Foraging biology and habitat use
of the southern African ice rat
Otomys sloggetti robertsi
Ute Heidrun Schwaibold
A thesis submitted to the Faculty of Science,
University of the Witwatersrand, Johannesburg,
in fulfilment of the requirements for the
Degree of Doctor of Philosophy.
Johannesburg, 2005
ii
DECLARATION
I declare that this thesis is my own, unaided work. It is being submitted for
the Degree of Doctor of Philosophy in the University of the Witwatersrand,
Johannesburg. It has not been submitted before for any degree or
examination in any other University.
_________________________
Ute H. Schwaibold
___________day of_________________________2005
iii
ABSTRACT
Animals living in cold environments show physiological, morphological and behavioural
adaptations to low temperatures. The African ice rat, Otomys sloggetti robertsi, which is
endemic to the southern African Drakensberg and Maluti mountains above 2000m, is an
interesting exception since, unlike most alpine small mammals, it does not hibernate or
display torpor and is physiologically poorly adapted to low temperatures. It is a strict
herbivore, feeding on a low quality diet. Ice rats do show some morphological (e.g. short
tails) and behavioural (e.g. communal huddling; constructing underground burrows)
adaptations, but little else is known about their biology, particularly how they maximise
energy gain to meet thermoregulatory requirements, especially during cold periods.
Since feeding represents the primary method of energy gain in endotherms, I studied
aspects of the foraging biology of ice rats, including gut structure, foraging patterns and
habitat choice. The gut structure of O. s. robertsi is well adapted for a high fibre,
herbivorous diet and shows broad similarities with those of its mesic- and arid-occurring
relatives. However, O. s. robertsi showed increased dimensions of several foregut organs
which may be adaptations for increased energy uptake and/or poor diet quality in alpine
environments. Furthermore, females had a larger stomach as well as a longer caecum,
small and large intestine in summer than in winter but the gut of males was unaffected;
such sexual asymmetry may be related to increased energy requirements of females
during pregnancy and lactation.
Environmental influences on the aboveground behaviour of O. s. robertsi were
investigated by recording the duration of behaviours as well as sequential transitions
among behaviours. Ice rats spent most of their day foraging and basking, and much time
was spent in their underground burrows. Seasonal comparisons revealed that ice rats
spent significantly more time acquiring energy through foraging in winter, whereas they
remained below ground for longer periods of time during the middle of the day in
summer to escape extreme heat and solar radiation.
To understand how low temperatures and predation influenced foraging patterns,
the behaviour of ice rats was studied in summer and winter in a population where
predators were minimal and in another population which experienced higher levels of
predation. Ice rats are central place foragers that travel short distances to forage and
display significant seasonal variation in their foraging patterns. In the absence of
predation risk, ice rats generally returned to a central place with forage, even though
iv
returning to a burrow after foraging in winter was energetically costly. However, these
costs must be weighed against the benefits of avoiding exposure to low temperatures by
feeding under cover as well as the loss of collected food and possible injury associated
with aggressive interactions with conspecifics. Under moderate predation pressure in
both seasons, ice rats followed a central place foraging strategy to minimise predation
risk, always returning to a burrow entrance with forage collected elsewhere. However,
when no perceivable threat was observed, ice rats displayed ?optimal? foraging patterns
in summer similar to those recorded in the absence of predation pressure and only
returned to a burrow with forage as distance from that burrow increased, suggesting that
ice rats display facultative foraging decision making in response to multiple
environmental cues.
The distribution of occupied ice rat burrows was correlated against several
environmental factors to determine microhabitat requirements. Ice rat burrows were
situated in close proximity to herbaceous and wetland plants, but away from woody
vegetation, suggesting that habitat choice is related to the presence of food plants and
reduction of shade, facilitating short travel distances during foraging as well as
promoting basking.
Despite the physiological shortcomings of ice rats, the gut structure, foraging
behaviour, and habitat choice of the taxon are adapted for life in cold alpine habitats,
most likely by maximising energy intake. Similarities in foraging behaviour and habitat
use between O. s. robertsi with its closely-related arid-occurring relative Parotomys spp.
suggest phylogenetic influences, but it is possibly more a reflection of similar
phenotypic responses to the extreme habitats inhabited by these otomyines.
v
DEDICATION
In memory of my father
Wolfgang F. Schwaibold (1944-2000)
who supported me throughout my studies.
With thanks to my family:
Marianne and Marc
for believing in me.
vi
ACKNOWLEDGEMENTS
A huge thank you to my supervisor, Prof. Neville Pillay, for the opportunity to work on
such an interesting, yet challenging project, for his encouragement, support and advice,
and especially for his patience in teaching me to write scientifically.
A very special thank you to Andrea Hinze ? without her field work in Lesotho would not
have been as much fun or as entertaining.
Many thanks to Prof. Kevin Balkwill for jumping in when my co-supervisor resigned
and for helping me with the identification of my plant specimens.
I would like to thank the National Research Foundation (Grant number: 2053514) and
the University of the Witwatersrand for funding my study.
I am also grateful to everyone who helped me with field work over the last 4 years:
Hagen Hinze, without whom I still would not know how to use a dumpy level, Toby
Hibbits (its always good to have a man around who knows how to change a tyre on a
4x4), Tracy Aenmey for her patience in digging up soil samples, Ruben Gutzat and
especially Claire Knoop for never failing to make us laugh.
Thank you to Bongi Twala, Graig Marais and Stefan Muritz for data collection at Katse
Dam.
vii
A special thank you to Jonathan Aldous and the staff of the Sani Top Chalet who really
made Sani Top feel like a home away from home.
Lastly I owe a great deal of thanks to my family for their support and advice from
overseas and to Marc and his family for their continued interest, support and patience.
viii
CONTENTS
DECLARATION ............................................................................................................. ii
ABSTRACT .................................................................................................................... iii
DEDICATION ................................................................................................................. v
ACKNOWLEDGEMENTS ........................................................................................... vi
LIST OF CONTENTS..................................................................................................viii
LIST OF FIGURES........................................................................................................ xi
LIST OF TABLES........................................................................................................xiii
CHAPTER ONE: Introduction...................................................................................... 1
Small mammals in alpine environments................................................................ 1
Habitat selection and use ....................................................................................... 2
Physiological adaptations ...................................................................................... 3
Behavioural adaptations......................................................................................... 4
Foraging behaviour.................................................................................... 5
The ice rat Otomys sloggetti robertsi..................................................................... 6
Phylogeny .................................................................................................. 7
Description................................................................................................. 8
Habitat ....................................................................................................... 8
Foraging behaviour and diet ...................................................................... 9
Sociality and reproduction....................................................................... 10
Physiological considerations ................................................................... 11
Motivation for the study ...................................................................................... 12
The study area...................................................................................................... 15
Arrangement of the thesis.................................................................................... 16
References............................................................................................................ 16
CHAPTER TWO: The gut morphology of the African ice rat, Otomys
sloggetti robertsi, shows adaptations to cold environments and
sex-specific seasonal variation (J. Comp. Physiol. B 173:653-
659). ............................................................................................................. 25
ix
CHAPTER THREE: Behaviour of free-living African ice rats Otomys
sloggetti robertsi: strategies for coping with harsh
environments .............................................................................................. 32
Abstract................................................................................................................ 32
Introduction ......................................................................................................... 33
Materials and Methods ........................................................................................ 37
Study site ................................................................................................. 37
Marking and behavioural observations.................................................... 38
Data analysis............................................................................................ 40
Results ................................................................................................................. 41
Discussion............................................................................................................ 46
References............................................................................................................ 53
CHAPTER FOUR: Fexible foraging decision-making in the African ice
rat, Otomys sloggetti robertsi...................................................................... 58
Abstract................................................................................................................ 58
Introduction ......................................................................................................... 59
Materials and Methods ........................................................................................ 63
The study site........................................................................................... 63
Behavioural observations......................................................................... 64
Data analysis............................................................................................ 66
Results ................................................................................................................. 67
Discussion............................................................................................................ 72
References............................................................................................................ 76
CHAPTER FIVE: Foraging in the African ice rat Otomys sloggetti
robertsi: conflicting demands of energy conservation and
predator avoidance..................................................................................... 81
Abstract................................................................................................................ 81
Introduction ......................................................................................................... 82
Materials and Methods ........................................................................................ 85
Study site ................................................................................................. 85
x
Behavioural observations......................................................................... 86
Data analysis............................................................................................ 88
Results ................................................................................................................. 89
Discussion............................................................................................................ 92
References............................................................................................................ 99
CHAPTER SIX: Microhabitat selection by the ice rat Otomys sloggetti
robertsi in Sani Valley, Lesotho............................................................... 105
Abstract.............................................................................................................. 105
Introduction ....................................................................................................... 106
Study area .............................................................................................. 109
Materials and methods....................................................................................... 109
Transect sampling.................................................................................. 110
Plant community structure..................................................................... 110
Diet ........................................................................................................ 112
Data analysis.......................................................................................... 112
Results ............................................................................................................... 113
Transect sampling.................................................................................. 113
Plant community structure..................................................................... 113
Diet ........................................................................................................ 116
Discussion.......................................................................................................... 117
References.......................................................................................................... 120
CHAPTER SEVEN: Discussion ................................................................................. 124
Gut structure ...................................................................................................... 124
Seasonal variation in aboveground behaviour patterns ..................................... 125
Foraging strategies ? predation versus thermoregulation.................................. 126
Habitat choice .................................................................................................... 127
Biology of other otomyines ............................................................................... 127
Coping with cold conditions.............................................................................. 129
Conclusions and further research....................................................................... 132
References.......................................................................................................... 133
xi
LIST OF FIGURES
CHAPTER ONE:
Figure 1. Mean annual minimum and maximum air temperatures at Sani Top,
Lesotho ....................................................................................................... 13
CHAPTER THREE:
Figure 1. The number of incidences of hoarding per hour displayed by male and
female O. s. robertsi in the mornings and afternoons in summer and
winter.. ........................................................................................................ 43
Figures 2. Positive transitions in the sequential order of six behaviours and
disappearance underground for Otomys s. robertsi in a) summer and b)
winter.. ........................................................................................................ 44
Figures 3. Negative transitions in the sequential order of six behaviours and
disappearance underground for Otomys s. robertsi in a) summer and b)
winter. ......................................................................................................... 45
CHAPTER FOUR:
Figure 1. Mean percentage of foraging bouts spent at a central place and in situ
for male and female O. s. robertsi in summer and winter. ......................... 68
Figure 2. Percentage of foraging bouts made at various distances from a burrow
entrance by O. s. robertsi in summer and winter........................................ 69
Figure 3. Proportion of foraging bouts spent in situ for all distance categories in
summer and winter. .................................................................................... 69
Figure 4. Mean duration of time spent in situ by ice rats in summer and winter....... 70
Figure 5. Foraging areas visited by O. s. robertsi during foraging bouts for all
distance categories in summer .................................................................... 71
xii
Figure 6. Mean percentage of acid detergent fibre, protein and nitrogen in
grasses, herbaceous plants and wetland plants determined on a 100%
dry matter basis........................................................................................... 72
CHAPTER FIVE:
Figure 1. Mean number of foraging bouts spent per hour for O. s. robertsi at
Sani Top and at Katse Dam in the presence and absence of predators in
summer and winter. .................................................................................... 89
Figure 2. Mean percentage of foraging bouts spent in situ at various distances
from a burrow entranceby O. s. robertsi in summer and winter at Sani
Top and at Katse Dam in the presence and absence of predators............... 90
Figures 3. Mean frequency of foraging bouts at each distance category in summer
and winter at Sani Top (a) and at Katse Dam in the presence (b) and
absence (c) of predators.. ............................................................................ 91
Figures 4. Mean frequency of foraging bouts spent in situ in each distance
category by ice rats in summer and winter at Sani Top (a) and at Katse
Dam in the presence (b) and absence (c) of predators................................ 93
Figure 5. Mean duration of time spent in situ by ice rats in summer and winter at
Sani Top (a) and at Katse Dam in the presence and absence (b) of
predators (c). ............................................................................................... 94
CHAPTER SIX:
Figure 1. Map of the study site near Sani Top, Lesotho, indicating the position of
the colonies selected for study as well as the transect lines. .................... 111
Figure 2. Mean percentage frequencies of various plant species in areas occupied
and unoccupied by O. s. robertsi. ............................................................. 115
xiii
LIST OF TABLES
CHAPTER TWO:
Table 1. Comparison of gastrointestinal morphology of Otomys sloggetti robertsi,
Otomys angoniensis and Otomys irroratus caught in summer... ................. 28
Table 2. Mean lengths of divisions of digestive tract as percentages of total gut
length in O. sloggetti robsertsi, O. angoniensis and O. irroratus caught
in summer..................................................................................................... 29
Table 3. Lengths of divisions of the hindgut expressed as a percentage of total
hindgut length (excluding stomach), and the ratio of large to small
intestine length of mesic- and arid-occurring otomyines. ............................ 29
Table 4. Comparison of gastrointestinal morphology of male and female O.
sloggetti robsertsi trapped in summer and winter........................................ 29
CHAPTER THREE:
Table 1. Comparison of seasonal, time of day and gender influences on the
proportion (x 100) of time that Otomys s. robertsi engaged in six
behaviours and time spent underground. ..................................................... 42
Table 2. Significant seasonal negative and positive transitions for between
sample effects for six behaviours and disappearance belowground
displayed by O. s. robertsi. .......................................................................... 47
CHAPTER SIX:
Table 1. Mean percentage vegetation cover and dominant species/vegetation
types in areas occupied and unoccupied by O. s. robertsi in summer and
winter.......................................................................................................... 114
Table 2. Dominant species of the woody and herbaceous vegetation in areas
occupied and unoccupied by O. s. robertsi at Sani Top and the plant
species consumed by ice rats...................................................................... 116
1
CHAPTER ONE: Introduction
Small mammals in alpine environments
The survival and reproductive fitness of any animal depends on its ability to allocate
sufficient time and energy to a range of competing demands such as foraging,
maintenance and reproduction (Schoener, 1971; Schultz et al., 1999). In alpine and
subalpine environments this ability becomes even more crucial. Small mammals in
these conditions must cope not only with low temperatures in summer and extreme cold
and snow in winter, but with unpredictable and changing weather patterns throughout
the year (Happold, 1998). In addition, the growing season is restricted to a few months
and food availability is limited (Killick, 1978; Barash, 1989), and it is therefore
essential that small mammals maximise their energy intake (e.g. through foraging)
while at the same time minimising energy loss (e.g. by exposure to low temperatures).
However small mammals, due to their small body size, are prone to rapid heat loss and
this, combined with their high metabolic rates, reduces their ability to store large energy
reserves internally (Schultz et al., 1999).
To cope with the demands of living in cold environments, small mammals
display several morphological, physiological and behavioural adaptations. These include
thicker pelage (Chappell, 1980), torpor and hibernation (Geiser and Ruf, 1995), elevated
metabolic rates (Weiner and Heldmaier, 1987), modified gut structure (Bozinovic et al.,
1990), changes in body tissue (Quay, 1984), sun-basking (Geiser et al., 2002), social
huddling and nest-building (West and Dublin, 1984; Schultz et al., 1999).
The effects of cold and especially the presence of snow in winter have formed
the basis for a range of studies on the biology of small mammals in alpine and subalpine
environments (reviewed in Happold, 1998). While an animal?s physiology is
2
undoubtedly important for survival under these extreme conditions, habitat selection and
behavioural adaptations have also been found to affect the ability of animals to cope
(Johnson and Cabanac, 1982; Happold, 1998; Schultz et al., 1999).
Microhabitat selection and use
Generally, habitat selection describes the process by which animals make behavioural
decisions about where to live, which is reflected in their use of space (Stapp, 1997). For
many animals these behavioural decisions are based on hierarchical responses to
multiple habitat cues, although these responses are less obvious in small mammals as,
due to their small size and thus based on the size of their home range or dispersal range,
they can only sample a small area within an otherwise extensive and possibly diverse
habitat (Johnson, 1980).
Most animals are capable of some degree of habitat selection. As the main reason
for animal movement within a habitat is finding more rewarding foraging patches
(Charnov, 1976), suitable habitats are often chosen based on proximity to these food
patches. Other important factors influencing habitat choice are predation pressure, in
which case animals tend to select habitats with more vegetation cover, and interspecific
competition (Falkenberg and Clarke, 1998) which may result in microhabitat partitioning
(Jorgensen, 2004).
In cold environments, other factors such as protection from low ambient
temperatures may influence microhabitat selection. Endotherms, for example, will
choose microhabitats with temperatures as close to their thermoneutral zone as possible
(Johnson and Cabanac, 1982), thereby reducing the need for active thermoregulation.
Furthermore, vegetation and topography may affect the microclimate experienced by
small mammals and may therefore significantly determine their microhabitat choice
3
within the limits of their distribution (Happold, 1998). Woodchucks Marmota monax
select suitable hibernating habitats based on sufficient plant cover such as brush or
forested areas which provide better insulation against prolonged persistence of snow
(Barash, 1989). However, general macroclimatic phenomena do not necessarily
correspond with the microclimate that small mammals may be experiencing, since the
climate (e.g. temperature, wind factor) close to the ground may differ from that above
the shrub layer (Geiger, 1965). For example, the shade from shrubs results in lower
temperatures at ground level than air temperatures, whereas at night shrubs act as a form
of insulation and buffer the ground against low ambient temperatures (Eurola et al.,
1984).
Physiological adaptations
Most small mammals living in cold environments cope with these extreme conditions
through physiological adaptations. Torpor and hibernation are common in high altitude
species such as marmots (Marmota spp.; Barash, 1989; M?ller, 1986). Other species
generate heat through shivering and non-shivering thermogenesis (e.g. degus Octodon
degus and the leaf-eared mouse Phyllotis darwini; Nespolo et al., 2001) or conserve heat
through increased vasoconstriction in appendages (Adolph and Lawrow, 1951) and
increased insulation through integumentary changes or added body fat in winter is
common in non-hibernating small mammals (e.g. deer mice Peromyscus spp. and voles
Microtus spp.; Quay, 1984). Morphological modifications may also serve a
physiological role. Bozinovic et al. (1990) found that the South American field mouse
Abrothrix andinus, a non-hibernating rodent found in the cold and harsh environments of
the Andes, showed significant increases in the length and mass of the whole gut, and the
4
lengths of the small and large intestine, which are likely to improve energy uptake
during digestion.
Behavioural adaptations
In addition to physiological adaptations to extreme cold conditions, most small
mammals also show behavioural adaptations (T?rk and Arnold, 1988), including social
huddling, nest-building and sun-basking. While communal huddling and nest-building
increase thermal insulation and reduce energy loss in rodents (Glaser and Lustick, 1975;
Andrews and Belknap, 1986), basking facilitates energy gain during cold periods via
absorption of radiant energy (Barash, 1989). Even though the most common behavioural
means of acquiring energy in small mammals is through foraging (Schultz et al., 1999),
energy gained from radiant heat may compensate for the limited energy intake from
lower quality food under cold conditions and allow for metabolic needs to be met. There
is growing evidence that mammals employ basking as a means of rewarming after
torpor, thus allowing for lost heat to be restored without any thermoregulatory costs
(Geiser et al., 2002). Other studies have found mammals to bask for thermal comfort and
energy conservation (Bartholomew and Rainy, 1971).
Nevertheless, in cold environments small animals are faced with conflicting
demands of gaining energy through foraging and energy conservation through reduced
exposure to low temperatures (Johnson and Cabanac, 1982). Also, time spent foraging
reduces the time spent in passive energy acquisition (e.g. basking), which in turn affects
overall energy gain. Therefore, small mammals usually display behavioural flexibility by
partitioning their time and energy spent on foraging, basking, huddling and other
maintenance behaviours (Schultz et al., 1999).
5
Foraging behaviour
Under natural conditions an animal?s fitness is directly affected by its ability to allocate
time and energy to finding, handling and consuming food, without impacting on the time
and energy spent on other behaviours (Schoener, 1971; Bautista et al., 1998), which is
the basis for optimal foraging theory. There are many demands on an animal?s time such
as sleeping or resting, nest maintenance and searching for mates, so that foraging will
not occupy all of the day (reviewed by McFarland, 1975). In addition, foraging is also
strongly influenced by numerous external factors such as predation risk (Lima and Dill,
1990) and food availability (Bautista et al., 1998), the presence of conspecific
competitors (Schr?pfer and Klenner-Fringes, 1991; Krebs and Davies, 1993) and
prevailing weather conditions (Stouder, 1987; Sergio, 2003). Grey squirrels Sciurus
carolinensis, for instance, reject more profitable food items if they locate larger items of
less profitable food that could be consumed under cover (Lima and Valone, 1986), thus
trading off energy gain against predator avoidance when the most profitable areas for
foraging are also the most dangerous areas. As environmental conditions vary over time
(e.g. from daily variations to seasonal changes), an animal may need to modify its
foraging behaviour temporally in response to changing energy needs (Schultz et al.,
1999) and increased thermoregulatory challenges will affect foraging patterns and may
result in trade-offs between foraging efficiency and reduced exposure to extreme
temperatures (Johnson and Cabanac, 1982). For example, desert antelope ground
squirrels Ammospermophilus leucurus (Hainsworth, 1995) and thirteen-lined ground
squirrels Spermophilus tridecemlineatus (Vispo and Bakken, 1993) ?shuttle? between hot
desert surfaces where they forage and cool burrows where they escape high
temperatures. Likewise, the South American degu (Octodon degus) adjusts its activity
patterns in response to increasing ambient temperatures by increasing time spent in
6
shade cover (vegetation, rocks; Kenagy et al. 2004) or underground if shade is absent
(Kenagy et al. 2002). Further, Bozinovic et al. (2000) found that degus reduce time
spent foraging when ambient temperatures increased. Similar patterns could apply to
rodents in cold environments.
Commonly, animals exposed to cold conditions are found to adjust their
behaviour patterns to facilitate increased foraging and thus increasing overall energy
intake (see Johnson and Cabanac, 1982; Perrigo and Bronson, 1985). Similarly, seasonal
behavioural changes have also been reported in hibernating species such as marmots (see
Barash, 1989). In addition, hoarding is a common behavioural strategy displayed by
animals in cold environments and occurs when food is abundant in preparation for future
limitations as a result of unpredictable food supply associated with a drop in
temperatures (Wood and Bartness, 1996).
Of the many theories associated with optimal foraging models, central place
foraging refers to animals that repeatedly return to a fixed point with food items gathered
elsewhere (Bryant and Turner, 1982). Typical examples of this behaviour are found in
animals that hoard food such as in the grey squirrel (Lessels and Stephens, 1983), as well
as animals coping with predators, since returning to a central place (e.g. burrow) reduces
predation risk (Lima and Dill, 1990).
The ice rat Otomys sloggetti robertsi
The ice rat Otomys sloggetti robertsi is poorly studied, which may be because of the
remote areas it occupies. In this section I provide some information about the aspects of
the general biology of O. s. robertsi which are essential for the aims of the study and
interpretation of results presented in this thesis. For comparison, I also provide
information for its closest relatives for which published information is available.
7
Phylogeny
The murid rodent subfamily Otomyinae is widely distributed in sub-Saharan Africa
(Kingdon, 1974). Two genera are recognised within the subfamily - the vlei rats Otomys
and the whistling rats Parotomys. In southern Africa, six Otomys and two Parotomys
species exist (Meester et al., 1986). These species are distributed across the primarily
east-west southern African rainfall gradient (Davis, 1974; Skinner and Smithers, 1990)
with representatives occurring in both the wettest and driest habitats. While Brants?
whistling rat Parotomys brantsii and Littledale?s whistling rat Parotomys littledalei are
endemic to the arid regions of southern Africa, the genus Otomys has representatives in
both the mesic and arid regions of the subregion. The vlei rats Otomys angoniensis and
Otomys irroratus are adapted to mesic environments, while the bush Karoo rat Otomys
unisulcatus is found primarily in arid environments. The ice rat Otomys sloggetti
robertsi Hewitt, 1927 is one of five subspecies of O. sloggetti that occur in the mountain
regions of the eastern parts of southern Africa (De Graaff, 1981) and is endemic to the
southern African Drakensberg and Maluti mountains (Roberts, 1951). It shares with
other members of this family characteristics reflecting adaptation to a mesic environment
such as renal morphology (Pillay et al., 1994), yet unlike its close relatives, the
subspecies is confined to altitudes exceeding 2000m, restricting it to the subalpine
(1830-2895m) and alpine (2860-3484m) phytogeographic belts (defined by Killick,
1978). It is apparently restricted to the microthermal highlands of Lesotho (Willan,
1990) and is the only O. sloggetti that has been karyotyped (2n=42; Contrafatto et al.,
1992).
In terms of the phylogenetic relationships within the subfamily, evidence from
sperm structure (Bernard et al., 1990; 1991), allozyme electrophoresis (Taylor et al.,
1989) and immunoblot (Meester et al., 1992) analyses shows a dichotomy between the
8
arid species restricted to the western parts of southern Africa (P. brantsii, P. littledalei
and O. unisulcatus) and the mesic species found in the eastern parts (O. angoniensis and
O. irroratus). Interestingly, O. s. robertsi falls into the arid group despite living in the
eastern parts of southern Africa. However, recent mtDNA studies suggest that the
position of O. s. robertsi within this arid group is equivocal, indicating that the
phylogeny is not yet resolved (Maree, 2002).
Description
The pelage of ice rats is reddish-brown, soft and thick with rusty-yellow colouring at the
sides of the snout and behind the ears. They have relatively short tails (60-70mm) and
reduced ears (16-17mm; Willan, 1990). Adults can reach up to 150-170 mm in length
and weigh between 120g and 140g, and males tend to be about 10% larger than females
(Willan, 1990).
Habitat
Otomys s. robertsi is abundant in suitable habitats with gently sloping ground and
surface rocks and they apparently avoid steep slopes, deep valleys and boggy areas
(Willan, 1990). Colonies of ice rats construct underground burrows with several entrance
tunnels, although they are also reported to nest in rock crevices (Willan, 1990). These
burrows may provide suitable warm microhabitats with below-ground temperatures
being 1-2? C higher than above-ground ambient temperatures (Hinze, unpublished).
The name ?ice rat? reflects its habit of emerging from shelter to sun itself during cold
weather, particularly in winter when ice or snow are on the ground (Skinner and
Smithers, 1990).
9
Among the arid-adapted otomyines, the microhabitat distribution of O.
unisulcatus is apparently related to the presence of suitable woody plants for nesting and
food (Brown and Willan, 1991), whereas P. brantsii prefers areas with deep sandy soils
for the construction of its complex underground warrens (du Plessis and Kerley, 1991),
and P. littledalei is restricted to areas with good soil for burrowing and adequate cover
(Jackson, 2000). Among the mesic-adapted species, at least in O. irroratus habitat
selection appears to be influenced by the presence of adequate plant cover (Willan,
1982; Pillay, 1993).
Foraging behaviour and diet
All otomyines are specialist herbivores that feed more or less exclusively on green plant
material (Roberts, 1951), although there is slight directional modification of the diet,
depending on the availability of suitable food plants (Jackson and Spinks, 1998). While
mesophylic otomyines such as O. irroratus feed primarily on green plant material
(Perrin, 1980), the ice rat has a varied diet within the constraints of herbivory and has
been found to feed on floral parts of grasses and herbaceous plants as well as on leaves
and stems (U. Schwaibold, unpublished data). A similar diet breadth has been found in
O. unisulcatus (Brown and Willan, 1991).
Previous studies on P. brantsii have shown that its foraging patterns change from
summer to winter (Nel and Rautenbach, 1974). Foraging time, for instance, has been
found to change in relation to season, being shorter during the summer season as more
time is spent underground during hot days (Jackson, 1998). Furthermore, P. brantsii was
shown to be a central place forager and its foraging behaviour was strongly determined
by predation pressure (Jackson, 2001). This species forages within the limits of its
warren systems and ventures out from protection to gather food, while P. littledalei
10
hardly ever leaves the protection of bushes to forage (Coetzee and Jackson, 1999).
Similarly, solitary foraging by O. unisulcatus appears to be restricted to the immediate
vicinity of cover, while groups forage further away from a nest (Vermeulen and Nel,
1988).
Sociality and reproduction
Within the otomyine family, O. irroratus (Davis and Meester, 1981), P. brantsii and P.
littledalei (Jackson, 1999; 2000) are solitary living, while O. angoniensis and O.
unisulcatus sometimes live in small groups (Skinner and Smithers, 1990). Otomys s.
robertsi has also been seen to live in groups (Willan, 1990), although previous research
by Hinze (unpublished) suggests spatial variation in sociality, with ice rats displaying
temporal territoriality aboveground as a result of competition for resources, and social
behaviour belowground for huddling.
The breeding season of the ice rat extends from October to March and in
captivity ice rats have shown a gestation period of about 38 days and mean litter size of
1.44 young (Willan, 1990). In fact, the litter size of all southern African otomyine
species never exceeds five pups; perhaps a consequence of females having only four
nipples and the young nipple-clinging (Pillay, 2001). Young ice rats are born semi-
precocial (10.6 ? 12.2g), weaned at 16 days of age and sexual maturity is reached at 16
weeks in males and 11 weeks in females (Willan, 1990). Despite the harsh
environmental conditions in its alpine habitat, the reproductive biology of O. s. robertsi
is characterised by low reproductive output (i.e. long gestation period, small litter size,
low reproductive effort and fecundity and well-developed parental care), apparently due
to the stable microclimate created by underground nests, huddling and hoarding (Willan,
1990).
11
Physiological considerations
Otomys sloggetti robertsi is not physiologically adapted to the temperature extremes in
its habitats. Laboratory experiments done by Richter et al. (1997) have shown that
oxygen consumption (VO2) decreases linearly with increasing temperature between
0.7?C and 26.0?C, with little variation between 26-28?C, the range defined as the zone of
thermoneutrality. In response to noradrenaline injections, VO2 was found to be 2.84 ?
0.4 ml g-1 h-1, which differs only slightly from the values obtained for O. irroratus.
The lower critical temperature was determined to be 25.3?C. Further, O. s. robertsi can
tolerate temperatures higher than those which are experienced in its habitat (e.g. 34?C in
contrast to the range of temperatures in its natural environment which is 15-23?C). Its
metabolic rate was not found to be higher than predicted, but thermal conductance was
greater than expected. The ratio of percentage metabolic rate and percentage thermal
conductance was 0.87, which corresponds to values obtained for many arid/warm-
adapted mammals. Its metabolic rate is thus not enough to counteract the relatively high
rate of heat loss at low temperatures as suggested by the animal?s minimal thermal
conductance. Body temperature does however appear to remain fairly constant even at
low temperatures, which is energetically costly, as metabolic rates are almost twice as
high at low temperatures than within the thermoneutral zone (Richter et al., 1997).
Despite these physiological shortcomings to alpine habitats, ice rats do not occur
at lower altitudes which Richter et al. (1997) suggest may be a result of interspecific
competition with O. irroratus. Even so, ice rats show behavioural thermoregulation
through huddling and sun-basking in response to low temperatures (Skinner and
Smithers, 1990; Willan, 1990; Richter et al., 1997). Otomys. s. robertsi also shows some
morphological adaptation to the cold such as a short tail and ears (De Graaff, 1981;
Willan, 1990).
12
Motivation for the study
Over the past few years, several geomorphological and climatological studies focussing
primarily on high levels of erosion have been conducted in the eastern Lesotho
Drakensberg (see Grab, 1999; Grab and Deschamps, 2004). Jacot-Guillarmod (1963)
originally associated this mass erosion and soil loss with overgrazing by domestic
livestock, although little attention has been given to the possible impacts of indigenous
fauna on the grazing resource. In particular, the ice rat O. s. robertsi is believed to
significantly contribute to the erosion process by grazing and burrowing (S. Grab, pers.
comm.). Field observations by researchers of the School of Geography, Archaeology and
Environmental Studies at the University of the Witwatersrand have indicated that
overgrazing and thus mass erosion has occurred in areas where ice rat populations have
increased dramatically (S. Grab, pers. comm.).
For many animals, predation pressure plays an important role in regulating
population numbers (Lima and Dill, 1990; Wilson et al., 1998). However, based on my
observations (from 1999 to 2003) and those of Willan (1990), as well as anecdotal
reports from local Basotho shepherds, predation pressure on O. s. robertsi in my study
site in the Sani Valley appears to be negligible in summer and virtually absent in winter.
Instead, population numbers are apparently regulated by density-dependent mortality as
a result of limited resource availability during cold winters, as well as prolonged periods
of snowfall and low winter temperatures (Willan, 1990; Lynch and Watson, 1992). The
winters over the past few years have been relatively mild with little snowfall. Moreover,
while maximum temperatures have remained constant, minimum temperatures have
increased substantially over the last decade (Lesotho Weather Service; Figure 1), which
would account for the lower levels of snowfall and better survival of ice rats in the
Lesotho Drakensberg.
13
-10.00
-5.00
0.00
5.00
10.00
1992 1994 1996 1998 2000 2002 2004
M
in
im
um
T
em
pe
ra
tu
re
(?
C
)
0.00
5.00
10.00
15.00
20.00
25.00
1977 1980 1983 1986 1989 1992 1995 1998 2001 2004
M
ax
im
um
T
em
pe
ra
tu
re
(?
C
)
Figure 1. Mean (? SD) annual minimum (1992-2004) and maximum (1977-2004) air
temperatures at Sani Top, Lesotho.
14
Questions were raised by researchers of the School of Geography, Archaeology
and Environmental Studies about the biology of the southern African ice rat, and after an
extensive literature review it was clear that very little was known about this subspecies,
especially under natural conditions. Clearly, there was a need to study the biology of the
ice rat, in particular its foraging behaviour, given the concerns about its role in the
overgrazing of wetlands.
The ice rat presents a unique study animal since, unlike most alpine small
mammals, it does not hibernate or display torpor and is physiologically poorly adapted
to low temperatures (Richter et al., 1997). It is a strict herbivore, feeding on a low
quality diet. Moreover, in the absence of predation pressure in many parts of its
distribution, it is an ideal model for studying changes in foraging activity in response to
changing physiological demands from summer to winter. Although ice rats do show
some morphological and behavioural (e.g. short tails; communal huddling; constructing
underground burrows) adaptations (Willan, 1990; Richter, 1997), little else is known
about their biology, in particular how they maximise energy gain to meet
thermoregulatory demands, especially during cold periods. As foraging represents the
primary method of energy gain in animals (Schultz et al., 1999), I studied aspects of the
foraging biology of ice rats, including the gut structure, foraging behaviour and habitat
choice, as survival in these harsh conditions is likely to be achieved by behavioural and
morphological adaptations to maximise energy gain while minimising energy loss.
The broad aims of my study were to investigate the morphological and
behavioural characteristics and foraging decisions of ice rats for life in alpine habitats.
This study was driven primarily by the question how an animal that shows only limited
physiological adaptation to its environment modifies its foraging biology to compensate
15
for its physiological shortcomings. Chapter 2 provides information on the seasonal and
gender variation in gut morphology of O. s. robertsi and comparisons are made with its
mesic and arid relatives. The aim of this study was to investigate how the gut structure of
ice rats is adapted to cold environments. In Chapter 3, I conducted field observations
over three years to investigate the behavioural patterns of the ice rat in summer and
winter. The emphasis of this study was on how ice rats allocate time to various
behaviours and how seasonal climatic changes affect behaviour. Underpinned by the
theoretical models of optimal foraging theory, Chapter 4 examines the foraging
decisions of O. s. robertsi in the absence of predation, and Chapter 5 provides a
comparison of the foraging behaviour of ice rats experiencing different levels of
predation pressure with the aim of comparing the interplay between predation risk and
climatic factors on foraging decisions. The final experimental chapter (Chapter 6)
focuses on the environmental factors determining microhabitat selection to explore
possible relationships between habitat choice and foraging behaviour.
The study area
Due to the inaccessibility of most of the Drakensberg region in Lesotho, the more easily
accessible Sani Valley area was chosen as the primary area of study. My main study site
was located south of the Sani River (29? 37? S; 29?14? E) about 5km west of Sani Top at
an altitude of about 2900m and was situated in one of the Sani tributary valleys. A second
site was selected later in my study, situated about 7 km south of Katse Dam along the
Sengu River at an altitude of about 2000m (29?21' S; 28?32' E). The Drakensberg/Maluti
massive consists of an ancient basaltic plateau marked by deep, steep-sloping valleys. As
a result of water seepage to lower ground, extensive bogs are formed in these valleys. Soil
depth decreases as gradient increases (Killick, 1978). Mean air temperature in the Lesotho
16
highlands ranges from 0?C in winter to 6?C in summer (Grab, 1997). Rainfall is high
(about 1200mm per annum) and snow can be expected at any time of the year (Willan,
1990). Shrubs and herbs (annuals and biennials, woody cushion plants and succulents,
aquatics and alien plants) are common and trees are absent.
Arrangement of the thesis
This thesis consists of the present introductory chapter, a general discussion and
conclusion chapter (Chapter 7) and the main body comprising five experimental chapters
(Chapters 2-6). The experimental chapters are written as manuscripts for publication,
with Chapter 2 on gut structure having already been published in the Journal of
Comparative Physiology B (Vol. 173, p. 653-659). Because of the format of this
publication, which includes substantial background information as well as an abstract
and a separate reference list, the subsequent chapters have been formatted in the same
manner. The tables and figures have been sequentially numbered for each chapter and
the pages of the thesis are numbered in sequence. References are provided in each
chapter.
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ORIGINAL PAPER
The gut morphology of the African ice rat, Otomys sloggetti
robertsi, shows adaptations to cold environments
and sex-specific seasonal variation
Accepted: 26 June 2003 / Published online: 19 August 2003
Springer-Verlag 2003
Abstract We studied the gut morphology of the ice rat
Otomys sloggetti robertsi, a non-hibernating murid
rodent endemic to the sub-alpine and alpine regions of
the southern African Drakensberg and Maluti moun-
tains. The gut structure of O. s. robertsi is well adapted
for a high fibre, herbivorous diet, as is the case with other
members of its subfamily Otomyinae. Despite the broad
similarity in gross gut morphology with mesic- and arid-
occurring otomyines, O. s. robertsi has a larger small
intestine, caecum, stomach volume and parts of the
colon, which we suggest are adaptations for increased
energy uptake and/or poor diet quality in alpine envi-
ronments. However, O. s. robertsi has a smaller larger
intestine than other otomyines, perhaps because it
occupies a mesic habitat. Seasonal sexual differences
occurred, with females increasing dimensions of the
stomach, small intestine length, caecum, and large
intestine in summer. Sexual asymmetry in gut morphol-
ogy may be related to increased energy requirements of
females during pregnancy and lactation, indicating
phenotypic plasticity in response to poor quality vege-
tation and a shorter growing season in alpine habitats.
Keywords Otomys sloggetti robertsi ? Gut morphology ?
Climate ? Diet ? Habitat
Introduction
Interspecific comparative studies have shown that
rodent digestive tract morphology largely reflects diet
(Vorontsov 1962; Perrin and Curtis 1980). Herbivorous
rodents, for instance, have a more developed large
intestine and caecum than omnivores of the same family,
since fibrous plant material is broken down by microbial
digestion in the caecum, forming compounds that can
then be absorbed by the large intestine (Lange and
Staaland 1970). Thus, a larger caecum and large intes-
tine are adaptations for a high fibre diet (Sperber 1968;
Perrin and Curtis 1980; Schieck and Millar 1985).
Generally, a decrease in food quality results in an
increase in gut length and capacity due to an increase in
energy demand (Gross et al. 1985; Hammond and
Wunder 1991). In addition, the hindgut is important in
water re-absorption in small mammals, and there are
usually changes in the relative size of the large intestine
in animals inhabiting arid regions, reflecting the need for
water conservation (Lange and Staaland 1970; Woodall
1987).
Many small herbivores occurring in cold regions will
either hibernate or exhibit short periods of torpor,
allowing them to conserve energy during the most
demanding times (e.g. winter). In contrast, non-hiber-
nating animals, such as arvicoline rodents (lemmings
and voles), must maintain a constant body temperature
by heat production or conservation, which is achieved
through morphological, physiological or behavioural
adaptations. The rate of energy acquisition may be
limited by seasonal changes in food quality as well as by
digestive tract morphology and physiology (Bozinovic
et al. 1990). The need for increased energy gain as well as
decreased diet quality requires increased food con-
sumption (Green and Millar 1987). Therefore, animals
such as the prairie vole (Microtus ochrogaster) that face
the challenge of cold temperatures as well as a high fibre
diet have a larger caecum and small intestine rather than
a larger large intestine (Hammond and Wunder 1991).
Increases in the length of sections of the gut are neces-
sary for digestion of food of high fibre content, since
food is retained for a longer time, enabling digestibility
of several components of the diet (Silby 1981). Fur-
thermore, a larger gut may increase the rate of digestion
J Comp Physiol B (2003) 173: 653?659
DOI 10.1007/s00360-003-0374-4
U. Schwaibold ? N. Pillay
Communicated by G. Heldmaier
U. Schwaibold ? N. Pillay (&)
Ecophysiological Studies Research Group,
School of Animal Plant and Environmental Sciences,
University of the Witwatersrand, Private Bag 3,
2050 Johannesburg, WITS, South Africa
E-mail: Nevillep@biology.biol.wits.ac.za
Tel.: +27-11-7176459
Fax: +27-11-4031429
and absorption due to an increase in transporters in the
gut lining, thus rendering a greater quantity of energy
per unit time (Karasov and Diamond 1988). However, a
larger gut is probably more important for the processing
of a greater quantity of food at a given time.
Digestive tract morphology is sometimes intraspecif-
ically labile. Changes in gut morphology can occur when
food quality varies between seasons (Hammond 1993),
and reflects changes in energy requirements due to low
temperatures in winter (Green and Millar 1987). In-
creased energy requirements in winter coupled with a
poor-quality diet may necessitate the consumption of
larger quantities of food. If retention time and digest-
ibility remain constant, an increase in gut dimensions is
expected, unless a decline in food quality corresponds
with a decrease in activity and thus energy requirements
(Green and Millar 1987). Conversely, increases in energy
demand because of lactation or increased activity can
lead to an increase in gut length in summer (Hammond
1993; Kenagy 1987). For example, female Djungarian
hamsters (Phodopus sungorus sungorus; Weiner 1987)
and wild rabbits Oryctolagus cuniculus (Silby et al. 1990)
demonstrate an increase in size of several digestive
organs (predominantly small intestine and caecum)
during reproductive periods, apparently to meet the
need for increased energy requirements during
pregnancy and lactation.
The murid rodent subfamily Otomyinae is widely
distributed across the primarily east-west southern
African rainfall gradient (Skinner and Smithers 1990).
All otomyines studied are specialist herbivores, feeding
more or less exclusively on green plant material includ-
ing shoots, stems, leaves and grasses, although some
species feed on fruit and flowers (Roberts 1951; Nel and
Rautenbach 1974; Curtis and Perrin 1979; Jackson
1998). Perrin and Curtis (1980) reported that the gas-
trointestinal tract of the Otomyinae is the most specia-
lised of any South African herbivorous rodent, and
includes a large and complex caecum and a well-devel-
oped large intestine.
Data on the gastrointestinal morphology of the
Otomyinae are available for two mesic-occurring
species, the vlei rat, Otomys irroratus, and the Angoni
vlei rat, Otomys angoniensis (Perrin and Curtis 1980) and
three arid-occurring species, the bush Karoo rat, Otomys
unisulcatus, Brants? whistling rat, Parotomys brantsii and
Littledale?s whistling rat, Parotomys littledalei (Jackson
and Spinks 1998). There is broad similarity in the gross
gastrointestinal anatomy among the species, but the
arid-occurring forms have an elongated large intestine
and a simultaneous reduction in the small intestine,
which may be related to water conservation (Jackson
and Spinks 1998).
In contrast to these other otomyine rodents, no
comparable data are available for the gut morphology of
the ice rat, Otomys sloggetti robertsi. The ice rat shares
some characteristics (e.g. kidney morphology; Pillay
et al. 1994) with mesic-occurring otomyines, yet unlike
other otomyines, O. s. robertsi is confined to altitudes
exceeding 2000 m, and is endemic to the southern
African Drakensberg and Maluti mountains. This dis-
tribution restricts them to the cold, harsh sub-alpine and
alpine phytogeographic belts (Killick 1978).O. s. robertsi
does not hibernate and apparently is physiologically
poorly adapted to the harsh alpine habitats, and instead,
its physiology (e.g. low metabolic rate and high thermal
conductance) is more typical of its congeners occurring
in warmer environments at lower altitudes (Richter et al.
1997). In addition, oxygen consumption of O. s. robertsi
decreases linearly with an increase in ambient tempera-
ture between 0.7 C and 26.0 C, and the zone of ther-
moneutrality is reached between 26 C and 28 C, which
is unusually high for a rodent living in a habitat that
rarely experiences such high temperatures (Richter et al.
1997). To cope with low temperatures, O. s. robertsi
employs behavioural (e.g. sun-basking, huddling) and
morphological (e.g. short tails and small ear pinnae)
adaptations (Willan 1990). O. s. robertsi has a varied diet
within the constraints of herbivory (Rowe-Rowe 1986;
U. Schwaibold, personal observation).
In this study, we compared the gastrointestinal
morphology of the ice rat with that of two mesic-
occurring otomyines and to the published data available
for three arid-occurring otomyines. We predicted that
the gut morphology of ice rats would be similar to
mesic-occurring otomyines.We also asked two questions:
1. Do ice rats show modifications of the gastrointestinal
morphology associated with increased energy
requirements in the cold, harsh environments they
inhabit?
2. Are there seasonal differences in the gut structure
between the sexes in response to increased energy
demands on females imposed by pregnancy and
lactation, and ultimately by the short growing season
in alpine environments?
Materials and methods
Eight male and eight female adult O. s. robertsi were captured in
summer (October 2000, January and February 2001) and eight
female and seven male adults were captured in winter (June and
August 2000) at Sani Top in the Lesotho Drakensberg (2937? S;
2914? W). Sixteen adult O. angoniensis and O. irroratus (eight of
each sex) were captured during summer (November 2000 and
January 2001), respectively, at Hazelmere (2934? S; 3101? E) and
Karkloof (2917? S; 3011? E) in KwaZulu-Natal Province, South
Africa. Individuals were live-trapped within 4 days of each other
during each trapping session. Captured animals were removed from
traps within 30 min of entering traps and killed (overdosed with IM
Sodium Pentobarbitone 200 mg, Benzyl Alcohol 2%, dosage: 1 ml/
kg body weight). Thereafter, mass (to nearest gram measured with
a Pescola spring balance) and head-body length (to nearest milli-
metre) were established for all animals before their digestive tracts
from the gastro-oesophageal junction to the anus were removed
and preserved in 70% alcohol for no longer than 2 weeks (range
10?14 days) until examination at the University of the Witwaters-
rand. We assumed that any size and shape changes in the tissue
because of fixation would have been similar across all samples. To
test this assumption, we took linear measurements from each of
654
three O. s. robertsi, O. angoniensis and O. irroratus digestive tracts
immediately after they were killed and again after preservation for
14 days in 70% alcohol. All digestive tracts showed a similar 1?2%
reduction in size.
The preserved digestive tract of each individual was cleared of
surrounding adipose and connective tissue, blotted to remove
excess alcohol, and weighed with its contents to the nearest 0.01 g
with a bench top Mettler balance. The digestive tract was
straightened but not stretched and, after measuring the total length
of the gut on a clean flat surface to the nearest 0.1 mm, the tract
was separated into stomach, small intestine, caecum and large
intestine. The following mass, linear measurements and counts
were then recorded (after Perrin and Curtis 1980; Jackson and
Spinks 1998): stomach empty mass (i.e. cleared of contents), length,
width and volume; length and mean width of small intestine; length
and mean width of large intestine; number of spiral loops in the
colon; number of caecal haustra, height and mean width of haustra,
caecum volume, mass (empty) and mean width and diameter of
caecum. Width in each case was determined as an average of five
separate measurements along the length of the organ. The volume
of the stomach and caecum were calculated using the formula pr2l,
where r is average organ radius (calculated as the mean of five
measurements taken along the length of the organ) and l is organ
length. The following proportions were also determined: length of
hindgut to body length; stomach, small, large intestine and caecal
lengths to total gut length.
Statistical analysis
Comparisons among and within taxa were done using an analysis
of variance (ANOVA) for single measurements, and a multivariate
analysis of variance (MANOVA) was used for several dependent
variables (e.g. measurements from the same organ, such as stomach
width and length; Zar 1996). A Kruskal-Wallis ANOVA was used
for comparisons of ratios (Zar 1996). Tukey HSD and Dunn?s
post-hoc tests were used to identify specific differences in para-
metric and non-parametric tests respectively. All tests were two-
tailed and a was set at 0.05.
Regression analyses did not show any significant correlation
between body mass, length and gut morphometrics. Accordingly,
gut morphometrics were not standardised relative to body mass or
length.
Results
Interspecific comparisons in summer
Interspecific comparisons were made with animals
caught during summer. Body mass varied significantly
across the three taxa (F2,42=16.59; P<0.0001), with
O. s. robertsi (mean?SE: 130.8?4.6 g) weighing more
than O. angoniensis (106.8?2.1 g) and O. irroratus
(106.7?3.0 g); there were no sex (F1,42=0.3; P>0.05) or
taxa?sex interactions (F2,42=2.8; P>0.05). In terms of
head-body length, O. s. robertsi (149.88?2.46 mm) and
O. irroratus (150.06?4.20 mm) were significantly longer
than O. angoniensis (131.38?2.02 mm; F2,42=20.87;
P<0.0001), and males were significantly longer than
females (F1,42=10.70; P<0.01). There was a significant
taxa?sex interaction (F2,42=11.41; P<0.001), with
O. irroratus males having the greatest and O. angoniensis
females the shortest lengths.
O. s. robertsi had the longest gut compared to
O. angoniensis and O. irroratus (Table 1). The stomach
of all three taxa was a simple unilocular sac with very
little morphological specialisation. The stomach of O. s.
robertsi was larger (volume) compared to the other taxa,
while stomach length was similar in O. s. robertsi and
O. irroratus but shorter in O. angoniensis. In terms of the
post-gastric morphology, O. s. robertsi had the largest
small intestine (length) and caecum (mass, length, vol-
ume) but smallest large intestine (length; Table 1). The
length of the small intestine was almost double the
length of the large intestine in O. s. robertsi but was close
to parity in O. angoniensis and O. irroratus (Table 1).
While O. s. robertsi had the most spiral loops in the large
intestine, it also had the shortest hindgut to head-body
ratio (Table 1). The hindgut (large intestine and caecum)
showed female-biased sexual asymmetry across all three
taxa, and there were taxa?sex interactions that mirrored
the trends observed in the taxa comparisons, although it
is notable that female O. s. robertsi had heavier stomachs
(empty mass) than their male conspecifics.
Expressed as a percentage of total gut length, the
stomach length of O. s. robertsi was similar to that of
O. irroratus and greater than that of O. angoniensis
(Table 2). The relative contribution of the small intestine
and caecum to the length of the gastrointestinal tract
was significantly greater in O. s. robertsi than in the
other two otomyines (Table 2). Conversely, the large
intestine was shorter in O. s. robertsi than in O. angon-
iensis and O. irroratus. The relative length of the caecum
was greater in females than in males.
Comparison of the gut structure of the three mesic-
occurring otomyines with published data of three arid-
occurring otomyines indicated that O. s. robertsi had a
longer small intestine and caecum than the other
otomyines (Table 3). It is also apparent that the large
intestine is relatively longer in the arid-occurring taxa
(especially in Parotomys littledalei) than in the mesic-
occurring taxa. In contrast, the caecum is relatively
larger in the mesic-occurring taxa. Consequently, the
small:large intestine ratio is greater in the mesic-occur-
ring than the arid-occurring otomyines (Table 3). Fur-
thermore, the small:large intestine ratio of O. s. robertsi,
which is greater than all the other otomyines, is more
than double that of P. littledalei whose distributional
range includes the most arid regions occupied by any of
the otomyines.
Seasonal and sexual comparisons in O. s. robertsi
There was an increase in the height of the caecal haustra
in O. s. robertsi caught in summer compared to those
trapped in winter (Table 4). The length of the small
intestine showed female-biased sexual asymmetry. The
statistical interaction between season and sex is impor-
tant, since it allows us to answer our question about
whether there are sex differences in gut morphology
between summer and winter. In general, females caught
in summer had larger guts than males in both seasons
and females in winter (Table 4). From winter to summer,
655
Tabl
e
1
C
om
pa
ris
on
o
fg
as
tr
oi
nt
es
tin
al
m
o
rp
ho
lo
gy
o
fOtomy
ssloggett
iroberts
i(Os
r),
Otomy
sango
niensi
s
(O
a)
an
d
Otomy
sirroratu
s
(O
i)caugh
ti
n
summer
.
Value
s(mas
si
n
grams
,
linea
r
measurement
s
in
millimetres
,volum
e
in
centimetre
s
squared
)giv
en
a
s
mea
n
(?SE)
.(
SI
sm
a
ll
intestine
,L
I
larg
e
intestine
,n
s
no
t
significant
)
Parameter
s
O
.s
.
roberts
i
O
.angoniensi
s
O
.irroratu
s
Statistic
s
Male
s
Female
s
Male
s
Female
s
Male
s
Female
s
Tax
a
Se
x
Tax
a?
Se
x
Tota
llengt
h
o
fgu
t
753.73(33.14
)
831.53(33.93
)
706.51(10.72
)
677.19
(9.85
)
655.61(7.40
)
668.98(7.01
)
**Osr>Oa=O
i
n
s
n
s
Sto
m
ac
h
Empt
y
mas
s
1.02(0.36
)
1.52(0.17
)
1.20(0.10
)
1.15(0.12
)
1.32(0.08
)
1.30(0.08
)
n
s
n
s
***Os
r
(f)>Os
r(m
)
Widt
h
23.47(1.41
)
23.60(1.40
)
23.74(0.31
)
23.53(
0.36
)
24.50(0.63
)
24.06(0.40
)
n
s
n
s
n
s
Lengt
h
35.64(1.65
)
32.96(2.34
)
25.25(1.19
)
28.13(
0.77
)
31.38(0.26
)
31.50(1.52
)
***Osr>Oi>O
a
n
s
n
s
Volum
e
5.32(0.51
)
5.08(0.51
)
2.35(0.37
)
1.91(0.07
)
3.08(0.46
)
3.09(0.39
)
***Osr>Oi=O
a
n
s
n
s
Sm
al
lintestin
e
Lengt
h
359.56(18.63
)
419.41(20.64
)
297.93(4.23
)
291.85
(4.27
)
254.86(5.73
)
255.91(5.09
)
***Osr>Oa>O
i
n
s
**Os
r
(m
,f)>other
s
Widt
h
4.50(0.33
)
4.88(0.35
)
4.81(0.29
)
3.93(0.26
)
3.91(0.07
)
3.88(0.04
)
***Osr=O
a>
O
i
n
s
n
s
Larg
e
intestin
e
Lengt
h
218.33(0.23
)
226.67(12.16
)
260.33(5.14
)
240.10
(6.19
)
264.30(2.26
)
251.96(5.44
)
***Oi=Oa>Os
r
n
s
n
s
Widt
h
4.75(0.16
)
5.13(0.30
)
5.10(0.23
)
5.09(0.14
)
5.14(0.13
)
4.74(0.16
)
n
s
n
s
n
s
N
um
be
ro
fs
pi
ra
ll
oo
ps
5.
25
(0.
25
)
5.
54
(0.
27
)
4.
20
(0.
21
)
4.
12
(0.
16
)
4.
38
(0.
18
)
3.
75
(0.
25
)
*
*
*
O
sr
>
O
a=
O
i
n
s
n
s
SI:L
I
1.65(0.08
)
1.86(0.05
)
1.15(0.02
)
1.22(0.09
)
0.96(0.01
)
1.02(0.02
)
***Osr>Oa>O
i
n
s
-
a
Hindgut:bod
y
lengt
h
1.49(0.06
)
1.48(0.09
)
1.91(0.02
)
1.91(0.05
)
1.63(0.03
)
1.8
4
(0.07
)
***Oa>Oi>Os
r
*f>
m
-
a
C
ae
cu
m
Empt
y
mas
s
2.96(0.16
)
2.84(0.12
)
1.83(0.05
)
1.76(0.05
)
1.83(0.05
)
2.05(0.08
)
***Osr>Oi=O
a
n
s
Os
r
(m
,f)>other
s
Lengt
h
140.19(9.85
)
152.49(8.45
)
122.99(3.82
)
117.12
(2.30
)
105.08(3.71
)
129.62(4.45
)
***Osr>Oa=O
i
*f>
m
n
s
Mea
n
widt
h
16.92(1.52
)
22.74(0.61
)
22.63(1.35
)
25.63(
1.02
)
21.38(0.68
)
20.00(1.74
)
n
s
*f>
m
Os
r
(m)<other
s
Numbe
ro
fhaustr
a
28.00(1.67
)
30.00(1.00
)
28.13(2.15
)
27.3
8
(1.34
)
29.13(0.77
)
26.88(1.04
)
n
s
n
s
n
s
Heigh
to
fhaustr
a
5.25(0.37
)
5.25(0.25
)
5.13(0.23
)
4.75(0.25
)
5.25(0.25
)
5.25(0.25
)
n
s
n
s
n
s
Widt
h
o
fhaustr
a
4.38(0.26
)
4.88(0.23
)
4.00(0.00
)
5.13(0.30
)
4.25(0.16
)
4.88(0.13
)
n
s
n
s
n
s
Volum
e
19.96(2.58
)
24.10(1.41
)
13.79(3.84
)
12.38(
4.66
)
11.15(3.11
)
13.73(3.99
)
*Osr>Oa=O
i
n
s
n
s
*
P<0.05
;*
*
P<0.01
;**
*
P<0.00
1
(2
wa
y
ANOVA
,2
wa
y
MANOV
A
an
d
Kruskal
lWalli
stests)
.Tuke
y
HS
D
an
d
Dunn?
spost-ho
cresult
sindicate
d
if
sig
nifican
tdifference
soccurre
d
a
Kruskal
lWalli
s
ANOV
A
doe
sno
t
perfo
rm
tes
t
656
females increased their gut dimensions as follows:
stomach empty mass (25%), small intestine length (9%),
and caecum length (11%) and width (14%). Seasonal
differences in these dimensions ranged from <1?5% in
males. Within-season intersexual comparisons revealed a
largely female-biased size and mass difference in sum-
mer, which was not as pronounced or reversed in winter,
as follows (summer, winter): stomach empty mass (26%,
Table 3 Length of divisions of the hindgut expressed as a percentage of total hindgut length (excluding stomach), and the ratio of large to
small intestine length of mesic- and arid-occurring otomyines. Values for mesic-occurring taxa were obtained from this study and for the
arid-occurring taxa from Jackson and Spinks (1998)
Parameters Mesic-occurring Arid-occurring
O. s. robertsi O. angoniensis O. irroratus O. unisulcatus P. brantsii P. littledalei
Small intestine 51.12 43.74 40.59 43.20 41.20 36.70
Large intestine 28.08 38.36 40.26 43.60 45.40 50.90
Caecum 20.80 17.90 19.15 13.20 13.30 12.40
Small: large
intestine ratio
1.82 1.14 1.00 0.99 0.90 0.72
Table 2 Mean (?SE) lengths of divisions of digestive tract as percentages of total gut length in O. sloggetti robertsi (Osr), O. angoniensis
(Oa) andO. irroratus (Oi) caught in summer
Parameters O. s. robertsi O. angoniensis O. irroratus Statistics
Stomach 4.37(0.20) 3.87(0.13) 4.75(0.12) ***Osr=Oi>Oa
Small intestine 49.02(0.80) 42.65(0.31) 38.54(0.35) ***Osr>Oa>Oi
Large intestine 28.11(0.54) 36.14(0.39) 39.00(0.56) ***Oi=Oa>Osr
Caecum 18.50(0.64) 17.34(0.21) 17.70(0.58) *Osr>Oa=Oi
*P<0.05; ***P<0.001 (Kruskall Wallis tests). Dunn?s post-hoc results indicated if significant differences occurred
Table 4 Comparison of gastrointestinal morphology of male (m) and female (f) O. sloggetti robertsi trapped in summer (S) and winter
(W). Values (mass in grams, linear measurements in millimetres, volume in centimetres squared) given as mean (?SE)
Parameters Summer Winter Statistics
Males Females Males Females Season Sex Season?Sex
Total length of gut 753.7(33.14) 831.5(33.92) 816.0(32.15) 820.4(20.27) ns ns ns
Stomach
Empty mass 1.02(0.07) 1.52(0.17) 1.36(0.06) 1.14(0.03) ns ns ***S(f)>S(m)
Width 23.47(1.41) 23.59(1.40) 21.14(1.99) 26.88(1.16) ns ns ns
Length 35.64(1.65) 32.96(2.34) 32.29(1.54) 34.75(1.22) ns ns ns
Volume 5.32(0.51) 5.08(0.51) 4.30(0.43) 5.88(0.37) ns ns ns
Small intestine
Length 359.56(18.63) 419.41(20.64) 399.71(17.98) 404.50(13.95) ns *f>m S(f)>S(m)
Width 4.50(0.33) 4.88(0.35) 4.93(0.07) 5.00(0.33) ns ns ns
Large intestine
Length 218.33(10.14) 226.67(12.16) 237.14(12.36) 237.13(8.70) ns ns ns
Width 4.75(0.16) 5.13(0.30) 4.86(0.46) 5.13(0.23) ns ns ns
Number of spiral loops 5.25(0.25) 5.54(0.27) 5.29(0.36) 5.63(0.38) ns ns ns
SI:LI 1.66(0.08) 1.86(0.05) 1.70(0.06) 1.72(0.07) - - **S(f)>othersa
Hindgut:body length 2.50(0.09) 2.49(0.15) 2.54(0.15) 2.62(0.07) - - nsa
Caecum
Empty mass 2.96(0.16) 2.84(0.12) 2.86(0.16) 2.56(0.12) ns ns ns
Length 140.19(9.85) 158.49(4.45) 146.86(5.68) 141.13(6.57) ns ns *S(f)>others
Mean width 16.92(1.52) 22.74(0.61) 21.57(1.70) 19.50(1.87) ns ns *S(m)<others
Number of haustra 28.00(1.67) 30.00(1.00) 31.00(1.35) 31.88(0.69) ns ns ns
Height of haustra 5.25(0.37) 5.25(0.25) 4.71(0.47) 4.38(0.46) *S>W ns ns
Width of haustra 4.38(0.26) 4.88(0.23) 4.00(0.31) 4.38(0.26) ns ns ns
Volume 19.96(1.09) 24.10(2.58) 22.14(2.58) 25.10(1.41) ns ns ns
*P<0.05; **P<0.01; ***P<0.001 (2 way ANOVA, 2 way MANOVA and Kruskall Wallis tests). Tukey HSD and Dunn?s post-hoc
results indicates if significant differences occurred
aKruskall-Wallis ANOVA applied to ratio data by regarding each season and sex as separate entities
657
2%; winter favoured males), small intestine length (18%,
8%), and caecum length (7%, <1%) and width (13%,
3%; winter favoured males).
Discussion
Like the other otomyines (both mesic-occurring and
arid-occurring), the gut morphology of O. s. robertsi is
adapted for herbivory and for a diet of high fibre foods.
A relatively large caecum and large intestine are con-
sidered the best indicators of herbivory, since these
structures allow for longer retention of ingesta
(Vorontsov 1962; Green and Millar 1987) and a greater
surface area for microbial activity to break down cellu-
lose (Schieck and Millar 1985). Field observations con-
firm our findings since the diet of ice rats consists almost
exclusively of floral parts of grasses and herbaceous
plants, as well as leaves and stems (U. Schwaibold,
unpublished data).
O. s. robertsi has a longer gastrointestinal tract than
the two other mesic-occurring taxa (O. angoniensis and
O. irroratus), and a longer and larger small intestine and
caecum than the other otomyines, including the
three arid-occurring taxa (O. unisulcatus, P. brantsii,
P. littledalei). These differences indicate modification of
the digestive tract morphology of O. s. robertsi, and it is
apparent that the small intestine and the caecum are
important features. Increased dimensions of these
organs are characteristic of both hibernating and non-
hibernating small mammals in cold environments (Silby
1981; Karasov and Diamond 1988; Hammond and
Wunder 1991), and appear to be the case also in
O. s. robertsi.
A larger small intestine allows for increased retention
time of ingesta (Silby et al. 1990) and provides a larger
surface area for absorption of digested food, which can
be considered an adaptation to cold temperatures, since
it would improve the uptake of high-energy components
in the diet. An increase in the capacity of the caecum
appears to maximise digestibility of a high-fibre diet
(Hammond and Wunder 1991; Lee and Houston 1993).
Green and Millar (1987) reported that deer mice
(Peromyscus maniculatus) responded to a decrease in diet
quality and temperature between seasons by increasing
the length of the small intestine and caecum and showing
only slight changes in large intestine morphology.
Although the large intestine is an important feature in
the gut of herbivores, it is relatively short in O. s. robertsi
compared to the other otomyines. The large intestine is
important in water absorption, nutrient absorption and
possibly enhancing digestive efficiency (Woodall 1987).
An increase in large intestine size is expected when there
is a high-fibre diet, although the main function of the
large intestine is water resorption (Lange and Staaland
1970). Because of the similarity in the diets of the oto-
myines, Jackson and Spinks (1998) attributed the rela-
tively longer large intestine in the arid-occurring
otomyines to a need to improve water retention in arid
areas. The O. s. robertsi used in this study inhabit wet-
land habitats where it feeds primarily on wetland plants
with high water contents. Much of its water is obtained
from plants it consumes (Willan 1990), so that water
may not be a limiting resource, thereby obviating the
need for a longer large intestine.
The increased number of loops and folds of the colon
in O. s. robertsi compared to the mesic-occurring
O. angoniensis and O. irroratus may facilitate increased
nutrient absorption (Schieck and Millar 1985). The large
intestine is important for nutrient absorption from
fibrous material broken down in the caecum (Sperber
1968). The transverse muscular folds and loops possibly
aid in slowing down passage through the large intestine,
allowing more time for energy to be absorbed and fur-
ther promoting mixing and movement of the material
broken down in the caecum which in turn may promote
the fermentation process (Bruorton and Perrin 1988).
Stomach length and volume were significantly greater
in O. s. robertsi than O. angoniensis and O. irroratus.
Stomach fermentation is highly advantageous as it
occurs just before protein digestion. A larger stomach
volume furthermore provides a greater surface area for
enzyme release (Perrin and Curtis 1980), thus promoting
digestion. Also, larger quantities of ingested material
can be digested at any one time. Lee and Houston (1993)
maintained that an increase in stomach volume in bank
(Clethrionomys glareolus) and field voles (Microtus
agrestis) could decrease the time spent feeding in the
open, thus reducing the risk of predation. It is possible
that a larger stomach volume allows an animal to con-
sume more food at one time, thus reducing the frequency
of foraging bouts. It is uncertain whether the large
stomach volume in O. s. robertsi has similar (secondary)
functions in the exposed environments it occupies, as
predation risk is low (U. Schwaibold, unpublished data),
but structures that allow for minimal exposure to low
ambient temperatures may be adaptive. It is known that
increasing the rate of food intake results in an increased
passage rate and thus a decrease in digestibility of food
(Silby 1981; Gross et al. 1985). On the other hand, an
increase in gut volume allows ingesta to pass at a slower
rate as it is retained in each organ for a longer period.
Therefore, the longer total gut length in O. s. robertsi
may increase retention time and thus digestibility of
food.
During summer, female O. s. robertsi showed an
increase in the size of those regions of the gut that
are essential for increased energy uptake, such as caecum
and small intestine. Males did not show such increases.
Similar findings were reported in wild rabbits (Oryctol-
agus cuniculus; Silby et al. 1990) and the South American
field mouse (Abrothrix andinus; Bozinovic et al. 1990), a
non-hibernating rodent found in the cold and harsh
environments of the Andes. Bozinovic et al. (1990)
reported significant increases in the length and mass of
the whole gut and the lengths of the small and large
intestines in winter, and significant differences in the
dimensions of several digestive organs were found
658
between males and females during the reproductive
season. These female-biased sexual differences in gut
dimensions between seasons are thought to reflect the
need to improve energy acquisition during pregnancy
and lactation (Weiner 1987; Sibly et al.1990). Female
O. s. robertsi may be similarly constrained by the poor
quality of the vegetation and the shorter growing season
in their alpine habitats (Willan 1990).
In conclusion, our study reveals significant differences
in the gastrointestinal morphology of O. s. robertsi on
two levels. Interspecific comparisons within the otomy-
ines suggest that the gut morphology of O. s. robertsi is
adapted for cold environments because of the need to
increase energy intake, although the gut structure may
reflect also the poor quality diet of ice rats (U. Schwai-
bold, unpublished data). Intraspecific variation occurs
during the reproductive season as energy demands differ
between male and female ice rats, indicating a degree of
phenotypic plasticity. Clearly, there is still a need for
further physiological and biochemical studies to fully
explain the results presented here.
Acknowledgements We thank Andrea Hinze, Claire Knoop, Toby
Hibbits and Ruben Gutzat for technical assistance. Funding was
provided by the National Research Foundation (grant number Gun
2053514) and the University of the Witwatersrand. We declare that
the experiments comply with the current laws of the Republic of
South Africa. Animal ethics clearance number AESC 2000/21/2a.
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659
32
CHAPTER THREE:
Behaviour of free-living African ice rats Otomys sloggetti robertsi: strategies for
coping with harsh environments
Abstract
In this study, environmental influences on the behaviour of the southern African ice rat,
Otomys sloggetti robertsi, a herbivore endemic to the high altitude regions of the
southern African Drakensberg and Maluti mountains, were investigated. Ice rats do not
hibernate and are physiologically poorly adapted to low temperatures. O. s. robertsi was
studied in its natural environment during both summer and winter and the behaviour of
adult males and females was recorded by analysing the duration of behaviours as well as
sequential transitions among behaviours. Gender and time of day did not influence ice
rat behaviour and in both seasons ice rats spent most of their day foraging and basking,
with much time spent in their underground burrows. Seasonal comparisons revealed that
ice rats spent significantly more time foraging in winter whereas they remained
belowground for longer periods of time in summer. Hoarding behaviour increased
significantly from summer to winter and females showed higher levels of hoarding in
summer than males. Sequential analysis of behaviours showed that most behavioural
transitions in winter were strongly focused on foraging behaviours (searching, gathering
and consuming food), basking and aggressive interactions. Behavioural transitions in
summer were characterised by fewer transitions, with social interactions and basking
decreasing in frequency. The data suggest that seasonal changes influence the motivation
for, performance of, and sequences of behaviours in ice rats.
Key words: Otomys sloggetti robertsi, seasonal behaviour patterns, behavioural
sequences, thermoregulation, motivation
33
Introduction
Thermoregulation in cold environments imposes great energetic demands on
small mammals and coping with low temperatures is achieved by one or more of several
physiological, morphological and/or behavioural adaptations (Johnson and Cabanac,
1982; Eckert et al., 1988). Hibernation or entering into torpor are important
physiological responses to low temperatures (Eckert et al., 1988; Geiser and Ruf, 1995).
When faced with ambient temperatures below their thermoneutral zones, small mammals
which cannot reduce their metabolic rates need to modify their behaviour by either
increasing calorific intake (e.g. by feeding) and mobilising stored energy (Johnson and
Cabanac, 1982) or by reducing energy expenditure through basking and retreating into
thermally stable shelters (Schultz et al., 1999).
However, time spent acquiring energy (e.g. feeding) reduces the time spent in
passive energy acquisition (e.g. basking) which would reduce overall energy loss, so that
animals need to partition their time and energy among conflicting behavioural and
physiological demands in order to maximise fitness benefits. In cold environments such
trade-offs are crucial for survival and determine the behavioural strategy employed by
small mammals in these habitats (Schultz et al., 1999). Several small animal species
such as chicks (Rovee-Collier et al., 1997), house mice (Perrigo and Bronson, 1985) and
rats (Johnson and Cabanac, 1982) reduce time spent on energetically costly behaviours
in cold temperatures while increasing feeding time.
Behavioural strategies used by small mammals to regulate their body temperature
can be temporally labile depending on prevailing environmental conditions. Behavioural
responses can occur over a short term, such as when an animal moves from a shady,
wind-protected burrow entrance to a sunny foraging site (Johnson and Cabanac, 1982),
or they could occur in response to seasonal fluctuations in temperature (long-term
34
response). Bertolino et al. (2004) maintain that seasonal changes in the behaviour of
Finlayson?s squirrels Callosciurus finlaysonii may be related to internal factors such as
altered physiological demands (e.g. reproduction) and external factors such as
differences in food type and quantity between seasons, and also predation risk. Activity
patterns of the Arctic black-capped marmot Marmota camtschatica bungei change
markedly throughout summer, increasing rapidly after the animals emerge from
hibernation in spring and gradually decreasing towards late autumn (Semenov et al.,
2001). While behavioural changes from summer to late autumn/early winter in
preparation for hibernation (e.g. Barash, 1989; Semenov et al., 2001) have been studied
for several years, research dealing with the winter behaviour patterns of non-hibernating
alpine and subalpine animals has only recently emerged (see Kenagy et al., 2002).
Hoarding food is an important behavioural strategy employed by animals living
in cold environments (see Ellison, 1996). Typically, hoarding occurs when food is
abundant and accessible in preparation for future shortages due to climatic changes and
unpredictable food supply (Wood and Bartness, 1996) and is therefore common in
hibernating species. However, caching can also occur for other reasons. For example,
some diurnal animals store food for consumption overnight, as occurs in Brants?
whistling rat Parotomys brantsii (Jackson, 2001). Many rodents also collect plants for
use as nesting material (Barash, 1989). Whatever the reasons, time spent hoarding
reduces time spent performing other behaviours and it is clear that when faced with
thermoregulatory challenges, caching has to be traded off against feeding and basking
behaviours.
The African ice rat Otomys sloggetti robertsi is a good model for studying
behavioural strategies in harsh environments. This medium-sized (121-143g) murid
rodent is confined to the altitudes above 2000m and is endemic to the harsh
35
environments of the subalpine and alpine Drakensberg and Maluti mountains of southern
Africa (Killick, 1978). Importantly, although it occupies some of the coldest habitats in
the subregion, O. s. robertsi does not hibernate and apparently shows poor physiological
adaptations to cold temperatures, such as an elevated metabolic rate and a thermoneutral
zone above ambient temperature (Richter et al., 1997), thus making the taxon
particularly vulnerable to temperature extremes (Willan, 1990; Lynch and Watson,
1992). Instead, ice rats display a range of morphological (e.g. small tail, ear pinnae) and
behavioural (e.g. sun-basking, huddling) adaptations to cope with the low temperatures
(Willan, 1990; Richter, 1997). Ice rats live in colonies of up to 16 individuals and
construct complex underground burrows, into which they retire when temperature and
radiation levels are high in summer (Hinze et al., submitted).
Like all other members of its subfamily Otomyinae (De Graaff, 1981; Skinner
and Smithers, 1990), O. s. robertsi is strictly herbivorous, feeding on a wide range of
plant material (Willan, 1990). None of the otomyines are ruminants (see Perrin and
Curtis, 1980), necessitating frequent foraging bouts to acquire food to meet metabolic
demands. In a recent study I reported that, although there are broad similarities in the
overall gut morphology of ice rats compared with other mesic- and arid-living
otomyines, O. s. robertsi has a larger small intestine, caecum and stomach, which may
be adaptations for increased energy uptake and/or poor diet quality in cold alpine
environments (Schwaibold and Pillay, 2003; Chapter 2). In addition, female ice rats
increase the size of their gut in summer compared to winter, which apparently
corresponds to times of greater energy need during the breeding season; male gut
dimensions remain more or less unchanged seasonally (Schwaibold and Pillay, 2003).
Previous observations by Willan (1990) and by us, as well as anecdotal reports
by local Basotho shepherds in my study site in the Sani Valley, indicate that predation
36
pressure on ice rats is minimal in summer and virtually absent in winter, possibly due to
excessive hunting of predators by local inhabitants (Willan, 1990). Mortality rates of ice
rats appear to be regulated by snowfall and low winter temperatures (Lynch and Watson,
1992). Predation risk is an important determinant of the foraging behaviour of small
mammals (Bozinovic and Simonetti, 1992; Kotler et al., 1994; V?squez, 1994; Lima,
1998) but in the absence of high predation levels it is possible that, at least at my study
site, ice rat behaviour is primarily determined by environmental factors such as
temperature, particularly between seasons.
Ice rats are easily observed in their natural habitat as they are diurnal, quickly
habituate to the presence of observers, and because they inhabit areas with short
vegetation. Despite this, little is known of the behaviour of ice rats in their natural
environment. Even observations of their foraging and basking behaviour, which have
been noted by several workers (e.g. Willan, 1990; Lynch and Watson, 1992), are
anecdotal, despite these behaviours taking up much of their time as well as being
important behavioural adaptation for thermoregulation.
The present study was designed to compare the aboveground diurnal behaviour
of free-living ice rats between summer and winter. Generally, I asked whether O. s.
robertsi displays seasonally varying behavioural strategies, and how ice rats trade off
between various activities, particularly foraging and other behaviours, in winter when
food quality is poor (Schwaibold and Pillay, 2003). Specifically, five questions were
asked: 1) If ice rats are physiologically poorly adapted to cold environments, do they
show seasonal differences in behaviour, that is, do they display higher levels of foraging
and basking in winter than in summer to meet thermoregulatory demands? 2) Since
environmental conditions change during the course of the day, do ice rats adjust their
behaviour from morning to afternoon by increasing levels of hoarding and foraging in
37
the afternoon before they retire into burrows for the night, and increasing levels of
basking in the morning after they emerge from their burrows? 3) Because of the
energetic demands of pregnancy and lactation, I expected that females would forage for
longer in summer than males, but I also asked whether the increased gut capacity of
females in summer might offset the need to increase time spent foraging. 4) Is hoarding
behaviour greater in winter than in summer to compensate for the shorter foraging time
available due to shorter day length? 5) Do females hoard more food in summer
compared to males to meet the energetic requirements of reproduction?
To answer these questions, the duration of behaviours displayed by individual ice
rats was recorded quantitatively. Such data are useful for understanding how animals
distribute their time among various behaviours but do not tell us anything about the
structure of the behaviour (Spruijt et al., 1992). Behaviours are not static and do not
usually occur in discrete bouts. With this in mind, the structure of the behaviour of ice
rats was analysed using sequential transition matrices, since these may be more revealing
of changes in activity of an animal and are perhaps more likely to show trade-offs
between behaviours from moment to moment (Bakeman and Gottman, 1997).
Materials and Methods
Study site
Fieldwork was conducted on a 6 ha study site located in one of the Sani River valleys
(29?37? S; 29?14? E) about 5 km west of Sani Top in the south-eastern Maluti
mountains, Lesotho, at an altitude of about 2900 m. The study area was located along the
edge of one of the many wetlands in the valley. Weather conditions in the Lesotho
highlands are characterised by relatively low temperatures (mean temperatures around
0?C in winter and 6?C in summer; Grab, 1997) and high rainfall (mean annual rainfall is
38
1200 mm), and snow can be expected at any time of the year (Willan, 1990). These high
plateaus of Lesotho are prone to strong winds blowing towards the escarpment during
most of the day, although the early morning hours are usually calmest. Mist is common,
providing valuable moisture for plants (Hilliard and Burtt, 1987). Shrubs and herbs
(annuals and biennials, woody cushion plants and succulents, aquatics and alien plants)
are found most commonly in the Sani Valley and trees are absent. Vegetation in the
study area did not exceed 50 cm in height in the ice rat colonies.
Marking and behavioural observations
Experiments were conducted monthly in summer (October to March) and in winter (May
to August). During these periods, metal live traps (26 x 9 x 9 cm), baited with a mix of
fruits and vegetables (e.g. apple, cucumber, lettuce, spinach), were set during the early
morning and late afternoon when ice rats are most active. Traps were checked every 30
minutes to minimise the time that trapped individuals were exposed to lethal
temperatures. Trapped animals were weighed (to the nearest gram), sexed, fitted with a
uniquely coloured plastic cable tie neck band (length 200 mm, width 4.7 mm) and
released at the point of capture. Females were fitted with a white neck band and males
with a black one. A distinctive colour combination of insulation tape was taped on the
neck bands for individual identification. Collared individuals that were trapped later in
my study did not show any signs of distress or injury due to the neck bands. These
trapping and marking procedures were approved by the Animal ethics committee of the
University of the Witwatersrand (clearance number 2000/21/2a).
The behaviour of 30 adult ice rats (14 males and 16 females) in summer and of
another 28 adults (13 males and 15 females) in winter was studied. Care was taken to
observe the animals on days with similar weather conditions in each season.
39
Observations of focal individuals were made from a raised surface (about 1 m above the
ground) from a distance of approximately 5 to 20 metres, depending on the position and
movement of the individual in the landscape. Occasionally, 10x50 binoculars were used
when a focal individual was not clearly visible with the naked eye. Focal individuals
were observed for a total of five sessions per season, each session lasting one hour.
Because of seasonal differences in the timing of aboveground activity (i.e. mostly in the
morning and afternoon in summer and for most of the day in winter), observation
schedules were standardised by observing focal individuals in the mornings and
afternoons in both seasons: 05h00-12h00 and 13h30-17h30 in summer and 08h00-12h00
and 13h30-17h00 in winter. A total of two or three sessions were conducted per
individual in the morning and afternoon; whenever possible, the same animal was not
observed in the morning and afternoon of the same day.
Using continuous focal sampling (Martin and Bateson, 1986), the duration of six
behaviours was scored: 1) consuming (feeding on/grazing/ingesting food); 2) searching
for food (moving between food patches/sampling food); 3) gathering food (collecting
plant material, be it food or non-food plants, from a patch; it excludes actual
consumption or transport of food); 4) basking/stationary (upright posture without
locomotion mainly for basking or occasionally for vigilance); 5) social (socio-negative
and socio-positive) behaviour, and 6) burrow maintenance (cleaning out and re-
tunnelling of burrow entrances). The time spent belowground was also recorded, but it
was not known what animals did during this time. The number of incidences of hoarding
was also noted. Hoarding was assessed as the frequency of food transported by a given
individual into a burrow (the individual usually remained underground for no longer
than 5-8 seconds, indicating that food was not consumed).
40
Data analysis
Data for each focal individual were converted to proportions of the total time it was
observed in the morning or afternoon sessions. Data sets were arcsine transformed and
analysed using the general linear model (GLM) analysis for multiple dependents, in
which season, time of day (morning or afternoon) and sex were the fixed response
variables and the six behaviours and proportion of time spent underground were the
dependent variables. Specific differences were tested using Tukey post-hoc tests.
Incidences of hoarding between seasons and between morning and afternoon observation
sessions were compared using a ?2 test with Yates? correction. Two tailed tests were
used throughout and ? = 0.05.
The behaviour of ice rats was also analysed using sequential transition matrices,
as described by Van den Berg et al. (1999). Using the software Matman? (de Vries et
al., 1993), the sequence of all behaviours and disappearance underground were
transformed into transition matrices for each individual animal. These matrices
contained succeeding behaviours in the columns and the preceding behaviours of the
same individual in the rows. Transition matrices were summed per season, gender and
time of day. These summed matrices were used to calculate adjusted residuals, which
represented the difference between the observed and the expected values for the
transition frequency. Both positive (transitions occurring more often than expected by
chance) and negative (transitions occurring less often than expected by chance) residuals
were calculated and expressed according to a Z-distribution (for details see Van den
Berg et al., 1999). Since this method generates effects only within, but not between,
independent factors (e.g. season), matrices of adjusted residuals for each individual ice
rat were generated and the data set was analysed using a 3-way GLM analysis, in which
season, sex and time of day were fixed effects variables and a particular behaviour
In both seasons, O. s. robertsi spent more than 50% of its aboveground activity
consuming food and in stationary behaviour (i.e. mostly sun-basking; Table 1). In
addition, ice rats spent a large proportion of the remaining time in their underground
burrows. Statistical tests revealed that there were highly significant seasonal differences
in behaviours (F7,102 = 12.50; p<0.001) due largely to higher levels of gathering and
consuming food and basking behaviour in winter, and more time spent belowground in
summer (Table 1). Neither time of day (F7,102 = 1.21; p>0.05) nor sex (F7,102 = 0.85;
p>0.05) had any influence on the behaviour displayed. Likewise, no combination of the
interactions between season, gender and time of day had any influence on behaviours.
Results
transition (e.g. gathering-consuming) was the dependent variable; negative and positive
transitions were analysed separately and Tukey post-hoc tests were used to reveal
specific differences. Using these results, drawings for positive and negative matrices for
each season only were generated; drawings for gender and time of day are not provided
here for the sake of simplicity and since they influenced <5% of all transitions.
Hoarding behaviour was observed significantly more often in winter than in
summer (?21 = 39.60; p<0.001), both in the mornings (?21 =14.36; p<0.001) and the
afternoons (?21 = 7.30; p<0.01; Figure 1). Hoarding was greater in summer afternoons
compared to summer mornings, but this difference was not significant (?21 = 2.72;
p>0.05). This pattern was reversed in winter, with the incidence of hoarding increasing
in the mornings, but again this increase was not significant (?21 = 0.65; p>0.05). No
gender differences occurred in the number of hoarding incidences in winter mornings
(?21 = 0.14; p>0.05) or afternoons (?21 = 0.09; p>0.05; Figure 1), or in summer mornings
(?21 = 0.01; p>0.05) or afternoons (?21 = 1.08; p>0.05).
41
42
Table 1. Comparison of seasonal, time of day and gender influences on the proportion (x 100) of time that Otomys s. robertsi engaged in six
behaviours and time spent underground. Data presented as Mean (+SE).
Summer Winter
Morning Afternoon Morning Afternoon
Parameter Female Male Female Male Female Male Female Male
Gathering food *** 1.6 (0.6) 1.1 (0.5) 1.5 (0.4) 1.8 (0.6) 3.7 (0.7) 4.1 (1.0) 4.6 (1.5) 6.5 (1.5)
Searching for food 1.6(0.4) 1.2 (0.3) 1.7 (0.4) 1.1 (0.2) 1.5 (0.3) 1.1 (0.3) 1.6 (0.9) 2.7 (0.6)
Consuming food ** 33.6 (2.4) 33.2 (3.2) 35.3 (2.5) 28.8 (2.0) 43.9 (2.9) 36.8 (5.0) 41.6 (3.7) 36.7 (2.6)
Stationary/Basking* 28.7 (3.1) 35.1 (2.9) 31.6 (4.6) 30.8 (3.6) 36.1 (3.1) 37.2 (5.4) 38.9 (4.4) 36.8 (1.9)
Social behaviour 0.06 (0.02) 0.04 (0.02) 0.14 (0.12) 0.05 (0.03) 0.13 (0.07) 0.01 (0.01) 0.06 (0.04) 0.79 (0.29)
Burrow maintenance 1.5 (0.6) 0.7 (0.3) 0.6 (0.2) 0.5 (0.1) 1.3 (0.5) 1.7 (0.6) 0.7 (0.3) 1.8 (0.4)
Time underground*** 33.0 (3.4) 28.7 (4.1) 29.1 (3.6) 37.0 (2.7) 13.5 (1.9) 19.2 (2.8) 12.6 (3.5) 25.2 (4.5)
Asterisks = significant seasonal differences in behaviour: * p <0.05; ** p<0.01; *** p<0.001 (Tukey post-hoc tests)
There were six two-way negative transitions in summer (Figure 3a) and five in
winter (Figure 3b). Four transitions (consuming food and social behaviour, gathering
food and stationary/basking, gathering food and burrow maintenance, consuming food
and disappearance belowground) occurred less often than chance in both seasons. Other
food and stationary/basking, and stationary/basking and disappearance underground (all
in winter).
There were fewer two-way positive transitions in summer (Figure 2a) than in
winter (Figure 2b). In both seasons, strong two-way transitions occurred between burrow
maintenance and disappearance belowground (underground), and consuming and
gathering food. Seasonally-unique two-way transitions occurred between burrow
maintenance and social behaviour, stationary/basking and social behaviour, consuming
Figure 1. The number of incidences of hoarding per hour displayed by male and female
O. s. robertsi in the mornings and afternoons in summer and winter. The number of
hours of observation is shown above each bar.
0
0.2
0.4
0.6
0.8
1
1.2
1.4
morning afternoon morning afternoon
43
Summer Winter
Fr
eq
ue
nc
y
male
N=25 N=48
N=31 N=40
N=30
female
N=38
N=28 N=24
44
Consuming
Gathering
Stationary/
Basking
Underground
SearchingSocial
Burrow
Maintenance
Consuming
Gathering
Stationary/
Basking
Underground
Searching
Social
Burrow
Maintenance
(a) (b)
Figures 2. Positive transitions in the sequential order of six behaviours and disappearance underground for O. s. robertsi in a) summer and b)
winter. Transitions are depicted by lines and the thickness of the lines indicate the adjusted residual values in the transition matrix - thin lines =
p<0.01; thick lines = p<0.001.
Figures 3. Negative transitions in the sequential order of six behaviours and disappearance underground for O. s. robertsi in a) summer and b)
winter. Transitions are depicted by lines and the type and thickness of the lines indicate the adjusted residual values in the transition matrix -
dashed lines = p<0.05; thin lines = p<0.01; thick lines = p<0.001.
45
Consuming
Gathering
Stationary/
Basking
Underground
SearchingSocial
Burrow
Maintenance
(a) (b)
Consuming
Gathering
Stationary/
Basking
Underground
SearchingSocial
Burrow
Maintenance
46
two-way negative transitions were between burrow maintenance and consuming food
and between searching for food and disappearance belowground in summer, and
between gathering food and social behaviour in winter.
A total of 40 positive and 40 negative transitions were analysed for between
independent factor effects. Nineteen positive and 17 negative transitions were
influencedby season; sex and time of day influenced a total of four and three transitions
respectively and are not considered further. One positive transition occurred significantly
more often in summer than winter and 16 positive transitions occurred more frequently
in winter than in summer (Table 2). Five transitions occurred less often than predicted by
chance (i.e. negative transitions) in summer compared to winter, whereas eight negative
transitions were more common in winter than summer (Table 2). The relationship
between gathering and time spent underground (which demonstrates the sequence
leading to hoarding) was significantly stronger in winter. Unlike the ?2 tests, sequential
analyses revealed that females were significantly more likely to hoard food than males,
particularly in summer. Social interactions (predominantly socio-negative) followed
various behaviours more often in winter than in summer.
Discussion
The present study examined the diurnal behaviour of a non-hibernating, alpine
rodent, the ice rat O. s. robertsi, in its natural habitat, and tested whether ice rats have
different behavioural strategies in summer and winter and at different times of the day. I
also asked whether males and females behaved differently because of sex-specific
reproductive investment and previously reported sex-specific differences in gut structure
(Schwaibold and Pillay, 2003). My findings indicate that the diurnal activity of ice rats
47
Table 2. Significant seasonal negative and positive transitions for between sample
effects for six behaviours and disappearance belowground displayed by O. s. robertsi.
Seasonal effects were derived from post-hoc tests from GLM analyses.
Sequence
From To Seasonal effects
Negative Transitions
Consuming food Time underground winter > summer
Stationary/Basking summer > winter
Gathering food Time underground summer > winter
Searching for food winter > summer
Social behaviour winter > summer
Stationary/Basking winter > summer
Searching for food Consuming food winter > summer
Gathering food summer > winter
Social behaviour Consuming food winter > summer
Gathering food winter > summer
Stationary/Basking Burrow maintenance summer > winter
Gathering food winter > summer
Time underground Gathering food summer > winter
Positive Transitions
Burrow maintenance Searching for food winter > summer
Social behaviour winter > summer
Consuming food Searching for food winter > summer
Gathering food Time underground winter > summer
Social behaviour summer > winter
Consuming food winter > summer
Burrow maintenance winter > summer
Searching for food Social behaviour winter > summer
Burrow maintenance winter > summer
Social behaviour Stationary/Basking winter > summer
Burrow maintenance winter > summer
Stationary/Basking Burrow maintenance winter > summer
Consuming food winter > summer
Time underground winter > summer
Searching for food winter > summer
Social behaviour winter > summer
Time underground Stationary/Basking winter > summer
Gathering food winter > summer
48
primarily reflects their behavioural responses to changes in environmental conditions
between summer and winter.
Of the seven behaviours recorded, ice rats spent most time in energy acquiring
(gathering and consuming food) and energy saving (basking and belowground in their
burrows) activities. Small mammals have a high metabolic rate in relation to their size
(Schultz et al., 1999) and it was predictable that ice rats would spend much of their time
in thermoregulatory activities. Moreover, as herbivores, ice rats need to spend most of
their active time feeding, as less energy can be gained from low quality/high fibre plant
material than from an omnivorous diet (see Perrin and Curtis, 1980, for review).
However, the amount of time spent foraging is traded off against energy saving
behaviours such as basking and seeking refuge underground.
Incidences of gathering and consuming food were higher in winter than in
summer when conditions were more demanding. A similar pattern was found in desert-
living Brant?s whistling rat Parotomys brantsii (Jackson, 1998), a close relative of O. s.
robertsi. There are possibly three explanations for the increased foraging in winter.
Firstly, energy requirements are higher when temperatures are low, resulting in higher
metabolic demands (Ellison, 1996) and accompanied by greater energy intake through
feeding (see Hayne et al., 1986; Schultz et al., 1999). Secondly, since food availability
and quality diminish dramatically in winter in the Lesotho wetlands (Schwaibold and
Pillay, 2003; Chapter 2), high levels of foraging would increase net energy gain from the
limited food resources to compensate for the increased energy loss due to low
temperatures (Schultz et al., 1999). Thirdly, intensive foraging bouts might be needed to
compensate for the shorter day length in winter, since ice rats are not active aboveground
after sunset (see also hoarding below).
49
Winter behaviour was characterised by high levels of basking. As the ice rat does
not hibernate or enter bouts of torpor during extreme cold conditions, sun-basking is one
of the behaviours adopted to cope with low temperatures. Many small mammals bask to
overcome nocturnal hypothermia and to reduce the costs of metabolic heat production
(Barash, 1989; Hainsworth, 1995; Geiser, et al., 2002) and basking becomes
increasingly important when animals are thermally stressed and when forage is scarce
and of low quality. Sun-basking accelerates the warming-up process to a level that
allows for uninterrupted activity with very little thermoregulatory cost (Sale, 1970;
Geiser et al., 2002). Ice rats spent extended periods of time sun-basking when
temperatures dropped below 5?C (Hinze and Pillay, unpublished) and the energy gained
through basking may compensate for the reduced energy intake from lower quality food,
which may be adequate to meet metabolic requirements.
In contrast to winter, ice rats spent more time belowground in their burrows in
summer. This is most likely a response to prevailing environmental conditions, since a
concurrent study reported that ice rats avoid aboveground activity when ambient
temperatures and levels of solar radiation are highest during the day (Hinze et al.,
submitted), Similarly, black-capped marmots (Marmota camtschatica bungei)
compensate for physiological limitations by seeking refuge in a burrow or lying on rocks
to discharge excess heat when ambient temperatures were very high and potentially
lethal (Semenov et al., 2001). The South American degu (Octodon degus) also adjusts its
activity patterns as temperatures increase and has been found to spend more time in
shade or below-ground during the hottest times of the day (Kenagy et al., 2002; Kenagy
et al., 2004).
I predicted that ice rats would forage for longer in the afternoons since no
aboveground activity occurs at night, and that they would bask for longer periods in the
50
morning sun after they emerged from their burrows. Time of day had minimal influence
on ice rat behaviour, indicating similar behavioural priorities in the mornings and
afternoons. In contrast, the diurnal P. brantsii increases foraging and hoarding behaviour
substantially in the later hours of the day, thereby permitting them to feed belowground
at night when temperatures drop after sunset (Jackson, 2001). The weather in the
Lesotho mountains is unpredictable so that foraging throughout the day might be an
adaptation to optimise feeding when conditions are favourable.
An important aim of this study was to investigate the organization of behaviours.
In general, behavioural sequences also revealed significant seasonal differences with
little or no gender or time of day effects. Transitional matrices indicate the likelihood of
one behaviour following another. Compared to summer, there were many more positive
transitions in winter (i.e. one behaviour following another), strongly focussed on
foraging, hoarding and thermoregulation, which indicates that these three behaviours are
very likely to follow each other during the behaviour repertoire of an individual, while
other behaviours became less important. While the fewer transitions in summer may be
related in part to the increased time spent belowground, reasons for the greater number
of transitions in winter are not obvious, particularly in their relevance to energy
conservation, since one would have expected reduced activity and hence fewer
transitions in winter when energy loss would have been greatest (see Kluger, 1979). It
might be profitable in future to derive a cost-benefit analysis of energy gains and losses
from increased and reduced activity. Equally, an investigation of the temporal
motivational reorganisation of behaviours in summer and winter would be useful, since
it is known that animals will interrupt energy saving behaviours for energy demanding
ones in response to specific cues (Aubert, 1999).
51
More transitions led to aggressive encounters in winter, which were probably
ultimately related to heightened tension because of competition for optimal feeding sites
(Hinze and Pillay, unpublished). The relationship between searching, gathering and
disappearance underground was very strong, both in summer and winter, supporting the
increased incidence of hoarding described earlier.
No sexual differences were found in the time spent in each of the seven
behaviours and sexual differences in behavioural transitions were negligible. Since
female ice rats have post-partum oestrous (Willan, 1990), most would have been
pregnant and/or lactating during the summer observations. Therefore, I expected that
females would forage for longer than males in order to meet the energy requirements of
pregnancy and lactation. While one cannot rule out other reasons for the lack of
differences between the sexes, one reason for the similarity in foraging time may be that
the larger gut dimensions in females compared with males (see Schwaibold and Pillay,
2003) would reduce the need for extended foraging times of females in summer.
Hoarding is an adaptive response to changes in food availability and/or energy
needs (Wunder, 1984). Stored food and nesting material provide food and warmth
during unfavourable aboveground conditions and a decline in ambient temperature can
result in significant increases in hoarding (Barry, 1976; Masudu and Oishi, 1988) and
explains the increase in hoarding behaviour by both male and female ice rats in winter.
The shorter day length in winter may also have influenced hoarding, since hoarded food
extends foraging times after dark. In addition, feeding belowground in winter would
decrease the time that ice rats are exposed to extreme temperatures aboveground. Hinze
et al. (submitted) found evidence of food storage chambers in ice rat burrow systems,
confirming that food plants are hoarded when they are accessible during clear days in
preparation for times when aboveground food is not accessible (e.g. cold nights, rainy
52
days, snow days). Some of the plant species collected both in summer and winter were
not part of the ice rat?s diet (Schwaibold and Pillay, unpublished; Chapter 6), suggesting
that plant material was collected for food as well as bedding, as also occurs in Marmota
spp. (Barash, 1989).
Female rodents increase food hoarding behaviour when they are caring for young
(Smith and Reichmann, 1984). Similarly, hoarding was seen significantly more often by
female than male ice rats during summer. Compared to other members of its subfamily
Otomyinae (Pillay, 2001), young ice rats complete weaning almost a week later at 16
days (Willan, 1990) and they emerge aboveground only about 4-5 weeks after birth
(Hinze and Pillay, unpublished). Plant material taken belowground would be important
both as food and as nesting material for physiologically weaned but dependent young.
An animal?s fitness depends on its ability to effectively divide its time and
energy among competing behavioural demands (Schoener, 1971; Schultz et al., 1999). In
cold environments, animals must have access to adequate food supplies and nesting
opportunities to maintain their body weight and normal body temperature, but when they
have to search for food elsewhere, they are faced with increased thermoregulatory
demands (Johnson and Cabanac, 1982). This is especially crucial for small mammals
because their high metabolic rate and high surface area: volume ratio results in high
thermal conductance (Schultz et al., 1999). Ice rats are faced with the conflicting
demands of energy intake and energy saving, and this study indicates that they have
adapted their behavioural patterns seasonally. Foraging and basking behaviours are
traded off against reduced exposure to low temperatures in winter, while ice rats escape
lethal ambient temperatures and solar radiation levels in summer by retreating
belowground. Further studies are needed on how ice rats modify their behaviour patterns
during short term environmental changes (e.g. under various weather conditions during
53
summer), how they respond to periods of prolonged snowfall, and whether high energy
demands in winter may be met by energy conservation and huddling belowground.
Finally, since predation pressure in the Sani Valley is negligible, this study reveals that
the behaviour O. s. robertsi in the Sani Valley, Lesotho is strongly dictated by
environmental influences. It would be interesting to examine ice rat behaviour in areas
with greater predation risk to define behavioural priorities under challenging
environmental conditions (e.g. low temperatures) and predation risk.
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58
CHAPTER FOUR:
Flexible foraging decision-making in the African ice rat, Otomys sloggetti robertsi
Abstract
I investigated the foraging behaviour of the southern African ice rat, Otomys sloggetti
robertsi, a diurnal herbivore endemic to the southern African Drakensberg and Maluti
mountains at altitudes above 2000m. Ice rats do not hibernate and show little
physiological adaptation to their cold environment. Instead, they rely on a range of
behavioural and morphological adaptations. Ice rats are central place foragers and travel
short distances (<50 cm) to forage. They display significant seasonal variation in their
foraging patterns. The further a foraging site is from a burrow, the greater the tendency
for consuming food at the foraging site in summer, but in winter ice rats mostly return to
a burrow, regardless of distance travelled. No relationship was found between distance
travelled and time spent at a foraging site in summer, although in winter there was a
strong negative relationship between these two variables. Predation risk is negligible in
ice rats, so while the costs of returning to a burrow after foraging in winter may be
energetically demanding, these must be viewed against the benefits accrued through
avoiding exposure to low temperatures by feeding in a burrow, as well as the loss of
collected food and possible injury associated with aggressive interactions with
conspecifics.
Key words: Otomys sloggetti robertsi, central place, diet, foraging behaviour
59
Introduction
Understanding foraging decision-making is best encapsulated by mathematical
models generated by optimal foraging theory, which has attempted to show how
foraging behaviours of animals are adapted, through natural selection, to maximise
fitness by balancing their net rate of energy gain (foraging) against their rate of energy
loss through optimal searching, feeding and diet selection (Charnov, 1976; Pyke et al.,
1977; Sih, 1980; Lima and Dill, 1990; Hughes, 1993). As a derivative of the optimal
foraging theory, central place foraging specifically describes the behaviour of animals
that repeatedly return to a fixed point with food items collected elsewhere (Orians and
Pearson, 1979; Stephens and Krebs, 1986). Support for these models has been provided
by numerous empirical studies which largely consider the rate of energy intake as the
critical determinant of foraging patterns (see Lima, 1985; Nonacs and Dill, 1990;
V?squez, 1994; Jackson, 2001 ) and fitness increases as a function of the rate of energy
gain per unit of time spent foraging (Charnov, 1976).
Nonetheless, other conditions to which animals are exposed are sometimes
overlooked in these models. For example, predation risk (see Lima and Dill, 1990; Lima,
1998), the presence of competitors (see Schr?pfer and Klenner-Fringes, 1991; Krebs and
Davies, 1993) and food handling times (see Guerra and Ades, 2002) can also affect
foraging decisions. An important factor often ignored in most foraging models is the
influence of environmental factors, such as prevailing weather conditions, on foraging
decisions, possibly because of the difficulty of identifying appropriate empirical vectors
(Jackson, 2001), but see Stouder (1987) and Sergio (2003). Since environmental
conditions vary over time (e.g. from daily variations to seasonal changes), an animal
might need to modify its foraging behaviour temporally in the face of changing energy
demands associated with temperature fluctuations. When ambient temperature falls
60
below the thermoneutral range, animals with access to sufficient food and a thermally
stable refuge can maintain normal body temperature by eating more or higher quality
food and by spending more time in the refuge. However, if animals must leave their
stable microenvironments to obtain food elsewhere, they will face increased
thermoregulatory challenges. This problem is especially acute for small mammals
because of their large surface area to volume ratio (Johnson and Cabanac, 1982).
Intuitively, selection should favour flexible decision-making to maximise energy
gain, which is often likely to be achieved as a series of trade-offs of various behaviours
(Schoener, 1971; see Schultz, et al., 1999, for review). Desert antelope ground squirrels
Ammospermophilus leucurus (Hainsworth, 1995) and thirteen-lined ground squirrels
Spermophilus tridecemlineatus (Vispo and Bakken, 1993), for example, ?shuttle?
between hot desert surfaces to forage and cool burrows to escape high temperatures. In
cold environments, small animals would be expected to trade off between foraging
activity, which is the most common means of acquiring energy (Schultz et al., 1999),
and escaping prolonged exposure to low temperatures (Johnson and Cabanac, 1982b).
For example, black-capped chickadees Parus atricapillus may gain some thermal benefit
from carrying food items back to cover for consumption rather than eating in the open at
the foraging patch, particularly on cold or windy days (Lima, 1985). Also, Caraco et al.
(1990) found that yellow-eyed juncos (Junco phaenotus) changed their foraging patterns
during the day in relation to ambient temperature by displaying risk-averse bahaviour
during the warmer periods of the day when a positive energy budget could be expected,
while colder periods of the day brought about risk-prone behaviour as the energy budget
was expected to be negative.
The aim of the present study was to investigate the foraging behaviour of free-
living African ice rats, Otomys sloggetti robertsi. This medium-sized (121-143 g),
61
burrow-dwelling, diurnal murid rodent is an interesting subject for studying foraging
decision-making because of its unique biology coupled with its geographic distribution.
Otomys s. robertsi is confined to altitudes exceeding 2000 m, and is endemic to the harsh
subalpine and alpine Drakensberg and Maluti mountains of southern Africa (Killick,
1978) but it does not hibernate and its physiology is apparently similar to congeners
inhabiting warmer and lower altitudes (Richter et al., 1997). Instead, it employs a range
of behavioural adaptations (e.g. sun-basking and huddling) to cope with low
temperatures (Willan, 1990; Schwaibold and Pillay, unpublished; Chapter 3).
Ice rats are specialist herbivores, feeding more or less exclusively on green plant
material with a high fibre content, including stems, leaves, and grasses (Willan, 1990)
and only have access to high-quality plant parts such as flowers and new shoots for a
short time in summer (Schwaibold and Pillay, 2003; Chapter 2). This, coupled with the
high metabolic rates of small animals (Schultz et al., 1999) means that O. s. robertsi
needs to maximise overall food intake in order to gain as much energy during foraging
as omnivorous or granivorous rodents (Perrin and Curtis, 1980; Green and Millar, 1987).
Moreover, the poorer diet quality of its herbivorous diet (Green and Millar, 1987;
Hammond, 1993) and the short growing season in the alpine habitats (Killick, 1978)
would presumably influence the foraging behaviour of ice rats. In recent examinations of
gross gut anatomy, we reported that O. s. robertsi has a larger small intestine, caecum,
stomach volume and parts of the colon compared to its relatives living at lower and
warmer altitudes, and we suggested that these morphological adaptations increase energy
uptake from a poor quality diet (Schwaibold and Pillay, 2003; Chapter 2). In addition,
while male gut dimensions did not change seasonally, female ice rats showed increased
gut dimensions in summer compared to winter, most likely because for increased energy
requirements during pregnancy and lactation (Schwaibold and Pillay, 2003).
62
Predation pressure on O. s. robertsi in my study site in the Sani Valley appears to
be minimal (Willan, 1990) and anecdotal reports from local Basotho shepherds and my
own observations from 1999 to 2003 indicate that predation on ice rats is negligible in
summer and virtually absent in winter. Instead, population numbers are regulated by
snowfall and low winter temperatures (Willan, 1990; Lynch and Watson, 1992). In the
absence of high predation levels, it is possible that, at least at my study site, ice rat
foraging behaviour is mainly determined by environmental factors such as temperature.
Pilot studies have indicated that ice rats may possibly be central place foragers,
collecting food and returning to a burrow for consumption. While returning to a central
place may impose an energetic cost compared with staying at the foraging site (in situ),
remaining in situ exposes the ice rat to potentially lethal temperatures, especially in
winter. In summer, foraging occurs mainly during the cooler mornings and late
afternoons, and aboveground activity is reduced during the middle of the day when
temperatures and radiation levels are highest, whereas in winter, aboveground activity is
more or less uninterrupted from morning to late afternoon; no aboveground activity has
been observed at night (Hinze and Pillay, unpublished).
I asked whether the foraging decisions of ice rats could be influenced by seasonal
changes in environmental conditions within the constraints of central place foraging.
Specifically, three predictions were made: (1) Since winter in my study area is
characterised by very low temperatures (often below 0? C), often far below the
thermoneutral zone of ice rats (Richter et al., 1997; Hinze and Pillay, unpublished) and
by poor food quality and availability (Schwaibold and Pillay, 2003), I asked how ice rats
trade off between energy conservation and energy-acquiring foraging activities in winter,
which would expose them to potentially lethal temperatures (ice rats are physiologically
stressed at low temperatures, which may incur costs (Richter et al., 1997)). If avoidance
63
of low temperatures is the primary concern for ice rats, I predicted that distances
travelled for foraging would be comparatively short and that the incidence of returning
to a protective burrow entrance with collected food items would be more common in
winter compared to summer, regardless of the distance travelled. Alternatively, if
acquisition of better quality food is more important, I predicted that ice rats would travel
further in winter than in summer to find food and that, as distances from burrow
entrances increased, ice rats would be more likely to consume food in situ, allowing
them to feed for longer and increase energy intake. (2) Because of the energetic demands
of pregnancy and lactation, I expected gender differences in foraging behaviour, but I
also asked whether the increased gut capacity of females in summer might influence
their foraging behaviour by compensating for the increased energy requirements, thereby
making behavioural changes to increase energy intake unnecessary. (3) I also
investigated the food type and quality of food and non-food plants in the ice rat?s habitat
and predicted that they would prefer food plants with lower levels of digestible fibre and
higher levels of protein.
Materials and Methods
The study site
Fieldwork was conducted on a 4 ha site in the Sani Valley (29? 37? S; 29?14? E),
about 5 km west of Sani Top in the south-eastern Drakensberg Mountains in Lesotho.
The study site was located at an altitude of 2900 m along the edges of one of the many
wetlands in the Sani Valley. Mean air temperature in the Lesotho highlands ranges from
0?C in winter to 6?C in summer (Grab, 1997). Precipitation is high (about 1200 mm per
annum) and snowfall can be expected at any time of the year (Willan, 1990). Shrubs and
herbs (annuals and biennials, woody cushion plants and succulents, aquatics and alien
64
plants) are common in the Sani Valley, and trees are absent. Vegetation in my study area
did not exceed 0.5 m in the colonies, making direct observations of ice rat behaviour
possible.
Behavioural observations
The foraging behaviour of 18 adults (8 females and 10 males) was studied in summer
(October to March) and of 14 adults (7 females and 7 males) in winter (May to August).
Animals were live-trapped in three colonies and to facilitate later identification, each
individual was fitted with a distinctively coloured plastic cable tie neck band (length 20
cm, width 4.7mm) and released at the point of capture. The procedure of using neck
bands for identification is described by Jackson (1998). Females were fitted with a white
cable tie and males with a black one. A distinctive colour combination of insulation tape
was taped on to the cable tie for individual identification. This marking method
permitted animals to be easily recognised in the field and was approved by the animal
ethics committee of the University of the Witwatersrand (clearance number 2000/21/2a).
Tagged individuals were observed directly using 10x50 binoculars from a raised
surface, about 1m above the ground, at a distance of between 10 and 30 m (ice rats
habituate quickly to the presence of people). To allow tagged individuals to become
accustomed to the neck bands, they were observed no earlier than five hours after
tagging. Each individual was observed in one season only. Observations were made in
the early morning (05h00 - 11h00) and afternoon (13h30 - 17h30) during summer and
during most of the day (09h00 - 15h00) in winter, coinciding with the most active times
in each season (Hinze and Pillay, unpublished). The foraging behaviour of each tagged
individual was recorded using continuous focal sampling in 20 different foraging bouts
per individual over several days and at various times of the day. A foraging bout started
65
when the animal gathered and consumed food and ended when the animal changed
behaviours, disappeared into its underground burrow or changed to a new location to
forage. Data were collected whenever an individual was foraging, although no individual
was observed more than once per day to allow for a representative data set over several
days and at various times of the day; there was no time limitation to this data collection.
Ice rats consumed collected food in situ or took it back and consumed it in a
burrow entrance (i.e. a central place). Incidences of hoarding behaviour were not scored
because individuals often alternated between entrance holes during hoarding, and thus
clear bouts could not be established. Also, since plant species were difficult to identify, it
was uncertain whether the plant material gathered was used for nesting or caching. The
distances that food was carried during foraging bouts were standardised against the body
length of an ice rat. In addition, colour-coded wooden peg markers were arranged in a
4x4 metre grid over each colony. Using these indicators, the distances an ice rat travelled
from a start point (e.g. burrow entrance) were categorized as follows: 1-15 cm (estimated
from the length of an adult ice rat); 16-30 cm (up to twice the length of an ice rat); 31-50
cm (less than one eighth the length between two grid markers); 51-100 cm (up to a
quarter the length between two grid markers); 101-150 cm (one quarter to one third the
length between two grid markers); 151-200 cm (up to half the length between two grid
markers); 200-400 cm (more than half the length between two grid markers). Food eaten
at a central place was scored as 0 cm.
The habitat of ice rats consisted of a variety of plants such as small woody shrubs
(Helichrysum spp.), various grass species, herbaceous plants and wetland vegetation, of
which only the herbaceous and wetland vegetation were consumed. The plants present in
the habitat were identified to species level where possible but as ice rats fed on very
short grass and wetland plants, they usually collected as many different plant types as
66
possible before consumption. This made it difficult to identify the species collected
during a foraging bout (due to the small size of the sedges and lack of floral parts on
grasses). Therefore, the plant species collected for consumption were categorised as
wetland vegetation, herbaceous plants or grass. Foraging areas (i.e. areas regularly
visited by ice rats during foraging bouts) were categorised according to the percentage
cover of herbs (wetland and herbaceous vegetation) and grass present, which was
determined in a 2 m radius around each burrow frequently used during foraging bouts.
The frequency of visits to each of these patches was determined for each distance
category in summer. Plant data were not collected in winter as it was very difficult to
distinguish between the types of grasses and herbaceous vegetation when they were dry
and often covered with ice. Samples of each of these plant types in the colonies under
observation were collected and sent to the Institute for Commercial Forestry Research in
Pietermaritzburg, South Africa, to obtain measurements of fibre (acid detergent fibre),
protein and nitrogen levels. The size of the food items was not recorded because ice rats
tended to collect as much plant material as would fit into their mouths before
consumption, making estimation of size difficult.
Data analysis
The proportion of all bouts spent in situ and at a central place was calculated for males
and females in summer and winter. The data set was arcsine transformed and a general
linear model (GLM) was used to analyse whether season and gender (independent
factors) influenced the proportion of times ice rats consumed food items in situ
(calculated as a proportion of the total number of bouts per individual). A Tukey HSD
post-hoc test was performed to determine specific differences. A Spearman Rank
correlation with a Bonferroni adjustment was used to analyse the relationship between
67
the frequency of foraging bouts and the distance travelled by each gender in summer and
winter. The same tests were also used to establish the relationship between the distance
travelled for foraging and the time spent at the foraging site, and between distances
travelled and the frequency of staying in situ. I did not consider the colony affiliation of
individuals in the analysis of foraging behaviour because of low sample sizes and since
another study revealed no significant differences in the behaviour of ice rats of different
colonies in a particular season (Schwaibold and Pillay, unpublished; Chapter 3). The
time of day when observations were made did not statistically influence foraging
behaviour and was not considered further.
The preference of ice rats for particular foraging areas was analysed using linear
regression analysis, and chi-squared tests with Boferroni adjustment were used to assess
differences between distances travelled and the type of food collected. The average
proportion of fibre, protein and nitrogen content was calculated for the three plant types
(i.e. grasses, herbaceous plants and wetland plants) consumed by the ice rat, the data
were arcsine transformed and analysed using a GLM model and Tukey HSD post-hoc
analyses.
Results
In approximately 65% of a total of 564 observations, ice rats left a burrow entrance,
collected plants some distance away and returned to the same burrow entrance, strongly
suggesting that ice rats are central place foragers. In the remaining 35% of observations,
ice rats spent significantly more bouts in situ in summer than in winter (F1,41 = 23.09;
p<0.001). There was no significant differences in the number of bouts spent in situ
between males and females (F1,41 = 0.40; p=0.53; Figure 1). The season x sex interaction
was also not significant (F1,41 = 0.08; p=0.78).
68
0
10
20
30
40
50
60
70
80
90
100
male summer female summer male winter female winter
N
um
be
r o
f b
ou
ts
(%
)
central place in situ
Figure 1. Mean (?SE) percentage of foraging bouts spent at a central place and in situ
for male and female O. s. robertsi in summer and winter.
There was a strong negative relationship between the proportion of foraging bouts
and distances travelled by ice rats in summer (r119=-0.86; p<0.01) and winter (r70=-0.82;
p<0.0001). There were no gender differences in this relationship (Bonferroni tests). In both
seasons, most foraging occurred within 10-15 cm of a burrow and foraging frequency
decreased sharply towards 100 cm, with little foraging occurring beyond 100 cm of a
burrow entrance (Figure 2).
The relationship between the number of times food was consumed in situ and
distances travelled from a central place (i.e. burrow entrance) revealed dichotomous
seasonal patterns (Figure 3). In summer, as the distance travelled from a central place
increased, the frequency of remaining in situ also increased, resulting in a weak positive
relationship (r45 = 0.39; p=0.01). In winter, however, there was a strong negative
relationship between the frequency of bouts spent in situ and the distance from a central
place (r22 = -0.71, p=0.0002).
69
0
10
20
30
40
50
60
70
80
90
100
0-1
5
30
-50
10
0-1
50
>2
00
Distance categories (cm)
N
um
be
r o
f
bo
ut
s
(%
)
Summer
Figure 2. Mean percentage (including minimum and maximum values) of foraging
bouts at each distance category in summer (N=17) and winter (N=13). Regression lines
are included: summer: y = 48.19 - 0.849x; winter: y = 28.76 - 0.494x.
Figure 3. Mean frequency (including minimum and maximum values) of foraging bouts
spent in situ for all distance categories in summer (N=17) and winter (N=13). Regression
lines are included: summer: y = -895.0 + 9.29x; winter: y = 2015.1 ? 19.45x.
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
1
0-15 15-30 30-50 50-100 >100
Distance categories (cm)
Fr
eq
ue
nc
y
of
b
ou
ts
s
pe
nt
in
s
itu
Summer Winter; ;
0-15 15-30 30-50 50-100 >100
Winter
0-15 15-30 30-50 50-100
; ;
70
In both summer and winter, as the distance from a central place increased, the
time spent in situ decreased (Figure 4). A Kruskal-Wallis ANOVA showed no gender
differences for any of the distance categories, but seasonal differences were found in the
15-30 cm (H1,30 =13.11, p=0.0003) and 30-50 cm (H1,30 = 4.06, p=0.04) categories, and
in both cases ice rats spent more time in situ in summer than in winter. In winter, there
was a strong negative relationship between distance travelled and time in situ: foraging
occurred for the longest period close to a burrow entrance and foraging bouts became
shorter with increasing distance from a central place (r19 = -0.74; p<0.00032). A weak
non-significant negative relationship was observed in summer (r49= -0.24; p>0.10),
indicating that ice rats spent a similar duration of time at each distance category. No
gender differences were found in winter (r19=0.39; p=0.10) or in summer (r 49=0.04;
p=0.78).
0
Figure 4. Mean duration (including minimum and maximum values) of time spent in
situ by ice rats in summer (N=17) and winter (N=13). Regression lines are included:
summer: y = 0.11 ? 0.008x; winter: y = 0.19 ? 0.06x.
50
100
150
200
250
300
350
0-15 15-30 30-50 50-100 >100
Distance categories (cm)
Ti
m
e
sp
en
t i
n
si
tu
(s
ec
on
ds
)
Summer Winter
0-15 15-30 30-50 50-100 >100
; ;
71
In summer, ice rats displayed some preference for the areas visited for foraging.
Those containing more than 50% herbaceous plants (of which most were wetland plants)
were visited more often than those that contained more grass species, with the majority
of visits taking place in areas containing 50-75% wetland/herbaceous plants (Figure 5).
A regression analysis however showed that this relationship was neither strong nor
significant (r8= 0.41; p=0.32). This analysis was not performed in winter because plants
were difficult to identify.
0
20
40
60
80
100
120
0-25 25-50 50-75 75-100
% herbaceous plants
To
ta
l n
um
be
r o
f v
isi
ts
Figure 5. Foraging areas visited by O. s. robertsi during foraging bouts for all distance
categories in summer.
The three plant types collected by ice rats varied significantly in fibre, nitrogen
and protein content (F6,24= 9.96; p= 0.00015), with wetland vegetation (the preferred
food type) containing the lowest levels of digestible fibre and grasses (the less preferred
food type) the highest (post-hoc tests). In contrast, grasses had the lowest levels of
72
protein and nitrogen (Figure 6). Analyses of non-food plants such as Helichrysum spp.
revealed very high levels of fibre (mean = 46.90%) and very low levels of protein (mean
= 5.47%) and nitrogen (mean = 0.88%).
0
10
20
30
40
50
60
Fibre Protein Nitrogen
P
er
ce
nt
Grasses Herbaceous plants Wetland plants
Figure 6. Mean (+SE) percentage of acid detergent fibre (ADF), protein and nitrogen in
grasses, herbaceous plants and wetland plants determined on a 100% dry matter basis.
Discussion
During foraging bouts, ice rats mainly (65%) returned to a central place (i.e. the
burrow) or sometimes (35%) remained and fed in situ. Ice rats are central place foragers
and their foraging behaviour appears to be strongly influenced by seasonal changes in
environmental conditions. Central place foraging theory maintains that animals return to
a central place with collected food items if the distance travelled to the foraging site is
short but that food should be consumed in situ if the distance travelled is further away.
As the distance from a central place increases, the energy cost of travelling the distance
73
outweighs the benefits of protection against risks such as predation (Orians and Pearson,
1979; Lima et al., 1985). Otomys s. robertsi displayed such behaviour in summer: as
distance travelled from a central place to a foraging site increased, the tendency to
consume food in situ also increased. In winter, O. s. robertsi displayed a different
foraging strategy. As the distance travelled from a burrow to a foraging site increased,
the tendency to return with the collected food items increased. Not only did ice rats
return from foraging bouts more often in winter than in summer, they also spent less
time in situ.
Otomys s. robertsi travelled short distances to forage in both summer and winter
and there were only a few occasions when foraging occurred more than 50 cm away
from a burrow. In comparison, some small mammals which are of similar size and have
a similar diet to ice rats travel further to forage. For example, Brants? whistling rat
Parotomys brantsii (a close relative of the ice rat; Jackson, 2001) travels over 200 cm
from its burrow to forage, and experiments by Anderson (1986) encouraged mice
(Peromyscus maniculatus) and voles (Clethrionomys gapperi and Phenacomys
intermedius) to travel distances over 14 meters in cold conditions. The short distances
travelled by the ice rat may be explained by the short distances between burrows and
food plants (Schwaibold and Pillay, unpublished; Chapter 6).
Lima (1985) proposed that animals concerned mainly with foraging efficiency
would tend to feed in situ, whereas those at risk of predation would always return to the
relative safety of cover, regardless of distance travelled. However, in most cases animals
will trade off these two conflicting needs against each other (Caraco, 1979; Sih, 1980;
Lima, 1985; Lima et al., 1985). In many ways the foraging behaviour of ice rats,
particularly in winter, appears to minimise risk and resembles the behaviour of animals
subjected to high predation risk (Lima, 1985). However, potential predators in the Sani
74
Valley were rarely observed and predation risk is unlikely to have influenced foraging
behaviour. If it did influence foraging decisions, I would have predicted higher
incidences of returning to a central place and shorter time spent in situ in summer when
a few raptors were sighted in the study area. I suggest that there are two non-mutually
exclusive reasons for ice rats returning more frequently to a central place and spending
less time in situ in winter. Firstly, ice rats reduce their exposure to low temperature if
they spend less time in situ. Winter temperatures (Killick, 1978; Grab, 1997) are well
below the thermoneutral zone of ice rats (see Richter et al., 1997) and it appears that the
benefits of returning to cover with forage may outweigh the costs of energy loss through
travelling. Secondly, although ice rats in a colony nest communally, they display
temporal territoriality aboveground and colony mates either ignore one another or
interact aggressively (Hinze and Pillay, unpublished). Moreover, competition for
limiting food resources among colony members is intense in winter, resulting in highly
aggressive interactions (Hinze and Pillay, unpublished), leading to damaging fights
(Willan, 1990). I suggest therefore that ice rats avoid competition with neighbours by
consuming food at the burrow. Group-living striped mice Rhabdomys pumilio show a
similar response by leaving a foraging site when another conspecific arrives, thereby
avoiding aggressive encounters (Schradin, 2004).
No differences were found in the foraging patterns of male and female ice rats.
Since female rodents generally have higher energy needs during the reproductive season
(Weiner, 1987; Silby et al., 1990), significant gender differences in foraging behaviour
in summer were expected. However, in the harsh alpine habitats, reproductively active
female O. s. robertsi have to compromise among caring for young, foraging, basking and
territory defence (Schwaibold and Pillay, unpublished; Chapter 3). Female ice rats show
a significant increase in gut dimensions during summer, which potentially allows them
75
to extract more energy per unit mass of food than males (Schwaibold and Pillay, 2003;
Chapter 2), which may explain why females may not need to change their foraging
behaviour in summer.
Furthermore, a previous study has shown that ice rats spend more time basking in
winter than in summer (Schwaibold and Pillay, unpublished; Chapter 3) and this is
increasingly important when animals are thermally stressed and forage is scarce and of
low quality. Marmots (Marmota spp.) have also been found to facilitate energy gain
during cold periods by utilising radiant energy through basking (Barash, 1989). Energy
intake through basking may compensate for the reduced energy intake from lower
quality food in winter, thus allowing metabolic requirements to be met.
Fibre, nitrogen and protein analysis of various plants found in the ice rat?s habitat
revealed that wetland sedges such as Haplocarpa nervosa have the lowest levels of
digestible fibre (ranging from 27% to 35%), followed by herbaceous plants, while the
grass species have relatively high levels of fibre (40% - 53%). As patches consisting
predominantly of herbaceous and wetland vegetation were preferred by ice rats, this
comparatively low fibre contents may allow the rodents to gain as much energy as
possible from easily digestible food items. In comparison, non-food plants such as the
Helichrysum spp were found to have very high levels of fibre and comparatively low
levels of protein and nitrogen, possibly making them unpalatable to ice rats. This is
supported by the animal?s patch preferences. Although most patches visited in summer
contained grasses and very few non-food plants, mainly wetland plants and herbaceous
vegetation were consumed. Unfortunately, no winter data were available, but if the
levels of digestible fibre are in fact the driving force behind patch choice, I would
predict the same pattern in winter with a stronger emphasis on the presence of wetland
vegetation and herbaceous plants.
76
In conclusion, this study reveals that ice rats modify their foraging behaviour
between seasons. In summer their behaviour is typical of animals following a central
place foraging strategy, but in winter they almost always return to a central place,
possibly to minimise exposure to low temperatures and competitive neighbours. Otomys
s. robertsi is physiologically poorly adapted to low temperatures (Richter et al., 1997),
so its flexible foraging behaviour pattern is no doubt an adaptation for life in a harsh
environment. In order to fully understand the foraging efficiency of O. s. robertsi, future
studies should investigate which food items are collected in summer and in winter, and
the size and energy values of the food items relative to the distances travelled should be
established, both of which could not be established in this study. A future consideration
should be to study the foraging patterns of ice rat populations which experience
significant predation risk.
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81
CHAPTER FIVE:
Foraging in the African ice rat Otomys sloggetti robertsi: conflicting demands of
energy conservation and predator avoidance
Abstract
According to optimal foraging theory, an animal is expected to make foraging decisions
which maximise energy gain. However, many environmental factors shape foraging
decisions and thereby the potential for energy maximisation. I investigated the
influences of two environmental factors, predation pressure and cold temperatures, on
the foraging behaviour of the African ice rat, Otomys sloggetti robertsi. Ice rats are
diurnal herbivores endemic to the subalpine regions of the southern African Drakensberg
and Maluti mountains, but are physiologically poorly adapted to low temperatures. In a
population with negligible predation (Sani Top), foraging behaviour was seasonally
variable: in summer, ice rats only returned to their burrow with forage as distance
travelled increased, whereas they always returned to a burrow in winter. In another
population (Katse Dam) experiencing higher predation pressure, ice rats always returned
to a burrow entrance with forage when predators were present. Similar behaviours were
observed when predators were absent, but ice rats also modified part of their foraging
repertoire, which resembled that of their counterparts at Sani Top. Ice rats responded to
the two environmental cues in a hierarchical manner, with foraging decisions being
primarily determined by predation risk. However, foraging decisions in winter in the
absence of predation resembled foraging decisions made when predators where present,
indicating that low temperatures also pose a risk. Such facultative responses are adaptive
in response to multiple cues.
82
Key words: Otomys sloggetti robertsi, foraging behaviour, predation risk, multiple cues,
facultative decision making
Introduction
Optimal foraging theory has been used to describe and understand the foraging
behaviour of many animals (reviewed in Stephens and Krebs, 1986). This theory
highlights how animals trade-off between different behaviours (e.g. what to eat, how
long to remain in a food patch) to optimise energy gain (Lima and Dill, 1990). Many
factors have been shown to influence foraging behaviour, such as competition among
conspecifics (Giraldeau et al., 1994; Rita and Ranta, 1998), food availability (Bautista et
al.,1998), thermoregulatory costs (Bozinovic and V?squez, 1999; Krijgsveld et al.,
2003), weather patterns (Sergio, 2003), reproductive activity (Frey-Roos et al., 1995)
and predation risk (Lima and Dill, 1990).
Predation risk is possibly the most important underlying determinant of foraging
behaviour, especially for small mammals (Lima, 1985; Lima and Dill, 1990; Lima,
1998). As a result, many small mammals facing high levels of predation display a central
place foraging strategy, by repeatedly returning to a fixed point with forage collected
elsewhere to consume it under the protection of cover (Orians and Pearson, 1979; Lima,
1985; Lima and Dill, 1990; Lima et al., 1985; Anderson, 1986). Although returning to
the safety of a central place reduces the risk of predation, there are energetic costs
associated with carrying food to cover rather than feeding at the foraging site (Orians
and Pearson, 1979; Lima et al., 1985; V?squez, 1994). Therefore, most foragers trade off
the demands of maximising foraging efficiency with the need to minimise time exposed
to danger. For example, remaining at a foraging site (in situ) to consume food increases
overall energy intake by reducing energy loss, but increases time exposed to risks such
83
as predation and other environmental influences (Lima, 1985).
Ambient temperatures influence time and energy allocation to different
behaviours (Huey, 1991; Bozinovic and V?squez, 1999). Anderson (1986) suggested
that exposure to cold temperatures may be viewed as a significant risk to small
mammals, particularly in winter. Since thermal physiology may be a significant factor
influencing foraging behaviour (Caraco et al., 1990), endothermic animals select
microhabitats with temperatures close to their thermoneutral zone, but several
behaviours such as foraging and mating require that the animal leaves this favourable
microenvironment (Johnson and Cabanac, 1982) such as a burrow or nest, resulting in
exposure to extreme environmental temperatures. Harsh environmental conditions may
therefore limit the use of space and time for foraging and other maintenance behaviours
in small endotherms such as rodents (Melcher et al., 1990; Kenagy et al., 2002), as
activity time (and therefore time available for foraging) is traded off against other
thermoregulatory costs (Belovsky and Slade, 1986). Although returning to a suitable
microhabitat while foraging reduces exposure to low temperatures, energy will be lost
through carrying food to cover rather than consuming it in situ (Schwaibold and Pillay,
unpublished; Chapter 4). Therefore, there must be a trade off between the demands of
maximising foraging efficiency and the need to minimise time exposed to the cold.
While most studies focus on the influence of only one factor on foraging
decisions and efficiency (see Lima, 1985; Lima and Dill, 1990; Schr?pfer and Klenner-
Fringes, 1991; Jackson, 2001; Powell and Banks, 2004), little is known about how the
foraging behaviour of small mammals is determined by a combination of factors (e.g.
predation and low temperature). Such studies could answer questions about the
motivation of animals to make decisions when faced with multiple cues (see Morrell,
2004). For example, are there predictable trade-offs between cues in relation to
84
prevailing conditions and do the response to the cues follow hierarchical rules (i.e.
response is stronger to some cues than others; Balasko and Cabanac, 1998; Morrell,
2004)?
The African ice rat Otomys sloggetti robertsi is an ideal model for studying how
environmental factors influence foraging behaviour in small endothermic animals. The
ice rat is a medium-sized (121-143 g), herbivorous, diurnal murid rodent, endemic to the
harsh subalpine and alpine environment of the Drakensberg and Maluti mountains of
southern Africa (Killick, 1978) at altitudes exceeding 2000 m. Ice rats do not enter into
torpor or hibernate and are physiologically poorly adapted to the temperature extremes
in their habitats (Richter et al., 1997). Instead, they display a range of morphological
(e.g. short limbs and tails; Richter, 1997) and behavioural (e.g. sun-basking and
huddling; Willan, 1990) adaptations to cope with their environment, particularly with
low temperatures. In addition, ice rats live in colonies of up to 16 individuals and
construct complex underground burrow systems with insulated nests, which create
favourable microclimatic conditions and also provide opportunities for social huddling
(Hinze et al., submitted).
In a previous study, I reported that ice rats are central place foragers (Schwaibold
and Pillay, unpublished; Chapter 4) since they collect food in open areas which is
consumed when ice rats return with it to a burrow (central place). This study population,
located at Sani Top, Lesotho, was exposed to little or no predation risk, and I concluded
that returning to a central place was related to environmental cues, particularly low
ambient temperatures (Chapter 4). I recently located another ice rat population (i.e. near
Katse Dam, Lesotho) that is subjected to significantly higher levels of predation than the
population in my earlier study. Ice rats here also experience similar environmental
conditions to those at Sani Top, and so afford the opportunity for studying how both
85
predator risk and low temperatures influence foraging. If predator avoidance is the main
priority, one would expect these animals to consume food at a central place. However, if
the priority is energy conservation, forage should be consumed in situ (Lima, 1985),
although these probably represent extreme responses along a continuum because of the
spatio-temporal distribution of both predation risk (Lima and Dill, 1990) and
environmental temperature (Johnston and Bennett, 1996).
I compared the foraging behaviour of individual ice rats exposed to moderate
levels of predation (Katse Dam) with data from a previously completed study on an ice
rat population near Sani Top (only two predation attempts were observed during more
than 625 hourse of study, about 0.3%). My aim was to compare the foraging behaviour
of ice rats when they are faced with little or no predation risk (Schwaibold and Pillay,
unpublished; Chapter 4) with that of ice rats which experience moderate levels of
predation, both when predators were present and absent, since foraging decisions are
shaped by a perceived risk (Lima and Dill, 1990; Yl?nen and Magnhagen, 1992). I asked
two questions: (1) Does the foraging behaviour of ice rats follow hierarchical rules (i.e.
foraging is primarily shaped by predation risk and then by thermoregulatory cost) or do
they trade off between predation and thermal costs? (2) Do ice rats in predation risky
areas respond differently to an immediate threat (i.e. predator present) than when
predators are absent?
Materials and Methods
Study site
The study was conducted near the Sengu River, about 7km south-east of the Katse Dam
(29?21' S; 28?32' E) in Lesotho. The site was situated at an altitude of approximately
86
2000 m. The ice rat population experienced moderate predation pressure, and predation
attempts were observed on 27 occasions during the five months of study, mainly (74%)
by jackal buzzards Buteo rufofuscus (20 occasions) and occasionally by barn owls Tyto
alba. Ice rats are also hunted by indigenous Basotho herdsman, but I did not observe
hunting during my study. The study area comprised mainly shrubs and herbs and trees
were absent, and vegetation never exceeded 0.5 m.
The data collected for this study will be compared to data obtained from Sani
Top in the Sani valley, located in eastern Drakensberg Mountains in Lesotho (29? 37? S;
29?14? E; altitude: 2900m). While predation pressure in this area is negligible,
temperature means in the Lesotho highlands are low (from 0?C in winter to 6?C in
summer; Grab, 1997). Rainfall is high (around 1200mm per annum) and snow can be
expected at any time of the year (Willan, 1990).
Behavioural observations
The methods used here were similar to those of a previous study (Schwaibold and Pillay,
unpublished; Chapter 4). The foraging behaviour of 20 adult ice rats (10 of each sex)
was studied in summer (January to March) and 20 different ice rats (8 males, 12
females) were studied in winter (May to August). Animals were live-trapped (metal live
traps, 26 x 9 x 9 cm) in four colonies. Each individual was fitted with a uniquely
coloured plastic cable tie neck band (length 20 cm, width 4.7 mm) and released at the
point of capture (see Chapter 4). Females were marked with a white cable tie and males
with a black one, and a unique colour combination of insulation tape was taped onto the
cable tie for individual identification. Excess cable was cut off. This marking method
facilitated easy recognition of individual ice rats in the field, and was approved by the
animal ethics committee of the University of the Witwatersrand (clearance number
87
2000/21/2a). Individuals were not observed on the day they were tagged to allow them to
become familiar with the neck bands. Each individual was observed in one season only,
as it was not always possible to find marked individuals again in the next season.
Collared individuals were observed directly using 10x50 binoculars from a raised
surface at a distance of between 30-50 m; this distance was further away from colonies
than observations in my other study (3-30 m) but I could not approach ice rats too
closely in the Katse colonies. Observations were made in the early morning (05h00 -
11h00) and afternoon (13h30 - 17h00) during summer, and during most of the day
(09h00 - 15h00) in winter, coinciding with the most active times in each season (Hinze
and Pillay, unpublished). Continuous focal sampling was used to study the foraging
behaviour of each individual ice rat during 20 foraging bouts over several days and at
various times of the day. A foraging bout began when an ice rat gathered and consumed
food and ended when it changed behaviour, disappeared into an underground burrow or
changed its central place. Data were collected whenever an individual was found to be
foraging, although no individual was observed more than once per day. Times were
adjusted based on the presence/absence of predators at Katse Dam.
The distances that food was carried during foraging bouts were estimated relative
to the body length of an ice rat. Furthermore, wooden peg markers were arranged in a
4x4 metre grid over each colony and used to categorise the distances an ice rat travelled
from a start point (e.g. burrow entrance) as follows: 1-15 cm (estimated from the length
of an adult ice rat); 16-30 cm (up to twice the length of an ice rat); 31-50 cm (less than
one third the length between two grid markers); 51-100 cm (up to a quarter the length
between two grid markers); 101-150 cm (one quarter to one third the length between two
grid markers); 151-200 cm (up to half the length between two grid markers); 200-400
cm (more than half the length between two grid markers). Food consumed at a central
88
place was scored as 0 cm.
Data were collected when predators were visible in the vicinity of the colonies
(i.e. flying overhead) and also when no predators were observed. For the predator absent
treatment, I collected data no earlier than one hour after a predator was seen.
Data analysis
I compared the data collected here with those obtained in my other study at Sani
Top (Schwaibold and Pillay, unpublished; Chapter 4). Data were averaged for each
individual and tested for normality before analysis. Data sets were transformed when
necessary. General linear models (GLM) were used to analyse both the number of
foraging bouts per hour and the proportion of times ice rats consumed food items in situ
(calculated as a proportion of the total number of bouts per individual), in which
location/predation, season and gender were independent factors. A Tukey HSD post-hoc
test was used to determine specific differences in foraging patterns.
A Spearman Rank correlation with Bonferroni adjustment was used to analyse
the relationships between three sets of variables in relation to location/predation risk and
gender, including 1) frequency of foraging bouts and the distance travelled by each
individual, (2) distances travelled and the frequency of staying in situ, and (3) distances
travelled for foraging and the time spent at the foraging site. I did not consider the
colony affiliation of individuals in the analysis of foraging behaviour because of low
sample sizes and since another study revealed no significant differences in the
behaviours of ice rats of different colonies in a particular season (Chapter 4).
89
Results
The average number of foraging bouts per hour was significantly influenced by
location/predation risk categories (F2,100 = 17.07, p<0.001) but not by season (F1,100 =
0.16, p=0.69), gender (F1,100 = 1.91, p=0.17) and the interactions between these variables
(F1,100 = 0.91; p=0.34; Figure 1).
0
2
4
6
8
10
12
M
ea
n
nu
m
be
r o
f b
ou
ts
p
er
h
ou
r
Sani Top Katse -predator present Katse -predator absent
Figure 1. Mean (+SE) number of foraging bouts spent per hour for O. s. robertsi at Sani
Top and at Katse Dam in the presence and absence of predators in summer and winter.
A GLM analysis for the foraging bouts spent in situ (Figure 2) revealed no
gender differences (F1,113 = 0.0001, p=0.99) but significant differences in
location/predation risk (F2,113 = 11.27, p<0.001), with ice rats at Sani Top remaining in
situ more frequently than those at Katse Dam (predator: p=0.0001; no predator: 0.04).
Interestingly, ice rats at Katse Dam were more likely to stay in situ when predators were
absent than when predators were present. Irrespective of location/predation risk, ice rats
were twice as likely to remain at a foraging site in summer than in winter (F1,113 = 37.04,
p<0.001). The statistical interaction between location/predation risk and season also
90
0
10
20
30
40
50
60
70
Summer Winter
Fo
ra
gi
ng
b
ou
ts
sp
en
t i
n
si
tu
(%
)
Sani Top Katse -predator present Katse -predator absent
Figure 2. Mean (+SE) percentage of foraging bouts spent in situ at various distances
from a burrow entrance (central place) by O. s. robertsi in summer and winter at Sani
Top and at Katse Dam in the presence and absence of predators.
influenced the frequency of foraging bouts spent in situ (F2,113 = 10.92, p<0.001), being
greatest at Sani Top in summer, followed by Katse Dam/predators absent in summer,
while the remainder of the season-location/predation risk categories were significantly
lower (Figure 2).
In both summer and winter, there were significantly negative relationships
between the distance categories travelled and the frequency of travel in the Katse Dam
population in the presence of predators (summer: r140 = -0.91; p<0.01; winter: r140= -
0.89; p<0.01; Figure 3b = -0.89; p<0.01; Figure 3b) and the absence of predators
(summer: r140 = -0.91; p<0.01; winter: r140 = -0.92; p<0.01; Figure 3c) and at Sani Top
(summer: r119 = -0.86; p<0.05; winter: r70 = -0.82; p<0.005; Figure 3a). I found no
seasonal or gender patterns (p>0.05).
91
0
20
40
60
80
100
0-15 15-30 30-50 50-100 100-150 150-200 >200
Distance categories (cm)
N
um
be
r
of
b
ou
ts
(
%
)
Summer Winter
0-15 15-30 30-50 50-100 100-150 150-200 >200
; ;
(a)
0
20
40
60
80
100
0-15 15-30 30-50 50-100 100-150 150-200 >200
Distance categories (cm)
N
um
be
r o
f b
ou
ts
(%
)
Summer Winter
0-15 15-30 30-50 50-100 100-150 150-200 >200
; ;
(b)
0
20
40
60
80
100
0-15 15-30 30-50 50-100 100-150 150-200 >200
Distance categories (cm)
N
um
be
r o
f b
ou
ts
(%
)
Summer Winter
0-15 15-30 30-50 50-100 100-150 150-200 >200
; ;
(c)
Figures 3. Mean frequency (including minimum and maximum values) of foraging bouts at each
distance category in summer and winter at Sani Top (a) and at Katse Dam in the presence (b) and
absence (c) of predators. Regression lines: Sani Top - summer: y = 51.44 ? 9.29x; winter: y =
47.99 ? 8.43x; Katse Dam predators present - summer: y = 52.27 ? 8.99x; winter: y = 49.31 ?
8.76x; Katse Dam predators absent - summer: y = 48.21 ? 8.48x; winter: y = 51.64 ? 9.34x.
92
The relationship between the distance travelled and frequency of foraging bouts
spent in situ revealed several patterns in relation to location/predation risk and season. In
summer, ice rats in Sani Top displayed a significant but weak positive relationship
between distance travelled and the frequency of bouts spent in situ (r46 = 0.38, p=0.01)
(Figure 4a). In winter, this population had a strong negative relationship between these
variables (r22 = -0.71, p<0.0001). In the Katse Dam population in the presence of
predators (Figure 4b) there was a significant but weak negative association between
distances travelled from a burrow and the frequency of remaining in situ decreased, both
in summer (r59 = -0.38, p=0.003) and in winter (r58 = -0.49, p<0.0001). Similar patterns
occurred when predators were absent (Figure 4c), although this relationship was only
significant in winter (r59 = -0.27, p=0.04) and not in summer (r64 = -0.16, p=0.20).
In winter, ice rats at Sani Top spent less time in situ as the distance from a burrow
entrance increased (r19 = -0.74, p<0.001) but no clear pattern was observed in summer (r49 = -
0.24, p>0.05; Figure 5a). At Katse Dam, this relationship was weakly negative but significant
when predators were present (summer: r80 = -0.40, p<0.0005; winter: r80 = -0.56, p<0.0005;
Figure 5b) but strongly negative and significant when predators were absent (summer: r80=-
0.60, p<0.0001; winter: r80 = -0.83, p<0.0001; Figure 5c). In all cases, no gender differences
were found.
Discussion
I compared the foraging behaviour of ice rats at Katse Dam, a population that
experiences moderate predation pressure, with ice rats exposed to minimal or no
predation (i.e. Sani Top; Schwaibold and Pillay, unpublished; Chapter 4). By studying
foraging in summer and winter and when predators were absent and present at Katse
93
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
1
0-15 15-30 30-50 50-100 100-
150
150-
200Distance categories (cm)
Fr
eq
ue
nc
y
sp
en
t
in
s
it
u
Summer Winter
(a)
0-15 15-30 30-50 50-100 150-200100-150 >200
; ;
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
1
0-15 15-30 30-50 50-100 100-
150
150-
200
>200
Distance categories (cm)
Fr
eq
ue
nc
y
sp
en
t
in
s
it
u
Summer Winter
(b)
0-15 15-30 30-50 50-100 150-200100-150 >200
; ;
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
1
0-15 15-30 30-50 50-100 100-
150
150-
200
>200
Distance categories (cm)
Fr
eq
ue
nc
y
sp
en
t
in
s
it
u
Summer Winter
(c)
0-15 15-30 30-50 50-100 150-200100-150 >200
; ;
Figures 4. Mean frequency (including minimum and maximum values) of foraging bouts
spent in situ in each distance category by ice rats in summer and winter at Sani Top (a) and at
Katse Dam in the presence (b) and absence (c) of predators. Regression lines: Sani Top -
summer: y = 0.06 ? 0.09x; winter: y = 0.40 ? 0.74x; Katse Dam predators present - summer: y
= 0.77 ? 0.13x; winter: y = 0.75 ? 0.12x; Katse Dam predators absent - summer: y = 0.83 ?
0.13x; winter: y = 0.71 ? 0.11x.
94
0
50
100
150
200
250
300
350
400
450
0-15 15-
30
30-
50
50-
100
T
im
e
sp
en
t
in
s
it
u
(s
ec
on
ds
)
500 (a)
Discussion
0
50
100
150
200
250
300
350
400
450
0-15 15-30 30-50 50-100
Distance categories (cm)
T
im
e
sp
en
t
in
s
it
u
(s
ec
on
ds
)
Summer Winter
0-15 15-30 30-50 50-100
; ;
(b)
0
50
100
150
200
250
300
350
400
450
0-15 15-30 30-50 50-100
Distance categories (cm)
T
im
e
sp
en
t i
n
si
tu
(s
ec
on
ds
)
Summer Winter
0-15 15-30 30-50 50-100
; ;
(c)
Figure 5. Mean duration (including minimum and maximum values) of time spent in situ by
ice rats in summer and winter at Sani Top (a) and at Katse Dam in the presence and absence (b)
of predators (c). Regression lines: Sani Top- summer: y = 172.49 ? 34.46x; winter: y = 138.31
? 39.19x; Katse Dam predators present- summer: y = 124.51 ? 15.92x; winter: y = 108.52 ?
13.11x; Katse Dam predators absent- summer: y = 317.73 ? 55.64x; winter: y = 270.15 ?
66.93x.
95
Dam, I investigated how ice rats respond to two environmental cues: low temperatures
and predation risk.
My data revealed several location/predation risk and seasonal patterns. In
response to predation threat at Katse Dam, O. s. robertsi foraged close to a burrow and
for shorter periods, which would reduce exposure to predators and characterises rodents
foraging in risky habitats (Brown, 1988; Mohr et al., 2003). I recorded similar foraging
behaviour patterns when predators were not observed at Katse Dam, suggesting that the
perceived threat of predators shapes foraging decisions. Perceived safety strongly
influences foraging decisions for animals (Whishaw et al., 1992). However, the
frequency of bouts spent in situ was higher in summer than in winter, indicating that
some decision-making rules change in the absence of predation. I observed a similar
seasonal pattern at Sani Top (minimal predation risk), which I related to higher
thermoregulatory costs in winter (Schwaibold and Pillay, unpublished; Chapter 4).
However, in summer ice rats at Sani Top tended to stay in situ the further they travelled
from a burrow and their foraging time was similar at different distances travelled. While
ice rats at Sani Top made fewer foraging trips regardless of season, ice rats at Katse Dam
foraged more frequently but for shorter periods. Such a trade-off is presumably a
response to predation risk and the need to obtain sufficient energy to meet
thermoregulatory needs (Ludwig and Rowe, 1990; Duriez et al., 2005). Interestingly, ice
rats at Sani Top did not show a similar trade-off in winter (i.e. fewer and shorter
foraging bouts).
The number of foraging bouts spent in situ in summer was significantly greater
than in winter for ice rats at Sani Top (52% in summer and 16% in winter). Similarly,
when no predators were observed at Katse Dam, ice rats spent 35% of their foraging
bouts in situ in summer and only 15% in winter. However in the presence of predators
96
ice rats spent only about 16-18% of their bouts in situ in both seasons. Thus ice rats
respond to low, potentially lethal temperatures in the same way as they do to predation
risk, suggesting that cold temperatures in winter may represent a significant risk. Winter
temperatures (mean air temperatures range from 0?C in winter to 6?C in summer; Grab,
1997) are well below the thermoneutral zone (25.3?C to 28?C) of ice rats (Richter et al.,
1997), so that the benefits of returning to a favourable microclimate, such as a burrow,
with food items may outweigh the costs of energy lost through travelling. Moreover,
individual ice rats defend individual territories aboveground and colony members
compete for limited food in winter (Hinze and Pillay, unpublished), so that returning to a
central place may also reduce intraspecific competition and damaging fights (Willan,
1990).
Central place foraging theory maintains that animals travelling relatively short
distances to a foraging site should return to a central place with food items collected
elsewhere, but should consume food items at the foraging site if the distance travelled is
greater, since the energetic cost of travelling back to cover would be high (Orians and
Pearson, 1979; Lima et al., 1985). Ice rats at Sani Top adopted a central place foraging
strategy in summer (see also Chapter 4): the tendency to consume food items in situ
increased as distance travelled from a central place to a foraging site increased, while in
winter they returned to cover with forage even when the distance travelled increased. In
contrast, in the presence of predators, ice rats displayed the same foraging patterns in
summer and winter and always returned to a central place. Lima (1985) suggests that
animals concerned predominantly with increasing foraging efficiency (i.e. reducing
energy loss) should never carry food back to cover, but if risk avoidance is the main
concern, food items should always be carried back to safety. Several studies indicate
that, in most cases, animals will trade off between these two conflicting needs (Caraco,
97
1979; Sih, 1980; Lima, 1985; Lima et al., 1985).
While it appears that ice rats primarily respond to predation risk, most biotic and
abiotic variables are not constant and vary in time and space. Therefore decision-making
during foraging, like any other behaviour, is motivated by several non-mutually
exclusive internal and external factors. Internal factors include several physiological
mechanisms such as levels of hunger (Milinski and Heller, 1978; Croy and Hughes,
1991; Gentle and Gosler, 2001), previous activity and cumulative thermal budgets
(Bozinovic and V?squez, 1999). Two examples of external factors include (i) patch
quality, which would promote differential exploitation of patches (Stephens and Krebs,
1986; Valone and Brown, 1989), assuming that foraging rate is a function of resource
density (Brown, 1988; Arcis and Desor, 2003); and (ii) food handling time, which would
result in different strategies for staying in situ or returning to a central place, so that if
handling time is very short, one could predict that animals would consume food in situ,
even in risky patches (Lima et al., 1985; Newman, 1991). When faced with
physiological stress, it is predicted that the optimal foraging strategy of a food-deprived
animal would be to maximise instantaneous harvest rate and reduce feeding time
(Bozinovic and V?squez, 1999), thereby minimising exposure to extreme temperatures.
Although I did not quantify the factors motivating foraging behaviour in ice rats, as a
herbivorous rodent they are restricted to a low-calorific high fibre diet (Van Soest, 1982)
and this decreased food quality means that they need to forage for most of the day as
they need to consume more food to gain sufficient energy for survival (Green and Millar,
1987) Also, ice rats are faced with increased energy demands in their cold environment
(Green and Millar, 1987), further reinforcing the need to maximise foraging efficiency.
Harvest time in the absence of predation is relatively short, with ice rats collecting up to
12 mouthfuls per foraging session (U. Schwaibold, pers. obs.). Handling time was
98
variable but never exceeded one minute. No data are available for the harvest rate for ice
rats at risk of predation and as it was difficult to define patch entities within wetland
vegetation, patch use time could not be established for the Sani Top and the Katse Dam
populations. These factors should be considered in future studies to establish a more
definite measure of foraging efficiency in ice rats.
Predation pressure in any environment also varies in space and time (Kotler et
al., 1994), however few studies consider temporal variation in predation risk and its
effects on the foraging behaviour of prey aninmals. V?squez (1994) found that the
nocturnal leaf-eared mouse Phyllotis darwini adjusts its foraging pattern according to a
perceived risk of predation related to an environmental cue (levels of illumination).
Sundell et al. (2004) reported that the foraging behaviour of bank voles Clethrionomys
glareolus (housed in 0.25 ha outdoor enclosures) did not change in response to temporal
variation in predation risk, but foraging effort was significantly lower in high risk areas
compared to low risk areas. In contrast, ice rats did not show spatial variation in predator
response, but rather temporal/seasonal variation (i.e. staying in situ in summer in the
absence of predators). One reason could be differences in habitat structure between the
species, with the bank voles benefiting from cover provided by bush and tall grass
vegetation, and ice rats always occurring in open habitat and therefore being more likely
to detect predators.
In laboratory experiments, Sih (1980) and Nonacs and Dill (ants; 1990) reported
that, if energy demands and predation risk are experimentally manipulated, individuals
will trade off one variable against the other, thereby neither maximising energy gain nor
minimising predation risk. In contrast, in this study, which examined the influence of
more than one environmental cue on foraging behaviour in free-living animals, foraging
behaviour was influenced by predation risk and ambient temperatures (i.e. mainly low
99
temperatures in winter) in a hierarchical fashion. In the presence of predators, the
foraging behaviour of ice rats was similar in summer and winter, indicating that
predation risk is a primary determinant of foraging decisions. The influence of predators
on foraging behaviour is a universal phenomenon (Lima, 1985; Lima et al., 1985;
Milinski and Heller, 1978; Brown, 1988; Lima and Dill, 1990; Kotler et al., 1994; Mohr
et al., 2003; Powell and Banks, 2004; Sundell et al., 2004). In the absence of predators,
O. s. robertsi at Katse Dam still responded to a potential threat, but there were some
differences in behaviour in summer. Moreover, foraging in winter at Sani Top resembled
foraging under predation risk, and it is clear that thermoregulatory homeostasis also
influences foraging behaviour in ice rats (see also Bozinovic and V?squez, 1999).
Facultative foraging responses are adaptive in habitats where animals experience
multiple environmental cues.
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CHAPTER SIX:
Microhabitat selection by the ice rat Otomys sloggetti robertsi in the Sani Valley,
Lesotho
Abstract
We studied the relationship between several environmental factors and the distribution
of the ice rat Otomys sloggetti robertsi in the Sani Valley, Lesotho. Ice rats are
herbivorous burrow-dwelling rodents, endemic to the southern African Drakensberg and
Maluti mountains at altitudes above 2000m. Several parameters including aspect, soil
compactness, soil types and moisture content, percentage vegetation cover and
percentage cover of various plant types were measured along three 500-1000m transect
lines starting at the top of a hill and ending in a wetland. The correlation between the
parameters measured and the presence of occupied ice rat burrows, revealed that the
presence of food plants (i.e. wetland vegetation and other herbaceous plants) were the
main determinants of the presence of ice rats. Unexpectedly, soil characteristics and
vegetation cover were of less importance. Vegetation cover as well as plant community
structure differed significantly between areas occupied and unoccupied by ice rats in
both summer and winter. The data indicate that habitat selection by the ice rat is
primarily determined by proximity to food plants, thereby reducing the distances
travelled to forage and thus decreasing the time exposed to low temperatures.
Key words: Otomys sloggetti robertsi, alpine environment, habitat selection, vegetation
106
Introduction
The ice rat Otomys sloggetti robertsi (Muridae, subfamily Otomyinae) is
endemic to the alpine and subalpine regions of the Drakensberg and Maluti mountains in
southern Africa, and is restricted to altitudes above 2000 m (Killick, 1978). Despite its
occurrence in such harsh environments, it does not hibernate (Willan, 1990) and shows
little physiological adaptations to cold conditions (Richter et al., 1997). Instead, ice rats
have morphological (e.g. small ears and tail; Richter, 1997) and behavioural adaptations
(e.g. sun-basking, timing aboveground activity with favourable conditions; Willan, 1990;
Hinze and Pillay, unpublished). They are diurnal and live in colonies of up to 16
individuals which construct complex underground burrow systems that provide
opportunities for social huddling (Hinze et al., submitted), even though aboveground
social interactions are generally characterised by high levels of aggression among colony
members, especially in winter (Hinze and Pillay, unpublished). An important
consideration is that the growing season in the ice rat?s habitat is restricted to six to
seven months in a year, interrupted by very cold winters, often characterised by heavy
snowfall (Killick, 1978), which limits the availability of high quality food (Willan,
1990).
Like their otomyine relatives, which occur in the driest (e.g. whistling rats
Parotomys spp.) and wettest (e.g. vlei rats Otomys spp.) parts of southern Africa
(Skinner and Smithers, 1990), ice rats are specialist herbivores, feeding more or less
exclusively on plant material including herbaceous stems, leaves, flowers and grasses
(Schwaibold and Pillay, unpublished data). I reported in an earlier study that ice rats
have a longer small intestine compared to its closest mesophyllic and xerophyllic
relatives, which is likely to facilitate an increased energy uptake from a high fibre
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herbivorous diet to meet greater metabolic requirements in cold environments
(Schwaibold and Pillay, 2003).
The ice rat has been poorly studied in the past, possibly because of the remote
areas it occupies. However, information is available for microhabitat selection in some
of its relatives occurring at lower altitudes. Like O. s. robertsi, Parotomys brantsii and
P. littledale, which are endemic to the arid western parts of southern Africa, also
construct complex underground burrows (Jackson, 2000). Due to the complexity of these
burrow systems, the distribution of P. brantsii and P. littledale is strongly influenced by
suitable soil to construct burrows (du Plessis and Kerley, 1991; Jackson, 2000). While P.
brantsii constructs burrows in both closed areas and areas with limited plant cover, P.
littledale is restricted to areas with cover (Jackson, 2000). Similarly the bush Karoo rat
O. unisulcatus, another arid-living relative, is restricted to areas with good plant cover
(du Plessis and Kerley, 1991). This species constructs characteristic ?lodges? with
collected sticks under or in which it nests, and habitat selection seems to be driven by the
nature of the woody vegetation, which provide opportunities for constructing these
lodges (Vermeulen and Nel, 1988; Brown and Willan, 1991) and for food (Brown and
Willan, 1991).
Comparative information is available for only two mesic occurring otomyines in
southern Africa. The vlei rats O. irroratus and O. angoniensis inhabit the more mesic
eastern parts of southern Africa (Skinner and Smithers, 1990), with the former inhabiting
areas along wetlands or vleis, and the latter being restricted to the drier areas close to
water bodies or wetlands (Skinner and Smithers, 1990), particularly when these two
species occur syntopically. Both species nest under overhanging grass or rocks, although
they will use abandoned burrows of other animals (Davis, 1972; Packer, 1980; Phillips et
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al., 1997). Therefore, the habitat requirements of both species are strongly associated
with cover provided by plants (Willan, 1982; Pillay, 1993; Phillips et al., 1997).
Our study was designed within a framework of a broader behavioural ecological
investigation to ascertain the microhabitat requirements and use by O. s. robertsi. In a
recent review of microhabitat use by small mammals, Jorgensen (2004) argued that the
concept of microhabitat is clouded by imprecise definition and biased by modest
sampling effort, mainly because of the use of small spatial scales and because the
responses of small mammals to similar and different microhabitats in adjoining
vegetation are not considered. To address these concerns, I define microhabitat as being
composed of environmental variables that affect individuals (after Morris, 1987) within
their home range (after Johnson, 1980; Morris, 1987). In addition, I studied the
distribution of ice rat colonies at two spatial scales. Firstly, I sampled along three
transect lines with varying aspect, vegetation type and cover, and soil characteristics, to
establish the relationships between these parameters and colony location. Secondly, I
compared vegetation types and cover in areas occupied by ice rats and in adjoining
unoccupied areas; measurements were made in summer and winter to investigate
seasonal changes. I asked two broad questions. 1) Is the ice rat microhabitat distribution
limited by soil qualities appropriate for burrowing? In particular, do ice rats prefer areas
with softer, drier soils? 2) Does plant type influence their microdistribution? How do the
distribution of wetland and herbaceous vegetation (food) and woody vegetation (cover)
influence the distribution of ice rats?
For central place foragers like the ice rat (Schwaibold and Pillay, unpublished;
Chapter 4), microhabitat selection is coupled with the optimal use of resources
(Rosenberg and McKelvey, 1999). The distribution of these resources within a selected
microhabitat will affect the size of the animal?s home range (Rosenberg and McKelvey,
109
1999). It is not clear though what drives the choice of habitat for a central place forager.
Choice can be based on the proximity of resources, but also on the habitat requirements
of that central place, such as a nest or burrow (Rosenberg and McKelvey, 1999).
Study area
The study was undertaken in one of valleys of the Sani River (29? 37? S; 29?14? E),
about 5 km west of Sani Top in the south- eastern Maluti Mountains, Lesotho at an
altitude of about 2900m. The weather conditions in the Lesotho highlands area are harsh
and unpredictable, with mean air temperatures ranging from 6? C in summer to 0? C in
winter (Grab, 1997). Rainfall is high (mean annual ~1200 mm), and snow can be
expected at any time of the year (Willan, 1990). The high plateaus of Lesotho are prone
to strong winds blowing towards the escarpment during most of the day; the early
morning hours are usually calmest. Shrubs and herbs (annuals and biennials, woody
cushion plants and succulents, aquatics and alien plants) are found most commonly in
the Sani Valley, and trees were absent in my study area; vegetation rarely exceeded
0.5m.
After an extensive search of Sani Top and the surrounding areas for the presence
of ice rats (ice rats are easily observed in nature because of the short vegetation) and the
presence of their distinctive burrow entrances (Hinze et al., submitted), I selected an area
of 6 ha for my study, which comprised an area located along the fringes of one of the
many wetlands in this valley.
Materials and methods
The study took place between May 2000 and January 2002 inclusive. Fieldwork
totalled 14 days. Reference collections of all plants species collected on site have been
110
prepared as voucher specimens and are housed in the CE Moss Herbarium of the
University of the Witwatersrand.
Transect sampling
To ascertain the microhabitat selection of O. s. robertsi in the study site, several
parameters were measured along three different transect lines of between 500 and 1000
m long, starting from the edge of the wetland to the top of the hills surrounding the
wetland (Figure 1). At every 50 m interval, I noted the presence or absence of active
burrows (i.e. burrows that were inhabited by ice rats) and measured the slope (aspect)
using a dumpy level and soil compactness using a penetrometer. In addition, soil
samples (approximately 100-150 g) were collected at a 20 cm depth, weighed and taken
back to the University of the Witwatersrand in sealed airtight plastic bags to calculate
soil moisture content. Soil types (or classes) were established by determining the
proportions of silt, clay and sand in the soil samples through a particle size distribution
(Hillel, 1982). The particle size distribution data were used to determine soil texture
using a texture triangle (Hillel, 1982). At each 50m interval, I also estimated the overall
percentage vegetation cover from 10 1m2 quadrates, as well as the mean percentage
cover of the major vegetation type (i.e. Helichrysum bushes, grass, herbaceous and
wetland vegetation).
Plant community structure
I compared the vegetation in 10 occupied (identified by the presence of burrows that
were being used by ice rats) and 10 unoccupied areas using a paired designed. I selected
occupied areas of at least 5m2 in size and sampled the vegetation using a semi-random
sampling method: a 5m x 5m string frame subdivided into 0.5 x 0.5 m blocks was laid
Transect
lines
Colonies
111
Figure 1. Map of the study site near Sani Top, Lesotho, indicating the position of the colonies selected for study as well as the transect lines. Since the
boundaries of the wetland and Helichrysum sections were seasonally dynamic, boundary lines are estimated for summer.
50 m
N
Dirt road
Wetland
Helichrysum spp.
Slope
Wetland
112
over the sampling area. In 10 random 0.5m x 0.5m blocks (selected using a random
numbers table), I calculated the plant species composition and frequency (proportion of
blocks within which a species occurred), mean percentage vegetation cover (proportion
of the ground covered by the aerial parts of the plant) as well as mean percentage cover
of woody vegetation (predominantly Helichrysum spp.), grasses, herbaceous plants and
wetland vegetation. Using the same techniques, measurements were also made in
unoccupied areas, which were 15 m away from occupied areas; unoccupied areas were
selected if they contained the same broad vegetation type (e.g. wetland plants, bushes) to
avoid biasing the sampling.
Diet
The general diet of the ice rat was determined during 150 hours of direct observations
using 10x50 binoculars. I recorded the foraging behaviour of ice rats in different patches,
and determined the vegetation types present and, where possible, food plants were
identified to species level.
Data analysis
Regression analyses were used to assess the relationships between the presence of active
burrows and each of the environmental factors measured along the transects. A general
discriminant analysis was then performed to establish the relationship between
combinations of environmental parameters and the presence of ice rats.
For the analysis of plant community structure, mean percentage cover was
calculated for each occupied and unoccupied patch, and a Wilcoxon paired rank test
(abbreviated H) was used to compare the vegetation cover between occupied and
unoccupied areas in all four sample months (two months per season). Bonferroni
113
adjustments were used to establish specific differences. Seasonal differences in plant
cover were established by calculating the difference between the percentage cover of
occupied and unoccupied areas and comparing the relative difference using a Mann-
Whitney-U test (abbreviated Z). The frequency of species occurring in occupied and
unoccupied areas was compared for each sample month using a ?2 contingency table.
Results
Transect sampling
General regression analyses revealed that the presence of occupied ice rat burrows was
correlated with only two environmental factors measured. There was a significant
relationship with the presence of herbs (wetland plants and herbaceous vegetation; r63 =
0.45, p<0.001) and the absence of Helichrysum (taller bushy vegetation; r63= -0.44,
p<0.001). A discriminant analysis revealed that a high percentage cover of herbaceous
vegetation (excluding all woody vegetation and grasses) significantly influenced the
presence of ice rats (?1,54 = 4.89, p=0.03). The data indicate that slope/aspect was not
important (?1,54 = 2.20, p=0.89), which was confirmed by my observations of burrows in
both the flattest and steepest areas along the transects. Soil moisture content was also not
significant (?1,54 = 0.01, p=0.97), since burrows were found in the wettest and driest
areas. Burrows also occurred in both compact and the soft soils (?1,54 = 1.03, p=0.32), in
various soil types (?5,54 = 1.39, p=0.24) and with varying overall vegetation cover (?1,54
= 0.86, p=0.36).
Plant community structure
There were no differences in respect of vegetation cover between months of the same
season, and the data were pooled by season. Predictably, vegetation cover (Table 1) was
114
Table 1. Mean (? SE) percentage vegetation cover and dominant species/vegetation
types in areas occupied and unoccupied by O. s. robertsi in summer and winter.
Season Use % Cover Dominant Vegetation1
occupied 57.96 ? 4.61
grasses
wetland plants
Geranium multisectum
Helichrysum sp
Winter
unoccupied 86.58 ? 3.27
grasses
wetland plants
Haplocarpha nervosa
Ranunculus multifidus
occupied 56.28 ? 1.86
grasses
wetland plants
Geranium multisectum
Summer
unoccupied 83.76 ? 2.73
grasses
wetland plants
Geranium multisectum
Ranunculus multifidus
1 Taxonomic name provided if known.
significantly greater in unoccupied areas than in occupied areas, both in summer (H10,10 =
3.92, p<0.0001) and winter (H10,10 =3.88, p<0.0005). Relative differences in vegetation
cover between occupied and unoccupied areas (i.e. mean cover in occupied areas ? mean
115
cover in unoccupied areas) revealed no significant variation between summer (27.49%)
and winter (28.62%; Z10,10 = 0.15, p=0.88).
Woody vegetation was sparse in both occupied and unoccupied patches, while
herbaceous vegetation cover ranged from 30-100% in both patch types. Grasses and
herbs occurred most frequently in both occupied and unoccupied areas, although there
was no consistent difference between occupied and unoccupied areas with regard to the
most common plant species present (Figure 2). Haplocarpha nervosa was the dominant
wetland species, followed by Ranunculus multifidus (wetland plants present are listed in
Table 2). No significant differences were found in overall plant frequencies between
occupied and unoccupied areas in May (?2 11= 6.33, p>0.05), August (?2 8= 4.60, p>0.05),
October (?2 11= 3.70, p>0.05) and November (?211 = 5.48, p>0.05).
0
5
10
15
20
25
30
35
40
45
GR SE HC Hsp HT CL GM HN HF Tsp Other
M
ea
n
fr
eq
ue
nc
y
of
s
pe
ci
es
(
%
) occupied unoccupied
Figure 2. Mean (?SE) percentage frequencies of various plant species in areas occupied and
unoccupied by O. s. robertsi (GR=Pentaschistis sp; SE=Wetland plants; HC = Helichrysum
cymosum; Hsp=H. sp; HT=H.trilineatum; CL = Crassula lanceolata; GM = Geranium
multisectum; HN = Haplocarpa nervosa; HF = Helichrysum flanaganii; Tsp = Taraxacum sp.
116
Table 2. Dominant species of the woody and herbaceous vegetation in areas occupied
and unoccupied by O. s. robertsi at Sani Top and the plant species consumed by ice rats.
Vegetation Type Species Consumed by ice rats
Grasses Pentaschistis oreodoxa Yes
Limosella vesiculosa Yes
Trifolium burchellianum Yes
Ranunculus multifidus Yes
Haplocarpha nervosa Yes
Cotula paludosa Yes
Wetland Plants
Saniella verna Yes
H. cymosum No
H. subglomeratum No
H. trilineatum No
Helichrysum sp.
H. flanaganii No
Crassula lanceolata No
Geranium multisectum Yes
Selago flanaganii Yes
Selago galpinii No
Other herbaceous vegetation
Eumorphia sericea No
Diet
Behavioural observations of the foraging patterns of O. s. robertsi revealed that its diet
consisted predominantly of wetland plants and herbaceous vegetation (Table 2). Both the
117
green and floral parts of H. nervosa were consumed and collected by ice rats.
Herbaceous and floral parts of R. multifidus and Trifolium burchellianum were also
eaten but to a lesser extent. I did not observe ice rats feeding on Helichrysum spp.
Discussion
The microhabitat selection and use by burrowing small mammals is influenced by
several environmental parameters, including food availability (Rosenberg and
McKelvey, 1999), plant species composition (Brown and Willan, 1991), cover
(Falkenberg and Clarke, 1998; Jackson, 2000) and soil characteristics (du Plessis and
Kerley, 1991).
The Afro-alpine giant molerat Tachyoryctes macrocephalus appears to select
suitable habitats according to, among other factors, soil moisture content, as burrows
were found mainly along seasonally waterlogged swamps (Sillero-Zubiri et al., 1995).
Neither aspect nor soil composition (i.e. soil type, moisture content) were good
predictors of the location of O. s. robertsi colonies. Ice rats are known to construct
burrows in soil substrates differing in water content, such as harder organic and softer
mineral soils, and interestingly, burrow systems were more extensive and complex in the
harder organic soils than in softer sandy soils (Hinze et al., submitted). Reasons for the
these differences in burrowing behaviour are not fully understood but may be related to
soil compactness, although both this study as well as the study by Hinze et al.
(submitted) suggest that soil characteristics do not influence habitat choice. However, I
found that previously waterlogged tunnel systems (i.e. burrows that were flooded due to
spring rains and melting ice in the wetland) were not re-inhabited and no burrows were
found in the wetland (which was not included in the transect; pers. obs.), possibly due to
the high risk of flooding in summer and freezing over in winter.
118
Of the five environmental variables measured, only the presence of herbaceous
plant material and the absence of woody Helichrysum species influenced the
microhabitat distribution of ice rats. The diet of ice rats consists mainly of relatively
fresh plant material, such as wetland vegetation and other herbaceous species. Two
advantages appear to accrue to O. s. robertsi as a result of occupying patches with food
plants. 1) Travelling short distances to forage may be related to a need to minimise
energy loss through exposure to cold temperatures (Johnson and Cabanac, 1982),
particularly since ice rats are physiologically poorly adapted to extreme cold (Richter et
al., 1997). As herbaceous food quality decreases in winter (Van Soest, 1982) and more
food needs to be ingested to meet increased metabolic requirements (Batzli and Cole,
1979), reducing energy loss through travel is essential. Indeed, ice rats are central place
foragers, which very rarely forage more that a metre away from the nearest burrow
entrance (Schwaibold and Pillay, unpublished; Chapter 4). 2) Despite its colonial
existence, members of an ice rat colony maintain defined territories aboveground
apparently to defend food patches, and interactions between colony members are rare but
mostly aggressive when they meet (Hinze and Pillay, unpublished). Therefore, feeding
within the confines of the home range may reduce intraspecific competition. Similarly,
P. brantsii is able to reduce competition with its two potential counterparts, P. littledalei
and O. unisulcatus, by foraging almost entirely within the limits of its burrow system,
thereby gaining access to otherwise unavailable resources and eliminating the need for
extensive plant cover for protection (Jackson, 2000).
In many rodents, predation pressure may drive selection for areas with extensive
cover, whereas interspecific competition may result in the use of areas with poor cover
(reviewed in Falkenberg and Clarke, 1998), and the rationale for many studies of
microhabitat use in small mammals has been to understand microhabitat partitioning
119
between syntopic species (see Jorgenson, 2004). Both of these factors do not appear to
influence ice rat distribution. Based on our observations over the past 13 years, predation
pressure in the Sani Valley is negligible (as it is in most localities where ice rats occur;
Willan, 1990), and the ice rat here does not share its habitat aboveground with other
small mammals, although the appearance of distinctive mounds suggests that mole-rats
also occurred at my study site.
The absence of woody vegetation in ice rat colonies was unexpected, as
Helichrysum spp. bushes would provide adequate cover from possible predators (which
are discounted here) and, more importantly, would act as a wind break (see Willan,
1990). However, Helichrysum spp. is not consumed and its presence may affect the
microclimate experienced close to the ground due to shading (Eurola et al., 1984),
thereby influencing the growth of food plants consumed by ice rats. In another study, I
showed that ice rats spend a large proportion (28-38%) of their aboveground activity
engaged in sun-basking (Schwaibold and Pillay, unpublished; Chapter 3). Basking is an
important behavioural thermoregulatory activity, shared by many other alpine rodents
(e.g. marmots Marmota spp.; Barash, 1989), and which may compensate for the reduced
energy intake from lower quality food in winter by accelerating the warming-up process
to a level that allows for uninterrupted activity with very little thermoregulatory cost
(Sale, 1970; Geiser, et al., 2002). Marmots also facilitate energy gain during cold
periods by utilising radiant energy through basking as this may compensate for the
reduced energy intake from lower quality food in winter and thus allow for metabolic
requirements to be met. I suggest that excess woody vegetation in an ice rat colony,
which can reach up to 50 cm in height, may result in increased shading of the colonies
which in turn may negatively influence basking opportunities.
120
Vegetation cover in areas occupied by ice rats was significantly less than in
unoccupied areas in both summer and winter. One reason may be that they select areas
with less cover due to the need for sun-basking. This is unlikely, however, and a more
plausible explanation may be that the foraging activity of ice rats reduces cover. This
highlights the fact that cover is not an important determinant of ice rat microdistribution.
The arid-occurring otomyine Parotomys brantsii requires deep sandy soils to
construct complex burrow systems (du Plessis and Kerley, 1991), which determine the
habitats it occupies within its distribution range. In contrast, ice rats are not limited by
soil type, and instead locate their colonies in food patches. Although I did not measure
the production of edible plant material, the high density of ice rats (up to 100 individuals
per ha; Hinze and Pillay, unpublished), suggests that the carrying capacity for ice rats in
my site is high. Nonetheless, Willan (1990) and later Lynch and Watson (1992)
maintained that the population numbers appeared to be regulated by density dependent
mortality due to resource-limitation during the cold winters, coupled with prolonged
periods of snowfall.
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Stanford.
Batzli, G.O. and Cole, F.R. (1979). Nutritional ecology of microtine rodents:
digestibility of forage. J. Mammal. 60: 740-750.
Brown, E. and Willan, K. (1991). Microhabitat selection and use by the bush Karoo rat
Otomys unisulcatus in the Eastern Cape Province. S. Afr. J. Wildl. Res. 21: 69-75.
Davis, R. M. 1972. Behaviour of the vlei rat, Otomys irroratus (Brants, 1827). Zool. Afr.
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7: 119-140.
du Plessis, A. and Kerley, G.I.H. (1991). Refuge strategies and habitat segregation in
two sympatric rodents Otomys unisulcatus and Parotomys brantsii. J. Zool., Lond.
224: 1-10.
Eurola, S., Kuyll?nen, H. and Laine, K. (1984). Plant production and its relation to
climatic conditions and small rodent density in Kilpisj?rvi region (69?05?N,
29?40?E), Finnish Lapland. In: Winter Ecology of Small Mammals (Ed. by J. F.
Merritt). Carnegie Museum of Natural History Special Publication No. 10.
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Falkenberg, J.C. and Clarke, J.A. (1998). Microhabitat use of deer mice: effects of
interspecific interaction risks. J. Mammal. 79: 558-565.
Geiser, F., Goodship, N. and Pavey, C.R. (2002). Was basking important in the
evolution of mammalian endothermy? Naturwissenschaften 89: 412-414.
Grab, S. (1997). An evaluation of the periglacial morphology in the High Drakensberg
and associated environmental implications. Ph.D. thesis, University of Natal,
Pietermaritzburg.
Hillel, D. (1982). Introduction to soil physics. Academic Press, London.
Hinze, A., Pillay, N. and Grab, S. The burrow system of the African ice rat Otomys
sloggetti robertsi: adaptation for living in cold environments. Submitted.
Jackson, T.P. (2000). Adaptations to living in an open arid environment: lessons from
the burrow structure of the two southern African whistling rats, Parotomys brantsii
and P. littledalei. J. Arid Environ. 46: 345-355.
Johnson, D. H. (1980). Comparison of usage and availability measurements for
evaluating resource preference. Ecology 61:65-71.
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Johnson, K.G. and Cabanac, M. (1982). Homeostatic competition in rats fed at varying
distances from a thermoneutral refuge. Physiol. Behav. 29: 715-720.
Jorgensen, E.E. (2004). Small mammal use of microhabitat reviewed. J. Mammal. 85:
531-539.
Killick, D.J.B. (1978). The Afro-alpine region. In: Biogeography and ecology of
southern Africa. (Ed. by M.J.A. Werger). Junk, The Hague, pp 515-560.
Lynch, C. D. and Watson, J. P. (1992). The distribution and ecology of Otomys sloggetti
(Mammalia: Rodentia) with notes on its taxonomy. Navorsinge van die Nasionale
Museum Bloemfontein 8: 141-158.
Morris, D. W. (1987). Ecological scale and habitat use. Ecology 68:362?369.
Packer, W. C. (1980). Nest-building and activity patterns in four sympatric rodent
species. S. Afr. J. Zool. 15: 50-55.
Phillips, J., Kearney, T., Pillay, N. and Willan, K. (1997). Reproduction and postnatal
development of the Angoni vlei rat Otomys angoniensis (Rodentia, Muridae),
Mammalia 61: 219-229.
Pillay, N. (1993). The evolution and socio-ecology of two populations of the vlei rat
Otomys irroratus. Ph. D. thesis (unpublished). University of Natal, Durban.
Richter, T.A. (1997). Does the southern African ice rat (Otomys sloggetti) show
morphological adaptation to cold? J. Zool., Lond. 242: 384-387.
Richter, T.A., Webb, P.I. and Skinner, J.D. (1997). Limits to the distribution of the
southern African Ice Rat (Otomys sloggetti): thermal physiology or competitive
exclusion? Funct. Ecol. 11: 240-246.
Rosenberg, D.K. and McKelvey, K.S. (1999). Estimation of habitat selection for central-
place foraging animals. J. Wildl. Manage. 63: 1028-1038.
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Sale, J.B. (1970). The behaviour of the resting rock hyrax in relation to its environment.
Zool. Afr. 5: 87-99.
Schwaibold, U. and Pillay, N. (2003). The gut morphology of the African ice rat,
Otomys sloggetti robertsi, shows adaptations to cold environments and sex-specific
seasonal variation. J. Comp. Physiol. B 173: 653-659.
Sillero-Zubiri, C., Tattersall, F.H. and Macdonald, D.W. (1995). Habitat selection and
daily activity of giant molerats Tachyoryctes macrocephalus: significance to the
Ethiopian wolf Canis simensis in the afroalpine ecosystem. Biol. Conserv. 72: 77-
84.
Skinner, J.D. and Smithers, R.H.N. (1990). The mammals of the southern African
subregion. University of Pretoria, Pretoria.
Van Soest, P.R. (1982). Nutritional ecology of the ruminant. O and B Books. Corvallis,
Oreg.
Vermeulen, H.C. and Nel, J.A.J. (1988). The bush Karoo rat Otomys unisulcatus on the
Cape West coast. S. Afr. J. Zool. 23: 103-111.
Willan, K. (1982). Social ecology of Otomys irroratus, Rhabdomys pumilio and
Praomys natalensis. Ph. D. thesis (unpublished). University of Natal,
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35: 39-51.
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CHAPTER SEVEN: Discussion
The ice rat Otomys sloggetti robertsi is an interesting model to study the effects
of low temperatures on the behaviour patterns of small mammals as it is one of
only few high altitude small mammals that does not hibernate or display torpor.
It shows poor physiological adaptations (Richter et al., 1997) and apparently
shows a range of morphological and behavioural adaptations for life in cold
alpine habitats (De Graaff, 1981; Willan, 1990; Richter et al., 1997). Little was
known about the ice rat before this study, and I studied the behavioural and
morphological responses in respect of foraging in O. s. robertsi by investigating
its gut morphology, aboveground behaviour (mainly foraging behaviour) and
habitat choice.
Gut structure
The aim of the study was to establish whether the gut of ice rats is modified for low food
quality and high energy demands associated with the cold Lesotho environment. The
morphology of the digestive system of ice rats is well adapted for a high fibre,
herbivorous diet, as is the case with all other otomyines (Perrin and Curtis, 1980).
Compared to both its mesic and xeric-occurring relatives, there were directional
modifications of the gut including an increase in length of the large intestine and colon,
and an increase in stomach volume. Both hibernating and non-hibernating small
mammals in cold environments display an increase in size of these organs (Silby, 1981;
Hammond and Wunder, 1991), suggesting that such anatomical modifications may be
adaptations to coping with cold conditions as they facilitate increased energy uptake
through improved breakdown of low quality/high fibre plant material and increase the
125
surface area available for absorption of high energy dietary components (Silby, 1981;
Schieck and Millar, 1985).
Seasonal gender differences were also found with females increasing dimensions
of the stomach, small intestine, caecum, and large intestine in summer. This sexual
dimorphism in gut structure may be related to increased energy requirements of females
during pregnancy and lactation (Weiner, 1987; Silby et al., 1990).
Seasonal variation in aboveground behaviour patterns
An animal?s fitness depends on its ability to effectively allocate its time and energy to
competing behavioural demands (Schoener, 1971; Schultz et al., 1999). I investigated
the variation in aboveground behaviour of O. s. robertsi in response to seasonal changes
in temperature. Ice rats face the conflicting demands of energy gain and energy
conservation, and my study suggests that foraging behaviour is traded off against
thermoregulation in winter, while ice rats escape high ambient temperatures and solar
radiation levels during the middle of the day in summer by disappearing belowground.
Due to the increased metabolic rate of small mammals (Schultz et al., 1999) it is
predictable that ice rats should spend most of their time on energy acquisition and
energy conservation. Furthermore, the food available in the habitats of ice rats is of low
quality due to a high fibre content (Killick, 1978; Green and Millar, 1987), resulting in
an increase in foraging activity to meet metabolic requirements, particularly in winter
when ambient temperatures were around freezing point. In winter, ice rats also spent
much time basking, thus gaining energy through radiant heat. Similar behaviour patterns
are found in other high-altitude small mammals such as marmots (Marmota spp.), which
show seasonal changes in activity with foraging increasing in preparation for hibernation
126
(Barash, 1989). Marmots spend much of their day basking to facilitate energy gain
through radiant heat (Barash, 1989), but they will avoid the afternoon heat by escaping
underground (T?rk and Arnold, 1988).
Foraging strategies ? predation versus thermoregulation
Foraging behaviour is strongly influenced by a variety of environmental factors (e.g.
weather conditions; Sergio, 2003; food availability; Belovsky and Slade, 1986). I
investigated the effects of seasonal differences on the foraging decisions of O.s. robertsi.
Ice rats are central place foragers and their foraging behaviour at my primary field site
(i.e. Sani Top) in the absence of predators appears to be strongly influenced by seasonal
changes in environmental conditions: in summer, ice rats remained in situ as the distance
from a burrow increased, conforming to predictions made by central place foraging
theory. In contrast, in winter, foraging patterns were determined by low temperatures,
with ice rats returning to the protection of their burrows with forage regardless of
distance travelled.
Since predation risk is often regarded as the main factor dictating foraging
behaviour in small mammals (Lima, 1985; Brown, 1988; Lima and Dill, 1990; Kotler et
al., 1994; Mohr et al., 2003; Powell and Banks, 2004; Sundell et al., 2004), I also
studied the foraging behaviour of ice rats near Katse Dam; this population experiences
moderate levels of predation, particularly from birds of prey. I tested how ice rats
respond to two environmental cues: low temperatures and predation risk. In addition, I
established foraging behaviour in the presence and absence of predators. Ice rats
responded to the presence of predators by always foraging close to a burrow and for
shorter periods in both summer and winter, in contrast to ?optimal? foraging patterns in
the absence of any predation threat in summer, when ice rats were more likely to forage
127
in situ as distances from a burrow increased, indicating that predation is the main
determinant of foraging behaviour. The foraging behaviour of ice rats in winter without
the risk of predation matched the behaviour of ice rats facing predation pressure,
indicating that low temperatures pose as significant a threat as predation.
Habitat choice
I set out to identify the microhabitat requirements of O. s. sloggetti. Of all the
environmental factors recorded, the presence of herbaceous vegetation and the absence
of woody vegetation appeared to constitute suitable microhabitats for ice rats, suggesting
that habitat choice may be related to the presence of food plants and reduction of shade.
Habitat selection is influenced by multiple variables including the intrinsic
features of an animal as well as biotic and abiotic environmental factors (V?squez,
1996), of which predation risk is thought to be one of the most important factors
influencing space use (Kotler et al., 1994). As food patches within any given habitat will
vary with regards to the effort required to select suitable forage, habitat selection is often
dependent on physiological trade-offs and constraints (Bozinovic and V?squez, 1999)
and the choice of habitat translates as fitness consequences (Jorgensen, 2004). For
central place foragers, microhabitat selection is usually associated with the optimal use
of resources as well as the habitat requirements of their central place, such as a nest or
burrow (Rosenberg and McKelvey, 1999). The proximity to forage allows them to
reduce exposure to risks such as predation (Lima, 1985) and temperature.
Biology of other otomyines
The murid subfamily Otomyinae consists of representatives living in a variety of habitats
in sub-Saharan Africa (Kingdon, 1997). Although very little is known about many
128
otomyine species (De Graaff, 1981; Skinner and Smithers, 1990), published information
is available for several species (reviewed in the introduction), and I compare my results
with information for these species in this section.
Ice rats are apparently closely related to arid-occurring southern African
otomyines species (see introduction). One of these, Brants? whistling rat Parotomys
brantsii, prefers areas with deep sandy soils within relatively open areas (Jackson, 2000)
to construct complex underground burrow systems (du Plessis and Kerley, 1991) which
provide a suitable microclimate, buffering temperature extremes above ground (Jackson,
2000). In contrast, not much is known about the habitat requirements of Littledale?s
whistling rat P. littledalei which also constructs complex underground burrow systems
with several nest chambers, although it is thought that the association of these warrens
with areas providing good cover could reduce risk of predation (Jackson, 2000). The
bush Karoo rat O. unisulcatus prefers areas with suitable woody vegetation to construct
its stick lodges and for food (Brown and Willan, 1991). Although little is known about
the behaviour of P. littledalei or the thermal characteristics of lodges of O. unisulcatus, it
is likely that their nesting habits are adapted for life in harsh arid environments (Brown
and Willan, 1991; Jackson, 2000). All three species forage in close proximity to the nest
site, apparently to reduce predation risk (Brown and Willan, 1991; Coetzee and Jackson,
1999; Jackson, 2001).
Unlike the arid-occurring otomyines, the mesic-occurring vlei rats O. irroratus
and O. angoniensis do not excavate complex underground warrens. Instead they nest
under overhanging grass or rocks and will occasionally use abandoned burrows of other
animals (Davis, 1972; Packer, 1980; Phillips et al., 1997), and the habitat requirements
of both species are strongly associated with adequate plant cover (Willan, 1982; Pillay,
1993; Phillips, et al., 1997).
129
Details of foraging behaviour are available only for P. brantsii, possibly because,
like O. s. robertsi, it is easily observed in nature. Jackson (2000) reported that P. brantsii
is a central place forager. Individuals travel up to 200 cm from their burrows to forage,
generally carrying larger food items back to be consumed under cover or storing them
underground, and foraging bouts increase significantly in the afternoons in preparation
for the night (Jackson, 2001). In turn, P. littledalei is hardly ever found to leave the
protective cover of bushes and shrubs to forage (Coetzee and Jackson, 1999).
Although the foraging patterns of the other otomyine species has not been
studied in great detail, some general information is available. Otomys unisulcatus
forages on the ground or aboreally and restricts its foraging activity to between 5-10 m
of cover, sometimes retreating to cover with collected food items, possibly as an anti-
predator tactic (Brown and Willan, 1991), suggesting that it, too, is a central place
forager to some degree.
Coping with cold conditions
Optimal foraging theory maintains that an animal performs a particular activity
depending on associated costs and benefits (Schoener, 1971). Models generated from
optimal foraging theory emphasise foraging strategies, since these form the major
components of energy acquisition (Stephens and Krebs, 1986). When foraging, an
animal makes particular decisions that are thought to be optimal in terms of energy
intake rate (Stephens and Krebs, 1986), although this depends on the ecological context
in which foraging takes place (Bozinovic and V?squez, 1999). Theoretically,
maximising energy gain through foraging enhances fitness (Schoener, 1971).
While the role of predation in influencing foraging is well documented (Lima,
1985; Lima et al., 1985; Milinski and Heller, 1987; Brown, 1988; Lima and Dill, 1990;
130
Kotler et al., 1994; Powell and Banks, 2004; Sundell et al., 2004), thermal conditions
also influence foraging decision making (Bozinovic and V?squez, 1999) because
ambient temperatures influence thermoregulatory homeostasis in animals. Since
physiological states influence behavioural motivation (Dugatkin, 2004), it is predicted
that in cold environments (i.e. under physiological stress) animals should follow energy-
maximising foraging patterns. Indeed, animals exposed to cold conditions adjust their
behaviour patterns to facilitate increased foraging, thus increasing overall energy intake
(see Johnson and Cabanac, 1982; Perrigo and Bronson, 1985). Lima (1985) suggests that
returning to cover for food consumption could provide thermal benefits compared to
foraging in the open, and the conflict between the benefit of reduced exposure to cold
and the cost of travelling back to cover may resemble foraging responses under
predation risk. Thus, depending on the extent of thermal stress, it would be expected that
food would be consumed under cover if the benefits of foraging in a thermally stable
microenvironment outweigh the costs of travel, while foraging in situ should occur if
energy lost through travel outweighs energy saved from foraging under cover.
The climate of the Lesotho highlands is characterised by a low temperature
profile and high rainfall; the growing season is short and primary productivity is low
(Killick, 1978). Willan (1990) describes the climate within the distributional range as
predictably harsh. Ice rats are adversely affected by low temperatures in their habitats
and they experience density-dependent mortality in winter because of diminishing food
resources (Willan, 1990).
While many small mammals in cold environments hibernate or go into torpor to
conserve energy during cold periods (M?ller, 1986; Barash, 1989; Geiser and Ruf,
1995), non-hibernating small mammals might compensate for the lack of hibernation
and torpor by maximising energy gain during this time. The results of my study indicate
131
that O. s. robertsi appears to be very efficient in its energy gain by reducing exposure to
low temperatures. It travels short distances to forage and, in winter, it returns to a burrow
with forage, regardless of distance travelled. Colonies are established in areas with food
plants. Apart from providing a thermal buffer against lethal temperatures and high levels
of solar radiation aboveground, the complex underground burrow system of ice rats
(Hinze et al. submitted) would promote foraging in close proximity to food, thereby
reducing excess energy expenditure and ultimately resulting in central place foraging.
Basking in winter and social huddling belowground (Hinze and Pillay, unpublished) are
likely to result energy savings. Moreover, the gut morphology of ice rats appears to be
adapted to increase energy uptake from poor quality forage and sexual dimorphism in
gut structure in summer may compensate for the lack of other gender differences in
behaviour and morphology by providing physiological means for females to extract
more energy from their food source...
The similarity in foraging behaviour in winter at Sani Top and in the presence of
predators in both seasons at Katse Dam suggests that low temperatures pose a risk for
foraging and highlights how foraging decisions are shaped by thermal conditions.
Otomys s. robertsi shares similar foraging behaviour with its arid-occurring relatives, the
Parotomys species, suggesting phylogenetic influences, but is possibly more a reflection
of similar phenotypic characteristics in the extreme habitats inhabited by these
otomyines.
Based on the physiological limitations of O. s. robertsi, Richter et al. (1997)
maintained that the allopatric distribution of O. s. robertsi and O. iroratus might have
been a consequence of interspecific competition for available resources, resulting in ice
rats being restricted to higher altitudes. Nonetheless, the data presented here suggest that
ice rats have modified their foraging behaviour and gut morphology for life in alpine
132
habitats, both of which are phenotypic characters that often show high levels of plasticity
(see Bozinovic et al., 1990; Stirling and Roff, 2000).
Conclusions and further research
My research has significantly increased our understanding of the biology of O.
s. robertsi by providing new insights into its foraging biology in its natural
environment. The variation in predation levels at the two study sites allowed me
to study the effects of predation on foraging behaviour under natural conditions
and without using surrogate measures of predation (e.g. predator odours; Powell
and Banks, 2004; illumination; Kotler, 1984 and V?squez, 1996). The Sani Top
site provided ideal conditions to study the response of ice rats to cold
temperatures with little or no influence from predation or interspecific
competition; ice rats were the only non-fossorial small mammal at this site.
This study has shown similarities in behaviour of the ice rat compared to
its otomyine relatives, but several differences were identified, mostly reflecting
the harsh alpine habitats inhabited by ice rat. I set out to provide broad
background information on the foraging biology of this taxon, since little data
were available regarding its behaviour in its natural environment. Thus, my
research focussed mainly on the behavioural strategies employed by the ice rat
to maximise energy gain while minimising energy loss. Further quantitative
research is needed on the energetic costs and benefits of various behaviours.
Due to the seasonal variation in temperature and the associated changes in
energy requirements, metabolic rates of free-living ice rats should be examined,
for example, by using implanted data loggers (see Taylor et al., 2004). Such
devices may be able to also relate internal physiological states to foraging need
133
(i.e. internal motivation). More precise measurements are also needed of
external factors which influence foraging decisions such as patch quality and
food handling time, which are traditionally used to investigate foraging decision
making (Lima and Dill, 1990; Bozinovic and V?squez, 1999).
It would also be interesting to investigate the histology of the
gastrointestinal tract of the ice rat in more detail to determine any physiological
adaptation in gut structure (e.g. intestinal nutrient transporters; Karasov and
Diamond, 1988). Other anatomical adaptations to cold temperatures could be
revealed by investigating seasonal changes in adipose and cardiovascular tissue
(Quay, 1984). Finally, a more detailed investigation of digestive efficiency
should be conducted by examining the energy assimilation from their food
plants.
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