjursgenetik
Rapport 142
Publication No. 142
Swedish University of Agricultural Sciences Uppsala 2004
Department of Animal Breeding
ISSN 1401-7520
and Genetics
ISRN SLU-HGEN-R--142--SE
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Table of Contents
1. Introduction ........................................................................................................ 1
2. Foraging theories ................................................................................................ 3
2.1 Hierarchical foraging................................................................................... 3
2.1.1 Patch level............................................................................................ 3
2.1.2 Landscape level ................................................................................... 3
2.1.3 Regional level ...................................................................................... 4
2.2 Optimal foraging.......................................................................................... 4
2.3 The marginal value theorem........................................................................ 5
3. Empirical studies ................................................................................................ 7
3.1 Species and scale dimensions...................................................................... 7
3.1.1 Northern Ungulates.............................................................................. 7
3.1.2 Geographical range.............................................................................. 7
3.2 Patch level.................................................................................................. 11
3.2.1 Forage quality and availability.......................................................... 11
3.2.2 Forage morphology............................................................................ 11
3.2.3 Movement and patch-edge recognition............................................. 12
3.3 Landscape level ......................................................................................... 14
3.3.1 Interactive factors .............................................................................. 14
3.3.2 Non-interactive factors ...................................................................... 14
3.4 Regional level ............................................................................................ 15
3.4.1 Migration and seasonal change ......................................................... 15
3.4.2 Predation ............................................................................................ 15
3.4.3 Site fidelity and social structure ........................................................ 16
4. Conclusions ...................................................................................................... 17
5. Literature........................................................................................................... 19
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1. Introduction
The importance of scaling in ecology has been evident to ecologists for at least three
decades (Peterson & Parker, 1998). Scaling refers to the physical dimensions of observed
entities and phenomena. Scale is recorded as a quantity and involves measurements and
units. As a rule of thumb, when we use the term scale, we should be able to assign or
identify dimensions and units of measurements (Peterson & Parker, 1998). Things,
objects, processes, and events can be characterized and distinguished from others by their
scale, such as the size of an object or the frequency of a process. In ecology it is important
to remember what scale stands for, as there is no such thing as the “scale of the
ecosystem”. Scale rather refers to hierarchical levels in ecological organisation that result
from differences in the kind of and number of interactions under study (Hobbs, 2003). The
frequencies and rates of activities are useful for defining hierarchical scales (Allen &
Staar, 1982).
Here some foraging theories and empirical studies which are unified by the scale
perspective with focus on hierarchical foraging theory will be reviewed. A number of
different systems for describing the hierarchy of scales at which foraging behaviour can
be viewed have been described (Senft, et al., 1987; Bailey, et al., 1996). Patterns of
foraging at the level of the landscape represent to a certain extent an integration of
decisions made at smaller scales, and are therefore important to understand (Duncan &
Gordon, 1999). The hierarchical theory gives a good multi-scale perspective of the
foraging decisions of the animals, and is thus presented as a framework for this review.
The aim is to distinguish what are the common foraging deciding factors and not for
different species of ungulates, and to enlighten deciding factors for different species at
different levels and how important these factors are.
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2
2. Foraging theories
2.1 Hierarchical foraging
In grazing ecology of large herbivores the term hierarchical foraging is used. This is based
on the way that herbivore behaviour can be separated in levels on a scale where the
number of decisions made for one action or number of actions decides the scale. Senft et
al. (1987) described hierarchical foraging in large herbivores where different foraging
response patterns are displayed at three different levels, these levels are described below.
Table 1 show the interactive (biotic) and non-interactive (abiotic) factors affecting the
habitat use at the different scales according to Senft et al. (1987). Further in Table 2, all
the species reviewed are listed with the interactive and non-interactive factors that have
been found important.
2.1.1 Patch level
The lowest level of selection, in which the feeding station and then the plants and plant
parts are selected, is the patch level. Ungulates take approximately 107 bites a year and
each bite represents a decision about what plant or plant part to eat (Senft, et al., 1987).
Foraging ungulates must solve two problems at the patch or plant community scale: which
plants or plant parts should be selected from the array of immediately available material
(diet selection) and how they should move through the area (location selection). Plants can
be aggregated in patches and a patch can be defined as a spatial aggregation of bites over
which instantaneous intake rate remains relatively constant (Illius & Hodgson, 1996). The
definition or size of a patch can therefore vary with the herbivore, and their choice of
forage e.g. for woodland caribou during winter the mean inter-patch movement were 450
m (Johnson, et al., 2002b), and for reindeer during summer there were no strong patch
selection rather a selection for a certain plant species (Mårell, et al., 2002). A tree can also
be a patch, for example when moose browse on aspen stands or reindeer feed on arboreal
lichens (Johnson, et al., 2001; Edenius, et al., 2002).
2.1.2 Landscape level
At the landscape level herbivores select larger patches, plant communities or feeding sites
(equivalent to each other) that have high abundance and/or nutritive quality of the
preferred plants in the community (Senft, et al., 1987; Bailey, et al., 1996). This is also
equal to a collection of patches in a contiguous spatial area where animals graze during a
foraging bout. Further up in the hierarchy, forage depletion in the patch and expectations
of intake opportunities in other patches will motivate the animal to move on (Baumont, et
al., 2000). Large herbivores may cross plant-community boundaries up to as many as 50
times a day, which implies a decision frequency of 104 times a year (Senft, et al., 1987).
The distances moved from day to day vary depending on species and season but they
usually do not move more than 2 km a day (Rettie & Messier, 2001; Johnson, et al.,
2002b; Fortin, et al., 2002).
At the landscape level the forage biomass and nutrition level are still interactive factors,
but non-interactive factors such as weather, topography and water location become more
important, than at the patch level (Senft, et al., 1987).
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2.1.3 Regional level
At the regional scale, foraging decisions deal with migration between different seasonal
areas or home-range areas, leading to only a few decisions a year for the animal. Then the
animal can move several hundred kilometres between the seasonal ranges. Limiting
factors at the regional scale are still forage as an interactive factor, geomorphology,
regional climate, water locations and physical barriers (Senft, et al., 1987), and when
relevant, predation risk as non-interactive factors (Nicholson, et al., 1997; Rettie &
Messier, 2000; Schaefer, et al., 2000).
Table 1. Interactive and non-interactive factors at the three different levels of action
according to Senft et al. (1987).
Foraging component
Units of selection
Levels of action
Patch
Plants and plant parts
Feeding station
Landscape
Feeding site
Communities
Large patches
Region
Home range
Landscape
Seasonal areas
Interval between
decisions
5-100 sec
1-4 hours
1 month-2 years
Interactive factors
Forage biomass
Nutritive quality
Plant morphology
Forage biomass
Nutritive quality
Forage biomass
Non-interactive
factors
Micro-site variables
Substrate
Topography
Water location
Microclimate
Geomorphology
Regional climate
Physical barriers
Water location
2.2 Optimal foraging
There are other theories that discuss only one or two lower levels of this hierarchical
division. Optimal foraging theories provide a functional approach for examining grazing
behaviours, including diet selection, patch selection and movements. They generally
assume that foraging behaviour is heritable and that animal fitness is related to foraging
behaviour and, that energy can be used to link foraging behaviour with fitness.
The theories predict that foraging animals should aim at maximizing their rate of intake of
the nutrient most limiting for growth and/or reproduction. Intake rate maximization is
constrained by the nutritional quality of available food items and by their abundance
(Duncan & Gordon, 1999), and by the size of the bites (Shipley & Spalinger, 1992). This
is also called the functional response of the animal.
The trade-off between quality and quantity is a key factor in determining the diet that
different herbivores ultimately select, and is responsible for the variation in optimal diet
selection solutions for different sizes of herbivores (Illius & Gordon, 1992). Therefore
there is a strong interaction at this level between the forager and the forage (biomass,
quality and morphology). Farnsworth & Beecham (1999) for example showed how the
forager can interact with the environment and change the spatial pattern of the resource
abundance. There can also be an overlap in time between handling and searching, unlike
the constraint of exclusive searching and handling. Although herbivores have to finish
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chewing one bite before they can take the next, they can use the time spent chewing to
search for the next bite (Illius, et al., 2002).
There have been relatively few optimal foraging theory studies on large herbivores,
primarily because of complications imposed by digestive constraints and the difficulty in
defining discrete food items or quality (Bailey, et al., 1996).
2.3 The marginal value theorem
Patch selection and patch residence time by herbivores has been examined using
approaches based on the marginal value theorem. In the marginal value theorem, the
primary assumption of is that an optimal forager will maximize its overall intake of a
resource (usually energy) during a bout of foraging, taken as a whole. Energy will, in fact,
be extracted in bursts if the food is distributed patchily. The forager may then sometimes
move between patches and during this movement the intake of energy is assumed to be
zero (Begon, et al., 1996). When a forager enters a patch, its rate of energy extraction is
initially high (especially in a highly productive patch or where the forager has a high
foraging efficiency) but this rate declines with the time as the patch becomes depleted
(Begon, et al., 1996).
Charnov (1976) found that the optimal solution for the forager is to leave all patches,
irrespectively of their profitability, when they have reached a certain extraction rate,
which should be the same for all patches (i.e. the marginal value). The model therefore
projects that the optimal stay-time should be greater in more productive patches than in
less productive patches (Charnov, 1976).
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3. Empirical studies
3.1 Species and scale dimensions
3.1.1 Northern Ungulates
This review will cover studies of northern wild living ungulates from the Cervidae and the
Bovidae families with the main focus on species from North America and northern Europe
(Table 2). These families are ruminants and are considered to be the most advanced
artiodactyls. Their stomachs have four chambers which allow for the proliferation of
microorganisms which are able to digest tough vegetation which would otherwise be
unavailable to the animal. Ungulates reviewed from North America are caribou (Rangifer
tarandus), mule deer (Odocoileus hemionus), white-tailed deer (Odocoileus virginianus),
American elk or wapiti (Cervus canadensis), muskoxen (Ovibos moschatus), and
American bison (Bison bison). From northern Europe the semi-domesticated and the wild
reindeer (Rangifer tarandus tarandus), moose (Alces alces), roe deer (Capreolus
capreolus), red deer (Cervus elaphus) and fallow deer (Dama dama) are considered. The
moose and the muskoxen exist in both Europe and North America but the European
muskoxen was reintroduced to Scandinavia in the beginning of the 20th century.
Elk, fallow deer, caribou and reindeer are both browsing and grazing, while moose, roe
deer and white-tailed deer are browsing, and muskoxen are grazing (Hofmann, 1989).
Differences in foraging patterns between browsing and grazing are possible since the bite
size may vary. The grazing animals take larger bites but at a low foraging rate, while
browsing species take smaller bites at a higher rate. The feeding rhythm is much higher
for a browser than for a grazer, for example the roe deer can have up to twelve feeding
cycles (eating, ruminating or resting) a day and a grazer can have as low as three cycles a
day (Hofmann, 1989).
For some species the social structure is of large importance, e.g. the herd can have a
leader that takes decisions when to move on and when to stay and forage (Thomson,
1972).
3.1.2 Geographical range
The geographical ranges for the different levels vary among the reviewed studies. The size
of a patch can vary depending of the size of the animal, their social structure, and the type
of landscape they are living in. It is sometimes difficult to separate which scale different
authors have defined for a certain level. For instance, is a patch the same as a feeding site
or is a patch an aggregation of several feeding sites? However, in an overview of the
geographical ranges of the studies they match quite well (Table 3).
The patch level studies are often performed at the meter scale, the landscape level studies
up to 1-2 km scale, and the regional level at large distances up to several hundred
kilometres. In this context it is also important to notice how the scales were established.
Are they established from the perspective of the animal or from what is most practical for
the researcher?
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Table 2. Reviewed northern ungulate species and their relation to suggested deciding
factors at different levels in their foraging decisions sorted in accordance with the levels
of Senft et al. (1987).
Animal
Reindeer
Caribou
(Rangifer tarandus)
Factors found deciding at the levels of action
Patch
Landscape
Region
Nutritive quality8,14
Forage biomass14
Site fidelity19
Snow depth9
Predation7,9,16
Predation16,17
Random search14
Red deer
(Cervus elaphus)
Forage 5
Slope5
Muskoxen
(Ovibos moschatus)
Forage abundance18
Plant species6,18
Snow depth6,18
Forage biomass6
Snow depth6
Elk
(Cervus canadensis)
Plant morphology12
Nutritive quality10,12
Habitat diversity 10
White-tailed deer
(Odocoileus
virginianus)
Plant morphology2
Frequency dependent2
Forage biomass2
Social factors20
Timber harvesting20
Snow depth20
Forage11,15
Forage maturation15
Snow depth15
Predation15
Spatial heterogeneity11
Social factors13
Snow conditions13
Mule deer
(Odocoileus hemionus)
Roe deer
(Capreolus capreolus)
Forage availability13
Cover13
Human settlements13
Moose
(Alces alces)
Nutritive quality1
Forage 1
Bison
(Bison bison)
Plant morphology4
Frequency dependent4
Snow depth4
Water location4
Fallow deer
(Dama dama)
Forage biomass3
Random search3
13
1
(Edenius, et al., 2002)
2
(Etzenhouser, et al., 1998)
3
(Focardi, et al., 1996)
4
(Fortin, et al., 2002)
5
(Hester, et al., 1999)
6
(Ihl & Klein, 2001)
7
(Johnson, et al., 2002a)
8
(Johnson, et al., 2001)
9
(Johnson, et al., 2002b)
10
(Jones & Hudson, 2002)
11
12
8
(Kie, et al., 2002)
(McCorquodale, 1993)
(Mysterud, et al., 1999b)
(Mårell, et al., 2002)
15
(Nicholson, et al., 1997)
16
(Rettie & Messier, 2000)
17
(Rettie & Messier, 2001)
18
(Schaefer & Messier, 1995)
19
(Schaefer, et al., 2000)
20
(Tierson, et al., 1985)
14
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Table 3. The geographical range of the different levels in the reviewed studies. The
numbers in italic are real measure of the animal’s movement or home ranges etc. The
other figures are set by the researcher during the study of the animal. The references are
the same as in Table 2.
Levels of action
Animal
Reindeer
Caribou
(Rangifer tarandus)
Patch
1*4 m 13
0.50*0.50 m 8
Landscape
Diameter-feeding site - 480
m6
Intrapatch move - 450 m 9
Interpatch move - 1268 m 9
50*50 m or 100 m line 8
Radius - 1000 m 16
1-200 m2 5
Region
Annual mean range size
208-1240 km2 17
Collection of patches
0.48-1.6 km
Transects –feeding sites 100
m 18
Transects 5.8 km 17
Elk
(Cervus canadensis)
Site level – 400 m2 10
Home range 23 km2 10
White-tailed deer
(Odocoileus
virginianus)
10 000 m2
Summer 2.25 km2 20
Winter 1.35 km2 20
Red deer
(Cervus elaphus)
Muskoxen
(Ovibos moschatus)
In craters 0.25*0.25 m
8
400-450 km 19
18
2
4.1-11.3 km, 8.6-19.8
km 15
Home range - 0.39-28.8
km2 11
Radius - 0. 250,
0.500,1, 2 km 11
Mule deer
(Odocoileus hemionus)
Roe deer
(Capreolus capreolus)
2*2 m 13
Moose
(Alces alces)
100 m2
Bison
(Bison bison)
Walk dist. - 1300-2000
m/day 4
Fallow deer
(Dama dama)
300*700m 3
10
1
20*20 km 1
3.2 Patch level
At the patch level the interactions between the forager and the forage are important,
this implies studies of the forage quality and availability, the morphology of the forage,
and animal species movement and patch-edge recognition are often studied since these
are among the most important foraging deciding factors.
3.2.1 Forage quality and availability
Feeding site and plant selection studies demonstrate that forage nutrition level and
accessibility are important for the forager (Ihl & Klein, 2001; Johnson, et al., 2001).
Caribou in winter selected specific species of terrestrial lichens high in energy
(Johnson, et al., 2001). They chose feeding sites where the selected lichens were most
abundant and the snow shallow. Not unexpectedly, animals during winter selected for
thin or soft snow cover and high food abundance (Johnson, et al., 2001; Mosnier, et al.,
2003). When snow conditions limited accessibility, caribou in the forest began feeding
on arboreal lichens (Johnson, et al., 2001). Thereafter the choice of feeding site, i.e. a
tree was a consequence of the abundance of arboreal lichen, snow depth, density and
hardness. During summer foraging reindeer had strong selection for plant parts with
high nitrogen concentration, such as buds and flowers (Mårell, et al., 2002).
Even though foraging decisions for muskoxen in winter were consistent across all
scales, they selected for higher graminiod abundance and for thinner and softer snow
cover at successively smaller scales (Schaefer & Messier, 1995). Muskoxen and
reindeer habitat and diet selection during winter was sorted in scales to see how much
their habitats overlapped and at what scale (Ihl & Klein, 2001). Both ungulates foraged
primarily in upland habitats with low snow depth that had more lichen cover and less
graminoid cover than other vegetation types. Reindeer selected mainly lichens when
foraging, while muskoxen selected more sedges and mosses. They both selected against
snow depth and hardness when choosing cratering areas within the feeding sites. On
their upland feeding sites muskoxen faced a trade-off between suitable snow conditions
and abundance of graminoids. For reindeer, this compromise may not have been
necessary, because in these exposed locations high lichen availability coincide with
low snow depth.
During winter foraging roe deer was found to select feeding sites with higher food
availability index than random sites (Mysterud, et al., 1999b).
Elk feed preferably in open areas that had high grass cover, compared to bedding sites
and other available habitats (Jones & Hudson, 2002). At the stand level, elk selected
meadows due to their concentration of grasses while other habitats were used in
proportion to their availability.
3.2.2 Forage morphology
As mentioned above, other factors than the nutritional values of the plants ingested are
also important. Fortin et al. (2002) studied bison foraging decisions at a patch in a
temporal scale, and found that the animals preferred plants that made them maximise
their short-term energy intake. The authors suggested that several non-interactive
factors could contribute to short-term energy maximisation; for example they may need
to avoid insect harassment or scan for predators. Disturbance by predators or humans
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can prematurely terminate foraging for the animal. Such interruptions may push bison
toward the utilisation of plants that give them energy faster than from other plant
species (Fortin, et al., 2002). The same pattern were found for white-tailed deer, the
foraging rate was higher in patches with the preferred guajillo bush than when they
feed on other bushes such as black brush (Etzenhouser, et al., 1998). This allowed the
deer to spend less time feeding and more time searching, while maintaining nutrient
intake at a sufficient level.
In other species the animal feeding pattern adapts to the nutrition level. Foraging rate
for Rangifer increased with the available plant biomass (Trudell & White, 1981). Elk
selected the best bites spread in a larger biomass of less preferred forage; given the
limited number of best bites available in each patch, the availability of these best bites
would rapidly decrease and a patch change would be predicted (McCorquodale, 1993).
3.2.3 Movement and patch-edge recognition
To investigate how grazers distributed themselves on the patch level, modelling of
movement patterns can be done (Mårell, et al., 2002). These authors studied reindeer
summer foraging patch choice without assuming discrete patches in the models. This
study considers a scale which is intermediate between patch and landscape selection
levels. They concluded that the reindeer adopted a random search strategy when the
food items were outside their sensory-detection range. This takes the reindeer into new
and unexploited areas with a higher probability than using other search strategies.
Fallow deer had a search behaviour that could be described as a first order biased
random walk (Focardi, et al., 1996). There were no clear evidences of patch-edge
recognition or “patchy” behaviour, for either the fallow deer or the reindeer (Focardi, et
al., 1996; Mårell, et al., 2002). However, food quantity was important at the
intermediate scale of habitat selection for both species. They based their decisions to
forage or not on the occurrence of preferred plant species during late spring and
summer. Suggested explanation for the inability to find a patchy behaviour was that the
food abundance was good but of poor nutritional quality (Focardi, et al., 1996). For
example, caribou foraged intensively at relatively small patches and then moved some
distances to a new patch during autumn, winter and spring seasons, compared to
summer when they showed a less patchy behaviour (Johnson, et al., 2002a). This may
be because the environment is less patchy during summer and forage is more abundant,
which could also be true the for studies by Mårell, et al. (2002) and Focardi et al.
(1996).
In studies of moose browsing intensity on individual aspen in aspen stands, and in
random locations, were compared to find out if moose perceive stands as patches
(Edenius, et al., 2002). It was found that the browsing intensity on aspen was similar on
both sites, supporting the view of Mårell et al. (2002) that large herbivores do not
recognise patches that are of higher quality at distance, but they stay and feed if they
come over a high quality patch.
Etzenhouser et al. (1998) compared the foraging by white-tailed deer and goats using
fractal dimensions of the animals foraging path. Foraging behaviour was clearly
dependent on the spatial distribution of food and non-food items in the landscape. The
deer appeared to be influenced by environmental elements at greater distances than
goats, probably because deer cover greater distances via a straighter and faster foraging
path than goats. Goats were more social and stayed in groups even if the forage is
scarce. Deer and goats thus responded differently to similar environmental
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conditions, probably due to the difference in domestication, behaviour and body size.
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3.3 Landscape level
The selections for good quality forage does not always take place at the patch level, the
animals can select for quality forage at a higher level in the hierarchy, i.e. at the
landscape level. Nevertheless, the non-interactive factors have a much greater influence
on the habitat selection at the landscape level than at the patch level.
3.3.1 Interactive factors
Edenius et al. found that moose selection and the intensity of use of aspen ramets were
higher than at random sites, where the availability and abundance of aspen was lower,
indicating that large herbivores such as moose specialise and over-utilise palatable
browse species where they are rare. The authors suggest that this is done because large
generalist herbivores strive to maintain a mixed and balanced diet. Edenius et al.
(2002) contend that moose select feeding sites at broader landscape scale based on
forage abundance. The grazing intensity was higher on aspen ramets in aspen stands
located in young pine forest compared to aspen stands in old forest, meaning that they
prefer the young pine forest and that the selectivity of aspen may reflect variation in
food availability at the habitat or landscape scale (Edenius, et al., 2002).
Habitat rankings based on habitat selection of free-ranging sheep and roe deer were
predicted by the availability of the food resource on both study area and home range
scale (Mysterud, et al., 1999a). Roe deer used habitats with a higher average
availability of herbs when foraging. There was also a direct evidence for a trade-off
between selection of food availability and both canopy cover and distance to human
settlements for roe deer.
Caribou was seen to use a landscape with a higher availability of high quality forage
during winter. They choose landscapes with old spruce forests since these are where the
arboreal lichens are most abundant (Apps, et al., 2001).
3.3.2 Non-interactive factors
Johnson et al. (2001) compared caribou habitat use in forest and alpine environments
and found that in the alpine environment neither lichen biomass nor snow influenced
patch use. However, three factors were important when caribou selected patches in the
forest: the abundance of two lichen species, snow depth and hardness. Ihl & Klein
found that shallow snow rather than soft snow were important in the initial selection of
feeding sites within habitats for both muskoxen and reindeer. In a study of bison, other
factors than the abundance of the preferred food types influenced the distribution of the
animals across the landscape (Fortin, et al., 2003). Female bison, for example adjusted
their use of meadows according to the snow depth in winter, and the preferred
vegetation of meadows surrounded by water was more likely to be used in summer.
For both male and female roe deer habitat selection at the landscape level in winter
sites with more cover during cold weather was more important than the forage
abundance (Mysterud, et al., 1999b). Female roe deer also tended to select foraging
sites that were even more sheltered than those of male roe deer.
American elk (females) had no special preferences for food or safe habitats, nor did
they select for any thermal shelter at the landscape level. Instead, they selected bedding
sites with lower thermal shelter quality than the available habitat (Jones & Hudson,
2002). These opposing results may be due to the elk study being done in a
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landscape that was predominately forested. The elk also selected for home ranges with
a lower road density, they therefore did not need to avoid human disturbances since
they had already selected against it. It was also found that the ranges elk selected in
winter had a greater abundance of infrastructure (i.e. seismic lines, cut-lines, and power
lines and pipelines) than surrounding ranges. This might be surprising as it has been
found that caribou and wild reindeer tend to avoid areas with pipelines and power lines
(Dyer, et al., 2001; Nellemann, et al., 2003). The home ranges for elk had furthermore
a smaller mean patch size and greater patch density (Jones & Hudson, 2002). The
authors suggest that heterogeneity could be important at the landscape level selection,
since large herbivores seem to require temporally and spatially diverse habitat elements
such as food and cover.
3.4 Regional level
At the regional level all the large scale movements take place, as the migrations
between the seasonal ranges. The decisions taken are often due to seasonal changes in
weather conditions, such as to much snow on the ground.
3.4.1 Migration and seasonal change
Migrations between seasonal areas are the common movements at the regional level.
Mule deer trade-offs in relation to migration were associated with low temperatures,
high precipitation, the photoperiod, and maturation of the vegetation (Nicholson, et al.,
1997). Forage quality was also a limiting factor. Migratory mule deer always selected
the habitat with the highest quality, which was only seasonally available in contrast to
the habitat the resident deer selected (Nicholson, et al., 1997). The length of the winter
season was important at a larger spatial scale. Caribou, for example, made elevation
shifts from mid-elevations forests to sub-alpine parkland areas earlier when the snow
accumulated fast (Terry, et al., 2000).
3.4.2 Predation
Caribou in North America is a typical migrating species where avoidance of predators
might be a driving force. Woodland caribou was observed to choose between two
landscape types that differ in biomass and accessibility of lichens (Johnson, et al.,
2001). Relative to the forest living animals, caribou in the alpine landscape foraged
across an environment with shallower and more variable snow cover, and less abundant
more variably distributed lichens. Thus, Johnson et al. (2001) suggested that alpine
caribou probably stayed in the alpine environment to avoid predation and not because
of the forage.
Nicholson et al. (1997) discussed if mule deer displayed a trade-off between migrating
or staying to avoid predation. Mortality in migratory mule deer females occurred
exclusively during migrations whereas mortality in resident mule deer was limited to
winter and then especially to periods with deep snow. For caribou, predation risk was
most important during inter-patch movements (Johnson, et al., 2002b). This seemed to
coincide with the animals moving between patches transiting high risk habitat types
such as rivers, and patches of spruce wetlands. Consequently, the authors found at the
smaller scale (the patch selection at the landscape level) with the exception of one
winter that predation risk was low. Rettie and Messier (2000) meant that the strongest
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selection at the regional scale for woodland caribou was for habitats with less predation
risk. If the caribou failed to avoid predation risk at this level they must continue to
select habitats with reference to predation risk at each finer scale of selection, since this
is the factor that has the greatest potential to limit their individual fitness. Rettie and
Messier (2001) studied predator avoidance further in a non-migratory herd and they
found that the animals adopted range-use and movement behaviour consistent with
predator avoidance at all the scales investigated. If herbivores move randomly through
the landscape, they can avoid predators more effectively since it will be difficult for the
predator to foresee random movements (Mitchell & Lima, 2002).
3.4.3 Site fidelity and social structure
Since migrating species often move between seasonal areas, site fidelity can be an
important factor. Schaefer et al. (2000) studied site fidelity in relation to seasonal
migration of caribou. They found that philopatry of migratory caribou was a highly
scale-dependent pattern. Fidelity to calving and summer range disappeared when
viewed at a smaller scale, corroborating earlier suggestions that females are philopatric
to their traditional calving grounds but not to precise locations within these grounds.
The pattern for sedentary caribou, on the other hand, persisted across scales, indicating
consistent site fidelity from calving to breeding periods, regardless of the extent of their
observations. Site fidelity and spatial scale were inexorably linked. Their analysis
underscored previous studies indicating ecotypic differences in the dominant factors of
population limitation. Migrating and escaping predation makes food becoming a
limiting factor. Instead it is the migratory animals that are regulated by the competition
for high-quality forage at the new ranges.
White-tailed deer in Adirondack Mountains also showed fidelity to specific seasonal
ranges (Tierson, et al., 1985). The movement from summer to winter ranges started
when snow depth approached a certain level, whereas the ambient temperature was of
little importance. Instead they identified a number of social groups among the study
animals which shows that the animals social structure was of large importance for there
movements. The white-tailed deer chose home ranges primarily based on social factors
and not on habitat types.
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4. Conclusions
Most of the empirical studies conclude that there is scale dependence in the foraging
decisions of large herbivores. At all scales, forage is the overall deciding factor. At the
patch level the food nutritional quality and availability is of larger importance than at
higher levels. The herbivores consequently choose plants and feeding sites that are of
high nutritive quality.
At the patch level, the other foraging theories are useful to understand the interaction
between the herbivore and the plant species, for example the functional response in
terms of the plant morphology. It is sometimes essential to be able to eat the plant fast,
and a plant can simply be chosen because it takes less time to eat than a plant with
higher nutritive quality.
For Rangifer and muskoxen, winter and summer conditions result in different patch
sizes. In summer there is often a continuum of forage and it is hard to distinguish
patches, while winter foraging often requires cratering in the snow. The craters are
done in restricted areas because of the effort of cratering and the animals only crater if
they can sense good quality forage under the snow.
The higher up, in the hierarchical scale of foraging decisions the less important the
interactive factors have for the decisions the animal eventually take (Table 1). At the
landscape level, there can be a trade-off between cover and food for example. During
winter the snow depth is crucial for all the species even though some species can
handle a thicker snow cover better than others. The non-interactive factors also have
importance for the decisions made at the lower levels. If the animals are forced to select
an area because of the weather and the possibility to find cover, there may not be any
preferred forage in this area. Some authors suggest that herbivores do not plan their
foraging, they move randomly in the landscape and forage whenever they come across
good forage.
The factors determining movements, such as migration between seasonal ranges, are
often abiotic factors like increasing snow depth, temperature, and biotic factors such as
growing periods for the plants and depletion of forage in one seasonal range. Migration
or large scale movements are not always coupled with forage limitations. Predation risk
is an important factor even though predation increased during the migration period for
some species. Some species show site fidelity to different seasonal ranges but they do
not return exactly to the same spot, maybe because they want to avoid the possibility
for the predator to learn exactly where they are.
For gregarious species (e.g. Rangifer) the large scales as well as small scale movements
are coupled to the whole herd movements. Surprisingly few of the reviewed studies
discuss this issue. However, this may not be a problem for the researcher studying the
animal since the animal that takes the decision for the herd probably do this within the
concept of scaling.
With the hierarchical perspective in mind, it is especially interesting to investigate how
abiotic or non-interactive factors may have importance for the animals’ choices at
lower levels. Are they using optimal areas in the view of the animal, or do the abiotic
factors force them to choose areas that are less optimal for foraging? Even though they
try to forage optimally they do not always succeed. Snow, weather, insect harassment,
17
predation and human disturbances may force the animals to choose non-optimal areas
sometimes or move from the optimal areas chosen.
To be able to argue for important habitats for a species, the hierarchical approach
seems to be a good start, and even though there are consistencies across species’
responses it is always necessary to study the species in mind to catch the local and
between species variation.
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