Cognition; Neoteny; Philopatry; Psychological investment; Rutting area. 1. .... Fidelity of the tagged lambs to their birthplace for the successive rutting periods.
Behavioural Processes 35 ( 1996) 9% 100
ELSEVIER
Philopatry in mouflon rams during the rutting season: Psycho-ethological determinism and functional consequences Michel Dubois *, Institut
de Recherche
Kamran
sur les Grands
Khazrziie, Colette Guilhem, Marie-Line Maublanc, Yvonnick Le Pendu
Mammiferes,
INRA, CRA Toulouse,
BP 27.31326
Castanet
Tolosan
Cedcr.y. France
Accepted 2 March I995
Abstract Our study of mouflon (Ouis musimon) rams in the Caroux-Espinouse massif (southern France) shows that several forms of philopatry occur. Some of the rams were sedentary, as were the ewes, up to the age of four years. Most of the rams, however, started to enlarge their home range from the age of two years. Rams of intermediate age visited their birth ranges during various periods of the year, whereas the adult males returned only during the rut. As potential mates were present on the home ranges of most of the dispersive males, it is difficult to interpret this process merely in terms of adaptation. We propose, instead, a psycho-ethological explanation, whereby the physiological disturbances intervening during the rut alter the significance of the range, the ram having to update the whole set of its sensory-motor past. This interpretation suggests that the animal has no representation of any pre-defined place, nor of any fixed aim. Rams would be able to reduce the imbalances they experience by creating a type of behaviour driven by a self-referential process, where spatial investment would outweigh any other evaluation, as an adaptative cost related to a possible inbreeding. This approach leads to reconsider the importance of spatial investment in animal’s cognition and generally speaking the way an animal relates to its environment. Keywords:
Cognition;
Neoteny; Philopatry;
Psychological
investment;
Rutting area
1. Introduction Studies on animal dispersion have demonstrated that the majority of species predominantly show 1983). Dispersion consists in long range male dispersion (Greenwood, 1980; Waser and Jones, movements without return to previously established home ranges whereas individuals that are faithful to their natal and breeding site are termed philopatrics (Greenwood, 1980). The functions of this type
* Corresponding
author.
0376.6357/96/$15.00 0 SSDI 0376-6357(95)00044-5
1996
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of dispersion as well as philopatry have often been dealt with in ecoethology (see review: Pusey and Packer, 19871, but researchers have focused on the cost/payoff ratio and have not taken into account the psychological processes which generate them (Gaines and McCleghan, 1980). Although they are difficult to investigate, it could be worthwhile to do so since they may help to understand how the animal’s Umwelt, as defined by von Uexkull (19561, is organised. The aim of our work was to provide a new analysis of a spatial dispersion phenomenon, by means of a psycho-ethological approach (Gallo, 1988). We investigated a polygynous ungulate of the genus Ovis, the mouflon, which presents social and spatial characteristics that appeared appropriate for the present study. For instance, progressive sexual segregation outside the restricted breeding season is found in wild sheep and in many other species of ungulates (see review by Bon, 1991a). It is expressed both socially and spatially, and may be associated with dispersion of males. Nevertheless, ungulates commonly show strong attachment to their home range (Jarman, 19701, especially for the particular area where they have been reared (Chesser and Ryman, 1986). On the other hand, different studies show that ungulates are also faithful to their rutting area (Dubois et al., 1993; Staines, 1974). According to these different patterns, it seems that during their development males would be confronted with a paradox which concerns, firstly, spatial attachment and, secondly, segregation of the sexes leading to dispersion. In a general manner, inductive value of precocial attachment is important in the dynamics of spatial behaviour, individuals holding their position close by or at a distance from their attachment unit (Hinde and Atkinson, 1970; Vidal, 1987). It therefore appears appropriate to evaluate the weight of a ram’s spatial attachment to its birth range by measuring its tendency to move closer to it or away from it (Wickler, 1976). In a previous paper dealing with older males (Dubois et al., 19931, we reported the ontogenetic character of the patterns of space occupation as well as a steady lengthening of their home range. Two types of males can be schematically distinguished: residents and dispersers. The disperser males leave their reproduction range after the rut but remain faithful to it during later ruts. Greater variability in temporal space occupation patterns is observed in younger rams which, while they are occupying a given non-rutting range, also tend to frequent their rutting range. This paper is intended to complement what we have already described by examining in juvenile animals the evolution of the paradox between spatial attachment and dispersion. In the light of our results, we now test, by following the natal dispersion of tagged individuals, the hypothesis that the location/specific to precocial experience affects animal’s psychological investments, and induces spatial attachment and so philopatry. This procedure can investigate two types of question allowing to reconsider the styles of cognition of the animal. One involves the way an animal relates to its environment and the other the importance of spatial investment process.
2. Materials and methods The study area is the hills of Caroux-Espinouse, situated between the Montagne Noire and the Causses in the north-west of the department of the HCrault (South of France). Our study was based on both radio-tracking and visual sightings. From spring 1987 to the beginning of 1992, some mouflons were monitored and others, which were marked with highly visible tags as lambs, were observed by chance observation. Each ram’s age was incremented by one
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on 15 April of each year (Bon, 1991b). The mating period occurs in autumn but we note an arrival of young males on their rutting ground as early as September (Dubois et al., 1993). Concerning the visual sightings, 32 lambs were marked (8 in 1987, 8 in 1988 and 16 in 1989). The stability of ewes at the moment of capture (Dubois et al., 1992), leads to the likely assumption that lambs are trapped around their birthplace and so, belong to that valley. When animals were located on their original valley during the rutting season (September to December), they were considered as faithful to their birth home range for rutting activities. Concerning the tendency for dispersion, a previous study (Dubois et al., 1993) showed that rams did not disperse in their first year. We only made observations of animals over one year and determined an outside rut centre of activity (Hayne, 1949) which we compared with the point of original capture. We found (Dubois et al., 1993) that certain males of 4 years of age do not disperse outside the rut. For these rams, the maximum distance between the center of activity for October and the extreme monthly centre of activity is 1.0 km. Rams tagged as lambs whose outside rut centre of activity was found at least 1.0 km away from the point of original capture were classified as dispersing individuals, while those for which the considered centre of activity was found less than 1.O km were treated as non-dispersing individuals. Because of a lack of observations outside the rut, we could only consider the dispersion tendency of 17 tagged individuals. Concerning radio tracking, 20 males were followed from summer 1987 to the beginning of 1992. The radio-tracking system employed has already been described (Dubois et al., 1992, 1993). The data were recorded on a detailed map ( 1:25 000) of the study site, overlaid with a scaled grid of 125 X 125 m quadrats. The males were aged by counting the horn annuli (Pfeffer, 1967; Geist, 1971); they ranged in age from less than one year to around 9 years at the moment of capture. According to the hypothesis of philopatry of males (Dubois et al., 19931, we consider the original valley as the valley where the animal was trapped. We used the point of original capture as reference point of dispersion. To evaluate the spatial dynamics of these rams and the degree of elongation of the home range, we based our analysis on the position of the rutting ground. To represent it, we used the centre of activity of the first month of effective rutting activities in October (Bon, 1991b) and calculated the distance between this point and the centre of activity of each monthly range. In the case of multiple comparisons, the threshold of binary tests (one-sided probability) was systematically lowered to 0.05/c (where c is the number of binary test), so that the risk of stating that at least one sample differs from the others when the null hypothesis is true, does not exceed the threshold of 0.05 (see Sherrer, 1984).
3. Results 3.1. Dynamics of spatial occupation and dispersion For the rams followed by radiotracking, dispersion movements may be important and the mean distance recorded between the trap site and the most extreme location was 3.0 km (range = 1.7-5.4 km). As with the lambs followed by radio tracking (Dubois et al., 19931, the tagged individuals showed a steady lengthening of their home range and thus moved further away from their birth range (Fig. 1).
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7000C Y ***
B .z
Y
8 ‘, B
-T
6ooo; 3000
P
S 4000 5000
***
O1 year2 years
2 years 3 years
3years4 years
Fig. 1. Distance of male lambs from their birth range against age. (Evaluated from the yearly observation furthest from the capture site). * * * P < 0.05 (Wilcoxon signed rank test).
This movement was significantly smaller between 1 and 2 years of age than after the age of 2 (P < 0.05/3, Wilcoxon signed rank test, T = I1 and T = 0). Concerning the same individuals, we were only able to establish the non-rutting range for 17 of them. Only 7 set up their non-rutting range at more than 1 km from their birth place (Mean = 2.1 km, range = 1.1-3.2 km) and could be considered as dispersers. Of the 10 other individuals, only 3 could be qualified as residents, being observed over the years and during different seasons on their birth ranges. The seven other rams were observed in their original valley only during the spring. As already reported for young animals fitted with radio collars (Dubois et al., 1993) odd visits can occur during this season. Therefore, the observations do not mean that the animals remain there all the year. This is supported by the fact that outside the rutting period males tend to occupy wooded habitats (Auvray, 1983; Dubois, 1990) where the detectability of the animals is reduced. For the 15 other animals, we were not able to collect sufficient data to determine a non-rut range, but isolated sightings very far from their birth ranges suggest that they disperse and occupy wooded areas where observation is difficult. For all the animals considered, the average distance recorded between the place of capture and the furthest location was 3 km (range = 1.7-6.3 km).
Table 1 Fidelity of the tagged lambs to their birthplace for the successive rutting periods
Faithfulness Unfaithfulness No. of animals with no resighting during the current rut
1st year N=32n=O
2nd year N=27n=5
3rd year N=24n=8
4th year N=12n=4
5th year N=7n=l
18 0 14
17 1 9
6 0 18
5 0 7
4 1 2
N = number of animals known to be alive; n = number of animals considered as dead.
M. Dubois et al. / Behauioural
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35 (1996)
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Distance from the first month of rutring (in meters)-
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-------------
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Fig. 2. Distance between the centre of activity Examples given in lambs and residents in (a); indicated after the number of each one. In order no difference between the individuals above and whilst deviations donwards are negative).
3.2. Faithfulness
I
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7
8
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for the first month of October and the other monthly centres of activity. examples given in dispersers in (b). The age of individuals at capture is to explain the design of the ‘ y’ axis, we can note that in each graph there is below the 0 line (deviations from 0 in an upward direction are not positive,
to the rutting area or to the birthplace area
Concerning males marked with visual tags as lambs, from Table 1, we could consider that faithfulness is strong even if the number of animals with no resightings is high. Nevertheless, these animals cannot be classed as unfaithful because depending upon the years, they were observed in their birthing area, and so faithful or not, they were never observed outside it during the rut. With the exception of two individuals which were observed outside their original valley during the rut, in spite of a very close watch, we did not observe other cases of unfaithfulness or actual dispersion. Concerning males followed by radio tracking, we indicate in Fig. 2 examples of the dynamics of spacing for lambs and residents in (a) and disperser individuals in (b). By using radio tracking data or direct observations (after breakdown of the transmitter), we noted that the 20 individuals originally marked with radiotransmitters showed strict faithfulness to the birthplace or to the rutting area for the successive rutting periods.
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4. Discussion The progressive segregation of the sexes outside the rutting period, previously reported for our study population (Bon and Campan, 19891, is associated with a steady changes occurring in the space occupation patterns. The segregation is apparent not only socially but also spatially, since the home range elongates and becomes differentiated into a rutting and a non-rutting range (Dubois et al., 1993). Schematically, this space occupation pattern stresses the existence of a paradox, mentioned in the introduction, of two poles of attraction. As in other sheep (Grubb and Jewell, 1966; Geist, 19711, the young males leave their mother’s group after their first or second year. The dispersion can be permanent like in the red deer (Cervus elaphus), where no overlap with the maternal range is observed after 2 years of age (Clutton Brock et al., 1982). However, site fidelity has been well documented in different ungulates where sexual segregation exists (Bowyer, 1984; Scarbrough and Krausman, 1988). In this context, we only observe a progressive social segregation indicated by a shift in the types of groups with which males and females associate. In our study, the phenomenon of dispersal is not at all obvious since some rams are sedentary and, in spite of a progressive dispersion of the others, males are faithful not only to the same rutting area but also to their birth place. Even as dispersers, rams of l-3 years of age occupy their birthing area in non-rut periods. Like bucks of white-tailed deer (Odocoileus virginianus) studied by Nelson and Mech (19841, their spatial behaviour appears to be less fixed than that of older ones. According to the definition of Greenwood (1980: see above), our hypothesis is confirmed and the rams we studied are philopatrics. These facts highlight a spatial attachment of individuals to this particular area which outweigh the possibility and functional consequences of inbreeding. Various studies in ungulates have shown that the process of separation of the young males from their native range is progressive (Cederlund et al., 1987; Lidfors and Jensen, 1988). Nevertheless, before achievement of this process, the individual usually maintains contact with familiar space (Salzen, 1967; Vidal, 1987). Disturbances in this general process may have spatial consequences. Holzenbein and Marchinton (1992) noted that in white-tailed deer, orphaned males maintained greater affinity to their natal range than did non-orphans. For Thorhallsdottir et al. (1987), young sheep are sensitive to social influences and for Festa Bianchet (19861, at some times the tendency for young rams to follow attractive males may be greater than the tendency to stay in the area they are attached with. Male social ‘preferences’ may induce their dispersion since maturing rams tend to follow the largest-homed males (Geist, 1971; Festa Bianchet, 1986) which are more likely to have a non-rut home-range (Dubois et al., 1993). For Geist (19711, the ram’s change in social preferences appears to result from the female’s unsatisfactory social responses. As in other ungulate species, mouflon rams seem to find in other males behavioural partners compatible with their juvenile behaviour (Geist, 1968), which would be an endogenous correlate of both masculinization (Meaney, 1988) and neoteny. The latter, an intra-specific heterochronic change in ontogeny related to a phyletic trend (Gould, 1977; Alberch et al., 19791, leads to the fact that rams continue their physical growth and behavioural development up to 8 years of age (Geist, 1971). The change in socio-spatial patterns (the ram’s return), which seems to be induced by the re-establishment of early spatial investment, is pronounced in the older males, since they are never observed in groups of ewes outside the rutting period (Bon et al., 1993) and do not return to the rutting range (i.e. the birth range), except for mating. Since the animals could mate outside their rutting range, as ewes are residing in the immediate vicinity, it seems that the females themselves are not the attractors. Geist (1971) noted that bighorn rams which could mate with females living in their
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summer range ignore them and can cover more than 20 km to get back to their usual rutting ground. The author notes that these males seem to be ‘blind’ to the opportunities they meet for mating and qualifies their behaviour as irrational. In our opinion, the physiological disturbances intervening during the rut would alter the significance of the range. At that time, the neotenic rams would update the set of their sensory-motor past. Once they have returned to the familiar area of their early experience, salient patterns, like oestrus scent (which is learned; Zenchak et al., 19811, would change the polarity of the investments which would be effectively driven by females, permitting a productive coupling. Rams would be able to reduce the imbalances they experience by creating a type of behaviour driven by a self-referential process, where spatial investment would outweigh any other adaptative consideration. This proximal interpretation suggests that the animal has no representation of any pre-defined place, nor of any fixed aim in an environment which meaning is not previously determined. In our opinion, this work provides a new analysis of a spatial dispersion phenomenon and leads to consider the way an autonomous animal relates to an environment.
Acknowledgements We are grateful to Raoul Taigneux, Lou Chamane and Elodie Koubivline for the helpful discussions, and to RenC Zayan and anonymous reviewers for their comments on earlier drafts. We also like to thank Peter Winterton from the University of Toulouse III who translated the manuscript.
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