Behavioral Ecology Vol. 15 No. 2: 262-268
Behavioral Ecology vol. 15 no. 2 © International Society for Behavioral Ecology 2004; all rights reserved
Early learning affects social dominance: interspecifically cross-fostered tits become subdominant
Department of Biology, University of Oslo, P.O. Box 1050 Blindern, N-0316 Oslo, Norway
Address correspondence to B. T. Hansen. Email: b.t.hansen{at}bio.uio.no.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Social dominance influences the outcome of competitive interactions over limited resources, and may hence be important for individual fitness. Theory thus predicts that its heritability will be low and that non-genetic determinants of dominance should prevail. In this field experiment we reciprocally cross-fostered great tits (Parus major) to blue tits (Parus caeruleus) to investigate the impact of early social experience on dominance status in competition over food during winter. Controlling for potential effects of age, size, sex and site-related dominance, we show that cross-fostered birds of both species were subdominant to conspecific immigrants, while controls originating from unmanipulated broods were dominant to conspecific immigrants. Furthermore, blue tits reared by blue tit parents but with at least one great tit broodmate had lower dominance status relative to conspecific immigrants than did controls. Although great tits generally dominated blue tits, cross-fostered birds of both species initiated marginally more fights against the other species than did their respective controls, suggesting faulty species recognition. Since both social parents and broodmates strongly influence the dominance behavior of offspring later in life, we conclude that social conditions experienced at an early age are crucial for the determination of subsequent social dominance.
Key words: dominance, aggression, cross-fostering, imprinting, Parus major, Parus caeruleus.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Being dominant in social interactions may confer advantages in survival (Arcese and Smith, 1985
; Desrochers et al., 1988) and reproductive success (Collias et al., 1994; Kikkawa and Wilson, 1983). Proximately, such advantages of dominance could relate to better resource access (Hogstad, 1988), higher feeding efficiency (Smith et al., 2001) and priority at safe feeding sites (Piper, 1990). Dominance may also incur specific costs, such as prolonged elevated excretion of stress hormones (Creel, 2001), higher metabolic rate (Hogstad, 1987; Røskaft et al., 1986) and higher fighting rate (Rohwer and Ewald, 1981). However, dominance is positively related to fitness, hence the benefits generally outweigh the costs. Dominance is potentially important whenever there is competition for a limited resource, and it has been studied in various contexts across many taxa (e.g., Abbot et al., 1985; Guilhem et al., 2002; Halley and Gjershaug, 1998; Holekamp and Smale, 1993; Moore, 1990). For birds living in flocks, winter food limitation is a common context in which to investigate social dominance (e.g., Desrochers et al., 1988; Jansson et al., 1981; Kikkawa, 1980).
Correlates of dominance are frequently inconsistent across studies, presumably because of species differences and differences in experimental design. Moreover, the outcome of fights may vary according to asymmetries between competitors in the value of the contested resource (Krebs, 1982; Nosil, 2002; Renison et al., 2002). A subdominant individual may therefore sometimes initiate more fights than a dominant individual if the limited resource is more crucial for its survival. However, sex, age, size and site-related effects often seem to be important in determining dominance (reviewed by Piper, 1997).
Although many potential correlates of dominance have been identified, they do not seem to fully explain the variation in dominance among conspecific individuals of the same sex. Piper and Wiley (1989) showed that as much as 50% of individual variation in dominance remained unexplained in an exhaustive study of dominance correlates in white-throated sparrows (Zonotrichia albicollis). They suggested that genetic and developmental effects may be of potential importance for this unexplained variance. Indirect genetic effects arising from social interactions have also been incorporated into a quantitative genetic model which attempts to describe the evolution of social dominance (Moore et al., 1997; Moore et al., 2002). In spite of this awareness of environmental influences, few have studied the effect of early social experiences on dominance ability, but the available evidence suggests that it might be important (Boag and Alway, 1980; Piper, 1995; Westman, 1990). A number of studies also suggest considerable effects of inheritance on dominance (Baker and Fox, 1978; Boag, 1982; Dewsbury, 1990; Moore, 1990; Moss et al., 1982; Nol et al., 1996).
We want to investigate the effects of early experiences on subsequent dominance status by interspecifically cross-fostering great tits (Parus major) to blue tits (Parus caeruleus) and vice versa. These species have similar diets and cross-fostered birds do not appear to be physically disadvantaged relative to controls (Slagsvold and Hansen, 2001; Slagsvold et al., 2002). We have previously shown that the recognition of potential mates (Slagsvold et al., 2002) and sexual rivals (Hansen and Slagsvold, 2003) is influenced by cross-fostering in both species. Here we look for effects of interspecific cross-fostering on dominance in aggressive interactions over limited food, using a multivariate approach to control for established correlates of dominance. In addition to giving information about a potential determinant of dominance that has not been extensively studied (reviewed by Piper, 1997), the findings may be relevant to the practise of interspecific cross-fostering to save endangered species (e.g., Butler and Merton, 1992).
If early social experiences influence intraspecific dominance status, we expect cross-fostered birds to have a lower dominance status than controls. This could result from cross-fostered birds not having acquired the aggressive behavior patterns neccessary for successful intraspecific competition, or a lack of motivation to attack conspecifics due to mistaken species recognition. Alternatively, if early social experiences are unimportant, we expect the intraspecific dominance status not to differ between cross-fostered and control birds. Finally, cross-fostered birds may be willing to invest more in intraspecific fighting than are controls, e.g. because of a higher hunger level resulting from poorer species-specific foraging skills, in which case differences in motivation may override any effect of social experience. With regard to interspecific dominance interactions, the inherent size asymmetry between great tits and blue tits may determine such behavior regardless of any effect of social experience on dominance. Alternatively, cross-fostered birds may be more inclined to interact with heterospecifics than are controls, due to mistaken species recognition.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Study area and species
The fieldwork was conducted in a 1.6 km2 nestbox plot near Oslo in 1998–2002. Each year, some 70 pairs of great tits and 80 pairs of blue tits bred in the nestboxes. Blue tits and great tits are closely related (Kvist et al., 1996
) but are easily distinguishable. The great tit is socially dominant to the blue tit (Haftorn, 1993; approximate adult weights, great tit: 18g; blue tit: 11g). They often form mixed-species flocks in the non-breeding season.
Brood manipulation
There were three kinds of focal birds in this study: (1) interspecifically cross-fostered birds, (2) birds reared by their own species but with 1–2 heterospecific broodmates (blue tits only), (3) control birds (i.e. unmanipulated birds).
Blue tits and great tits were reciprocally cross-fostered to investigate how parents and siblings might influence subsequent behavior. Cross-fostering was done during egglaying or incubation by switching clutches between nests ("whole broods"; all broodmates conspecific to each other) or adding 1–2 eggs to a clutch and removing some host eggs ("mixed broods"; consisting of both great tit and blue tit individuals). Control individuals mostly originated from unmanipulated broods in the study area. However, since there were few blue tit controls, we also included 28 immigrated individuals in the blue tit control group. Too few great tits of group (2) interacted for statistical testing.
Young were weighed and banded when 15 days old. We captured adults and juveniles throughout each autumn and gave unique band-combinations to recaptured young reared in the study plot and to some immigrated blue tits. We measured wing and tarsus length, and weighed birds at their first capture. The majority of immigrants were not given unique band-combinations because we could not generate enough combinations. Separate combinations were given to immigrants each year, and to first year (1Y) and older (2Y+) birds (Jenni and Winkler, 1994) within each year.
The study was conducted under licenses from the Directorate for Nature Management and the National Animal Research Authority in Norway. The cross-fostering was done so that the demands of cross-fostered broods should not exceed those of the natural broods of foster parents. Cross-fostered individuals of both species thrived in the nest of their heterospecific foster parents and their recruitment did not differ from that of unmanipulated controls (Slagsvold et al., 2002).
Aggressive interactions
We provided sunflower seeds and fat balls at several feeding sites throughout autumn and winter. Between November and April 1999–2002 we videotaped fat balls. Each recording lasted three hours. 198 focal birds interacting in 1461 dyads during approximately 420 hours of video form the basis of the analyses of this paper. Not all focal birds interacted with all classes of opponents, thus the sample sizes differ across response variables. We only recorded one type of behavior, namely aggressive interactions characterized by an "initiator" clearly attacking or threatening a "recipient" individual, whereupon the recipient usually was displaced. Initiators usually win and recipients usually lose interactions over food (Bekoff and Scott, 1989; Halley and Gjershaug, 1998; Jackson, 1991; Nuyts et al., 1996).
We extracted separate responses of each focal bird against the following groups of opponents: (1) conspecific immigrants (of the same sex as the focal bird for great tits, but not separated by sex for blue tits), (2) conspecific birds of the other sex, (3) heterospecific birds of both sexes.
Male and female great tits have plumage differences that were evident on the videos, but this was not the case for blue tits. Hence, blue tit response to group (1) was based on interactions against all non-uniquely banded conspecific immigrants. The sample was limited to interactions between focal males and females for blue tit response to group (2) (we knew the sex of focal blue tits from handling them and from behavioral observations in the field).
Thirty seven different non-unique band combinations were seen on the video recordings (14 great tit male, 9 great tit female and 14 blue tit). We considered individuals bearing a non-unique combination as one individual (separated by species, and sex in the case of great tits). This procedure most likely underrepresented the number of unmanipulated individuals that actually interacted with the focal birds, but caused no bias or pseudoreplication.
Predictors
We measured the distance between a focal bird's territory and the feeding site where it interacted using a digital map. We defined four categories of departure points for focal birds: (1) the nestbox of the following breeding season, (2) the nestbox of the preceeding breeding season, (3) the nestbox in the area clearly occupied in the following or preceeding breeding season by non-breeding birds, (4) the nestbox closest to the site of capture (except when this was at any of the three main feeding sites in the study area).
We chose the first obtainable category for every focal bird. Only 4% of the focal birds were assigned a departure point of category (4), and 16 % could not be assigned a reasonable departure point. The distance moved from the departure point to the feeding site was log-transformed. We also counted the number of territories passed in a straight line from the departure point to the feeding site. If the focal bird interacted at more than one feeding site and/or in more than one year, we calculated weighted averages for the distance moved and the number of territories passed. Log(distance) better explained variation in the dependent variables than the correlated number of territories passed, hence we have excluded the latter from the analyses below.
We used age as a factor variable with three levels; 1Y: a bird in its first year; 2Y: a bird in its second year; 3Y+: a bird in its third year or older. Only 5% of the focal birds were more than 3 years old. A focal bird interacting in more than one year was assigned the age when it interacted most frequently. The correlated measures of tarsus length, wing length and weight at capture were combined into one variable ("size") by principal component analysis. The squared factor loadings for great tits and blue tits were, respectively: 78%, 56% (wing length), 41%, 67% (weight), 80%, 68% (tarsus length).
Initial analyses included a treatment predictor with separate levels for cross-fostered individuals from "mixed" and "whole" broods. It turned out that they did not differ in response (analyses not shown), and we have hence pooled data for the two cross-fostered groups in the analyses below.
Statistics
The response variable is a two-column matrix of the number of individuals against which a focal individual initiated and the number of individuals from which it received aggression. If the focal individual acted as both initiator and recipient towards the same bird, the fraction of initiations (and receptions) against this particular bird was used. The number of initiations and receptions were combined using the cbind function in Splus (Venables and Ripley, 1999), and we analyzed this response variable in generalized linear model (GLM) analyses of deviance, with binomial errors and a logit link function (McCullagh and Nelder, 1989; Thomson et al., 1998). Using the number of individuals interacted with rather than proportions of initiations of aggression is advantageous because it takes the quantity of observational units into account. We illustrate the response using the mean + SE number of individuals against which focal birds have initiated and received aggression.
We included several covariates in the initial regression model:
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We performed model selection using the AIC-value corrected for small samples (AICc, Burnham and Anderson, 2002). When the difference in AICc-value between models was small (<2), we chose the simplest model. The "treatment"-term was always retained whether or not it improved the AICc of the model. Goodness of fit was assessed by diagnostic plots and the statistical significance of the Pearson chi-square of the fitted model. Three models were significantly overdispersed and they were remedied by quasi-likelihood.
The significance of the terms in the GLMs are based on the difference in deviance (
D) and degrees of freedom (df) of models with and without the predictor in question (likelihood ratio tests). For binomial models, the chi-square test was applied, and for quasi-likelihood models, the F-test was applied. Terms were added sequentially, with the "treatment"-term added last.
Coefficients from GLMs are expressed as natural logarithms unless stated otherwise. All p-values are two-tailed. Non-parametric tests were corrected for ties. Tests were performed with S-plus 6.0 or Statview 5.0.
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RESULTS |
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Interactions among great tits
Cross-fostered great tits initiated aggression against fewer and received aggression from more conspecific immigrants of the same sex than did controls (Table 1, Figure 1). The odds ratio shows that controls were 18.7 ± 1.7 times more likely than cross-fostered great tits to initiate an interaction with a conspecific immigrant of the same sex.
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Interactions among blue tits
Cross-fostered blue tits initiated aggression against fewer and received aggression from more immigrant blue tits than did controls (Table 2, Figure 2). The odds ratio between controls and cross-fostered birds was 4.6 ± 1.5.
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Blue tits reared by blue tit parents but with 1–2 great tit broodmates also had a lower dominance status than controls in interactions against conspecific immigrants (Table 2, Figure 2). Their odds ratio against controls was similar to that of cross-fostered blue tits (4.1 ± 1.6). This shows that even broodmates can influence subsequent dominance status. There was some correlation between the estimates of treatment and sex in the model (r = 0.23; there were 10 female controls, but only one female in the contrasting sample), but exclusion of females did not alter the results qualitatively.
Species comparison
We contrasted the performance of cross-fostered and control birds of the two species in interactions with conspecific immigrants of both sexes. The interaction-term between treatment and species was hence included in the model regardless of its effect on goodness of fit. The analysis shows that there was no difference between great tits and blue tits in interactions with conspecific immigrants (Table 3, Figure 3). Hence, interspecific cross-fostering seems to have affected the dominance status of both species similarly.
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Interspecific and intersexual interactions
Great tits generally dominated blue tits (Figure 4). Cross-fostered and control individuals of both species differed in the tendency to act as initiator and recipient against heterospecifics, though the effect fell short of significance in great tits (Table 4). Since only the initiating response is active and thus might reveal a social inclination by the initiator towards the recipient, we performed separate post-hoc tests for initiating and receiving aggression in interactions with heterospecifics. Cross-fostered birds of both species tended to initiate against a higher number of individuals of the other species than did controls (Mann-Whitney U tests, great tits: Z = 1.78, n = 39, 31, p = 0.075; blue tits: Z = 1.98, n = 28, 26, p = 0.048), while there was little difference between treatments in the number of heterospecific individuals they received aggression from (great tits: Z = 1.03, p = 0.30; blue tits: Z = 0.13, p = 0.89). Blue tits reared by blue tit parents but with 1–2 great tit broodmates tended to act as both initiator (Z = 1.96, n = 12, 26, p = 0.051) and recipient (Z = 1.93, p = 0.054) against a higher number of great tit individuals than did controls (Figure 4).
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Males generally dominated conspecific females, and there was no difference between controls and cross-fostered birds in this respect (each sex modelled separately, all analyses
df = 1; great tit females: D = 0.03, p = 0.82 great tit males: D = 0.46, p = 0.5, blue tit females: D = 0.003, p = 0.96, blue tit males: D = 1.24, p = 0.27).
Covariate effects
Distance between the territory of a focal bird and the interaction site proved significant in most models; the odds for initiating consistently increased with decreasing distance. Not surprisingly, sex was also important in all models where the opponents to the focal birds were not sexed. In these cases, the odds for initiating were higher for males than for females. Size was retained in two models. Note that the coefficients of size and sex were correlated (r = 0.64 and 0.61 in the analyses of Tables 2 and 4; males are larger than females), meaning the two effects cannot be properly separated. Age proved important in one model, and its effect was influenced by a correlation with the coefficient of treatment (r = 0.66; there were relatively more 1Y and less 3Y+ cross-fostered than control birds in this sample; the results did not change qualitatively when limiting the analysis to 1Y birds only). The species effect in the comparison of great tits' and blue tits' response to conspecific immigrants was that great tits interacted somewhat more than blue tits. Interaction-terms did not significantly improve any model.
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DISCUSSION |
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Interspecifically cross-fostered blue tits and great tits clearly had a lower dominance status relative to conspecific immigrants than did unmanipulated controls. They both received aggression from more and initiated aggression against fewer conspecific immigrants than did controls. Blue tits reared by their own parents but with at least one heterospecific broodmate also had a lower dominance status than controls in interactions with conspecific immigrants. Cross-fostered blue tits initiated against more individuals of the other species than did blue tit controls, and a similar trend was evident for great tits, indicating mistaken species recognition in cross-fostered birds. The findings support the hypothesis that early social experiences have a long-lasting influence on subsequent dominance ability.
Cross-fostering leads to subdominance
Letting young be reared by parents unrelated to them may break up parent-offspring coadaptations, which by itself is predicted to lower fitness (Wolf and Brodie, 1998). Employing intraspecific cross-fostering, Agrawal et al. (2001) demonstrated that variation in maternal care stem from two distinct sources: variation among offspring in their ability to elicit care and variation among parents in their response to offspring signals. Furthermore, cross-fostered strains of mice obtain more resources from foster mothers of the same strain as their natural mother (Hager and Johnstone, 2003). Thus, cross-fostered offspring and their foster parents may reciprocally be poor at eliciting adequate behavior. The interspecifically cross-fostered tits in the present study may hence have become subdominant because their foster parents represented inadequate role models for the learning of dominance skills. Alternatively, they may have learned heterospecific skills which did not function in conspecific interactions. Third, cross-fostered and control birds may have differed in motivation because the former did not recognize conspecifics as such. The social dominance observed in competition for food may also serve other purposes, notably related to breeding (Otter et al., 1998; Otter et al., 1999). Because the cross-fostered birds are sexually misimprinted (Hansen and Slagsvold, 2003; Slagsvold et al., 2002), winning food-fights against conspecifics may not have served their mating interests, hence they may have become submissive targets of attack for dominant conspecifics. We cannot distinguish between these possibilities. The aggressive behavior patterns of great tits and blue tits seem virtually identical (Hinde, 1952; Stokes, 1962), and potential differences between controls and cross-fostered birds in this reportoire were too subtle to be confidently quantified.
Some studies have indicated that early social experience might affect dominance. The dominance rank of captive gallinaceous birds may be influenced by the number of same-sex siblings (Boag and Alway, 1980), but this effect may be overridden by inheritance (Boag, 1982). Westman (1990) reported a correlation between the dominance rank of great tit females and their foster chicks. Further, hand-reared white-throated sparrows partially reared in isolation, attain a different dominance status than individuals with no experience of isolation (Piper, 1995). The sample sizes were low in the two latter studies. Finally, Drummond and Osorno (1992) showed that the dominance relationship between blue-footed booby (Sula nebouxii) nestlings did not change even though the size asymmetry between them was reversed. However, they did not control for differential testosterone investment in eggs, which also could explain this behavior (Gil et al., 1999; Schwabl, 1993).
Siblings affect dominance
There was no difference in the dominance status of cross-fostered birds from the whole and mixed broods in any of the species, but, surprisingly, blue tits reared by blue tit parents but with at least one great tit broodmate had a lower dominance status than controls when interacting with conspecific immigrants. It hence seems like the effect of parents on dominance status overrides the effect of siblings since the latter effect only is expressed in the absence of the former. The finding that individuals from manipulated broods seem to suffer from inferior fighting abilities irrespective of how their brood was manipulated, indicates that even quite modest interspecific brood manipulations may have severe consequences.
Drummond and Osorno's (1992) scenario for boobies may explain why blue tits from mixed broods became subdominant. The cross-fostered great tits in such broods might have dominated all blue tit broodmates, hence training them to become submissive loosers. Indeed, such a mechanism could explain a lot of the natural variation in dominance since causing behavioral polymorphism within broods also would ensure variation within populations.
Other determinants of dominance
Apart from experimental treatment, the only other predictor that proved consistently important in our models, was the distance between the territory of the interacting bird and the site of interaction. There was a negative relationship between dominance ability and distance moved, as has been reported in other studies (e.g., De Laet, 1984; Piper and Wiley, 1989). Interestingly, the relatively few cross-fostered birds that behaved dominantly mostly resided quite close to the interaction site. This shows that even the experience of being cross-fostered not always prevailed in determining dominance. Note also that age may be a more important determinant of dominance than is indicated here, because 66 % of the focal birds in this paper were yearlings. Finally, the fact that controls dominated conspecific immigrants suggests an impact of prior residency on dominance, as has been established previously (Sandell and Smith, 1991; Krebs, 1982).
Being reared by heterospecifics is beyond the extremes of rearing conditions experienced by most species in nature. Under natural conditions, other determinants of dominance may indeed prove more important than they appeared in this experiment. However, rearing conditions and hence dominance learning may vary considerably within species, for instance through death or attainment of a second brood by one of the parents (influencing parental presence), population density and resource access (influencing degree of competition) and parental dominance status itself.
Species recognition and conservation
Although great tits mostly dominated blue tits, the hypothesis that controls and cross-fostered birds would not differ in this respect was not supported. Instead, cross-fostered birds of both species tended to initiate aggression against more individuals of the other species than did their respective controls. Cross-fostered birds thus seem to have been more likely than controls to perceive the other species as competitors, suggesting faulty species recognition. However, this effect was not strong and, surprisingly, it was strongest in blue tits which presumably pay a higher cost for such interspecific fighting. There was little difference between the treatments in the number of heterospecifics they received aggression from, indicating that cross-fostered birds and controls of one species were not perceived as different by the other species.
Interspecific cross-fostering is used in conservation biology to boost the populations of endangered species by inducing them to produce repeated clutches, and then putting the eggs in nests of more common species (Curio, 1998; McLean, 1997). It is well-known that such practise may influence mating preferences (e.g., Butler and Merton, 1992; ten Cate and Vos, 1999), and this study suggests that species recognition in a non-sexual context also may be affected. Furthermore, we show that an additional worry is the influence of early learning on the determination of subsequent social dominance. It is notable that this effect is very strong even in populations reared in an environment otherwise natural to them with conspecific neighbors behaving normally. One recommendation emerging from this study regarding the practise of cross-fostering is that whole clutches should be cross-fostered because siblings may influence various aspects of behavior.
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ACKNOWLEDGEMENTS |
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We thank Torbjørn Ergon and Leif Christian Stige for statistical advice. Øistein Haugsten Holen, Lars Erik Johannessen, Allen Moore, Per Terje Smiseth, Leif Christian Stige and an anonymous reviewer improved an earlier draft of this paper. Highly appreciated field assistance was given by Øistein Holen, Lars Erik Johannessen, Tor Egil Kjenn and Per Kristian Slagsvold. We also thank the Haakonsen, Johnsen and Westgård families for kind permission to work on their premises.
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