Download A CRITIQUE CAN THE ACTIVITY BUDGET HYPOTHESIS EXPLAIN

A CRITIQUE
CAN THE ACTIVITY BUDGET HYPOTHESIS EXPLAIN SEXUAL
SEGREGATION IN DESERT BIGHORN SHEEP?
by
PETER NEUHAUS1) and KATHREEN E. RUCKSTUHL
(Department of Zoology, LARG, University of Cambridge, Downing Street Cambridge
CB2 3EJ, UK)
(Acc. 16-I-2004)
The study of sexual segregation in social animals, primarily ungulates, has
lately been the focus of many studies (Bowyer et al., 2002; Ruckstuhl &
Kokko, 2002; Ruckstuhl & Neuhaus, 2002; DePerno et al., 2003; Mooring et al., 2003, to list just a few) Since several, partially contradicting, hypotheses have been put forward to explain this phenomenon, we recently did
a review (meta-analysis) to find out if one of the main hypothesis used to
explain sexual segregation in social ungulates could be used as an ultimate
causal explanation of this phenomenon (Ruckstuhl & Neuhaus, 2002). To do
this we compared the so-called predation-risk (or reproductive strategy) hypothesis, the forage-selection (or sexual dimorphism-body-size) hypothesis
and the activity budget (body-size predation) hypothesis on over 30 species
of ungulates. Our study showed that the only hypothesis that has the potential
to be used as a general explanation for social sexual segregation in ungulates
is the activity budget hypothesis. A recent study on desert bighorn sheep
(Ovis canadensis mexicana) by Mooring et al. (2003) claims that the activity
budget hypothesis does not explain social segregation in their study population. This is a very important claim since if this were true, recent advances in
the understanding of social organization in ungulates would be questioned.
1)
e-mail address: [email protected]
© Koninklijke Brill NV, Leiden, 2004
Behaviour 141, 513-520
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However, we think that the claim done by Mooring et al. is wrong due to
several reasons. Firstly, there are strong misconceptions about what the different hypotheses really stand for, and secondly the methods used for data
collection by Mooring et al. are inappropriate to answer their questions correctly.
What does the activity budget hypothesis explain?
All three main hypotheses are capable of explaining sexual segregation for
certain species or in certain circumstances. With very few exceptions all studies have been done on single species, which is also true for the development
of the most recent hypothesis, the activity budget hypothesis (Conradt, 1998;
Ruckstuhl, 1998). While in the original idea of this new explanation predation and differences in food quality have been discussed, the main message
was, that while such measures can be additional proximate causes for sexual
segregation, one would expect segregation even in their absence. The main
prediction of the activity budget hypothesis is that animals with similar activity budgets will form groups. In other words, even if there was only one
habitat type, with one evenly distributed food item, and no predation at all,
animals with similar body sizes and energetic needs (thinking here also of
lactation and gestation) would aggregate socially (because their activity budgets are similar) and therefore segregate from animals with different body
size and energetic needs (Ruckstuhl, 1998, 1999). Hence in a species with
strong sexual body size dimorphism we would expect sexual segregation.
Apart from segregation by sex, one might further expect lactating females
to segregate from non-lactating females, subadults from adults etc., provided
groups of the same class of animals are large enough (Ruckstuhl & FestaBianchet, 2001). The advantage and beauty of this idea is its simplicity. We
strongly believe that differences in activity budgets can be the underlying,
proximate cause, which leads to sexual segregation in sexually dimorphic
social ungulates.
What is wrong with the assumptions/predictions in Mooring et al.’s
(2003) paper?
In their study, Mooring and co-workers compared the three above-mentioned
hypotheses and the competition avoidance hypothesis. Since the competition
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avoidance hypothesis has never been more than a theoretical idea without
much support from any empirical studies (Clutton-Brock et al., 1987; Conradt et al., 1999, 2001) we will from now on ignore this part of the Mooring
paper. In a table Mooring et al. described the three main hypotheses together
with predictions to test them on their desert bighorn sheep population. While
the general description of the three hypotheses can be accepted as they are,
some of the predictions are questionable while others are basically wrong:
– In comparison to the original reproductive strategy-predation risk hypothesis (Bowyer, 1984; Jakimchuk et al., 1987; Main & Coblentz,
1990; Main et al., 1996) the authors added a new prediction: females
with young will occur closer to water sources than mature males. This
new prediction is not in line with the rest of the predictions where females forego better feeding conditions to ensure safety from predation.
Although Bowyer (1984) found sexual segregation in southern mule
deer to be driven by increased water requirements of females, surely
one has to expect more predators around water sources than elsewhere,
especially in an arid landscape. Furthermore, one would expect that
close to water sources the forage should be better quality than further
away. Following the reasoning of the predation risk hypothesis there is
absolutely no logical explanation why one would predict females to be
closer to water than males — one would rather expect the contrary. In
several studies it has actually been shown that female ungulates sometimes leave their young in ‘kindergartens’ or do reciprocal baby-sitting
to be able to go to places of higher risk such as water sources or salt
licks (Kohlmann et al., 1996; Ruckstuhl & Ingold, 1998).
– Under the forage selection hypothesis, prediction 2 states that: ‘Females
will selectively feed on less abundant, higher quality forage’. This again
is not strictly true. Females are predicted to selectively feed on highquality forage — even if it is less abundant. They are predicted to do
so to compensate for the lower digestive efficiency compared to the
larger males who would go for high food abundance rather than forgo
quantity in favour of high quality (McCullough, 1979; Beier, 1987). If
high quality food is available and abundant, females are not expected
to select to feed in a place were food is less abundant.
– All four predictions given for the activity budget hypothesis are actually an extension of it, in which Mooring et al. mix up the actual activity
budget hypothesis and the forage selection hypothesis: Their first two
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predictions imply a difference in food quality between the sexes and
therefore differences in forage selection and/or habitat use. While such
differences are expected in the forage selection hypothesis, the activity
budget hypothesis only predicts that groups of bigger individuals have
different time budgets than groups of smaller individuals, and that their
movement rates might differ. Mooring et al.’s third prediction states
that females should be more selective than males, therefore taking more
steps while foraging. This is one of several possible ways for females
to compensate for a less efficient digestive system than males (due to
smaller body size). Showing the absence of differences in food selectivity itself does, however, not reject the activity budget hypothesis as inferred by Mooring et al. Therefore the third prediction is not valid to test
the activity budget hypothesis. Ruckstuhl (1998), for example, found no
difference in steps taken per minute foraging (and no difference in diet
quality), but found a big difference in time spent foraging, which led to
higher movement in females than in males. Mooring et al.’s fourth prediction on the activity budget hypothesis is imprecise. Here they state
that ‘subadult males will forage more like females than mature males’.
However, what Ruckstuhl (1998, 1999) postulated was that subadult
males in female groups should forage more like females while subadult
males in male groups would forage more like males, to adjust their behaviour to that of the group — however, if there are enough subadult
males in the population they actually should build a group of their own
because they differ in their optimal activity budgets from adults (Ruckstuhl, 1999; Ruckstuhl & Festa-Bianchet, 2001). The optimal activity
budget of subadult males would depend on their body size, first being
closer to females, and then gradually changing towards those of males
(Ruckstuhl, 1999). In their study, Mooring et al. did only differentiate
between yearling males and older males and have therefore no subadult
males of older ages to compare them with.
How did Mooring et al. test these hypotheses?
Another problem we had with the discussed paper is the methods used to
compare and test the different hypotheses. We recap here the methods, as
we understood them, because they are not clearly stated in the paper. As we
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understood the methodology, data was exclusively collected in the mornings,
when most animals were active. Observations on the animals were done during 10-min focal animal samplings on unmarked individual sheep. During
these ten minutes, the authors wrote down each minute (at that precise moment, and not for the whole minute) what the activity of the animal was.
This approach is a mixture of focal observations and scans on one single individual at a time. Within these 10-minute observations they further stopped
the total time spent feeding by a focal animal, but did not do so for other
behaviours than feeding. From these 10-min focal samples the authors then
somehow calculated daily means for certain behaviours. We believe this is
what is found in Table 2 — there is however no reference to this table in
the results. Further we think that the numbers in this table do not refer to
daily means but rather add up to hourly means. However, how exactly they
calculate these means is not described in the methods.
The authors also used single males in their data, likely the reason for the
high vigilance in males compared to females, which is inappropriate if looking at social segregation since a single animal is not social. While we had
difficulties understanding how the data collection and the analyses were carried out, it seems safe to say that from such 10-minute focal samples it is
impossible to test the activity budget hypothesis. In groups animals have to
adapt to the activities of the group to stay cohesive. To get data on the average activity bout length of all behaviours, and each group type (female
groups, bachelor groups etc.), an observer would have to stay with a group
of sheep through several bouts of feeding and resting. The 10-minute focal
samples only give us information about how the observed individuals spend
10 minutes of active time in the morning. Furthermore, even if the calculations of daily means of different behaviours in Mooring et al.’s paper were
right (which we doubt), this does not mean that the activity budget hypothesis
was proven wrong: Let us imagine that males have an optimal activity budget
of two hours feeding followed by two hours resting, while females have their
optimum at one hour feeding and one hour resting. Females and males would
both spend 50% feeding and 50% resting, but would still be best off segregating by sex according to the activity budget hypothesis. Mooring et al. did
however not even look at a single activity bout length.
While the lack of understanding what the activity budget hypothesis actually stands for is the main problem we have with the way data was collected
and interpreted, there are other problems with some methods used in this
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paper. The authors claim to be able to predict what the animals are eating
based on transects done in the vicinity of the place where the animals were
feeding. Surely the animals do not eat the exact proportion of what is accessible in the closest transect to where they have been sighted, especially not in
such a diverse and patchy environment as the desert or half desert. Further,
food choice could be very different between males and females, something
the authors claimed to have observed not to be true (through telescopes from
distances between 500-1000 meters). While we agree with the authors that
it would be surprising if males choose to forego good abundant forage when
it is available in big enough quantities, it is also not true that they actually
showed with their data that this is not the case. In other words this study
failed to appropriately test and reject the sexual dimorphism-body size hypothesis.
What can be concluded from Mooring et al.’s study?
Sexual segregation does occur in desert bighorn sheep. Besides using the
same habitat as females, males additionally used habitat where forage availability was better. Females did not use these sites, which were in more open,
flat areas, sticking to the more rugged terrain with less visibility but better escape terrain. These two results do partially support the predation risk
hypothesis. While Mooring et al. found no support for the forage selection
hypothesis, they did show that areas exclusively used by males had higher
quantity of forage than areas used by females. Since this higher quantity was
due to higher cover by grasses compared to the areas where females did occur, we suggest that this could be viewed as actually supporting the main assumption of the forage selection hypothesis (which predicts that males would
forage in areas with higher quantity of food while females prefer areas with
higher quality instead).
There was no difference between males and females in steps taken during
feeding bouts, a result in accordance with what was found in Rocky Mountain bighorn sheep (Ruckstuhl, 1998; Ruckstuhl et al., 2003). Finally, the
activity budget hypothesis was not accurately tested, since insufficient data
on activity budgets were collected.
We do understand that the problems we listed here were basically caused
by a misconception or an over-extension of the different hypotheses. However, Mooring et al. are not alone in failing to correctly interpret the different
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hypotheses on sexual segregation and in particular the activity budget hypothesis. Part of the problem is the frequent renaming and re-categorizing
of the different hypothesis, for which we too must take part of the blame
(Ruckstuhl & Neuhaus, 2000). We therefore think it is important to clarify
these issues in our comments here. It is clear that if in a sexually segregating species males and females use different habitats, the activity budget
hypothesis alone cannot explain the whole phenomenon, because it mainly
explains social segregation, and not habitat segregation. However, we claim
that, to date, the only hypothesis that has the potential to explain the main
underlying causal factor of social, sexual segregation is the activity budget
hypothesis. Additional factors such as predation, different food selection or
social affinities will almost always play additive roles in segregating social
ungulate species.
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