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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 Also available online - 514 NEUHAUS & RUCKSTUHL 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 A CRITIQUE 515 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 516 NEUHAUS & RUCKSTUHL 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 A CRITIQUE 517 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 518 NEUHAUS & RUCKSTUHL 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 A CRITIQUE 519 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. 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