Integrative and Comparative Biology Advance Access originally published online on June 13, 2007
Integrative and Comparative Biology 2007 47(2):245-257; doi:10.1093/icb/icm030
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||
Sexual segregation in vertebrates: proximate and ultimate causes
Department of Biological Sciences, University of Calgary, 2500 University Drive NW, Calgary, Alberta, T2N 1N4, Canada
Correspondence: 1E-mail: kruckstu{at}ucalgary.ca
 |
Synopsis |
|---|
Top
 Synopsis What is sexual segregation?Hypotheses explaining social...Sexual dimorphism in body...Models and experiments to...Is there a unifying...AcknowledgmentsReferences |
|---|
Sexual segregation is very common in vertebrates that live in groups. In this article, I will review proximate and ultimate causes of sexual segregation in social species and in particular in ungulates in which the bulk of research on the topic has been carried out. In most social ungulate species, males and females live in separate groups outside the breeding season, sometimes using different home ranges and types of habitat. In most of these species, males are larger than females. Dimorphism in body size can lead to sexual differences in ecology and behavior making it difficult for the two sexes to stay in the same group. It is important for our better understanding of the evolution of sociality, sexual dimorphism and different mating systems to determine why sexual segregation is so widespread not only in ungulates but also in other vertebrates. In this article, I discuss the ecology of the two sexes by reviewing proximate and ultimate causes of sexual segregation. To do this, I compare a range of studies of ruminants and include explanations for social segregation as well as for habitat segregation by gender. This leads into a review and updates current knowledge of the phenomenon. Although I present a number of different hypotheses, I focus in particular on predation risk, forage selection and activity budget and discuss the social-factors hypothesis. I stress that the key in solving the enigma of sexual segregation lies in clearly separating hypotheses that try to explain social segregation and habitat segregation, as well as in including experiments or model systems. To that end, I present a preliminary study on a test of the activity-budget hypothesis in three-spine sticklebacks and explain why I believe that shoaling fish are useful for analysing the underlying processes and mechanisms that lead to sexual segregation in animals. Lastly, I argue that it is unlikely that a single factor can explain social segregation or habitat segregation but that a model integrating different factors and different levels of segregation might succeed in describing proximate and ultimate causes of sexual segregation.
|
What is sexual segregation? |
|---|
|
Top
SynopsisWhat is sexual segregation?Hypotheses explaining social...Sexual dimorphism in body...Models and experiments to...Is there a unifying...AcknowledgmentsReferences |
|---|
Sexual segregation is widespread in vertebrates (Ruckstuhl and Neuhaus 2005
) and especially well researched in ungulates (Main and Coblentz 1996; Ruckstuhl and Neuhaus 2002; Bowyer 2004). Sexual segregation has been defined by some authors as the segregation of males and females into different groups, but others have not accepted this definition. Bowyer (2004), for example, stated that the definition of sexual segregation traditionally has been the differential use of space by males and females. MacFarlane and Coulson (2005)remarked that a widely accepted definition of the term is lacking altogether. These and other statements, along with the liberal use of various definitions and different names for the same hypotheses, have left the field of sexual segregation in a state of confusion and probably also contributed to its slow progress over the years. Conradt (1999, 2005) made a deliberate effort to clarify this situation by insisting that one must avoid the term sexual segregation because the sexes can be segregated in three different ways: socially, spatially, or by habitat (Fig. 1). Although she proposed a useful index that allowed measuring the three components of sexual segregation, she cautioned that spatial segregation ought to be treated as an auxiliary concept (Conradt 2005), as both habitat segregation and social segregation can lead to spatial segregation. She also cautioned against using the word "ecological segregation," an ambiguous term that could reflect sexual differences in use of microhabitat or occupancy of niches, sexual differences in habitat use, or even sexual differences in selection of forage within the same habitat. It is thus better to describe such phenomena as sexual divergence in type of prey or in selection of niche.
|
We are thus left with social segregation and habitat segregation as descriptors of sexual segregation. Some authors have assumed social segregation to be a by-product of habitat segregation (Bowyer et al. 2002
) but it is now commonly acknowledged that social segregation should be investigated and can occur independently of habitat segregation (Conradt 1999). If habitat segregation and social segregation are two types of sexual segregation, how can sexual segregation in ungulates be best explained? |
Hypotheses explaining social segregation and habitat segregation |
|---|
|
Top
SynopsisWhat is sexual segregation?Hypotheses explaining social...Sexual dimorphism in body...Models and experiments to...Is there a unifying...AcknowledgmentsReferences |
|---|
Many hypotheses have been proposed to explain sexual segregation in ungulates. I will review them by separately treating habitat segregation and social segregation (Table 1).
|
Habitat segregation
Hypotheses explaining habitat segregation include sexual differences in risk of predation and in reproductive strategies (labeled the predation-risk hypothesis), differences in selection of forage and in digestive capabilities (labeled the forage-selection and the gastro-centric hypothesis, respectively), and scramble competition (labeled the indirect-competition or scramble-competition hypothesis) (Miquelle et al. 1992
; Main and Coblentz 1996; Ruckstuhl and Neuhaus 2000; Bowyer 2004). All hypotheses proposed for ungulates base their arguments on sexual differences in body size resulting in either sexual differences in vulnerability to predation, in risk-taking or reproductive strategies, in digestive abilities and therefore forage selection, or sexual dimorphism in bite sizes and competitive abilities on preferred feeding sites. The predation risk and forage selection hypotheses have been researched most. I will, therefore, first focus on these two hypotheses and then discuss alternative hypotheses. According to the predation-risk hypothesis males select high-risk, high-energy gain habitats, whereas females trade off food quality of the habitat in favour of safety to their offspring (Main et al. 1996). Habitat segregation is thus ultimately due to sexual differences in reproductive strategies and predation risk. In agreement with the predation risk hypothesis, Kohlmann et al. (1996) reported on a case where Nubian ibex (Capra ibex nubiana) neonatal young had been accidentally confined to a natural series of ledges in a steep canyon wall that was safe from predators. Until the young were physically strong enough to scale the walls, their mothers left them behind to go on foraging trips. Mothers of confined, safe young selected richer food habitats and spent more time feeding per day than females whose young were with them. The authors argued that minimizing predation risk to offspring was a key constraint in mothers with young at heel.
The forage-selection hypothesis states that females need higher-quality foods due to their smaller body size and their lower digestive efficiency when consuming low-quality foods than males (Table 1). Males on the other hand rely on high-biomass forage because of their larger size and hence trade quantity for quality (Beier 1987; Barboza and Bowyer 2000). The hypothesis thus predicts that females should be found in high quality habitat and males in habitat with abundant forage. The forage selection hypothesis provides a proximate explanation for why the sexes segregate by habitat.
The indirect scramble-competition hypothesis proposes that males and females segregate into different habitats or use different microhabitats because one sex competitively excludes the other from preferred feeding sites (Clutton-Brock et al. 1987). This is thought to be an indirect process, and a proximate mechanism, that does not involve active competition or displacement. Sexual differences in grazing abilities in red deer (Cervus elaphus), or indirect competition for preferred feeding heights in giraffes (Giraffa camelopardalis), for example, could result in the exclusion of males by females from preferred feeding sites (Clutton-Brock et al. 1987; du Toit 2005). Experimental removal of female red deer from preferred habitats, however, did not result in males moving back into those sites (Conradt et al. 1999, 2001). Kie and Bowyer (1999)also showed that female white-tailed deer (Odocoileus virginianus) were not better at competing with males for closely-cropped forages. Predator control in their study population led to an increase in population density, which resulted in males increasing their use of lower quality, safer habitats that were mainly used by females with young. Habitat segregation decreased with increasing population density and diet choice shifted with a greater shift towards graminoids and browse observed in males than females. When looking at female body condition, they were in poorer condition than the males, indicating that they were not superior competitors. The scramble-competition hypothesis has therefore limited potential in explaining habitat segregation in ungulates (du Toit 2005). A study of downy woodpeckers, Piciodes pubescens, on the other hand, has shown that if males are removed from preferred locations on a tree, females will start occupying those sites (Catry et al. 2005). It therefore seems reasonable to conclude that for some vertebrates sexual segregation by habitat could be a result of direct competition but it does not seem to apply to most ungulates. In ungulates, direct competition would only occur if patches were defendable and if there were no intrinsic sexual difference in niche preference. Because of the absence of overt competition for food in most ungulates, and because food patches are often undefendable, it is unlikely that direct competition could be responsible for habitat segregation in that group. After all, the sexes often differ significantly in their morphology (size, feeding apparatus, musculature), and therefore likely have different abilities to exploit resources and have different feeding preferences (Pérez-Barbería and Gordon 2000; Catry et al. 2005).
The debate on which hypothesis explains habitat segregation in ungulates is largely due to the fact that the two main hypotheses (predation risk and forage selection) have opposing predictions as to whether males or females should select higher quality habitats. Currently, there are more studies in support of the predation-risk hypothesis and fewer for the forage-selection hypothesis (Ruckstuhl and Neuhaus 2002; Main and du Toit 2005) (see Table 1for predictions for sexual differences in habitat selection).
Whether one or the other hypothesis finds empirical support also seems to depend on the system/study species at hand. The distribution and abundance of food, as well as habitat-specific levels of predation risk, can greatly differ even between populations of the same species. Possible explanations for sexual segregation by habitat might thus vary accordingly (Ruckstuhl and Neuhaus 2002). There is another problem with these hypotheses, however, namely that the degree of sexual segregation further depends on the females’ reproductive status outside the breeding season. According to the predation-risk hypothesis, for example, habitat segregation should be more pronounced at times when females have dependent, vulnerable offspring. Females of nonreproductive status and no dependent offspring should therefore not segregate from males unless the females are at considerably more risk of predation than adult males, or if males adopt a riskier foraging strategy than those of females (Ruckstuhl and Neuhaus 2000) (Table 1).
An alternative proximate explanation for habitat segregation was given by Cransac et al. (1998). They pointed out that in many species females seclude themselves from the group to give birth to their young. This change in behavior is likely due to hormonal changes that trigger the need for isolation. Isolation is more easily found in steep places, which might not always be safe for the young. Cransac et al. (1998)have argued that females giving birth in steep areas might actually expose their neonates to higher risks of injury or death from falls than females giving birth in level terrain-and they further argued that females of species living in level terrain also isolate themselves prepartrum. The authors do not really give an explanation why females should seek isolation at parturition, but it could possibly involve various factors such as lack of mobility in neonates that could make them easy targets for predators, a lack of predation risk dilution effects in groups if neonates are not able to keep up with fleeing group, and a need for individual bonding and recognition between mother and offspring to prevent abandonment of young or nonoffspring stealing suckles. This idea clearly needs more investigation and rigorous testing.
Lastly, we would not expect sexual segregation due to sexual differences in forage selection during the winter months in temperate regions. At that time, differences in quality of forage are minimal or absent but nevertheless sexual segregation still persists. The forage-selection hypothesis seems restricted to cases, where forage is either extremely limited but of very high quality, abundant but of low quality, or when the two types of forage are found in discrete, geographically separated patches. This does not seem very likely for ungulates for which forage is abundant, and there is scant evidence that the best forage is found in areas where risk of predation is high. The predictive power of both the predation-risk hypothesis and the forage-selection hypothesis is therefore specific to season and sometimes to particular species (Ruckstuhl and Neuhaus 2000, 2002). The above arguments are not intended to reject one or the other hypothesis but to simply point out that each of them has its strengths and weaknesses as an explanation of habitat segregation in ungulates.
Social segregation
Hypotheses explaining social segregation include sexual differences in activity budgets, in avoidance of oddity effects, in social preferences, and in, avoidance of intrasexual aggression in mixed groups (Table 1). The activity budget and the oddity effect hypotheses predict that size or/and visual sexual dimorphism will be the underlying factor leading to sexual segregation, while the social preference and avoidance of aggression hypotheses argue that gender differences in social preferences will lead to sexual segregation, irrespective of size. The social-preference hypothesis and the activity-budget hypothesis are currently thought to be most likely to explain social segregation (Michelena et al. 2004). The social-preference hypothesis, however, has only received limited attention. It proposes that there is an innate preference for males to interact and to group with other males and for females to be with other females, and that these preferences alone lead to social segregation. In sexually segregated groups, males learn and develop fighting skills and establish a dominance hierarchy, something which the proponents of this hypothesis suggest can be better done in sexually segregated groups than mixed ones (Bon 1991). Recent studies investigating this hypothesis have found some support for sexual differences in social preferences (Michelena et al. 2004, 2005; Perez-Barberia et al. 2005). There are two points to consider, however, when investigating the possibilities of social preferences driving social segregation: first, although it is likely that preference for the same sex exists in many dimorphic ungulates, one would need to test whether proximate or ultimate factors (or a combination of both) are driving this preference. For example, is segregation ultimately a prerequisite for learning these sex-specific skills? In other words, are males that are raised in an otherwise females-only group less able competitors in dominance fights later on in life? Do fighting and the establishment of a dominance hierarchy between males lead to females distancing themselves from males (avoidance of males by females as a driver for social segregation)? Or, are males less able to bond and learn fighting skills in the presence of females? Why would they segregate themselves on the basis of social preferences alone? Second, and more importantly, even if it is agreed that this preference exists, has it evolved because males and females learn different skills in these groups or because the sexes differ in their nutrient requirements, predator avoidance, reproductive strategies, or activity budgets from early in their ontogeny, and for that reason prefer to group with animals with similar needs/abilities? Some authors, among them Bon (1991), have focused their explanations of social segregation on a proximate or developmental approach. They argue that sexual differences in the social repertoire and motivation to interact with same-sex peers early in life as well as indifferences to, or avoidance of the opposite sex may have long-lasting consequences for social dynamics and grouping outside the mating season (Calhim et al. 2006).
We are currently unable to perform experiments to test the latter set of questions but it is certainly possible to raise males and females, singly within a group consisting of members of the opposite sex and determine whether these focal individuals do less well in their gender roles than do animals raised in mixed-sex or unisex groups. We can also investigate whether group composition early in life will affect group choice later in life by exposing young animals to different group types.
Michelena et al. (2005)gave Merino sheep (Ovis aries) a choice of either a caged male or female as a companion within an experimental arena. While males spent more time in the vicinity of the caged male than near the caged female, females given the same choice did not display any preferences. Another study showed that if males and females were put together in a pen, they did not really segregate, although males were often found at the head of the group (Michelena et al. 2006). It is unclear why they did not segregate but the authors mentioned that the species might have been bred to be gregarious, or the exclosures might have been too small. Further choice experiments, preferably with undomesticated animals, could lend insight into the proximate and ultimate causes of social preferences.
Weckerly et al. (2004)suggested that social segregation would occur if females avoided males because of increased aggression in mixed-sex groups. Both female and male Roosevelt elk (Cervus elaphus roosevelti) seem to be more aggressive toward conspecifics of the same sex in mixed-sex groups as opposed to unisex groups. Weckerly (2001)further argued that large males might be less social and thereby avoid aggression. If animals are more aggressive in mixed-sex groups then they would spend more time fighting and less time foraging, thereby negatively impacting their energy intake (Weckerly et al. 2001). This hypothesis has not yet been tested other than on the species for which it was proposed. However, there seems little indication of overt aggression in mixed-sex groups in ungulates outside the breeding season and males only actively drive away males from female groups during the breeding season. Nevertheless, this hypothesis needs further investigation.
The activity-budget hypothesis has been proposed both as a proximate and an ultimate explanation for social segregation in ruminants. Sexual differences in body size may lead to differences in time spent foraging and moving compared to lying down and ruminating (Ruckstuhl 1998). Synchronizing activity budgets and staying in mixed-sex groups could be costly if optimal activity budgets and associated optimal foraging strategies can not be pursued (Conradt 1998; Ruckstuhl 1999). Sexual differences in activities could thus lead mixed-sex groups to fission and later coalesce into unisex groups. Group fission would then be the result of gender incompatibilities in activity budgets or costs of behavioral synchrony. Synchrony of activities is important for group cohesion (Jarman 1974). Thus, animals need to synchronize their activities with other group members in order to stay in a group. Males and females of sexually size-dimorphic ungulates differ considerably in activity budgets, (Ruckstuhl and Neuhaus 2002) and hence would be better off in unisex groups in which activity budgets can be optimized rather than compromised. Several studies have found empirical (Ruckstuhl and Kokko 2002; Calhim et al. 2006; Ruckstuhl et al. 2006) and theoretical support (Conradt and Roper 2000; Ruckstuhl and Kokko 2002; Yearsley and Perez-Barberia 2005) for the activity-budget hypothesis, while some have not (MacFarlane 2006; Michelena et al. 2006). The activity-budget hypothesis needs to be tested empirically, theoretically (computer models; see Ruckstuhl and Kokko 2002), and experimentally. Calhim et al. (2006), for example, have found that sexual segregation in feral goats, Capra hircus, on the Isle of Rum is most likely explained by sexual differences in activity budgets but also suggested that social references could have a residual influence on segregation. Social preference of same-sex and same-size individuals could thus evolve via compatibilities in activity budgets and be an important driver in keeping groups together. Other researchers have not found support for the activity budget hypothesis which could be due to the fact that there is no difference in activities or due to the nature of data collected. To test the activity budget hypothesis appropriately, one needs detailed information on activity budgets and rates of movement for both sexes. This can only be achieved by studying recognizable and easily observable individuals over the course of several activity bouts. Both males and females need to spend a certain amount of time ruminating and digesting their forage before they can start another feeding bout. Males tend to invest more time in rumination than do females, while females graze for longer. The sexes might also differ in their movement rates and distances traveled (Ruckstuhl and Neuhaus 2002) which again would make synchrony difficult. We therefore need to collect data on several of these bouts to judge how much males and females differ in their activity and how little synchronized they may be in their activities. Unfortunately, these data are not easy to collect. Measuring sexual differences in activity budgets when both sexes are active, or calculation the proportion of animals that are active in a group, will not provide the necessary information to assess sex differences in time spent foraging and walking versus lying down (Mooring et al. 2003; Bowyer and Kie 2004; Neuhaus and Ruckstuhl 2004).
Furthermore, sex ratio and population size could also affect the degree of social segregation found in a population (Ruckstuhl and Festa-Bianchet 2001; Bowyer 2004). Group living is beneficial because of predator detection and dilution (Dehn 1990). Benefits of detection and dilution might thus outweigh costs of behavioral synchrony in populations that have a very low density, such as some desert bighorn sheep (Bleich et al. 1997). Ruckstuhl and Festa-Bianchet 2001, for example have clearly shown that group choice by subadult male bighorn sheep depends on the number of subadults in the population. In years, when numbers of subadults were low, this age class attached either to groups of adult males or groups of adult females, but in years when numbers of subadults were high the subadults formed groups of their own. If the number of peers of the same age or sex is limited, it might well be that the need to stay in a larger group outweighs the benefits of being segregated and one would thus expect the sexes and/or ages to aggregate in groups of mixed sexes and ages. Anecdotal evidence from observations on bighorn sheep in Sheep River Provincial Park, Canada, seems to suggest that population size and sex ratio might well affect grouping tendencies: a recent decline in adult females in the population had lead to females joining male groups and staying with males past the reproductive season and up to parturition. Now that numbers are up again they are segregated outside the rutting season, as expected. (Ruckstuhl, unpublished data).
Ungulates do not lend themselves easily to experimental manipulations. It would therefore be difficult to change group membership or to alter size-composition of the group in order to investigate incompatibilities of activity budgets and costs of behavioral synchrony without affecting other behaviors. A possible model species that could be used to test the activity-budget hypothesis and to assess the potential costs of behavioral synchrony will be presented in the next section.
Finally, another important factor to consider when investigating effects of age and sex on activity budgets is that age is not always a good predictor of size, and size of adults varies considerably among populations of the same species. If possible, it would thus be preferable to use body mass as an explanatory variable rather than some proxy such as age class or sex when testing the activity-budget hypothesis (Ruckstuhl 1999; MacFarlane 2006). Ruckstuhl and Neuhaus (2002)have shown that an increase in sexual difference in adult body mass leads to increasing differences in time spent feeding, lying, or walking. They also showed that size dimorphism is crucial in explaining degrees of sexual segregation: a threshold dimorphism of about 20% in mass seems necessary in ruminants for the sexes to segregate. This threshold might be even higher for nonruminants as they are more flexible in the time they allocate to foraging or digesting food; they need not lie down and ruminate before they can start a new feeding bout.
Lastly, (Geist 1988) proposed that male deer might avoid female groups when they carry antlers (an idea herein labeled the oddity-effect hypothesis) (Table 1). Animals carrying antlers would be more visible to predators and therefore have higher predation risk when in groups of females. He further proposed that male deer should join females as soon as they dropped their antlers. This hypothesis is obviously of limited general appeal as it is restricted to deer species. Furthermore, male and female caribou segregate even though both sexes have antlers (Jakimchuk et al. 1987). Because of the limited generality of the oddity hypothesis it will not be discussed any further in this review.
|
Sexual dimorphism in body size is a key in solving the enigma of sexual segregation |
|---|
|
Top
SynopsisWhat is sexual segregation?Hypotheses explaining social...Sexual dimorphism in body...Models and experiments to...Is there a unifying...AcknowledgmentsReferences |
|---|
There is agreement among researchers that sexual dimorphism in size is very important in driving sexual segregation in ungulates (Pérez-Barbería and Gordon 1998
; Mysterud 2000; Ruckstuhl and Neuhaus 2002). It is thus important to use dimorphism in size or mass of the body as predictors for testing the different hypotheses relating to sexual segregation. Ruckstuhl and Neuhaus (2002)tested the predation-risk hypothesis, the forage-selection hypothesis and the activity-budget hypothesis for ungulates that ranged from sexually monomorphic species to those that were extremely dimorphic in body size. They concluded that an increase in sexual dimorphism in body size leads to an increase in sexual differences in activity budgets and in movement rates. It was also predicted that if predation risk drives habitat segregation, monomorphic males and females should also be segregated outside the breeding season, because females with young are more vulnerable to predation than are males. Ruckstuhl and Neuhaus (2002)reasoned that if sexual differences in requirements for energy and food drove segregation, the sexes of monomorphic species should segregate into different habitats during late pregnancy and early lactation, when females have higher demands for energy and nutrients. Neither of these predictions was confirmed, leading the authors to conclude that the activity-budget hypothesis was the best general explanation for sexual segregation in ungulates.
Differences in body size were also used as a variable in a study of bighorn sheep (Ovis canadensis) (Ruckstuhl 1999). Subadult males of different ages were observed in both male and female groups. Activity budgets and degrees of behavioral synchrony (how much subadult males synchronize their activities with the rest of the group) were measured. Young males always synchronized their activity budgets with the group, independent of its composition, but the degree of synchrony depended on the difference between their own body size and that of the adults in the group. The study highlighted that it is important to test the activity-budget hypothesis and other hypotheses by comparing individuals of different ages, sexes or even reproductive status. Age and size, however, are not independent variables and growing individuals might face different trade-offs than would adults. Similarly, males and females do not only differ in size but in physiology and life history. A specific difference in size between the sexes might thus not lead to similar shifts in physiology or behavior in both sexes.
A study of Soay sheep (Ovis aries) investigated the effects of reproductive status among adult males that were segregated from females socially and by habitat, as well as by reproductive class within males. On the Isle of St. Kilda, growth of castrated and control rams were compared so as to assess the costs of reproduction (Jewell 1997). A study by (Clutton-Brock et al. 1990) on the osteology of these sheep reports that the castrates grew taller than control males but appeared phenotypically (shape and size of horns) similar to females. Castration is a perfect experiment for examining the effects of reproductive status in males on social segregation and habitat segregation. Ruckstuhl et al. (2006)found that castrates segregated themselves from females and normal males but did not seek out different habitats. Social segregation of castrates from entire males could thus have been driven by social factors or incompatibilities in activity budgets, or both. No data were available to investigate this possibility. This study nicely demonstrates that we need a model species or study system that allows changing variables such as body size, reproductive status, or group compositions experimentally, while being able to hold other variables constant or at least controlling for them. The species should be highly social, segregate by body size, but size should be, if possible, independent of sex or age. Unfortunately, no such ungulate species is known and we thus need to look elsewhere for a good model organism. Some species of shoaling fish, in which males and females have the same body size, could provide us with exactly that. Such shoaling fish are social and prefer the company of same-sized fish of either gender (Krause and Godin 1996; Krause et al. 1996). The following section of this review will therefore argue that studying sexual segregation in shoaling fish could provide important insights into the proximate and ultimate causes underlying sexual segregation in vertebrates.
|
Models and experiments to test proximate and ultimate causes of sexual segregation |
|---|
|
Top
SynopsisWhat is sexual segregation?Hypotheses explaining social...Sexual dimorphism in body...Models and experiments to...Is there a unifying...AcknowledgmentsReferences |
|---|
In fish, body size is not necessarily linked to sex but more often to environmental conditions or age. One could therefore investigate effects of body size on social preferences, activity budgets, predator avoidance or forage selection without sex as a confounding variable. Croft et al. (2006
)have devised a clever way to test the predation-risk hypothesis using wild guppies (Poecilla reticulata) in Trinidad. In guppies, males seem to be the more vulnerable sex (they are more colourful and larger than females) but they also harass females for mating opportunities. The researchers found that guppies were segregated by sex, with an increasing number of females occurring in deeper waters. Croft et al. (2006)then introduced wild-caught, caged females into different water depths and assessed the degree of predation risk and male harassment these females received. Deeper waters were more dangerous in terms of risk of predation but, as males tended to avoid such areas, females were less harassed compared to the incidence in shallower areas. The researchers concluded that the guppies might segregate into different habitats because females might seek refuge from harassing males even at the cost of higher predation risk. They also found that if the major predators were absent, females were just as likely to be harassed by males in deep water as in shallow water. This is an excellent study because they were able to perform experiments and look at the consequences of exposure to different habitats instead of merely inferring processes after animals had already selected a specific habitat. However, the shortcoming of this study is the sexual dimorphism evident in that species and the problem that we cannot differentiate between differences that are due to size and those due to gender effects.
Manica, Birch, and Astle (from the University of Cambridge) and I tested the activity-budget hypothesis and investigated the costs of behavioral synchrony by using shoaling fish. We used three-spine sticklebacks (Gasterosteus aculeatus) to investigate potential costs of behavioral synchrony in fish shoals. We carried out a series of trials in which a focal fish was placed in various shoals that either were composed of fish of the same body size as the focal fish, or were of smaller or larger fish. The idea of this experiment was to indirectly test the activity budget hypothesis—that animals of different sizes differ in their activity budgets and that they are better off in size-assorted groups where costs of synchrony of behavior would be minimal. If synchronizing of swimming speeds and feeding rates is necessary for group cohesion then odd-sized individuals in a school are expected to pay a higher cost of staying in these groups that same-sized fish. Swimming speeds, foraging rates, competitive interactions between group members, and individual changes in mass (as a measure of cost of synchrony) were recorded both for the focal fish and for the shoal fish. Our tests were carried out in December, at a time when sticklebacks are schooling in mixed-sex groups, are nonterritorial and not engaged in reproduction. Our experiments revealed that focal fish always closely synchronized their swimming speeds (Fig. 2) to those of the shoals but were less synchronized in foraging rates to those of the shoal (Fig. 3). We then looked at potential costs of this behavioral synchrony by measuring change in mass of a fish exposed to the different treatments over a three-day period. Over the three days of the trial, focal fish in size-assorted shoals gained mass and had higher foraging rates, whereas they foraged less and either lost mass (when with bigger fish) or stayed the same (when with smaller fish) in dissimilar shoals (Figs. 2and 4). Levels of aggression were not significantly different between treatments, and do not explain weight loss of the focal fish in heterogeneous groups. Food was provided in excess to their requirements. In this study we showed that synchrony in behavior is costly and that this could well be a novel explanation of why fish prefer size-assorted shoals. Other factors that have been reported to affect school choice in fish are shoal size, body size (Lindström and Ranta 1993), swimming speed (Robinson and Pitcher. 1989a) and level of satiety (Robinson and Pitcher. 1989b; Krause et al. 1999). Many fish species also differ greatly in their life history, reproduction, feeding physiology, and behavior, which might limit the potential to fully extrapolate findings in schooling fish to social mammals, for example.
|
|
|
However, segregation by body size is not only common in fish but also in ungulates where several species are reported to segregate according to gender or age (Villaret and Bon 1995
; Cransac et al. 1998; Ruckstuhl and Festa-Bianchet 2001; Neuhaus and Ruckstuhl. 2002a; Ruckstuhl et al. 2006). Research on causes and mechanisms of sexual segregation in shoaling fish could therefore at least partially be of relevance to ungulates and other species or vice versa. Maybe similar experiments could be carried out in ungulates but most of them, apart from domesticated species, do not lend themselves well to such an experimental setup. Also, the effect of being in a confined space might affect their natural preferences and behaviors. |
Is there a unifying theory of sexual segregation? |
|---|
|
Top
SynopsisWhat is sexual segregation?Hypotheses explaining social...Sexual dimorphism in body...Models and experiments to...Is there a unifying...AcknowledgmentsReferences |
|---|
Research on sexual segregation has suffered from misconceptions of what sexual segregation is and to what extent habitat segregation and social segregation are separate. Recently, however, researchers have begun to assess the topics of habitat segregation and social segregation separately. This is a major improvement. Bowyer (2004
)argued that social segregation cannot explain habitat segregation and vice versa. In general, I agree with that concept, and it is probably best to investigate these phenomena separately. However, the question about the origin of sexual segregation or the possible existence of an underlying force to explain sexual segregation in ungulates still remains unanswered. Jarman and Jarman (1973)proposed that ungulates started off as forest-dwelling, sexually monomorphic in size, and monogamous. With the expansion of open habitats, such as savannahs, these animals started to be more gregarious. With sociality came competition for food and mates as well as natural selection and sexual selection leading to larger body size in males than in females (Jarman 1983). With increasing dimorphism, males might have started to take more risks to accommodate increased energy demands, and therefore, segregated from females spatially or by habitat. If social segregation is only a consequence of habitat segregation the story ends. However, it is equally conceivable that with an increased sexual dimorphism in body size came sexual differences in activity budgets, movement rates, or social preferences, which in turn made groups less cohesive and eventually led males and females to segregate into different groups. Once these animals were segregated socially, seasonal demands of high energy intake by males or females and changes in vulnerability to predation, and other factors, could easily be accommodated by seeking out habitats or microhabitats that satisfy their demands. Under this scenario males and females would be socially segregated outside the breeding season and temporarily segregated by habitat at times when sex-specific requirements can not be adequately met in mixed-sex groups. This scenario, although hypothetical, seems to describe trends in sexual segregation in a variety of species, at times by habitat and at other times socially. We hence need to acknowledge that factors explaining sexual segregation are not always mutually exclusive and that habitat segregation and social segregation could be epiphenomena of each other. This line of thought needs to be explored in more detail before one can explain year-round sexual segregation rather than merely report on its temporal or seasonal aspects.
A multitude of factors including predation risk, forage selection, social preference, or differences in activity budgets could affect social segregation and habitat segregation in concert, sequentially, or in any combination. It is unlikely that one factor alone is completely sufficient for explaining this intriguing phenomenon in all its facets (Bonenfant et al. 2004; Loe et al. 2006). To make substantial headway in the study of sexual segregation we first and foremost need to look for alternative explanations and rigorously test opposing hypotheses for habitat or social segregation by subjecting them and the animals to different tests or by using appropriate computer models. Using game-theory models, for example, to analyze sexual differences in trade-offs due to predation, energetic needs or the need for behavioral synchrony of groups could shed light on the processes and causes of social and habitat segregation. Including varying degrees of sexual size dimorphism as an independent predictor variable might also help in solving the enigma of sexual segregation.
Likewise, instead of concentrating so much on species that segregate socially and by habitat, we should perhaps concentrate on species that would be expected to segregate but which do not. Monkeys and apes are perfect examples of species for which sexual segregation would be expected in those species that are sexually dimorphic in size. Sexual segregation, however, does not occur in many of them (Watts 2005). Why do they not segregate and what are the benefits and costs of staying in mixed-sex groups? It has been suggested that females profit from having males in their groups because males defend their groups against predation, infanticide, and harassment by other males. The males can also benefit through increased access to and monopoly over, females and through decreased risk of predation because of dilution effects and vigilance. The benefits of staying in mixed-sex groups must therefore outweigh its costs.
Further research on species in which sexual dimorphism is prominent but sexual segregation is absent (Watts 2005) or on species in which sexual segregation occurs in the absence of a sexual dimorphism in size (such as in bats) (Altringham and Senior 2005; Senior et al. 2005) would be extremely important for understanding the underlying causes and mechanisms of sexual segregation, not just in ungulates, but in all sexually segregating species. Finally, the examples of sticklebacks and guppies show how powerful an experimental approach can be in elucidating proximate and ultimate causes of sexual segregation.
|
Acknowledgments |
|---|
|
Top
SynopsisWhat is sexual segregation?Hypotheses explaining social...Sexual dimorphism in body...Models and experiments to...Is there a unifying...AcknowledgmentsReferences |
|---|
I am grateful for the Society for Integrative and Comparative Biology (SICB) for promoting and partially funding the symposium in which this paper was presented. I am also very grateful to Shawn Vincent, Simon Lailvaux, Anthony Herrel, and Emily Taylo for organizing the symposium and inviting me to contribute, as well as to the audience members for constructive discussions. Thank you also to Peter Neuhaus and Marco Festa-Bianchet for constructive comments and to J. Birch, C. Astle, and A. Manica for letting me use the data on the stickleback experiments in this review. Many thanks to the Integrative and Comparative Biology Editorial Office (in particular Hal) and two anonymous reviewers for their constructive and helpful comments on an earlier version of this manuscript. Lastly, I would like to thank the following granting agencies and organizations for their support of my studies and research over the years: NSERC (PDF and discovery grants), Swiss Academy of Science (travel grant), Swiss Science Foundation (PDF), Alberta Ingenuity (for a new faculty award), the University of Cambridge and the Clutton-Brock research group for many years of stimulating discussions, and the University of Calgary for a travel grant and continued support.
|
Footnotes |
|---|
From the symposium "Ecological Dimorphisms in Vertebrates: Proximate and Ultimate Causes" presented at the annual meeting of the Society for Integration and Comparative Biology, January 3–7, 2007, at Phoenix, Arizona.
|
References |
|---|
|
Top
SynopsisWhat is sexual segregation?Hypotheses explaining social...Sexual dimorphism in body...Models and experiments to...Is there a unifying...AcknowledgmentsReferences |
|---|
Altringham JD, Senior P. Social systems and ecology of bats. In: Sexual segregation in vertebrates: ecology of the two sexes—Ruckstuhl KE, Neuhaus P, eds. (2005) Cambridge: Cambridge University Press. 280–302.
Barboza PS, Bowyer RT. Sexual segregation in dimorphic deer: a new gastrocentric hypothesis. J Mammal (2000) 81::473–89.[CrossRef][Web of Science]
Barboza PS, Bowyer RT. Seasonality of sexual segregation in dimorphic deer: extending the gastrocentric model. Alces (2001) 37::275–92.
Beier P. Sex differences in quality of white-tailed deer diets. J Mammal (1987) 68::323–9.[CrossRef][Web of Science]
Bleich VC, Bowyer RT, Wehausen JD. Sexual segregation in mountain sheep: resources or predation? Wildl Monogr (1997) 134::1–50.
Bon R. Social and spatial segregation of males and females in polygamous ungulates: proximate factors. Spitz F, Janeau G, Gonzalez G, Aulagnier S, eds. (1991) Toulouse, France, Paris: SFEMP-IRGM. 195–8.
Bon R, Campan R. Unexplained sexual segregation in polygamous ungulates: a defence of an ontogenetic approach. Behav Proc (1996) 38::131–54.[CrossRef][Web of Science]
Bonenfant C, Loe LE, Mysterud A, Langvatn R, Stenseth NC, Gaillard JM, Klein F. Multiple causes of sexual segregation in European red deer: enlightenments from varying breeding phenology at high and low latitude. P Roy Soc Lond B (2004) 271::883–92.
Bowyer RT. Sexual segregation in southern mule deer. J Mammal (1984) 65::410–7.[CrossRef][Web of Science]
Bowyer RT. Sexual segregation in ruminants: definitions, hypotheses, and implications for conservation and management. J Mammal (2004) 85::1039–52.[CrossRef][Web of Science]
Bowyer RT, Kie JG. Effects of foraging activity on sexual segregation in mule deer. J Mammal (2004) 85::498–504.[CrossRef][Web of Science]
Bowyer RT, Stewart KM, Wolfe SA, Blundell GM, Lehmkuhl KL, Joy PJ, McDonough TJ, Kie JG. Assessing sexual segregation in deer. J Wildl Manage (2002) 66::536–44.[CrossRef]
Calhim S, Shi J, Dunbar RIM. Sexual segregation among feral goats: testing between alternative hypotheses. Anim Behav (2006) 72::31–41.[CrossRef][Web of Science]
Catry P, Phillips RA, Croxall JP. Sexual segregation in birds: patterns, processes and implications for conservation. In: Sexual segregation in vertebrates: ecology of the two sexes—Ruckstuhl KE, Neuhaus P, eds. (2005) Cambridge: Cambridge University Press. 351–78.
Clutton-Brock J, Dennis-Bryan K, Armitage PL, Jewell PA. Osteology of the Soay sheep. Bull Br Mus Nat Hist (1990) 56::1–56.
Clutton-Brock TH, Iason GR, Guinness FE. Sexual segregation and density-related changes in habitat use in male and female red deer (Cervus elaphus). J Zool (1987) 211::275–89.[Web of Science]
Conradt L. Could asynchrony in activity between the sexes cause intersexual social segregation in ruminant? P Roy Soc Lond B (1998) 265::1359–63.
Conradt L. Social segregation is not a consequence of habitat segregation in red deer and feral soay sheep. Anim Behav (1999) 57::1151–7.[CrossRef][Web of Science][Medline]
Conradt L. Definitions, hypotheses, models and measure in the study of animal segregation. In: Sexual segregation in vertebrates: ecology of the two sexes—Ruckstuhl KE, Neuhaus P, eds. (2005) Cambridge: Cambridge University Press. 11–32.
Conradt L, Clutton-Brock TH, Thomson D. Habitat segregation in ungulates: are males forced into suboptimal habitats through indirect competition by females? Oecologia (1999) 119::367–77.[CrossRef][Web of Science]
Conradt L, Gordon IJ, Clutton-Brock TH, Thomson D, Guinness FE. Could the indirect competition hypothesis explain inter-sexual site segregation in red deer (Cervus elaphusL.)? J Zool (2001) 254::185–93.[CrossRef][Web of Science]
Conradt L, Roper TJ. Activity synchrony and social cohesion: a fisson-fusion model. P Roy Soc Lond B (2000) 267::2213–8.
Cransac N, Gerard J-F, Maublanc M-L, Pépin D. An example of segregation between age and sex classes only weakly related to habitat use in mouflon sheep (Ovis gmelini). J Zool (1998) 244::371–8.[CrossRef][Web of Science]
Croft DP, Morrell LJ, Wade AS, Piyapong C, Ioannou CC, Dyer JRG, Chapman BB, Yan W, Krause J. Predation risk as a driving force for sexual segregation: a cross-population comparison. Am Nat (2006) 167::867–78.[CrossRef][Web of Science]
Dehn MM. Vigilance for predators: detection and dilution effects. Behav Ecol Sociobiol (1990) 26::337–42.[Web of Science]
du Toit J. Sex differences in the foraging ecology of large mammalian herbivores. In: Sexual segregation in vertebrates: ecology of the two sexes—Ruckstuhl KE, Neuhaus P, eds. (2005) Cambridge: Cambridge University Press. 35–52.
Geist V. On the relationship of social evolution and ecology in ungulates. Amer Zool (1974) 14::205–20.[Web of Science]
Geist V. Sexual dimorphism in the Cervidae and its relation to habitat. J Zool (1988) 214::45–53.[Web of Science]
Jakimchuk RD, Ferguson SH, Sopuck LG. Differential habitat use and sexual segregation in the Central Arctic caribou herd. Can J Zool (1987) 65::534–41.
Jarman MV, Jarman PJ. Daily activity of impala. E Afr Wildl J (1973) 11::75–92.
Jarman PJ. The social organisation of antelope in relation to their ecology. Behaviour (1974) 48::215–67.[CrossRef]
Jarman P. Mating system and sexual dimorphism in large, terrestrial, mammalian herbivores. Biol Reviews (1983) 58::485–520.[CrossRef]
Jewell PA. Survival and behaviour of castrated Soay sheep (Ovis aries) in a feral island population on Hirta, St. Kilda, Scotland. J Zool (1997) 243::623–36.[Web of Science]
Kie JG, Bowyer RT. Sexual segregation in white-tailed deer: density-dependent changes in use of space, habitat selection, and dietary niche. J Mamm (1999) 80::1004–20.[CrossRef][Web of Science]
Kohlmann SG, Müller DM, Alkon PU. Antipredator constraints on lactating Nubian ibexes. J Mammal. (1996) 77::1122–1131.[CrossRef][Web of Science]
Krause J, Godin J-GJ. Phenotypic variability within and between fish shoals. Ecology (1996) 77::1586–91.[CrossRef][Web of Science]
Krause J, Godin JGJ, Brown D. Size-assortativeness in multi-species fish shoals. J Fish Biol (1996) 49::221–5.[CrossRef][Web of Science]
Krause J, Hartmann N, Pritchard VL. The influence of nutritional state on shoal choice in zebrafish, Danio rerio. Anim Behav (1999) 57::771–5.[CrossRef][Web of Science][Medline]
Lindström K, Ranta E. Social preference by male guppies, Poecilia reticulata, based on shoal size and sex. Anim Behav (1993) 46::1029–31.[CrossRef][Web of Science]
Loe LE, Irvine RJ, Bonenfant C, Stien A, Langvatn R, Albon SD, Mysterud A, Stenseth NC. Testing five hypotheses of sexual segregation in an arctic ungulate. J Anim Ecol (2006) 75::485–96.[CrossRef][Medline]
MacFarlane AM. Can the activity budget hypothesis explain sexual segregation in western grey kangaroos? Behaviour (2006) 143::1123–43.[CrossRef]
MacFarlane AM, Coulson G. Synchrony and timing of breeding influences sexual segregation in western grey and red kangaroos (Macropus fuliginosusand Macropus rufus). J Zool (2005) 267::419–29.[CrossRef][Web of Science]
Main MB, Coblentz BE. Sexual segregation in rocky mountain mule deer. J Wildl Manage (1996) 60::497–507.[CrossRef]
Main MB, du Toit J. Sex differences in reproductive strategies affect habitat choice in ungulates. In: Sexual segregation in vertebrates: ecology of the two sexes—Ruckstuhl KE, Neuhaus P, eds. (2005) Cambridge: Cambridge University Press. 148–61.
Main MB, Weckerly FW, Bleich VC. Sexual segregation in ungulates: new directions for research. J Mammal (1996) 77::449–61.[CrossRef][Web of Science]
Michelena P, Bouquet PM, Dissac A, Fourcassie V, Lauga J, Gerard JF, Bon R. An experimental test of hypotheses explaining social segregation in dimorphic ungulates. Anim Behav (2004) 68::1371–80.[CrossRef][Web of Science]
Michelena P, Henric K, Angibault JM, Gautrais J, Lapeyronie P, Porter RH, Deneubourg JL, Bon R. An experimental study of social attraction and spacing between the sexes in sheep. J Exp Biol (2005) 208::4419–26.
Michelena P, Noel S, Gautrais J, Gerard JF, Deneubourg JL, Bon R. Sexual dimorphism, activity budget and synchrony in groups of sheep. Oecologia (2006) 148::170–80.[CrossRef][Web of Science][Medline]
Miquelle DG, Peek JM, Van Ballenberghe V. Sexual segregation in Alaskan moose. Wildl Monogr (1992) 122::1–57.
Mooring MS, Fitzpatrick TA, Benjamin JE, Fraser IC, Nishihira TT, Reisig DD, Rominger EM. Sexual segregation in desert bighorn sheep (Ovis candensis mexicana). Behaviour (2003) 140::183–207.[CrossRef]
Mysterud A. The relationship between ecological segregation and sexual body size dimorphism in large herbivores. Oecologia (2000) 124::40–54.[CrossRef][Web of Science]
Neuhaus P, Ruckstuhl KE. Foraging behaviour in Alpine ibex (Capra ibex): consequences of reproductive status, body size, age, and sex. Ecol Ethol Evol (2002a) 14::373–81.
Neuhaus P, Ruckstuhl KE. The link between sexual dimorphism, activity budgets, and group cohesion: the case of the plains zebra (Equus burchelli). Can J Zool (2002b) 80::1437–41.
Neuhaus P, Ruckstuhl KE. Can the activity budget hypothesis explain sexual segregation in desert bighorn sheep? Behaviour (2004) 141::513–20.[CrossRef]
Pérez-Barbería FJ, Gordon IJ. The influence of sexual dimorphism in body size and mouth morphology on diet selection and sexual segregation in cervids. Acta Vet Hung (1998) 46::357–67.[Web of Science][Medline]
Pérez-Barbería FJ, Gordon IJ. Body size dimorphism and sexual segregation in polygynous ungulates: an experimental test with Soay sheep. Oecologia (1999) 120::258–67.[CrossRef][Web of Science]
Pérez-Barbería FJ, Gordon IJ. Differences in body mass and oral morphology between the sexes in the Artiodactyla: evolutionary relationships with sexual segregation. Evol Ecol Res (2000) 2::667–84.
Perez-Barberia FJ, Robertson E, Gordon IJ. Are social factors sufficient to explain sexual segregation in ungulates? Anim Behav (2005) 69::827–34.[CrossRef][Web of Science]
Robinson CJ, Pitcher TJ. Hunger motivation as a promoter of different behaviours within a shoal of herring: selection for homogeneity in fish shoal? J Fish Biol (1989a) 35::459–60.[CrossRef][Web of Science]
Robinson CJ, Pitcher TJ. The influence of hunger and ration level on shaol density, polarization and swimming speed of herring, Clupea harengusL. J Fish Biol (1989b) 34::631–3.[CrossRef][Web of Science]
Ruckstuhl KE. Foraging behaviour and sexual segregation in bighorn sheep. Anim Behav (1998) 56::99–106.[CrossRef][Web of Science][Medline]
Ruckstuhl KE. To synchronise or not to synchronise: a dilemma for young bighorn males? Behaviour (1999) 136::805–18.[CrossRef]
Ruckstuhl KE, Festa-Bianchet M. Group choice by subadult male bighorn sheep: trade-offs between foraging efficiency and predator avoidance. Ethology (2001) 107::161–72.[CrossRef][Web of Science]
Ruckstuhl KE, Kokko H. Modelling sexual segregation in ungulates: effects of group size, activity budgets and synchrony. Anim Behav (2002) 64::909–14.[CrossRef][Web of Science]
Ruckstuhl KE, Manica A, MacColl ADC, Pilkington JG, Clutton-Brock TH. The effects of castration, sex ratio and population density on social segregation and habitat use in Soay sheep. Behav Ecol Sociobiol (2006) 59::694–703.[CrossRef][Web of Science]
Ruckstuhl KE, Neuhaus P. Sexual segregation in ungulates: a new approach. Behaviour (2000) 137::361–77.[CrossRef]
Ruckstuhl KE, Neuhaus P. Sexual segregation in ungulates: a comparative test of three hypotheses. Biol Reviews (2002) 77::77–96.
Ruckstuhl KE, Neuhaus P, eds. Sexual segregation in vertebrates: ecology of the two sexes. (2005) 1st. Cambridge: Cambridge University Press. 488.
Senior P, Butlin RK, Altringham JD. Sex and segregation in temperate bats. Proc Roy Soc Lond Series B (2005) 272::2467–73.
Villaret JC, Bon R. Social and spatial segregation in Alpine Ibex (Capra ibex) in Bargy, French Alps. Ethology (1995) 101::291–300.[Web of Science]
Watts DP. Sexual segregation in non-human primates. In: Sexual segregation in vertebrates: ecology of the two sexes—Ruckstuhl KE, Neuhaus P, eds. (2005) Cambridge: Cambridge University Press. 327–47.
Weckerly FW. Are large male Roosevelt elk less social because of aggression? J Mammal (2001) 82::414–21.[CrossRef][Web of Science]
Weckerly F, McFarland K, Ricca M, Meyer K. Roosevelt elk density and social segregation: foraging behavior and females avoiding larger groups of males. Am Midl Nat (2004) 152::386–99.[CrossRef]
Weckerly FW, Ricca MA, Meyer KP. Sexual segregation in Roosevelt elk: cropping rates and aggression in mixed-sex groups. J Mammal (2001) 82::825–35.[CrossRef][Web of Science]
Yearsley IM, Perez-Barberia FJ. Does the activity budget hypothesis explain sexual segregation in ungulates? Anim Behav (2005) 69::257–267.[CrossRef][Web of Science]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  T. Coppack and F. Pulido Proximate control and adaptive potential of protandrous migration in birds Integr. Comp. Biol., November 1, 2009; 49(5): 493 - 506. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D.P. Croft, S.K. Darden, and G.D. Ruxton Predation risk as a driving force for phenotypic assortment: a cross-population comparison Proc R Soc B, May 22, 2009; 276(1663): 1899 - 1904. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||