Uneven Large-Scale Movement Patterns in Wild and Reintroduced Pre-Adult Bearded Vultures: Conservation Implications

After the quasi-extinction of much of the European vertebrate megafauna during the last few centuries, many reintroduction projects seek to restore decimated populations. However, the future of numerous species depends on the management scenarios of metapopulations where the flow of individuals can be critical to ensure their viability. This is the case of the bearded vulture Gypaetus barbatus, an Old World, large body-sized and long-lived scavenger living in mountain ranges. Although persecution in Western Europe restrained it to the Pyrenees, the species is nowadays present in other mountains thanks to reintroduction projects. We examined the movement patterns of pre-adult non-breeding individuals born in the wild population of the Pyrenees (n = 9) and in the reintroduced populations of the Alps (n = 24) and Andalusia (n = 13). Most birds were equipped with GPS-GSM radio transmitters, which allowed accurate determination of individual dispersal patterns. Two estimators were considered: i) step length (i.e., the distance travelled per day by each individual, calculated considering only successive days); and ii) total dispersal distance (i.e., the distance travelled between each mean daily location and the point of release). Both dispersal estimators showed a positive relationship with age but were also highly dependent on the source population, birds in Andalusia and Alps moving farther than in Pyrenees. Future research should confirm if differences in dispersal distances are the rule, in which case the dynamics of future populations would be strongly influenced. In summary, our findings highlight that inter-population differences can affect the flow of individuals among patches (a key aspect to ensure the viability of the European metapopulation of the endangered bearded vulture), and thus should be taken into account when planning reintroduction programs. This result also raises questions about whether similar scenarios may occur in other restoration projects of European megafauna.     

Direct fitness benefits of group living in a complex cooperative society of carrion crows, Corvus corone corone

The social behaviour of carrion crows varies between populations. In northern Spain cooperatively breeding groups form through delayed natal dispersal and/or immigration of individuals (usually males) into the territory. In this population, carrion crows therefore breed as either unassisted pairs, pairs with nondispersing 1-2-year-old helpers (nondispersers), pairs with immigrant helpers or mixed groups (pairs with both immigrants and nondispersers). We used a microsatellite-based genotyping system to determine the parentage of 57 nestlings (19 broods). Polygamous mating was involved in 26% of the broods and reproduction was shared among group members of both sexes in at least three groups. Immigrants of both sexes can therefore gain access to mates by living in a group, while reproduction is unlikely to involve nondispersers. This implies that nondispersers and immigrants gain different sorts of benefits from group living and helping at the nest. Our genetic data confirmed that nondispersers associated with their parents on the natal territory and therefore that delayed natal dispersal leads to family formation in the carrion crow. Polygamous mating was not found in groups without immigrants, suggesting that, in this population, breeders lose parentage in their brood when sociality is extended beyond the limit of the nuclear family.Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

Evidence of repertoire sharing and stability despite a high turnover rate in a duetting neotropical wren

In songbirds, the spatial pattern of song sharing among individuals is influenced by the song learning and dispersal strategies within each species. In birds where females and males sing and create joint acoustic displays (duets), the processes defining the patterns of song sharing become more complex as there might be different selection pressures shaping the behaviour of each sex. To provide further insight into the vocal development and the dispersal strategy of duetting tropical species, we investigated the patterns of individual and pair repertoire sharing, as well as the stability of these repertoires, in a colour-marked population of riverside wrens, Cantorchilus semibadius, located in the Osa Peninsula, Costa Rica. Using data collected over a five-year period, we found considerable variation in the sharing levels of phrase and duet type repertoires among neighbouring individuals coupled with a general decline of repertoire sharing as distance increased between birds’ territories. These results are consistent with a pattern predicted in age-restricted learners that establish preferentially near their tutors. Furthermore, we found no evidence of individuals changing their phrase type repertoires over time, including after remating events. Duet type repertoires were also stable when pairs remained together. However, we observed a surprisingly high turnover rate. When individuals remated, even though the majority of the previous duet type repertoire remained, several new duet types were included. Taken together, our findings suggest that riverside wrens might create their individual repertoires by copying their same-sex parent and neighbouring individuals before dispersal. Additionally, we speculate that even though birds were able to create new duet types after changing partners, a substantial portion of their duet type repertoire might also be copied from their parents and neighbouring pairs during the initial critical period of song learning.     

East-west divergence in central Brazilian Cerrado revealed by cpDNA sequences of a bird-dispersed tree species

Population genetic studies of plant species can contribute to understanding the evolutionary history of the Brazilian Cerrado, a highly threatened hotspot and the richest tropical savanna in the world. Therefore, this study aimed at investigating the diversity and genetic structure of Byrsonima coccolobifolia (Malpighiaceae), one of the most common tree species in the Brazilian Cerrado, focusing mainly on the central area of the biome. This is a bird-dispersed species, and studies targeting species with this seed dispersal syndrome are scarce. First, we performed a careful screening of cpDNA markers to identify regions suitable for intraspecific genetic studies, and then we investigated the diversity and genetic structure in ten populations of B. coccolobifolia. The cpDNA regions selected (trnS-trnG and trnH-trnK) revealed considerable divergence among populations and a striking geographical structure, separating populations in two groups, east and west. Although seed dispersal by birds is expected to reach long distances, our results strongly corroborate studies targeting trees with limited seed dispersal. This suggests that historical fragmentation of Cerrado (possibly during cold and dry periods of the Quaternary) might have limited long distance dispersal events after climate amelioration even in bird-dispersed species, especially while Cerrado was expanding but still fragmented.     

Deep phylogeographic break among Octopus variabilis populations in China: Evidence from mitochondrial and nuclear DNA analyses

The genetic structure of marine populations is greatly influenced by the dispersal ability of the organisms, and it is intuitive that a limited dispersal capability would result in greater genetic differentiation. Octopus variabilis is a typical cephalopod species that shows limited dispersal potential, and previous genetic surveys by a mitochondrial DNA analyses revealed high levels of genetic differentiation among its populations, suggesting the existence of cryptic or subspecies. To test this hypothesis, amplified fragment length polymorphisms (AFLPs) and the cytochrome oxidase II (COII) gene sequence were used to re-evaluate the spatial genetic structure of five populations of O. variabilis along the coast of China. Four distinct groups were identified within these five populations: the Dalian + Qingdao, Zhoushan, Wenzhou, and Dongshan groups. A deep genetic break among the Dongshan, Wenzhou, and other two groups were specifically recognized by both genetic markers. A considerable number of distinct alleles for AFLP and a deep divergence of 13.9–19.4% in the COII gene sequences were found among them, suggesting the occurrence of potential cryptic or subspecies of O. variabilis. A genetic structure of isolation by distance was identified in O. variabilis by a Mantel test, with the geographic distance explaining 62% of the variation in genetic differentiation. This result suggests that gene flow is geographically restricted for this species and that limited dispersal may be the main reason for the genetic differentiation among O. variabilis populations. The present results indicate that special care should be taken in future fishery exploitation and conservation efforts for this species and that conservation management should include populations representing all lineages.     

No evidence for female kin association,indications for extragroup paternity,and sex‐biased dispersal patterns in wild western gorillas

Characterizing animal dispersal patterns and the rational behind individuals’ transfer choices is a long‐standing question of interest in evolutionary biology. In wild western gorillas (Gorilla gorilla), a one‐male polygynous species, previous genetic findings suggested that, when dispersing, females might favor groups with female kin to promote cooperation, resulting in higher‐than‐expected within‐group female relatedness. The extent of male dispersal remains unclear with studies showing conflicting results. To investigate male and female dispersal patterns and extragroup paternity, we analyzed long‐term field observations, including female spatial proximity data, together with genetic data (10 autosomal microsatellites) on individuals from a unique set of four habituated western gorilla groups, and four additional extragroup males (49 individuals in total). The majority of offspring (25 of 27) were sired by the group male. For two offspring, evidence for extragroup paternity was found. Contrarily to previous findings, adult females were not significantly more related within groups than across groups. Consistently, adult female relatedness within groups did not correlate with their spatial proximity inferred from behavioral data. Adult females were similarly related to adult males from their group than from other groups. Using R _ST statistics, we found significant genetic structure and a pattern of isolation by distance, indicating limited dispersal in this species. Comparing relatedness among females and among males revealed that males disperse farer than females, as expected in a polygamous species. Our study on habituated western gorillas shed light on the dispersal dynamics and reproductive behavior of this polygynous species and challenge some of the previous results based on unhabituated groups.     

The mating system of the White-throated Magpie-jay Calocitta formosa and Greenwood's hypothesis for sex-biased dispersal

Greenwood explained the different sex bias in dispersal of birds (usually female biased) and mammals (usually male biased) by a difference in mating systems: male birds primarily defend resources while male mammals primarily defend females. The White-throated Magpie-jay Calocitta formosa is unusual among birds in that females are philopatric and jointly defend permanent resource territories while males disperse before they are 2 years of age. One female in a group is the primary breeder. One male joins the group permanently as her mate. Males that do not have a permanent breeding position circulate among groups and attempt to mate with both the primary breeding female and other group females. Other females feed the primary breeder and her offspring and also pursue other reproductive behaviour, including secondary nesting in the territory and egg dumping into the primary breeder's nest. I argue that the unusual dispersal pattern in this species is a result of the alternative reproductive strategies that can be pursued by males and females excluded from being primary breeders. The White-throated Magpie-jay conforms to Greenwood's predictions: males pursue a mate defence rather than resource defence mating system and they are the dispersing sex. The primary factor influencing alternative reproductive tactics may be asynchronous reproduction among groups during the long breeding season arising from frequent renesting in an area of high nest predation.     

Social foragers adopt a riskier foraging mode in the centre of their groups

Foraging in groups provides many benefits that are not necessarily experienced the same way by all individuals. I explore the possibility that foraging mode, the way individuals exploit resources, varies as a function of spatial position in the group, reflecting commonly occurring spatial differences in predation risk. I show that semipalmated sandpipers (Calidris pusilla), a social foraging avian species, tended to adopt a riskier foraging mode in the central, more protected areas of their groups. Central birds effectively used the more peripheral group members as sentinels, allowing them to exploit a wider range of resources within the same group at the same time. This finding provides a novel benefit of living in groups, which may have a broad relevance given that social foraging species often exploit a large array of resources.     

Dispersal,Mating Events and Fine-Scale Genetic Structure in the Lesser Flat-Headed Bats

Population genetic structure has important consequences in evolutionary processes and conservation genetics in animals. Fine-scale population genetic structure depends on the pattern of landscape, the permanent movement of individuals, and the dispersal of their genes during temporary mating events. The lesser flat-headed bat (Tylonycteris pachypus) is a nonmigratory Asian bat species that roosts in small groups within the internodes of bamboo stems and the habitats are fragmented. Our previous parentage analyses revealed considerable extra-group mating in this species. To assess the spatial limits and sex-biased nature of gene flow in the same population, we used 20 microsatellite loci and mtDNA sequencing of the ND2 gene to quantify genetic structure among 54 groups of adult flat-headed bats, at nine localities in South China. AMOVA and F _ST estimates revealed significant genetic differentiation among localities. Alternatively, the pairwise F _ST values among roosting groups appeared to be related to the incidence of associated extra-group breeding, suggesting the impact of mating events on fine-scale genetic structure. Global spatial autocorrelation analyses showed positive genetic correlation for up to 3 km, indicating the role of fragmented habitat and the specialized social organization as a barrier in the movement of individuals among bamboo forests. The male-biased dispersal pattern resulted in weaker spatial genetic structure between localities among males than among females, and fine-scale analyses supported that relatedness levels within internodes were higher among females than among males. Finally, only females were more related to their same sex roost mates than to individuals from neighbouring roosts, suggestive of natal philopatry in females.     

Implications of movement patterns of a dietary generalist for mistletoe seed dispersal

Mistletoes are dispersed primarily by frugivorous birds and have highly aggregated distributions at multiple scales. Mistletoe specialist frugivores have been found to intensify infections within infected hosts and stands, and this is considered the most likely mechanism underlying clumped mistletoe distributions at these scales. How these patchy infections first develop and whether seed dispersers also contribute to aggregated mistletoe distributions at landscape and regional scales have not been evaluated. Here we predict the mistletoe seed shadow of a dietary generalist (spiny‐cheeked honeyeater Acanthagenys rufogularis Aves: Meliphagidae), by combining our observations of movements via radio telemetry with previous data on gut passage times to estimate seed dispersal curves for individual birds. There was considerable variation in movements and inferred seed dispersal between individuals, with non‐breeding birds predicted to regularly transport Amyema quandang (Santalales: Loranthaceae) seeds up to 700 m; well beyond the boundaries of an existing mistletoe infection. As the first work to consider explicitly the distance component of mistletoe seed dispersal by dietary generalists, this study poses further questions about the relative seed dispersal roles of dietary generalists and mistletoe specialists. Moreover, our findings highlight considerable intraspecific variation in movement and foraging behaviour, suggesting gender and reproductive status of birds should be considered explicitly when quantifying seed dispersal services.     

Fatal Attack on an Adult Female Cercopithecus mitis erythrarchus: Implications for Female Dispersal in Female-Bonded Societies

Female dispersal is uncommon among female-bonded primate societies, even though at times there may be considerable incentive to do so, e.g., to avoid potentially infanticidal males. Predation risk and the advantages of sharing the costs of group living, such as infanticide and resource defense, with close kin are assumed to limit female dispersal. However, we show that these costs may not be as important as the risks associated with integration into a new group in female-bonded societies. We report the death of a potentially dispersing solitary Samango (Cercopithecus mitis erythrarchus). She was unrelated to the females of a single group that killed her, and her death was not in the context of intergroup conflict or territorial defense. This fatal conflict is in contrast to the tolerance of female dispersal displayed by many folivorous and non-female-bonded primate species. In such non-female-bonded societies, there is less indirect fitness advantage to remaining in the natal group or to cooperate with kin to defend food patches, and consequently the risk of being rejected by another group is much reduced. Our observations show that dispersal between groups may be costly for solitary and unfamiliar females in a female-bonded society.     

The spatial distribution of avian relatives: do obligate army‐ant‐following birds roost and feed near family members?

The ocellated antbird ( Phaenostictus mcleannani ) feeds in groups and therefore is an informative species in which to study the biological factors that modulate avian group living. These birds congregate at swarms of army ants to capture fleeing prey, and previous observations suggest that males may be philopatric, feed with close relatives, and defend communal feeding ranges. We assessed whether kin selection could be an important factor maintaining group formation in a population of ocellated antbirds inhabiting continuous forest at La Selva Biological Station, Costa Rica, using radiotelemetry and 15 novel microsatellite markers. We predicted that the roosting areas of closely related adult males should overlap and that adult males feeding simultaneously at the same swarm should be highly related. We banded and genotyped 65 individuals (≥ 88% of the population) and radiotagged 30 of them. The results generally did not conform to our predictions. Little overlap occurred among the roosting areas of same-sex individuals, and nearest roosting neighbours (either same or opposite sex) were generally unrelated. A small proportion of male dyads suggested short-distance dispersal, but in general the distribution of genotypes within the study area approached randomness. We found little evidence of natal philopatry in either sex. Less than half of the feeding groups sampled included highly related males; most consisted of unrelated individuals. Hence, we found limited potential for kin selection to favour group living and suggest that other factors, particularly direct benefits (e.g. food intake), are probably more important than indirect effects (nepotism).     

Dispersal Patterns in <Emphasis Type="Italic">Tarsius spectrum</Emphasis>

One of the most widely accepted explanations for the difference in the sex bias between mammals and birds is that male-biased dispersal in mammals is due to the preponderance of polygynous mating systems exhibited by this class, whereas birds are predominantly monogamous. Spectral tarsiers (Tarsius spectrum) are unusual in that they exhibit variation in its mating system. Although the majority of spectral tarsier groups are monogamous, ca. 15% are polygynous. If mating system influences dispersal, then I predicted that the polygynous groups would exhibit male biased dispersal whereas I predicted that the dispersal patterns of the monogamous groups would be analogous to that exhibited by birds, specifically female biased. Alternatively, I hypothesized that ecological variation may influence dispersal habits in this species. Specifically, I predicted that polygynous groups would exhibit greater habitat quality than monogamous groups. The 2 hypotheses are not mutually exclusive. On the basis of 14 individuals birdbanded between 1994 and 1999, I determined that individuals of both sexes were equally likely to disperse (males, n = 5; females, n = 9). Males dispersed twice as far as females did. The mean dispersal distance for males was 660 m, and for females it was 266 m. Females (77%) were more likely to form a territory adjacent to the parental territory than were males (20%). Individuals exhibited relatively high amounts of site fidelity (86%) that were related to physical characteristics of the sleeping site. Adults that dispersed a second time (n = 4) initially resided in trees that were shorter and had a smaller diameter-at-breast height than the trees of individuals that exhibited site fidelity. The results of my study partly support the parental mating system hypothesis and also support the habitat quality hypothesis.     

Population genetic structure of the tree-hole tick Ixodes arboricola (Acari: Ixodidae) at different spatial scales

The endophilic tick Ixodes arboricola infests cavity-nesting birds, and its dispersal strongly depends on the movements of its host. Population genetic structure of I. arboricola was studied with seven polymorphic microsatellite markers. We collected 268 ticks from 76 nest boxes in four woodlots near Antwerp, Belgium. These nest boxes are mainly used by the principal hosts of I. arboricola, the great tit Parus major and the blue tit Cyanistes caeruleus. As these birds typically return to the same cavity for roosting or breeding, ticks within nest boxes were expected to be highly related, and tick populations were expected to be spatially structured among woodlots and among nest boxes within woodlots. In line with the expectations, genetic population structure was found among woodlots and among nest boxes within woodlots. Surprisingly, there was considerable genetic variation among ticks within nest boxes. This could be explained by continuous gene flow from ticks from nearby tree holes, yet this remains to be tested. A pairwise relatedness analysis conducted for all pairs of ticks within nest boxes showed that relatedness among larvae was much higher than among later instars, which suggests that larvae are the most important instar for tick dispersal. Overall, tick populations at the studied spatial scale are not as differentiated as predicted, which may influence the scale at which host–parasite evolution occurs.     

Effects of zoochory on the spatial genetic structure of plant populations

Spatial genetic structure (SGS) of plants results from the nonrandom distribution of related individuals. SGS provides information on gene flow and spatial patterns of genetic diversity within populations. Seed dispersal creates the spatial template for plant distribution. Thus, in zoochorous plants, dispersal mode and disperser behaviour might have a strong impact on SGS. However, many studies only report the taxonomic group of seed dispersers, without further details. The recent increase in studies on SGS provides the opportunity to review findings and test for the influence of dispersal mode, taxonomic affiliation of dispersers and their behaviour. We compared the proportions of studies with SGS among groups and tested for differences in strength of SGS using Sp statistics. The presence of SGS differed among taxonomic groups, with reduced presence in plants dispersed by birds. Strength of SGS was instead significantly influenced by the behaviour of seed dispersal vectors, with higher SGS in plant species dispersed by animals with behavioural traits that result in short seed dispersal distances. We observed high variance in the strength of SGS in plants dispersed by animals that actively or passively accumulate seeds. Additionally, we found SGS was also affected by pollination and marker type used. Our study highlights the importance of vector behaviour on SGS even in the presence of variance created by other factors. Thus, more detailed information on the behaviour of seed dispersers would contribute to better understand which factors shape the spatial scale of gene flow in animal‐dispersed plant species.     

Family living among birds

Family cohesion in birds is often explained as a product of limitations on breeding opportunities leading to delayed dispersal among the offspring. Yet, it is not independent reproduction but floating (queuing outside the natal territory for a breeding opportunity) that is the alternative to delaying dispersal. In contrast to a strong phylogenetic bias in cooperative breeding that has been taken to indicate a hard-wired behaviour maintained by evolutionary inertia, offspring behaviour is plastic and facultative in group living in the short term, indicating that family cohesion is under selection. Non-breeding offspring could gain inclusive fitness that would promote family cohesion from delaying dispersal and providing alloparental care to subsequent broods to boost group productivity. This holds in particular for offspring hatched from early broods in multi-brooded species that have the opportunity to gain inclusive fitness from help in rearing siblings hatched from later broods in the same season. Yet, seasonality will circumscribe the potential for alloparenting to be the immediate factor selecting for family cohesion. The option of gaining inclusive fitness from providing alloparental care is not open to the offspring among single-brooded species until after they have survived a non-breeding season, rather indicating kin cooperation returning enhanced survival prospects from general group living effects as a more immediate factor selecting for family cohesion. Indeed, a variety of family groups maintained in the absence of alloparental care underlines the capacity of general group living enhancing survival as a primary agent selecting for family cohesion. These seasonal constraints on fitness components selecting for family cohesion may contribute to the large scale geographical pattern with a relative paucity of family cohesions among bird species in the northern hemisphere.     

Evidence for female-biased dispersal in the protandrous hermaphroditic Asian Seabass, Lates calcarifer

Movement of individuals influences individual reproductive success, fitness, genetic diversity and relationships among individuals within populations and gene exchange among populations. Competition between males or females for mating opportunities and/or local resources predicts a female bias in taxa with monogamous mating systems and a male-biased dispersal in polygynous species. In birds and mammals, the patterns of dispersal between sexes are well explored, while dispersal patterns in protandrous hermaphroditic fish species have not been studied. We collected 549 adult individuals of Asian seabass (Lates calcarifer) from four locations in the South China Sea. To assess the difference in patterns of dispersal between sexes, we genotyped all individuals with 18 microsatellites. Significant genetic differentiation was detected among and within sampling locations. The parameters of population structure (F(ST)), relatedness (r) and the mean assignment index (mAIC), in combination with data on tagging-recapture, supplied strong evidences for female-biased dispersal in the Asian seabass. This result contradicts our initial hypothesis of no sex difference in dispersal. We suggest that inbreeding avoidance of females, female mate choice under the condition of low mate competition among males, and male resource competition create a female-biased dispersal. The bigger body size of females may be a cause of the female-biased movement. Studies of dispersal using data from DNA markers and tagging-recapture in hermaphroditic fish species could enhance our understanding of patterns of dispersal in fish.     

Fine-scale genetic structure and dispersal in cooperatively breeding apostlebirds

In cooperatively breeding species, restricted dispersal of offspring leads to clustering of closely related individuals, increasing the potential both for indirect genetic benefits and inbreeding costs. In apostlebirds (Struthidea cinerea), philopatry by both sexes results in the formation of large (up to 17 birds), predominantly sedentary breeding groups that remain stable throughout the year. We examined patterns of relatedness and fine-scale genetic structure within a population of apostlebirds using six polymorphic microsatellite loci. We found evidence of fine-scale genetic structure within the study population that is consistent with behavioural observations of short-distance dispersal, natal philopatry by both sexes and restricted movement of breeding groups between seasons. Global F(ST) values among breeding groups were significantly positive, and the average level of pairwise relatedness was significantly higher for individuals within groups than between groups. For individuals from different breeding groups, geographical distance was negatively correlated with pairwise relatedness and positively correlated with pairwise F(ST). However, when each sex was examined separately, this pattern was significant only among males, suggesting that females may disperse over longer distances. We discuss the potential for kin selection to influence the evolution and maintenance of cooperative breeding in apostlebirds. Our results demonstrate that spatial genetic structural analysis offers a useful alternative to field observations in examining dispersal patterns of cooperative breeders.     

Are dispersal and inbreeding avoidance related?

Sex differences in dispersal and inter-group transfer by birds and mammals are often considered to be evolved responses to the phenomenon of inbreeding depression. This belief is derived from ‘natural selection logic’, which holds that (1) because inbreeding depression is demonstrably costly, selection must have acted to minimize its occurrence, and (2) as sex differences in dispersal often appear to be the only thing preventing inbreeding, these sex differences must be the expected adaptations for avoiding inbreeding depression. However, although the sex differences in median dispersal distance observed among many small mammals and birds may reduce average levels of inbreeding within a population, they nevertheless leave the majority of individuals ‘at risk’ for inbreeding; such differences can be responses to inbreeding depression only in a group selection model. Furthermore, natal dispersal by both sexes occurs in many group-living species. In these species, emigration by individuals of one sex cannot easily be attributed to avoiding inbreeding because opposite-sex relatives also emigrate. Though most authors acknowledge that sexual dispersal patterns may be epiphenomenal consequences of other factors (e.g. intrasexual aggression), this point is rarely considered further. In this paper we critically review several frequently cited examples of differential dispersal, and conclude that ‘other factors’, such as intrasexual competition and territory choice, explain these observations more completely and consistently than does the inbreeding avoidance hypothesis. Observed dispersal patterns simply reflect sex differences in the balance between the advantages of philopatry and the costs of intrasexual competition.