Does the Jarman–Bell principle at intra-specific level explain sexual segregation in polygynous ungulates? Sex differences in forage digestibility in Soay sheep
The Jarman–Bell principle states that large-bodied mammalian herbivores can subsist on lower quality diets because of their lower metabolism requirement/gut capacity ratio. Two major hypotheses for sexual segregation (the behaviour in which animals of the same species aggregate by sex) base their foundations on extending this principle to the intraspecific level, despite the lack of experimental evidence to support this. The first proposes that the larger males can process fibre (low-quality diet) more efficiently than the smaller females, leading to sexual segregation by habitat partitioning due to selection of different food quality and/or quantity (sexual dimorphism–body size hypothesis). The second suggests that the longer time and extra rumination required to digest low-quality food will cause asynchrony of behaviour between males and females, which then leads to sexual segregation (activity budget hypothesis). To provide experimental evidence for the Jarman–Bell principle at the intraspecific level we carried out a set of digestibility trials in Soay sheep (Ovis aries) using grass hay as the diet to test whether sexual dimorphism in body mass can produce significant sexual differences in the efficiency of food digestion. Males were slightly more efficient in digesting forage than females that were at least 30% smaller than the males. Overall, there was a decrease in faecal output of 1 g/kg body mass in favour of males. These differences were not due to differences in food selection, passage rates or faecal particle size and it was not clear why males were more efficient in digesting forage. Although these results do not directly support arguments for either the sexual dimorphism–body size or activity budget hypotheses, they do indicate that the physiological argument upon which the Jarman–Bell principle is founded also operates at the intraspecific level and may be an important factor influencing sexual segregation.
KeywordsDigestibility Intake Faecal output Soay sheep
Sexual segregation is the behavioural phenomenon in which animals of the same species live in spatially segregated sex groups outside the mating season (Conradt 2005; Ruckstuhl and Neuhaus 2005a). Darwin (1859, pp 93–94) first put forward some ideas to explain sexual segregation. Although this phenomenon is common across polygynous ungulates, it has also been described in a variety of vertebrate taxa (Ruckstuhl and Neuhaus 2005b), which highlights its evolutionary, ecological and behavioural relevance.
Review of evidence supporting Jarman–Bell (J–B) principle at the intraspecific level
Sexual dimorphism–body size
Mooring et al. (2003)
Yearsley and Pérez-Barbería (2005)
Conradt and Roper (2000)
Pérez-Barbería and Gordon (1999a)
Gross et al. (1996)
Barboza and Bowyer (2000)
Bell (1971)e; (Jarman 1974)e; Geist (1974)e; Jenks et al. (1994)f; Demment and van Soest (1985)f; Demment (1982)f; Demment (1983); Short (1963)f; van Soest (1996)f; van Soest (1982)f; Owen-Smith (1988)f; Gross et al. (1996)f,g; Pérez-Barbería et al. (2001)f; Parra (1978)f; this studyf,g
The Jarman–Bell principle was originally formulated using allometric analyses between ungulate species that differed by 3 orders of magnitude in body mass, so it is questionable whether the relationship holds to the intraspecies level (Clutton-Brock and Harvey 1983; Bonenfant et al. 2004; Pérez-Barbería et al. 2007) and whether sexual dimorphism in body mass in extant ungulates is sufficiently marked to produce any difference in food digestion efficiency (Barboza and Bowyer 2000; Bonenfant et al. 2004; Pérez-Barbería et al. 2007).
There are two major hypotheses of sexual segregation that base some of their foundations on extending the Jarman–Bell principle to the intraspecific level.
The sexual dimorphism–body size hypothesis assumes that the MR/GC ratio (Demment and van Soest 1985) enables larger males to increase the retention time of food in their digestive tract, facilitating the activity of the symbiotic micro-organisms of the gut and consequently increasing their efficiency in digesting fibre in comparison with the smaller females (van Soest 1996); consequently, males in comparison with females can use habitats where food is less digestible but abundant.
The activity budget hypothesis states that segregation into sex groups or age classes arises when animals find it costly to synchronise their activity due to differences in body mass (Conradt 1998; Ruckstuhl 1998). This hypothesis is based on two main assumptions, that big differences in optimal activity budgets make synchronisation of behaviour costly, and that animals of small body size (females of polygynous species) are less efficient in digesting fibre than larger ones (males of polygynous species) due to body-size digestive constraints [smaller stomach and faster passage rate of food through their digestive system (Demment 1982; Robbins 1993)].
The aims of this study were: (1) to provide experimental evidence for the Jarman–Bell principle to the intraspecific level (inter-sex) by measuring food digestion efficiency in Soay sheep (Ovis aries), and (2) to present a cautionary note on the foundations of sexual segregation hypotheses based on this principle.
Materials and methods
Study area and animals
The experiment was carried out at the Macaulay Institute’s Glensaugh Research Station in north-eastern Scotland between 1 August and 9 September 2005. A total of 26 mature Soay sheep, 13 males (2–6years old, mean = 3.2) and 13 females (2–6 years old, mean = 4.3) were drawn from a large flock of sheep. Sheep were selected to meet the criterion of 20% minimum sexual dimorphism in body mass that Ruckstuhl and Neuhaus (2002) claimed necessary to induce segregation in ruminant species. We defined dimorphism as the difference between average male and average female body masses, as a proportion of average male body mass (Pérez-Barbería et al. 2002). In fact, sexual dimorphism in our sheep led to a sex body mass difference of 39% (females = 26.5 kg, SE = 0.67, n = 13; males = 43.8, SE = 0.70, n = 13).
The sheep were confined indoors, firstly in group pens, and then in individual pens. They were provided with clean bedding, water and fed on grass hay ad libitum. When the sheep were acclimatised to the indoor conditions (after 15 days), hay was weighed daily and offered to the sheep in two half rations at 0800 and 1400 hours GMT to minimise spillage. Next morning at 0700 hours feed refusals were weighed and rations recalculated accordingly to minimise any refusals. This was carried out until day 29 with the aim of stabilising the food intake of the sheep and prior to the trials to estimate digestion efficiency.
Measuring digestion efficiency
Intake was estimated as the difference between the hay offered and feed refusals in a 24-h period. Sheep were fitted with harnesses designed to carry mesh faecal bags (Leaver 1982) to calculate daily faecal output (van Soest 1982). Faecal bags and feed bins were emptied at 0730 hours every morning and the contents bagged and labelled. Daily total faecal output of individual sheep was oven-dried for 24 h to calculate the weight on a dry matter basis (±1 g). From the daily collection of feed refusals, faecal output and hay offered, subsamples were taken and frozen for chemical analysis and faecal particle-size measurements. The measurements were carried out for a period of 7 consecutive days (days 30–36).
The conventional way to express efficiency of digesting food is by the dry matter digestibility equation (DMD; van Soest 1982). DMD computes the difference between DM intake and DM faecal output in relation to DM intake (DM intake − DM faecal output/DM intake). However, because of the evident positive relationship between intake and faecal output (Demment and van Soest 1985) the use of this index fails to separate the effects that intake and faecal output have on food digestion. Therefore, we chose to assess sex differences in efficiency of digesting food by using faecal output as the response variable and intake as a covariate in a linear mixed model (see “Statistical analysis”), i.e. the lower the faecal output after having controlled for intake, the higher the efficiency in digesting food of the sheep.
Mean retention time
One of the main factors that affect fibre digestion is the time that food is retained in the digestive tract (Demment and van Soest 1985). Mean retention time (MRT) is the average time for water-soluble material or solid particles to travel from the mouth to the anus. To test whether sex differences in digesting food, or lack of them, were due to sexual differences in MRT we used C36n-alkane as an internal marker (Mayes and Dove 2006).
A MRT trial was started on day 37 and lasted for 3 days. At 0800 hours on day 37 (time 0) a single paper bung impregnated with 100 mg of C36 was administered to each animal and a sample of faeces was collected from the faecal bags at 5, 9, 12, 15, 18, 21, 24, 30, 36, 48, 60 and 72 h after time 0. One hour before each collection time, faecal bags were emptied to ensure that samples represented faeces voided within 1 h of the nominal collection time. Samples were bagged, labelled and kept in the freezer at −20°C until analysis. Samples were then freeze-dried, milled and C36 was extracted and its concentration determined by gas chromatography following Mayes and Dove (2006).
Similar double-exponential functions have been used in multi-compartmental kinetic models of faecal output (Dhanoa et al.1985).
Particle size in faeces and forage chemical analysis
Fibre digestion can be enhanced by increasing the food surface area exposed to microbial activity in the gut (Lanyon and Sanson 1986; Pérez-Barbería and Gordon 1998a, b). We estimated the faecal particle-size distribution of each sheep using a MasterSizer 2000 with Hydro G dispersal unit (Malvern Instruments). Individual sheep faecal particle size distributions were modelled using a gamma function (see “Mean retention time”). Particle size was characterised by the two parameters of the gamma distribution (αP, θP). The gamma function is a natural model for degradation processes in which deterioration is supposed to take place gradually over time in a sequence of tiny increments (Lawless and Cowder 2004). Comminution of food by mastication during ingestion and rumination fits well within these processes (Pérez-Barbería and Gordon 1998a). Matlab (2006), software and programming language was used for the modelling approach.
Samples of the hay offered were collected daily during the digestibility and MRT trials from each animal’s feed bin and pooled within day (n = 9). Faeces and feed refusals were collected from each animal during the same period and pooled within sheep (faeces, n = 26; refusals, n = 26).
Fibre content as acid detergent fibre (ADF) and lignin from hay offered and feed refusals were determined following Van Soest (1963) and neutral detergent fibre (NDF) as described in Van Soest and Wine (1967).
We used linear mixed models with residual maximum likelihood algorithm (REML) to account for different sources of variability, using individual sheep as a random effect. REML uses the Wald statistic test whose significance can be approximated by a χ2 distribution with the df of the fixed effect. For the variables in which there was only one source of variability and it was a complete factorial design (i.e. MRT, faecal particle size) we used ANOVA. The analyses were carried out using the GenStat 8 statistical package.
Faecal output, intake and sex effects
Predicted daily faecal output after controlling for intake was significantly less in males than in females (Wald = 4.4, df = 1, P = 0.037; males = 270 g, females = 285 g), which indicates that males were more efficient in digesting food than females. As expected, dry matter intake had a positive effect on faecal output (Wald = 495.3, df = 1, P < 0.001, slope = 0.50, SE = 0.025). The effect of sex was not significant when body mass was included in the model (Wald = 0.2, df = 1, P = 0.647), which corroborates that the sexual difference found in faecal output was due to sexual dimorphism in body size.
When the model was applied using only the six largest females and six smallest males, so that sexual dimorphism in body mass was reduced from 39 (analyses above) to 30%, the results were very similar (sex effect, Wald = 8.5, df = 1, P = 0.004; males = 273 g, females = 292 g).
Linear mixed effect models of sexual differences in fibre contenta [neutral detergent fibre (NDF), acid detergent fibre (ADF) and lignin] of food leftovers averaged across the experiment, and comparisons between the fibre content of food leftovers of each sex against the fibre content of the food offered. SED SE of the difference
Female versus offer
Female versus Male
Male versus offer
Dry matter intake differed between sexes [males = 658.9 g, females = 509.4 g, SE of the difference (SED) = 49.3; Wald = 9.20, df = 1, P = 0.002], as was expected by their difference in body mass. Consistent with the results of faecal output, when body mass was included in the model, sex differences in dry matter intake disappeared (Wald = 1.37, df = 1, P = 0.242).
Mean retention time
Parameter estimates of C36 faecal output using a gamma function in males and females of Soay sheep. CI Confident intervals at 95% of the respective parameter, MRT mean retention time as the time in hours for which the cumulative density function is equal to 0.5, Quartiles first and third quartiles of the gamma distribution, Adj_R2 adjusted R2 of the function fitting, RMSE root mean squared error (an estimate of the SD of the random component in the regression)
Males, n = 13
Females, n = 13
Particle size in faeces
Parameter estimates of particle size in faeces using a gamma function in males and females of Soay sheep. Median Median particle size (μm); for other abbreviations, see Table 3
Male, n = 13
Female, n = 13
Most researchers that test the sexual dimorphism–body size and activity budget hypotheses assume that the Jarman–Bell principle works within the range of sexual dimorphism in body mass existing in segregating species (Table 1). However, the literature indicates that there is little experimental evidence to provide support for the Jarman–Bell principle at the intraspecies level (Table 1). Consequently, hypothesis testing is pointless when the foundations of the hypothesis are weak. We aimed to provide some experimental evidence for the differences in efficiency of fibre digestion at the intraspecies level in an ungulate species.
We found sexual differences in the efficiency of food digestion when sexual dimorphism was as low as 30%. These findings were not due to sexual differences in food selection, since the amount of refusals was negligible and their chemical composition was similar between sexes. This is evidence that the Jarman–Bell principle holds when it is applied to the intraspecies level, at least if sexual dimorphism is of the order of 30%. The range of body masses of our animals did not allow testing of whether sexual dimorphism as small as 20% can cause any difference in digesting food; it has been suggested that this might be the size threshold in sexual dimorphism for segregating species (Ruckstuhl and Neuhaus 2002).
Diet quality plays an important role when considering differences in food digestion between animals of different size (Pérez-Barbería et al. 2004). If the percentage of fibre in the diet reaches a threshold beyond which animals of a certain MR/GC ratio cannot extract enough energy from the food to survive, then they are forced to be more selective for high-quality food. The key point in this rationale is that one of the sexes can experience constraints in food digestion depending on what food they are feeding on. For example, for alfalfa cellulose, any increment in body mass beyond 90 kg has no effect whatsoever on digestion of cellulose (van Soest 1996). This argument links with both the sexual dimorphism–body size and the activity budget hypotheses. In a habitat where the food available does not constrain the MR/GC ratio of both sexes, for example, where highly digestible food is abundant, then segregation should be expected to be minimal. In the case of the first hypothesis this is because there is no reason for males to use a diet of lower quality than the diet used by females (see discussion in Main et al. 1996; Pérez-Barbería and Gordon 1999a; Bowyer 2004). In the second hypothesis it is because the behaviour of both sexes would be fairly well synchronised because the grazing/rumination time ratio should be relatively similar between sexes, imposing only small energetic constraints (body size related) to maintain activity-coherent mixed-sex groups (Ruckstuhl and Neuhaus 2005a). A previous attempt of the experiment presented here comprised an experimental design with two diets contrasting in fibre content, but males and females were very selective when feeding from the low-quality diet, which defeated the purpose of the design. As we have used a medium-high quality diet (MAFF 1975; Equinews 2006) our results are supposed to reflect intermediate values of sexual differences in digestibility, as highly digestible forage does not require very long retention times (Demment and van Soest 1985).
The fact that increasing body size provides benefits only within a range of cellulose content and body size might be the reason why the spatial patterns of sexual segregation observed in nature do not follow a continuum in relation to increased body size.
We have failed to explain what causes the difference in the efficiency of food digestion associated with body mass. We tested two major factors to explain the difference in food digestion, retention time of the food in the digestive tract and faecal particle size (Demment and van Soest 1985; van Soest 1996), and found no difference between sexes. We expected that the sex with greater fibre digestion efficiency should also show a longer retention time. Our results contrast with those of Gross et al. (1996), who found that males of Nubian ibex (60 kg) retained forage in the digestive tract for longer than females (23 kg), but they also found no sex differences in the digestion of dry matter. They suggested that females might have improved the digestion of fibre by a more efficient comminution of the forage.
In our study, it can be argued that the error associated with the estimation of retention time is of a greater magnitude than the error associated with the estimation of faecal output and intake, since the latter are both straightforward measurements to make. This being the case it would have precluded detection of small differences in retention time associated with sex differences in food digestion, which is something that could have happened.
Among some other factors that might have caused the sexual differences in food digestion is the composition of the microbial flora in the gut (Murphy and Nicoletti 1984). However, this seems very unlikely for animals of the same species, managed in similar conditions and using the same food.
A key question, which is the foundation of the activity budget hypothesis, is whether the magnitude of these sexual differences in food digestion is enough to induce sexual asynchrony of behaviours that might generate segregation. This is a tricky question because it is conditional on external factors that affect energy expenditure in each sex and also presupposes a value of the potential benefits of social bonds (Pulliam and Caraco 1984). To simplify the scenario and provide some figures that help us to understand the magnitude of these differences in food digestion in terms of behavioural activity, we can estimate the energy costs of different behaviours. For example, consider an average body size male Soay sheep that has digested (after having controlled for intake), in comparison with an average size female, an extra amount of 15 g DM of ryegrass (metabolisable energy = 8.7 MJ/kg DM; MAFF 1975) per day in our experiment; this amount of food would yield the male an extra 0.13 MJ of energy, which would allow it to stand still looking for predators for 31 min or move a distance of 0.7 km on a flat surface at a speed of 7 km/h or 23 min ruminating-standing or 17 min grazing (Robbins 1993, p. 128, 133, 143). Seventeen minutes grazing on 10-cm-high leafy ryegrass represents about 3.3% of daily grazing time in Scotland in spring (Pérez-Barbería et al. 2007), a respectable time that could produce sexual asynchrony in grazing-resting behaviour and so induce sexual segregation. However, a very different matter is whether animals consider this amount of energy costly enough to sacrifice their social bonds and segregate from the group, something challenging to test, since it is difficult to assign an energy value to the potential benefits of group living. In terms of the number of ungulate taxa that might have this difference or larger in forage digestibility (i.e. 1 g faecal output/kg body mass) there are around 30% (43 out of 144, unpublished data). These are species that have a sexual dimorphism in body mass of 30% or bigger (unpublished data). This small difference in digestibility could not explain why males often use entirely different areas and habitats, which supports the idea that sexual segregation must be driven by a number of different factors.
The activity budget hypothesis states that sexual differences in activity patterns (resting-ruminating) are in part the consequence of the Jarman–Bell principle at the intraspecific level. With our results we could not corroborate this assumption because the greater efficiency to digest fibre in males was not achieved by a longer retention of the ingesta, which is what would have been expected to produce longer ruminating or resting bouts in males in comparison with the smaller females.
Although the activity budget and sexual dimorphism–body size hypotheses are both based on the Jarman–Bell principle, the predictions on the scale of segregation induced could be very different depending on each hypothesis. The activity-budget hypothesis has been classified within the social segregation group (Conradt 2005), i.e. animals form groups in relation to their body size independent of habitat partitioning. The sexual dimorphism–body size hypothesis assumes different food needs for each sex. Consequently, this hypothesis would explain the habitat partitioning between sexes observed in some species. However, in our opinion the difference between both predictions is not so clear. For example, the activity budget hypothesis could initially induce segregation within habitat that could lead to segregation at a large scale (areas, habitats), simply because one of the groups is left behind. Under this hypothesis there are no mechanisms to maintain spatial bonds between segregating groups, so there are no constraints to the spatial scale at which the segregation might result. In such a case, it would be impossible to discriminate which hypothesis explains the observed spatial patterns.
The generally accepted concept that mammalian herbivores are restricted to a range of food that varies in fibre content of which the lower limits (low in fibre) are determined by food abundance and the upper limits by body size-related digestive efficiency (Demment and van Soest 1985) has to be cautiously considered if applied to the intraspecific level, despite the findings of our study. In free-ranging animals as energy expenditure by each sex is strongly affected by external and physiological conditions it is difficult to know whether the magnitude of the sexual differences in food digestion found in our study might have a strong effect on segregation.
We thank Bob Mayes and Emily Green for their contribution to the alkanes analysis, Margaret Merchant in the running of the experiment, and the personnel of Glensaugh Research Station, Bettina Blanke, David Hamilton, and Donald Barrie. Craig MacEachern looked after the Soay sheep flock through the year. Jackie Potts provided statistical advice. The comments of Alan Duncan and three anonymous referees improved the drafts of this study. This research was funded by the Scottish Executive Environment and Rural Affairs Department. B. A. -E. and E. P.-F. were granted with a European Union Leonardo da Vinci training fellowship. The experiment was carried out in accordance with the UK Home Office Animals (Scientific Procedures) Act 1986.
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