1.4. The geese
The geese, subfamily Anserinae, tribe Anserini, are divided into two genera, ‘the grey geese’ Anser (10 species) and ‘the black geese’ Branta (five species). Earlier, the geese were divided into five genera: Anser, Philacte, Chen (present genus Anser), Branta and Nesochen (present genus Branta), and these old taxonomic affiliations are still used by some authors (Miller 1937, Delacour 1954, Bellrose 1980, Quinn et al. 1991). Goose species are considered relatively young, a notion that is supported by molecular genetic studies. The divergence time of genera Anser and Branta has been estimated to 5 My based on fossil data (Shields & Wilson 1987).
The geese are largely holarctic in their distribution and all species are highly migratory, with the exception of the endemic Hawaiian goose (Branta sandvicensis). The breeding areas are typically in the tundra and taiga, and for most species in the arctic or in high altitudes, as the bar-headed goose (Anser indicus). The only goose species having a strong association with the sea is the brent goose (Branta bernicla) which breeds mainly on small islands and winters in coastal areas.
Geese breed for the first time at the age of 2-3 years, and pair bonds are considered to be monogamous and long-term (Cramp & Simmons 1977). As in general for arctic species the incubation and fledging times are short due to a short favourable breeding season. Goose species breeding in high latitudes, e.g. the lesser white-fronted goose (Anser erythropus) and the brent goose, do not lay replacement clutches. Mainly due to unfavourable weather conditions and high numbers of native or introduced predators (mainly the arctic fox Alopex lagopus and, nowadays to a greater extent in Fennoscandia, the red fox Vulpes vulpes) there is a large variance in the yearly number of offspring produced.
Most non-breeding geese perform moult migrations at locations generally north of breeding areas. The evolution of moult migrations has been explained by the possibility of gaining access to easily digestible high-protein food resources provided by the early growth of grasses and sedges starting later in more northern areas to compensate for energy-loss during feather replacement and to avoid food competition with family groups (Salomonsen 1968, Owen & Ogilvie 1979). These moult flights can be extreme and sometimes involve crossing an open sea, as in bean geese (Anser fabalis) which moult largely on the Siberian archipelago (Ogilvie 1978, Alerstam 1990) or in the pink-footed goose which migrate from Iceland to Greenland (Christensen 1967). Breeding individuals remain with their mates and families and moult near the breeding areas where the moult of the parents is synchronised with the fledgling of their offspring (Cramp & Simmons 1977). The juveniles stay with parents at least through the first autumn and winter, but in some species juveniles may remain through to the following breeding season (Fox et al. 1995).
The culturally transmitted migratory flyways of the geese lead to the wintering areas through traditional stopover sites. Earlier, it was assumed that the breeding groups of the geese remained largely isolated from other breeding groups also during the nonbreeding season (Cramp & Simmons 1977). This was recently contradicted by ring-recovery data on the European white-fronted goose (Anser albifrons albifrons) indicating that the birds breeding in Taimyr Peninsula migrated as a wide front and were distributed over several wintering sites (Mooij 1996). However, it has been shown in the Pacific white-fronted goose (Anser albifrons frontalis) that while the spatially segregated breeding groups use the same staging areas, the groups still are temporally segregated (Ely & Takekawa 1996).
Geese generally overwinter in lowlands, farmlands and marshes. Recently, many goose species have shifted from natural habitats to using agricultural land for feeding in Western Europe in winter. As during the breeding season, weather plays an important role during winter. If the weather is harsh the geese move southwards to winter. Goose species are gregarious during the non-breeding season and families usually remain together throughout the winter (Cramp & Simmons 1977).
The spring migration routes of geese are not necessarily the same as in autumn. To maximise the chances for successful reproduction during the breeding season, the geese should arrive at the breeding grounds in good condition and with optimal timing to be able to use the short favourable season effectively. Therefore, good-quality wintering and staging areas along the migratory route are of utmost importance in augmenting body reserves prior to the onset of nesting (Ebbinge et al. 1982, Johnson & Herter 1990).
1.4.1. Life-histories and genetic consequences
The genetic structuring of geese populations are shaped by life-history and behavioural characteristics. The amount of inter-population movement defining the amount of gene flow and ultimately population structuring is an interplay of factors such as the degree of natal and breeding philopatry, winter philopatry, timing of pair-formation, pair-bond stability, assortative mating and gregarious behaviour.
The hypothesis proposed to explain the evolution of philopatric behaviour is related to the selective advantage of being familiar with an area and maintaining social bonds with conspecifics leading to a higher reproductive success as compared to dispersing individuals (ecological mechanisms) and mating with partners with which they share a specific level of genetic relatedness to gain optimal outbreeding and at the same time optimal inbreeding (genetic mechanisms) (Greenwood 1980, Weatherhead & Forbes 1994). Compared to most other bird species, geese show female-biased natal and breeding fidelity (Greenwood 1980). In the Canada goose (Branta canadensis) up to 79% of females returned to their natal site to breed, whereas 63% of the males were observed to breed outside their hatching site (Lessells 1985). None of the individuals exhibited breeding dispersal in subsequent years. However, the study was conducted with introduced mainly non-migratory Canada geese in Britain, and therefore the results may not apply to migratory geese. In breeding populations of the lesser snow goose (Anser caerulescens caerulescens) banding results clearly showed that female geese frequently returned to the natal colony to breed, whereas males seldom did (Cooke et al. 1975). Because a large proportion of the 2nd calendar year males were still seen in their natal colony during the breeding season but considerably fewer 3rd calendar year or older males were observed, the disappearance of the males may well be related to pair-formation and consequent emigration to the female’s natal colony. However, despite of female philopatry suggested by ringing data, a low level of genetic structuring in mtDNA among the breeding populations of the snow goose has been shown (Avise et al. 1992, Quinn 1992).
Winter philopatry, on the other hand, is considered male-biased in geese. The return rates (proportion of banded individuals returning to a wintering area in subsequent years) estimated for goose species have ranged from 50% in the brent goose to 85% in the white-fronted goose (Robertson & Cooke 1999 and references therein). However, as mentioned earlier, geese can use more than one area during one winter depending on the weather conditions and there are few data on the maintenance of flock integrity throughout the winter.
Timing of pair formation in migratory geese is essential in determining the amount of gene flow between breeding locations. Some studies have shown that pairing in mid-winter is not a rule in geese, as often has been assumed for waterfowl in general. In the lesser snow goose and the brent goose pair formation occurs in winter or spring, whereas in the emperor (Anser canagicus), white-fronted and the Canada goose pair formation occurs during spring migration or in summer (reviewed in Ely & Scribner 1994). If the pairs are formed on the wintering grounds where mixing of individuals breeding in different localities takes place and if a non-assortative pairing is assumed, a chance to pair with an individual from a non-natal group exists. If pair-formation occurs during the spring migration or on the breeding grounds when the individuals are already at least partially segregated, the magnitude of gene flow between breeding groups depends mainly on the degree of natal philopatry. On the other hand, if the species exhibit winter philopatry and flock integrity is maintained, the amount of gene flow can be restricted even if pair-formation takes place on the wintering grounds. Additionally, at least in the snow goose an assortative mating between the two colour-phases is known to take place (Cooke et al. 1972, Cooke & McNally 1975).
The life-history characteristics described above have different consequences for the amount of genetic differentiation observed in biparentally versus uniparentally inherited genetic markers. In avian species the female is the heterogametic sex (ZW) so that both the W sex chromosome and mtDNA are maternally inherited. The autosomal chromosomes and the Z chromosome are inherited through both parents and paternally inherited markers, such as mammalian Y chromosome, do not exist. In Fig. 2 the effect of these characters is depicted in terms of genetic structuring.
Figure 2. The effect of some life-history characteristics to the genetic structuring of the goose populations in maternally inherited mitochondrial DNA and W chromosome, and in biparentally inherited nuclear autosomal genes. In all the cases, the assumption is that the females show natal philopatry and the males wintering philopatry. In c) the degree of differentiation in nuclear genes depends on the degree of male natal philopatry. If assortative mating is involved, genetic structuring in both maternally and biparentally inherited markers may take place in a) trough c). Circle, a female; square, a male; solid line, female movements; dotted line, male movements.
1.4.2. Geese and conservation cases
During the past century, almost all goose species have faced threats leading to declining population trends. A common denominator for most cases showing a declining population trend is excessive hunting or a combination of hunting and other factors, such as habitat destruction and agricultural conflicts mainly at stopover sites and wintering grounds, and disturbance and predation especially on the breeding grounds. As with any migratory species, geese are constrained by factors at breeding, staging and wintering areas, all of which may have a different set of adaptive requirements. Also, some goose species show very narrow and specialised habitat requirements. For example, the population decline of the brent goose (Branta bernicla bernicla) in the 1930s was at least partially related to reduced abundance of the main food plant eelgrass Zostera marina in the wintering areas (Atkinson-Willes & Matthews 1960). Generally, geese are considered to have a good ability to adapt and have responded by e.g. changes in culturally transmitted migratory behaviour, shifts in distributional areas, use of agricultural land for feeding and the avoidance of predation by specialised nesting places.
One of the most famous examples of a conservation programme in geese is the endemic Hawaiian goose, which underwent a severe population bottleneck at the beginning of the last century due to habitat loss, introduced predators and over-hunting. By 1950 only 30 individuals of the estimated original 25 000 birds were left, and a captive propagation program was established (Kear & Berger 1980). By 1992 more than 2000 captive birds were released, but the population numbers are still today dependent on the number of birds released (Black et al. 1991). Because the captive stocks were founded by few individuals, high relatedness and consequent low levels of genetic variation were potential factors limiting population growth (Rave et al. 1994). However, low levels of genetic variation do not necessarily imply that the limited population growth is caused (solely) by inbreeding effects. Most likely, a combination of genetic (e.g. adaptation to captivity, inbreeding) and environmental factors (e.g. lack of grassland reserves, heavy predation) were responsible (Black 1994).
The threatened red-breasted goose (Branta ruficollis) breeds on the Russian arctic tundra at Taimyr, Gydan and Yamal Peninsula (Hunter et al. 1999). Because the breeding and wintering ranges of the species are very limited, it is especially sensitive to overexploitation by hunting and alterations in habitat quality. In the 1950s the population numbered 50 000-60 000 birds, but because of deterioration of previous wintering grounds in the Caspian region, the population declined to approximately 25 000 during the 1970-80s (Hunter et al. 1999). After the switch to the wintering quarters on the Black Sea coast and protective legislation, the present maximum population estimate is 75 000 individuals (Hunter et al. 1999). The expansion in the red-breasted goose numbers during the last decades also exemplifies the potential of goose species for expansive population growth.
The bean goose is a widespread species with a breeding distribution covering the Eurasian tundra and taiga zones (Cramp & Simmons 1977). The species shows a declining trend, and since the beginning of the 20th century parts of its former breeding areas in the eastern Palearctic and taiga zone have been abandoned as a consequence of increased human activities (Rogacheva 1992). The world population has declined from 1.5 million individuals in the 1960s to approximately 700 000 individuals in the 1990s (Mooij & Zöckler 1999, and references therein). A decrease in numbers has also been observed in the wintering areas in Europe (Cramp & Simmons 1977, van den Bergh 1999). In Finland, the status of taiga bean goose (Anser fabalis fabalis) is considered ‘near threatened’ in the national 2000 Red List for the first time, but the species is not listed in the 2000 IUCN Red List of Threatened species. The need for future conservation is obvious but at the same time hampered by an unclear taxonomy of the species and a lack of information regarding the connection between breeding, staging and wintering areas. Most of the census counts are carried out during winter in Europe and Asia, and without clear knowledge about migration routes and breeding grounds, the specific threats facing each group cannot be fully understood and proper conservation measures implemented. The taxonomy of the bean goose complex is unclear both at the species and subspecies level. Based on morphology and distributional ranges, most authors recognise two species, the pink-footed goose Anser brachyrhynchus and the bean goose with two subspecies breeding in the tundra and two or three subspecies in the taiga zone (Delacour 1954, Cramp & Simmons 1977, Mooij & Zöckler 1999). Recently, the Dutch committee for avian systematics (CSNA) has further divided the bean goose into two species, the taiga bean goose and the tundra bean goose, based on differences e.g. in plumage, vocalization, behaviour and feeding phenology (Sangster et al. 1999), although this does not represent a general consensus of opinion.
A recent challenge to the arctic breeding species is related to the impact of climate change to breeding areas. According to a model used by Zöckler & Lysenko (2000), a modest rise in the global temperature of 1.7˚C by the end of the 21st century would affect 76% of the current breeding range of the tundra breeding bean geese (Anser fabalis rossicus and A. f. serrirostris) and 67% of the red-breasted goose breeding area via changes in vegetation. The magnitude of the decrease in population numbers depends largely on the ability of goose species to adapt to the direct effects (e.g. affecting breeding success) and indirect changes (e.g. increased population densities, new species-interactions).
1.4.3. The lesser white-fronted goose
The lesser white-fronted goose is the most threatened of the Palearctic goose species and globally one of the most threatened bird species (Tucker and Heath 1994). The decline of the world population began in the first half of the 20th century and the current estimate is 25 000 individuals (Tolvanen et al. 1999). The formal conservation status of the species according to IUCN Red List of Threatened Animals in 2000 was defined as ‘vulnerable’ by criterion A1 (observed, estimated, inferred or suspected reduction of at least 20% over the last 10 years or three generations). According to BirdLife International the lesser white-fronted goose is classified as a species of European conservation concern SPEC category 1 ‘globally threatened’ with a status of ‘vulnerable’. In the EU Birds Directive the species is listed in Annex I (a subject of special conservation measures concerning their habitat to ensure their survival and reproduction in their area of distribution). In the Finnish, Swedish and Norwegian Red Data Lists the species is considered endangered as in most other relevant countries. The lesser white-fronted goose has no formal protection in Kazakhstan, whereas in China the protection status of this species is unclear due to confusion regarding its taxonomical status.
The breeding area of the lesser white-fronted goose extends from Fennoscandian Lapland to northeastern Siberia (Lorentsen et al. 1999). The former continuous breeding range has been fragmented into a few geographically distinct breeding areas. Four breeding concentrations are known: the Fennoscandian Lapland, Ural-Yamal, Taimyr and Indigirka (Lorentsen et al. 1999, Syroechkovsky 2000). In addition to Indigirka, there are probably other presently unknown breeding localities in the eastern distributional area. A migratory divide exists in Taimyr (Rogacheva 1992, Syroechkovsky 1996). Lesser white-fronted geese breeding in Taimyr and westwards over-winter in Greece and the border areas to Turkey and presently poorly known areas in the Black and Caspian Sea regions, whereas birds breeding eastwards from Taimyr over-winter mainly in central China (Lorentsen et al. 1999).
Reasons for a population decline in the lesser white-fronted goose are still somewhat obscure (Madsen 1996, Lorentsen et al. 1999). In the breeding areas in Fennoscandia, disturbance, habitat loss and predation by the increasing population of the red fox are likely to contribute to the decline. The breeding success in Fennoscandia is high and comparable to that in other known breeding areas (Aarvak et al. 1997) despite the small size of the population. This suggests that the main problems may lie outside the breeding areas. The most important factors causing the negative population trend are deterioration of the habitats and over-hunting in the staging and wintering areas. Adult mortality has been shown to have a more significant effect on the population trend compared to juvenile mortality (Lampila 2000). Therefore e.g. spring hunting in Russia and illegal poisoning of lesser white-fronted geese in winter and early spring in China are especially harmful for population recovery.
At the international level, conservation work directed at the lesser white-fronted goose is coordinated by the Lesser White-fronted Goose Task Force of Wetlands International and yearly updated Urgent Action Plan following the guidelines set in the International Action Plan for the lesser white-fronted goose (Madsen 1996). The main groups carrying out the research and conservation work are WWF Finland Lesser White-fronted Goose project, Lesser White-fronted Goose project of the Norwegian Ornithological Society, Goose and Swan Study Group of Eastern Europe and North Asia (RGG) and Japanese Association for Wild Geese Protection (JAWGP). Additionally, dozens of biologists, ornithologists and volunteers from European countries, Kazakhstan and China have co-operated and contributed to the conservation work.
One of the main aspects in conservation is to gain knowledge regarding a species’ ecology. Census estimates (reviewed in Lorentsen et al. 1999), estimates of breeding success (Aarvak & Øien 2000) and mortality (Aarvak et al. 1997, Markkola et al. 2000), behavioural studies, such as time-budget and interactions with other species (T. Aarvak & IJ Øien, unpublished, J. Markkola et al., unpublished), and research on feeding ecology (Aarvak et al. 1996, Niemelä 1998) have been mainly carried out in the western distributional area. Further, making firm conclusions is often difficult because studies are limited due to the restricted number of individuals present and, as with any migratory species, the use of many localities throughout the year. Therefore knowledge regarding e.g. breeding and wintering philopatry vs. dispersal and timing of pair-formation in the lesser white-fronted goose is limited.
The main problems facing lesser white-fronted goose conservation are related to the lack of knowledge regarding the breeding, staging and wintering areas, difficulties in accessing remote areas and the low number of (individually marked) individuals for observations. The use of satellite-telemetry for tracking individual movements has been of paramount importance in revealing the migratory flyways of lesser white-fronted geese breeding in Fennoscandia, Yamal and Taimyr (Fig. 3) (Karvonen & Markkola 1998, Lorentsen et al. 1998, Markkola & Arkiomaa 1998, Øien et al. 1999). Some previously unknown important staging areas, such as the Kanin Peninsula in northwestern Russia and Kustanay in northwestern Kazakhstan, were found with this method and conservation actions have been implemented accordingly (Prokosch 1997, Bragina 2000). Further information on the connections of breeding and non-breeding areas in western Europe have been clarified by identifying geese based on individual differences in belly patches and a few colour ring resightings (Øien et al. 1996, Aarvak et al. 1999, Aarvak et al. 2000). Still, it remains unknown to where lesser white-fronted geese continue from Kazakhstan for the winter.
Despite the main emphasis being on the protection and research of the wild populations, restocking or reintroduction of the lesser white-fronted goose has been carried out in Finland and Sweden. In Finland, captive-reared lesser white-fronted geese were released in the Finnish Lapland during the years 1989-1997 to increase the wild Fennoscandian population (Markkola et al. 1999) presently estimated at 30-50 breeding pairs (Lorentsen et al. 1999). Another objective was to gain information on the migratory routes, staging and wintering areas through resightings and ring-recoveries of the released birds carrying neck collars and leg-rings. The results indicated that the mortality of the released birds was very high, no breeding attempts were confirmed and the resightings suggested that the individuals joined flocks of bean goose rather than their conspecifics (Markkola et al. 1999). The Swedish wild sub-population was considered close to extinction and a reintroduction project was initiated in 1981 (von Essen 1999, Lorentsen et al. 1999). To diminish hunting pressure, the wintering area of the reintroduced lesser white-fronted geese has been changed to Western Europe by using barnacle geese (Branta leucopsis) as foster parents. Up to 1999, 348 individuals with captive origins have been released in Sweden, and approximately 50 individuals have been seen in the release area during the breeding season (von Essen 1999, von Essen et al. 2000). The number of successful breeding attempts exceeds twenty, but the population is neither self-sustaining nor expanding. The natural origins of the captive populations used for restocking and reintroductions are largely unknown. As a consequence of transferring individuals between different stocks, a common ‘practice’ in captive breeding to avoid inbreeding, the composition of the stocks in Finland, Sweden, Britain and central Europe is more or less the same (von Essen 1996).