Using historical captive stocks in conservation. The case of␣the␣lesser white-fronted goose

Many captive stocks of economically or otherwise valuable species were established before the decline of the wild population. These stocks are potentially valuable sources of genetic variability, but their taxonomic identity and actual value is often uncertain. We studied the genetics of captive stocks of the threatened lesser white-fronted goose Anser erythropus maintained in Sweden and elsewhere in Europe. Analyses of mtDNA and nuclear microsatellite markers revealed that 36% of the individuals had a hybrid ancestry. Because the parental species are closely related it is unlikely that our analyses detected all hybrid individuals in the material. Because no ancestral polymorphism or introgression was observed in samples of wild populations, it is likely that the observed hybridisation has occurred in captivity. As a consequence of founder effect, drift and hybridisation, captive stocks were genetically differentiated from the wild populations of the lesser white-fronted goose. The high level of genetic diversity in the captive stocks is explained at least partially by hybridisation. The present captive stocks of the lesser white-fronted goose are considered unsuitable for further reintroduction, or supplementation: hybridisation has involved three species, the number of hybrids is high, and all the investigated captive stocks are similarly affected. The results highlight the potential shortcomings of using captive-bred individuals in supplementation and reintroduction projects, when the captive stocks have not been pedigreed and bred according to conservation principles. Deceased 20 March 2004.     

DNA fingerprinting of captive breeding pairs of lesser white-fronted geese (Anser erythropus) with unknown pedigrees

For a number of decades, the lesser white-fronted goose (Anser erythropus) has been almost-absent from the Fennoscandian fauna and has a current population size of only about 60 breeding pairs, with fewer than 10 pairs in Sweden. During the period 1981–1991 more than 200 young have been reintroduced in northern Sweden. However, the origin and possible relatedness of lesser white-fronted individuals were unknown when the breeding program started. We have used DNA fingerprinting to assess the similarity of 18 individuals, i.e., the entire captive population used for breeding in 1991 and about 60% of the captive population used in 1981–1991. Minisatellite probe 33.15 provided an index for an average similarity of 0.39 between the mates of the 12 breeding pairs used for producing offspring for reintroduction. This is a higher similarity than in natural populations of birds in general but lower than in populations that have passed through serious population bottlenecks. Individuals originating from different breeders are more dissimilar than those from the same breeder. However, the close relationships (similarity, 0.5–0.6) found in a group of five individuals from different breeders show that selecting individuals from different breeding groups is not sufficient to prevent mating between closely related individuals.     

Population Genetic Structure and Conservation of the Lesser White-Fronted GooseAnser erythropus

The lesser white-fronted goose is a sub-Arctic species with a currently fragmented breeding range, which extends from Fennoscandia to easternmost Siberia. The population started to decline at the beginning of the last century and, with a current world population estimate of 25,000 individuals, it is the most threatened of the Palearctic goose species. Of these, only 30–50 pairs breed in Fennoscandia. A fragment of the control region of mtDNA was sequenced from 110 individuals from four breeding, one staging and two wintering areas to study geographic subdivisions and gene flow. Sequences defined 15 mtDNA haplotypes that were assigned to two mtDNA lineages. Both the mtDNA lineages were found from all sampled localities indicating a common ancestry and/or some level of gene flow. Analyses of molecular variance showed significant structuring among populations ( _ST 0.220, P < 0.001). The results presented here together with ecological data indicate that the lesser white-fronted goose is fragmented into three distinctive subpopulations, and thus, the conservation status of the species should be reconsidered.     

Variability of the mtDNA control region in goose <Emphasis Type="Italic">Anser albifrons</Emphasis> Scopoli, 1769

Sequence variation of the mtDNA control region was examined in greater white-fronted goose Anser albifrons Scopoli, 1769 individuals (n = 71). The obtained sequences were compared with those from the NCBI GenBank database. The high level of similarity of the sample from Primorye (A. albifrons) with the sample from Japan (A. a. frontalis) at the level of molecular variation, genetic distance, phylogenetic reconstruction, and haplotype network was demonstrated. A hypothesis on the ways of spring goose migration in the Far East was made. It was confirmed that white-fronted geese wintering in Japan fly to their breeding grounds through Kamchatka.     

Changes in abundance and spatial distribution of geese molting near Teshekpuk Lake,Alaska: interspecific competition or ecological change?

Goose populations molting in the Teshekpuk Lake Special Area of the National Petroleum Reserve—Alaska have changed in size and distribution over the past 30 years. Black brant (Branta bernicla nigricans) are relatively stable in numbers but are shifting from large, inland lakes to salt marshes. Concurrently, populations of greater white-fronted geese (Anser albifrons frontalis) have increased seven fold. Populations of Canada geese (Branta canadensis and/or B. hutchinsii) are stable with little indication of distributional shifts. The lesser snow goose (Anser caerulescens caerulescens) population is proportionally small, but increasing rapidly. Coastline erosion of the Beaufort Sea has altered tundra habitats by allowing saltwater intrusion, which has resulted in shifts in composition of forage plant species. We propose two alternative hypotheses for the observed shift in black brant distribution. Ecological change may have altered optimal foraging habitats for molting birds, or alternatively, interspecific competition between black brant and greater white-fronted geese may be excluding black brant from preferred habitats. Regardless of the causative mechanism, the observed shifts in species distributions are an important consideration for future resource planning.     

Diet selection of lesser white-fronted geese Anser erythropus at a spring staging area

We studied diet selection of the globally threatened lesser white-fronted goose Anser eythropus at a spring staging area on the island of Hailuoto (64°00'N, 24°45'E), off the western coast of Finland. We determined the diet using droppings, which were collected in late May, when the geese had left the area and migrated northwards. The sample potentially comprised of ejecta from 31 different individuals. Plant idengification was based on visual determination of epidermal fragments. A total of 100 droppings were sampled using a point quadrat method. We calculated the percentage of each idengified taxon in each dropping and related this to the availability of the corresponding taxon in the meadow. We measured preference for each taxon using Chesson's electivity index (ɛ_i) and tested them by bootstrap resampling. The diet contained 9 taxa of the ca 40 available. Almost all dietary items were Monocotyledons (99.9%), mostly grasses (88.7%) including Festuca rubra (43%), Phragmites australis (30%) and Calamagrostis stricta (13%). Only Phragmites (ɛ=0.73, p=0.000), Festuca (ɛ=0.52, p=0.004) and possibly Triglochin palustris (ɛ=0.70, p=0.125) were preferred, all other species were avoided. All preferred species were quite common and other goose species exploit them too. The lesser white-fronted geese preferred large natural meadows that were five times broader than an "average" Bothnian Bay meadow. All forms of mowing and grazing management benefit the restoration of lesser white-fronted goose habitats at the landscape level. Festuca and especially Triglochin benefit from such management. Reeds, Phragmites , whose spread has been the main cause of coastal meadow deterioration, can be controlled by management, but can also be maintained among other vegetation if mowing is less frequent or grazing not too intensive.     

Wild hybrids of Lesser White-fronted Goose (Anser erythropus)×Greater White-fronted Goose (A. albifrons) (Aves: Anseriformes) from the European migratory flyway

The Lesser White-fronted Goose [Anser erythropus (Linnaeus, 1758)] is one of the most threatened Palearctic goose species, with the Fennoscandinavian subpopulation in particular having seen a drastic decline over the last century. In the 1990s, captive-bred Lesser White-fronted Geese were used successfully for reintroduction and restocking in Sweden and Finland. The discovery of Greater White-fronted Goose [Anser albifrons (Scopoli, 1769)] mtDNA haplotypes in some of these captive-bred birds (Ruokonen et al. 2000) suggested that hybridisation had occurred during captive propagation and led to the discontinuation of the release of captive goslings. Here we report two hybrids of Lesser×Greater White-fronted Geese that were collected on their wintering grounds in England in 1936 and Holland in 1966. Birds from western Russia normally do not migrate south to Western Europe. Hence, these birds most likely originated from the Fennoscandinavian subpopulation and were collected prior to the commencement of the captive-breeding programmes. Both specimens show a heterogeneous set of morphological characters, some of which shared with the putative parent species and others being intermediate between the two White-fronted Goose species. A Canonical Discriminant Function analysis positions both specimens between the two putative parent species, making their hybrid status likely. We show, thus, that hybridisation between Greater and Lesser White-fronted Geese does occur naturally, albeit perhaps infrequently, and argue that the presence of Greater White-fronted Goose mtDNA haplotypes in Lesser White-fronted Goose may be the result of this naturally occurring hybridisation. Our data provide additional information on the debate whether the restocking programmes were halted for the right reasons and whether it is desirable to re-commence with the reintroduction programme.     

The Origin of the White Roman Goose

In order to avoid interference from nuclear copies of mitochondrial DNA (numts), mtDNA of the white Roman goose (domestic goose) was extracted from liver mitochondria. The mtDNA control region was amplified using a long PCR strategy and then sequenced. Neighbor-joining, maximum parsimony, and maximum-likelihood approaches were implemented using the 1,177 bp mtDNA control region sequences to compute the phylogenetic relationships of the domestic goose with other geese. The resulting identity values for the white Roman geese were 99.1% (1,166/1,177) with western graylag geese and 98.8% (1,163/1,177) with eastern graylag geese. In molecular phylogenetic trees, the white Roman goose was grouped in the graylag lineage, indicating that the white Roman goose came from the graylag goose (Anser anser). Thus, the scientific name of the white Roman goose should be Anser anser ‘White Roman.’     

Genetic diversity of Anser albifrons Scopoli, 1769 and Anser fabalis Latham, 1787 in the Russian Far East

Using RAPD PCR analysis and sequencing of the 5′ end segment of the mtDNA control region, the genetic diversity and differentiation of Far Eastern populations of greater white-fronted goose Anser albifrons Scopoli, 1769 and bean goose Anser fabalis Latham, 1787 were examined. Based on RAPD PCR data, the level of gene diversity (h) for A. albifrons (0.3634) and A. fabalis (0.3899) was calculated. Sequence data showed considerably higher level of inter-population diversity in A. fabalis (26.4%), compared to A. albifrons (1.88%). Similarly, the nucleotide and haplotype diversity parameters were somewhat higher in A. fabalis (0.01852 and 0.955). Phylogenetic reconstructions generated using neighbor-joining and maximum parsimony algorithms divided each of the examined species into two clusters that differ in the number of haplotypes included. These clusters can correspond to the subspecies that live in the Far East.     

Introduced Swedish Canada geese (Branta canadensis) have low levels of genetic variation as revealed by DNA fingerprinting

The Swedish, Finnish and Norwegian population of Canada geese (Branta canadensis), now amounting to some 30–50 000 birds, was founded by only five individuals. We used DNA fingerprinting to assess the level of genetic variability in minisatellite loci of Swedish Canada geese from two northern areas. For comparison, we estimated the minisatellite variability in lesser white-fronted geese (Anser erythropus), barnacle geese (Branta leucopsis) and a reintroduced stock of Canadian giant Canada geese (Branta canadensis maxima). The mean similarity between Swedish Canada geese was 0.76 ± 0.15, which is higher than recorded for any other natural bird population. The high similarity implies that a fourfold increase of homozygosity has taken place in this population. The probable cause for the loss of variation is the low number of birds originally introduced and a history of repeated translocations, leading to a sequence of founder events. As a consequence of the high similarity, it has not been possible to use DNA fingerprinting for determination of parenthood in the population studied.     

Wild hybrids of Lesser White-fronted Goose (Anser erythropus)×Greater White-fronted Goose (A. albifrons) (Aves: Anseriformes) from the European migratory flyway

The Lesser White-fronted Goose [Anser erythropus (Linnaeus, 1758)] is one of the most threatened Palearctic goose species, with the Fennoscandinavian subpopulation in particular having seen a drastic decline over the last century. In the 1990s, captive-bred Lesser White-fronted Geese were used successfully for reintroduction and restocking in Sweden and Finland. The discovery of Greater White-fronted Goose [Anser albifrons (Scopoli, 1769)] mtDNA haplotypes in some of these captive-bred birds (Ruokonen et al. 2000) suggested that hybridisation had occurred during captive propagation and led to the discontinuation of the release of captive goslings. Here we report two hybrids of Lesser×Greater White-fronted Geese that were collected on their wintering grounds in England in 1936 and Holland in 1966. Birds from western Russia normally do not migrate south to Western Europe. Hence, these birds most likely originated from the Fennoscandinavian subpopulation and were collected prior to the commencement of the captive-breeding programmes. Both specimens show a heterogeneous set of morphological characters, some of which shared with the putative parent species and others being intermediate between the two White-fronted Goose species. A Canonical Discriminant Function analysis positions both specimens between the two putative parent species, making their hybrid status likely. We show, thus, that hybridisation between Greater and Lesser White-fronted Geese does occur naturally, albeit perhaps infrequently, and argue that the presence of Greater White-fronted Goose mtDNA haplotypes in Lesser White-fronted Goose may be the result of this naturally occurring hybridisation. Our data provide additional information on the debate whether the restocking programmes were halted for the right reasons and whether it is desirable to re-commence with the reintroduction programme.     

Taxonomy of the bean goose-pink-footed goose

The bean goose Anser fabalis and the pink-footed goose A. brachyrhynchus breed in the tundra and taiga zones of Eurasia and eastern Greenland, and the taxonomy of the group based on morphology has been controversial. We investigated the phylogenetic relationships within the bean goose–the pink-footed goose complex using mitochondrial control region sequences of 199 individuals collected from the breeding areas in the Palaearctic and Eastern Nearctic. We found three mitochondrial clades geographically distributed to (1) Greenland, Iceland and Svalbard (A. brachyrhynchus), (2) the eastern taiga zone (former subspecies A. fabalis middendorffii), and (3) the western taiga and the tundra zone (subspecies A. fabalis rossicus, serrirostris and fabalis). MtDNA phylogeny suggests that morphological affinities between the taxa, e.g. in the bill structure, result from convergent evolution due to adaptation to similar habitats. Although a latitudinal cline in morphology was observed, clear phylogenetic discontinuities exist in the taiga and tundra zones supporting a species status for brachyrhynchus and middendorffii.     

Spring snow goose hunting influences body composition of waterfowl staging in Nebraska

A spring hunt was instituted in North America to reduce abundance of snow geese (Chen caerulescens) by increasing mortality of adults directly, yet disturbance from hunting activities can indirectly influence body condition and ultimately, reproductive success. We estimated effects of hunting disturbance by comparing body composition of snow geese and non-target species, greater white-fronted geese (Anser albifrons) and northern pintails (Anas acuta) collected in portions of south-central Nebraska that were open (eastern Rainwater Basin, ERB) and closed (western Rainwater Basin, WRB; and central Platte River Valley, CPRV) to snow goose hunting during springs 1998 and 1999. Lipid content of 170 snow geese was 25% (57 g) less in areas open to hunting compared to areas closed during hunting season but similar in all areas after hunting was concluded in the ERB. Protein content of snow geese was 3% (14 g) less in the region open to hunting. Greater white-fronted geese had 24% (76 g; n = 129) less lipids in the hunted portion of the study area during hunting season, and this difference persisted after conclusion of hunting season. We found little difference in lipid or protein content of northern pintails in relation to spring hunting. Indirect effects of spring hunting may be considered a collateral benefit regarding efforts to reduce overabundant snow goose populations. Disrupted nutrient storage observed in greater white-fronted geese represents an unintended consequence of spring hunting that has potential to adversely affect reproduction for this and other species of waterbirds staging in the region. © 2012 The Wildlife Society.     

A preliminary analysis of the diet composition of overwintering Bean geese (Anser fabalis) and greater white-fronted geese (A. albifrons) in Korea using PCR on fecal samples

Bean geese (Anser fabalis) and Greater white-fronted geese (Anser albifrons) are the dominant wintering waterfowl in South Korea. Although they are commonly observed in estuaries and rice fields during the winter, the diet composition of the geese during the winter has rarely been studied. In this study, we provide the results from preliminary analyses on the diet of these two geese species overwintering in Daebu Island of South Korea. We used a total of 13 fecal samples from Bean geese (n?=?4) and Greater white-fronted geese (n?=?9), and performed a BLAST search for the sequences obtained from 87 clones (n?=?36 for Bean geese and n?=?51 for Greater white-fronted geese). The diet of Bean geese consisted of five families of plants: Caryophyllaceae (75.0%), Poaceae (13.9%), Asteraceae (5.5%), Polygonaceae (2.8%) and Cucurbitacea (2.8%). On the other hand, the diet of Greater white-fronted geese consisted of 6 families of plants: Poaceae (74.5%), Caryophyllaceae (9.8%), Solanacea (5.9%), Portulacaceae (3.9%), Lamiaceae (3.9%) and Brassicaceae (2.0%). We found that plants of the rice family (Poaceae) are important in the diet of wintering geese, especially for Greater white-fronted geese. This knowledge can be used to establish conservation strategies of the geese overwintering in South Korea.     

Multicentric intramuscular lipomatosis/fibromatosis in free-flying white-fronted and Canada geese

Over a period of 9 yr, seven white-fronted geese (Anser albifrons) and one Canada goose (Branta canadensis) with multiple intramuscular mesenchymal tumors were encountered in Saskatchewan (Canada) and one similarly affected Canada goose was seen on Prince Edward Island (Canada). The tumors in these birds consisted either of adipose tissue, fibroblastic tissue, or a mixture of both types of tissues. The high prevalence of this condition in white-fronted geese suggested a genetic influence.     

Determining the subspecies composition of bean goose harvests in Finland using genetic methods

Management of harvested species is of great importance in order to maintain a sustainable population. Genetics is, however, largely neglected in management plans. Here, we analysed the genetics of the bean goose (Anser fabalis) in order to aid conservation actions for the commonly hunted but declining subspecies, the taiga bean goose (A. f. fabalis). We used mitochondrial DNA (mtDNA) and microsatellites to determine the subspecies composition of the Finnish bean goose harvest, as the hunting bag is thought to comprise two subspecies, the taiga bean goose and the tundra bean goose (A. f. rossicus). The latter subspecies has a more stable or even increasing population size. Other eastern subspecies (A. f. serrirostris, A. f. middendorffii) could additionally be part of the Finnish hunting bag. We estimated genetic diversity, genetic structure and sex-biased gene flow of the different subspecies. Most of the harvested bean geese belonged to the taiga bean goose, whereas most of the tundra bean goose harvest was found to be geographically restricted to south-eastern Finland. The mtDNA data supported strong genetic structure, while microsatellites showed much weaker structuring. This is probably due to the extreme female philopatry of the species. The taiga bean goose had lowered genetic diversity compared to other subspecies, warranting management actions. We also detected A. f. serrirostris mtDNA haplotypes and evidence of interspecific hybridization with two other Anser species.     

Temporal increase in mtDNA diversity in a declining population

In small and declining populations levels of genetic variability are expected to be reduced due to effects of inbreeding and random genetic drift. As a result, both individual fitness and populations’ adaptability can be compromised, and the probability of extinction increased. Therefore, maintenance of genetic variability is a crucial goal in conservation biology. Here we show that although the level of genetic variability in mtDNA of the endangered Fennoscandian lesser white‐fronted goose Anser erythropus population is currently lower than in the neigbouring populations, it has increased six‐fold during the past 140 years despite the precipitously declining population. The explanation for increased genetic diversity in Fennoscandia appears to be recent spontaneous increase in male immigration rate equalling 0.56 per generation. This inference is supported by data on nuclear microsatellite markers, the latter of which show that the current and the historical Fennoscandian populations are significantly differentiated (F_ST = 0.046, P = 0) due to changes in allele frequencies. The effect of male‐mediated gene flow is potentially dichotomous. On the one hand it may rescue the Fennoscandian lesser white‐fronted goose from loss of genetic variability, but on the other hand, it eradicates the original genetic characteristics of this population.     

Mitochondrial DNA Cleavage Patterns Distinguish Independent Origin of Chinese Domestic Geese and Western Domestic Geese

It has generally been assumed, based on morphology, that Chinese domestic goose breeds were derived from the swan goose (Anser cygnoides) and that European and American breeds were derived from the graylag goose (Anser anser). To test the validity of this assumption, we investigated the mtDNA cleavage patterns of 16 Chinese breeds and 2 European breeds as well as hybrids produced between a Chinese breed and a European breed. After 224 mtDNAs, isolated from the Chinese and European breeds, were digested by 19 restriction endonucleases, variations of the cleavage patterns were observed for four enzymes (EcoRV, HaeII, HincII, and KpnI). All Chinese breeds and their maternal hybrids except the Yili breed showed an identical haplotype, named haplotype I or the Chinese haplotype; the European breeds and the Yili breed showed another haplotype, named haplotype II or the western haplotype. None of the haplotype found in the Chinese type was detectable in the western type and vice versa. The two haplotypes were found to differ from each other at 8.0% of the sites surveyed and with a 0.72% sequence divergence. Using 2% substitution per million years calibrated from the genera Anser and Branta, the two domestic geese haplotypes were estimated to have diverged approximately 360,000 years ago, well outside the 3000-6000 years in domestic history. Our findings provide the first molecular genetic evidence to support the dual origin assumption of domestic geese in the world. Meanwhile, the four mtDNA restriction fragment length polymorphisms can be used as maternal genetic markers to distinguish the two types of domestic geese.     

Close relatedness between mitochondrial DNA from seven Anser goose species

The phylogenetic relationships of seven goose species and two of the subspecies representing the genus Anser were studied by approximately 1180 bp of mitochondrial DNA tRNAglu, control region and tRNAphe sequences. Despite obvious morphological and behavioural affinities among the species, their evolutionary relationships have not been studied previously. The small amount of genetic differentiation observed in the mitochondrial DNA indicates an extremely close evolutionary relationship between the Anser species. The sequence divergences between the species (0.9–5.5%) are among the lowest reported for avian species with speciation events of Anser geese dating to late Pliocene and Pleistocene. The species grouped into four mtDNA lineages: (1) snow and Ross’ goose, (2) greylag goose, (3) white‐fronted goose, and (4) bean, pink‐footed and lesser white‐fronted goose. The phylogenetic relationships of the most closely related species, bean, pink‐footed and lesser white‐fronted goose, indicate a period of rapid cladogenesis. The poor agreement between morphological relationships and the phylogenetic relationships indicated by mtDNA sequences implies that either ancestral polymorphism and lineage sorting, hybridization and introgression or convergent evolution has been involved.     

Condition Bias of Decoy-Harvested Light Geese During the Conservation Order

Evidence that decoy harvest techniques primarily remove individuals of poorer body condition is well established in short-lived duck species; however, there is limited support for condition bias in longer-lived waterfowl species, such as geese, where decoy harvest is considered primarily additive because of their high natural survival rates. We evaluated support for the harvest condition bias hypothesis of 2 long-lived waterfowl species, the lesser snow goose (Anser caerulescens caerulescens) and Ross's goose (Anser rossii). We used proximate analysis to quantify lipid and protein content of lesser snow and Ross's geese collected during the Light Goose Conservation Order (LGCO) in 2015 and 2016 during spring migration in Arkansas, Missouri, Nebraska, and South Dakota, USA. In each state, LGCO participants collected birds using traditional decoy techniques and we collected birds from the general population using jump-shooting tactics. Total body lipid content in both lesser snow and Ross's geese varied with age, region of harvest, and harvest type (decoy or jump-shooting). On average, adult lesser snow and Ross's geese harvested over decoys had 60 g and 41 g, respectively, fewer lipids than conspecifics collected using jump-shooting. We observed lower lipid reserves in decoy-shot geese in all 4 states sampled despite general gains in lipid reserves as migration chronology progressed. Our data support that the harvest condition bias extends to longer-lived waterfowl species and during a life-history event (spring migration) in which harvest is not normally observed. In the case of overabundant light geese, the disproportionate harvest of poorer-conditioned lesser snow and Ross's geese may serve as an additional challenge against any realized effects of harvest to reduce the population, in addition to extremely low harvest rates. © 2019 The Wildlife Society.