- Top of page
- Materials and methods
Natal dispersal, the net movement between the natal area and the site of first breeding (Howard 1960), is one of the most important individual life-history traits affecting population dynamics and species evolution (Greenwood 1980; Clobert et al. 2001; Nathan 2001). Natal dispersal is a three-stage process involving the decision to leave the natal area, a transient phase, and finally settlement in the adult home range (Stenseth & Lidicker 1992). However, despite its importance, natal dispersal is still poorly understood, and the factors shaping variation in both dispersal rates and distances remain unknown in most cases (Ronce 2007). The main ultimate causes of natal dispersal involve inbreeding avoidance, competition (for mates or resources and kin interactions) and habitat instability (Bowler & Benton 2005).
In most populations, not all individuals disperse, and dispersing individuals are generally not a random subset of the population (Ronce 2007). Indeed, the decision an individual makes to stay in the natal area or leave it may be condition dependent (Bowler & Benton 2005). The term condition dependence encompasses the effects of both the individual's phenotype (e.g. fat reserves, body size or competitive ability) and the animal's environmental features (e.g. population density or habitat quality) on dispersal behaviour (Ims & Hjermann 2001). Both sets of factors can interact with one another in complex and subtle ways to determine dispersal outcomes. Indeed, environmental factors can affect dispersal through a direct pathway or indirectly, mediated by changes in phenotypic attributes (Ims & Hjermann 2001). Condition dependence could translate into individual differences in dispersal behaviour and can thereby indirectly generate variability in dispersal propensity among individuals, implying that dispersal costs and benefits differ among individuals (Bowler & Benton 2005). Indeed, the balance between the costs and benefits of dispersal depends on the internal state of the individual (Clobert et al. 2009), involving either fixed (e.g. sex) or time-dependent (e.g. body condition) traits. That is, dispersal may allow animals to obtain good quality ranges or to escape local competition, but since dispersal is costly (Nunes & Holekamp 1996; Dufty & Belthoff 2001), animals face a conflict the resolution of which may depend on environmental conditions or individual phenotypic attributes. For example, individuals that disperse before they have attained a certain threshold of body condition may increase the mortality risk associated with dispersal (Dufty & Belthoff 2001). As a general rule, dispersal costs, and therefore mortality risk, increase with dispersal distance, as has been demonstrated, for example, in American marten Martes americana (Johnson & Gaines 1990). After long being ignored, it is now recognised that interindividual differences in dispersal are important (Gibbs et al. 2009).
Dispersal is usually described as a dichotomous variable, opposing dispersing animals with philopatric ones. However, dispersal may be better described as a continuum, because the distinction between dispersers and philopatric individuals can be difficult to assess using some arbitrarily defined criteria. Some studies have used both a binomial variable (disperse vs. philopatric) and the dispersal distance to assess fine scale patterns of natal dispersal (Gaillard et al. 2008 in roe deer Capreolus capreolus; Selonen & Hanski 2010 in Siberian flying squirrels Pteromys volans L.; Long et al. 2005 in white-tailed deer Odocoileus virginianus). However, these studies did not account for among-individual differences in ranging behaviour prior to dispersal. In the present study, we analyse dispersal both as a Bernoulli (binomial) and a Gaussian (continuous) process. For this latter approach, we used an individual-based standardised dispersal distance (IBSDD) as a metric. This was defined as the raw dispersal distance weighted by the spatial extent of an individual's pre-dispersal range.
The distribution of natal dispersal distances shapes the speed of population spread, and potentially has thereby a strong impact on population persistence (Sutherland et al. 2000; Bowler & Benton 2005; Ronce 2007). However, despite this theoretical interest, empirical measures of interindividual variability in dispersal distances and identification of the factors affecting it are still scarce (Lowe 2010). Our empirical understanding of the causes and consequences of variation in dispersal distances is limited to some studies that assessed the impact of different factors on dispersal distance (climatic conditions in the Arctic tern Sterna paradisaea, Moller, Flensted-Jensen & Mardal 2006; wing length in female house sparrows Passer domesticus, Skjelseth et al. 2007; personality in the invasive mosquitofish Gambusia affinis, Cote et al. 2010). Although several theoretical studies have identified body condition as a potentially important predictor of dispersal distance and settlement success (Stamps, Krishnan & Reid 2005; Stamps 2006), we still lack empirical studies that have tested for condition dependence of dispersal rate and distance (Clobert et al. 2009). Heavy dominant individuals were found to disperse more than smaller ones when dispersal is energetically costly (Ims & Hjermann 2001; Bowler & Benton 2005), as reported in ground squirrels Spermophilus beldingi (Holekamp & Sherman 1989) and owls Bubo bubo (Delgado et al. 2010). In contrast, no effect of body condition on dispersal propensity was found in red deer Cervus elaphus (Loe et al. 2010) or in Siberian ground squirrels Pteromys volans (Selonen & Hanski 2010). Furthermore, at the interspecific level, Sutherland et al. (2000) demonstrated that median and maximum natal dispersal distances are correlated with species body mass in birds and mammals. Finally, in terms of environmentally driven condition-dependent dispersal, some studies have assessed the impact of population density and environment on the intensity of natal dispersal. For example, landscape fragmentation led to greater dispersal distance in white-tailed deer (Long et al. 2005) and in nuthatches Sitta europeae (Matthysen, Adriaensen & Dhondt 1995). We aimed to investigate whether natal dispersal is driven by phenotypic and/or environmental condition dependence in a large herbivore, focusing on (i) natal dispersal propensity and (ii) using an original IBSDD that accounts for among-individual variation in natal home range size.
We investigated the proximal causes underlying natal dispersal in a roe deer population living in a spatially heterogeneous agricultural landscape. Roe deer are medium-sized, slightly dimorphic and weakly polygynous mammalian herbivores that are widely spread across Europe and have markedly expanded their range since the 1960s (Andersen, Duncan & Linnell 1998). Individual body mass is quite stable over the lifetime (Hewison et al. 2011) and provides a good proxy of individual quality (Toigo et al. 2006), with higher probability for heavy adult females to reach old age (Gaillard et al. 2000) and higher reproductive success among heavy males (Vanpé et al. 2010). To investigate condition-dependent dispersal, we quantified the effects of body mass and of the degree of habitat heterogeneity on dispersal initiation, propensity and our continuous dispersal distance metric. As dispersal is a costly process (Ronce 2007), heavier animals should be better able to cope with dispersal costs (Bowler & Benton 2005). From this, heavier than average roe deer should be more likely to disperse and should disperse earlier and further. Landscape heterogeneity is known to affect several aspects of roe deer ecology. In particular, deer in more open habitats have larger home ranges (Cargnelutti et al. 2002), higher diet quality (Abbas et al. 2011) and are thus heavier as adults (Hewison et al. 2009). Given this, we also expected landscape structure to exert an influence on dispersal propensity and distance in the studied population, with individuals from the more open areas more likely to disperse and to travel further. Based on previously published findings (Coulon et al. 2006; Gaillard et al. 2008), we expected no differences in dispersal patterns to occur between sexes.
- Top of page
- Materials and methods
Natal dispersal was observed in one-third of the juvenile roe deer and, in line with previous reports for this species, was not sex-biased. However, as expected, natal dispersal outcomes were dependent on both the phenotypic attributes of individuals (body mass) and environmental factors (habitat openness). Heavier individuals had a higher probability of dispersing and our IBSDD metric increased linearly with increasing body mass, with some support for a body mass threshold of 14 kg under which no dispersal occurred. The degree of habitat heterogeneity in the natal home range also influenced dispersal behaviour: individuals born in more open areas dispersed more and travelled further than individuals from closed habitats. Our study provides a rare example of multifactorial condition-dependent dispersal in a large herbivore and highlights the complexity of dispersal mechanisms, with several conditions or cues operating simultaneously to determine the dispersal decisions of individual animals (Clobert et al. 2009).
Dispersal rate and distance
Although dispersal rate is highly variable among roe deer populations, the rate of 33·9% that we observed in our study conforms to values previously reported (Wahlstrom & Liberg 1995; Gaillard et al. 2008). Compared to other large herbivores, this rate of dispersal is quite low for males, because 52% of juvenile white-tailed deer (Nixon et al. 2007) and 68·8% of male red deer (Loe et al. 2010) were reported to disperse. There are fewer studies of dispersal distances for large herbivores in general, although the estimate of 4·7 ± 8·4 km for our study site lies within the reported range for roe deer (1·1 ± 0·1 to 7·6 ± 3·0 km: Wahlstrom & Liberg 1995; Gaillard et al. 2008). The distribution of IBSDDs that we observed followed a classic leptokurtic or ‘tick-tailed’ distribution (Paradis et al. 1998), with relatively few individuals moving long distances and most moving shorter distances (Johnson & Gaines 1990; Bowler & Benton 2005; Ronce 2007), indicating a strong possibility for condition-dependent dispersal in our data set (see below). Indeed, leptokurtosis is thought to be driven by intrapopulation variation among individuals in dispersal tactic (Fraser et al. 2001) and by variation in habitat structure (Morales & Ellner 2002). This intrapopulation variation can be attributed to different ultimate causes, which may result in different optimal dispersal distances. For example, in white-tailed deer, longer dispersal distances seem necessary for avoiding inbreeding rather than mate competition (Long et al. 2008).
The date of dispersal initiation was highly synchronised among individuals, as previously reported in roe deer (Linnell, Wahlstrom & Gaillard 1998). There was clear evidence that heavier roe deer disperse earlier, a finding consistent with studies on male Belding's ground squirrels (Nunes & Holekamp 1996) and red foxes Vulpes vulpes (Gosselink et al. 2010). Early dispersal may be advantageous because early-dispersing individuals may have more time to locate, and/or may arrive first on, a vacant, high-quality home range. However, this relationship is unlikely to involve differences in maturation among juveniles. Indeed, births are highly synchronised in roe deer (Linnell, Wahlstrom & Gaillard 1998), with 80% occurring within 3 weeks, so that the impact of birth date on juvenile body mass at dispersal (10–12 months of age) is likely weak. While birth date influences both early growth and survival in roe deer (F. Plard et al., unpublished data), fawns that survive to their first winter seem able to compensate for a bad start because no relationship occurred between early growth and mass at 8–10 months of age (Gaillard, Delorme & Jullien 1993) in a population not markedly limited by food resources, as is the case in our study population.
Interestingly, we observed ‘pseudo-dispersal’ events in four males who left their natal range during the dispersal period, travelling a considerable distance (between 5·2 and 25 km), before returning several weeks later during summer to their natal range. Speculatively, we suggest that this potentially costly behaviour occurs when male juveniles are unable to locate a suitable vacant home range and so are forced to return to their natal range because of antagonistic social interactions with territorial adult males (Wahlstrom 1994). In roe deer, territoriality governs male–male interactions but not female–female or male–female ones (Hewison, Vincent & Reby 1998), and, indeed, we did not observe any similar pseudo-dispersal events among females in our population.
As expected, on average, male and female juvenile roe deer initiated dispersal events at approximately the same time, dispersed in similar proportions and travelled similar distances during the transience phase. This result is consistent with both genetic studies (in this same population: Coulon et al. 2006; see also Bonnot et al. 2011), but also with studies based on direct observations (Wahlstrom & Liberg 1995; Gaillard et al. 2008). The low sexual size dimorphism, the mating tactic of resource defence and the low level of polygyny of this species (Vanpé et al. 2008) may explain this absence of sex bias in roe deer dispersal (Gaillard et al. 2008). However, although dispersal outcomes are clearly similar in male and female roe deer, it is likely that the proximate mechanisms underlying dispersal decisions differ between the sexes. Indeed, Wahlstrom (1994) reported that the number of antagonistic interactions experienced by male yearling roe deer was positively correlated with antler size, and he suggested that these social interactions were the proximate cause of natal dispersal in juvenile males. As there is a strong allometric relationship linking antler length with body mass in this species (Vanpé et al. 2007), and in other deer (Plard, Bonenfant & Gaillard 2011), bigger juvenile males are predicted to suffer more male–male aggression, leading to the observed pattern of mass-dependent dispersal. However, this mechanism clearly does not hold for females who are not territorial (Hewison, Vincent & Reby 1998), hence, the cue for initiating dispersal of heavier juveniles (see below) likely differs between sexes.
Phenotypic condition-dependent dispersal: the role of body mass
Condition-dependent dispersal tactics should perform better than unconditional fixed tactics because they allow individuals to respond to variation in the costs and benefits of dispersal over the short term (Bowler & Benton 2005). We found that individual body mass played a crucial role in determining dispersal rate and distance, with heavier juveniles dispersing more frequently and travelling further and with some support for a body mass threshold under which roe deer juveniles cannot sustain the energetic costs of dispersal. Indeed, none of the eight roe deer weighing less than 14 kg dispersed. Similar results were found in Belding's ground squirrels (Holekamp 1986). However, this pattern contrasts with a study on red deer that reported no relationship between body mass and male dispersal propensity (Loe et al. 2010). Red deer and roe deer markedly differ in many life-history tactics. The red deer is a highly dimorphic and polygynous species (Clutton-Brock, Guinness & Albon 1982) and a grazer (Hofmann 1989); females are close to the capital end of the continuum of energy allocation to reproduction. In contrast, the roe deer is a weakly dimorphic species with a low level of polygyny (Vanpé et al. 2008) and a browser (Hofmann 1989); females are close to the income end of the continuum of energy allocation. It is thus not surprising that the pattern of natal dispersal also differs markedly between these two related species.
Dispersal is known to be a risky behaviour (Ronce 2007), and costs increase with increasing dispersal distance (Rousset & Gandon 2002; see Johnson et al. 2009 for a study case on American martens). Our study suggests that (i) there is a threshold of 14 kg minimum mass for an individual to be able to cope with the costs of dispersal, and (ii) the observed relationship between dispersal distance and body mass similarly suggests that only the heaviest juveniles are able to offset the costs of long-distance dispersal. The higher rate of movement necessary for dispersal could imply increased energetic expenditure. Indeed, we found evidence that dispersers moved greater distances per time unit during the dispersal event compared to the distances travelled over the same period of time by nondispersing individuals during their normal activities within their home range (N = 23, W = 34, P = 0·051). Evidently, for dispersal to evolve, it must also generate some benefits that, over the long term, compensate these costs. For example, more female dispersers attained dominant status than their philopatric counterparts in red fox V. vulpes (Soulsbury et al. 2008). While we are unable to conclude on the nature of the benefits obtained by dispersing roe deer in our study, we speculate that inbreeding avoidance is an important consideration in view of the lifelong sedentary nature of adult roe deer and the social system based on small family units (Hewison, Vincent & Reby 1998), which likely leads to substantial opportunity for inbred matings. Furthermore, Vanpé et al. (2009b) showed that roe deer fawns born from closely related parents survived less well over their first summer than those with unrelated parents. In general, the dispersal distance necessary to avoid kin competition or inbreeding is much longer and requires greater movement ability than that required to escape competition with nonrelatives (Ronce 2007; Long et al. 2008 in white-tailed deer).
In our population, not all heavy animals dispersed, suggesting that there was a choice available to disperse or not and that several factors were involved in that choice. Competitive ability may influence whether an individual disperses or not (Ims & Hjermann 2001). In this context, two contrasting hypotheses were proposed by Bowler & Benton (2005): first, heavier animals are more competitive than lighter ones, hence lighter animals are forced to disperse to avoid competition with heavy, more competitive individuals; alternatively, larger individuals may be more prone to disperse if they are more capable of immigrating into a new competitive patch successfully or if dispersal requires a certain amount of energy reserves. Roe deer seems to fit better with this latter scenario. For example, we have previously shown that only particularly heavy roe deer bucks are able to establish their first territory at 2 years of age (Vanpé et al. 2009a), and we speculatively suggest that high body mass may also be important in primiparous females for the acquisition of a high-quality fawning range. Moreover, as inbreeding has a cost in terms of fawn survival in roe deer (Vanpé et al. 2009b), dispersal could allow heavier individuals to increase their offspring survival.
Environmental condition-dependent dispersal: the impact of habitat heterogeneity
In our study, individuals inhabiting more open habitats dispersed more frequently and further than individuals living in more forested habitats. In open habitats, individual phenotypic quality, as indexed by body mass, is generally higher (Hewison et al. 2009); however, individuals in more open habitats dispersed more irrespective of body mass. This suggests that the degree of habitat heterogeneity could markedly impact dispersal propensity in this large herbivore. This pattern of habitat-dependent dispersal distance may be a general feature of heterogeneous landscapes, as mean dispersal distance of nuthatches was several times greater in a highly heterogeneous landscape compared to more densely forested landscapes (Matthysen, Adriaensen & Dhondt 1995), while dispersal distances of juvenile male white-tailed deer were greater in habitats with less forest cover (Long et al. 2005).
Implications of condition-dependent dispersal
Our results provide compelling empirical evidence for condition-dependent dispersal in a large herbivore, indicating that high phenotypic quality is a critical prerequisite to disperse successfully. Dispersing individuals are thus not a random subset of the population. We showed that dispersers are heavier than philopatric individuals, suggesting that immigrants to a given area may be more competitive than the philopatric individuals already present. Condition-dependent dispersal can have profound consequences for population and metapopulation dynamics (Clobert et al. 2001; Bonte & de la Pena 2009). For example, a change in average body condition can alter connectivity between populations and consequent gene flow (Bohonak 1999). In a simulation study, Bonte & de la Pena (2009) suggested that body condition-dependent dispersal tactics affect population dynamics and induce evolutionary rescue mechanisms in spatially structured populations. In particular, when dispersal is modelled as a condition-dependent tactic, local metapopulation extinction rates are always close to zero (Bonte & de la Pena 2009). A better understanding of the mechanisms involved in natal dispersal, such as condition dependence, will thus help us to understand the evolution of this behaviour, as well as providing a basis for better prediction of metapopulation functioning.