Arctic Geese (Anser) and Brants (Branta) of Eurasia: An Analysis of Factors That Control Population Dynamics and Geographical Ranges

ISSN 2079-0864, Biology Bulletin Reviews, 2016, Vol. 6, No. 5, pp. 436 455. Pleiades Publishing, Ltd., 2016. Original Russian Text S.B. Rozenfeld, I.S. Sheremetyev, 2016, published in Zhurnal Obshchei Biologii, 2016, Vol. 77, No. 1, pp. 16 37. Arctic Geese (Anser) and Brants (Branta) of Eurasia: An Analysis of Factors That Control Population Dynamics and Geographical Ranges S. B. Rozenfeld a, * and I. S. Sheremetyev b, ** a A.N. Severtsov Institute of Problems of Ecology and Evolution, Russian Academy of Sciences, Moscow, pr. Leninskii 33, Moscow, 119071 Russia b Institute of Biology and Soil Science, Far East Branch of the Russian Academy of Sciences, pr. 100-letia Vladivostoka 159, Vladivostok, 690022 Russia *e-mail: rozenfeldbro@mail.ru **e-mail: sheremetyev@ibss.dvo.ru Received September 10, 2014 Abstract Geese (Anser) and brants (Branta) are important elements of Arctic ecosystems, which attract the interest of biologists around the world. Due to this interest, a great amount of empirical data has been accumulated, including detailed descriptions of the morphology, nesting characteristics, trophic ecology, behavior, migrations, population geography, and other features of Arctic geese and brants. The extent of their range along the Arctic coast of Eurasia largely depends on population size. Therefore, all of the factors influencing population size also indirectly affect the range extent. Geese and brants species significantly differ in population size, range extent, and tendencies in their changes over time. We compared the available data in order to find out what, in which way, and to what extent determines the population size and range extent in geese and brants. The main contribution to a reduction in population size is made by extermination at nesting sites and along the flyways and the lack of food at overwintering sites. The species that do not use cultivated plants in winter are small population size. The next most significant factor is the feeding type, which is determined by body size and the ratio between beak length and head length. The population size is influenced much less by all other factors related to patterns of feeding and nesting. The absence of a significant effect of these characteristics on the population size and range of geese and brants may be interpreted as the result of anthropogenic impact, which does not yet seem to be able to be estimated quantitatively. The disappearance of geese and brants within considerable areas in the Arctic Region may cause serious ecological consequences. DOI: 10.1134/S2079086416050078 INTRODUCTION In Arctic ecosystems geese (Anser) and brants (Branta), together with rodents (Rodentia) and cloven-hoofed animals (Artiodactyla), play the important role of consumers of primarily terrestrial vegetation (Chernov, 2008). They themselves are an important trophic resource for Artic predators (Syroechkovskii, 2013). However, due to the low digestibility of phytomass and need for intensive feeding (Kondratyev, 2002), an even greater role is played by the acceleration of the return of matter into a state suitable for use by plants; this is ensured by birds (Graaf, 2006). The extinction of large herbivore mammoths (Vereshchagin, 1977; Zhegallo et al., 2001; Barnosky et al., 2004; Lyons et al., 2004; Zimov, 2005) made the ecological role of geese decisive in many places of the Artic region. It was achieved by them due to their mobility and migration activity (Madsen et al., 1999). This shows the importance of changes in the ranges and population sizes of geese and brants that were observed historically, particularly in the recent period (Owen, 1980). One more important function of intensively feeding herbivores is the formation of grazing-lawns and the initiation of a grazing succession of vegetation (Toit and Olff, 2014): rapidly growing short-grass vegetation, which has a high content of nonstructural carbohydrates, proteins, and water and is suitable for the feeding of other phytophages, rapidly forms in the place of tall grass with a high content of structural carbohydrates (Zimov, 2005; Graaf, 2006; Toit and Olff, 2014). Showing a high diversity of adaptations to high latitudes (Syroechkovskii, 1978, 1988), geese (Anserinae) can change vegetation to such an extent that it can be classified as damage (Tikhomirov, 1959; Bazely and Jefferies, 1986; Madsen and Mortensen, 1987). For example, at the coast of the Hudson Bay in America, geese aggregations create many environmental problems (Cargill and Jefferies, 1984; Kerbes et al., 1990; Gautier et al., 1997; Batt, 1997). This assessment of 436

ARCTIC GEESE (ANSER) AND BRANTS (BRANTA) OF EURASIA 437 the value of geese and brants arouses greatest interest in the structure and dynamics of their populations at the global and regional levels. This study is focused on eight species and subspecies of geese and brants that live in Eurasia and nest in the Russian Arctic and Subarctic. These are the brent goose (Branta bernicla), barnacle goose (B. leucopsis), red-breasted goose (B. ruficollis), bean goose (Anser fabalis) 1, greater white-fronted goose (A. albifrons), lesser snow goose (A. caerulescens) 2, lesser white-fronted goose (A. erythropus), and emperor goose (A. canagicus). The range extent and population size of geese and brants are determined by a set of characteristics, including the following: feeding and nesting properties (Owen, 1980; Kondratyev, 2002), timing and geography of migrations (Drent, 2006), habitat use (Owen and Black, 1991; Krechmar and Kondratyev, 2006), some morphological and behavioral characteristics (Syroechkovskii, 2013), and response to anthropogenic factors (Madsen et al., 1999; Fox et al., 2010). The most interesting property of geese and brants is their classification as obligate herbivores, which in general rarely occurs in the class of birds. Therefore, we first consider the patterns of feeding and their relationship with other aforementioned characteristics. Adaptation to feeding with terrestrial plants is associated with the need to tear fixed food and requires a strong beak with indented edges, strong muscles, and the additional support of the beak at the expense of the nasal bone (Dzherzhinskii and Grintsevichene, 2002). We can assume that the distinctions in feeding in jointly living and outwardly similar geese and brant species are due to morphological distinctions (Kondratyev, 2002), so the relationship between the trophic properties and morphological parameters is of significant interest. The feeding properties, which result from the low digestibility of plants and the need to feed intensively, are determined in geese and brants by the absence of cellulose-splitting symbionts and the small differentiation of the intestine in comparison to most herbivorous birds and mammals (Sedinger et al., 1989). Therefore, geese and brants are forced to spend much time and effort to search for plants with a high content of nonstructural carbohydrates, proteins, and water and to make distant migrations to the places where this search is efficient (Kondratyev, 2002). By the feeding type, like other large phytophages with a wide feeding range, geese and brants can be classified as browsers (browser selectively browsing species), gazers (non- 1 Populations of bean goose are represented in the present study only by the subspecies that nest in the tundra zone: the western tundra bean goose (Anser fabalis rossicus) and eastern tundra bean goose (A. fabalis serrirostris), which are considered jointly. 2 The overwhelming majority of the world population and the entire Eurasian population of snow goose are represented by the lesser snow goose (Anser caerulescens caerulescens), which dictates the need to use data that only relate to this subspecies. selectively grazing species), and mixed feeders (species that combines the features of browsers and grazers) (Robbins et al, 1995; Shipley, 1999; Rozenfeld, 2009; Toit and Olff, 2014). Browser brants are characterized by their small size and short neck and beak, and the ratio of head length to beak length (the beak index) is 0.23 0.40. Grazer geese are characterized by a large size, a long neck with strong muscles, and long strong beak; the beak index is 0.47 0.50. Mixed feeders have average sizes but short necks and beaks; their beak index is 0.3 0.4 (Rozenfeld, 2009). An important factor that determines the state of a population is a breeding success. The delayed development of goslings decreases their survivability in the first winter and the average clutch size (Sedinger, 1992; Syroechkovskii, 2013). Therefore, we consider the feeding properties in goslings rather minutely. Plant feeding in Arctic geese and brants involves a significant limitation hatching and brood rearing must fall in the first stages of food plant growth (Lack, 1947; Drent and Daan, 1980; Cooch et al., 1991; Jeugd et al., 2009). This is due to the fact that, in the first two weeks, goslings must obtain no less than 16% of protein with food and the minimum amount of structural carbohydrates (Sedinger and Raveling, 1984; Lindholm et al., 1994; Lepage et al., 1999). In most geese and brant species goslings, eat animal food only in the first days and then, like adult birds, they must consume a lot of vegetation in order to have time to develop for a short summer (Aubin et al., 1993). Under unfavorable feeding conditions, birds that arrive at nesting places may notbreed at all (Rozenfeld and Syroechkovskii, 1998; Baranyuk, 2007; Syroechkovskii, 2013). Large-size species, in which the period of incubation and development of goslings is longer than in small-size species, must start nesting earlier (Drent, 2006). One can assume that, under otherwise equal conditions in a relatively stable environment, species with a strongly pronounced specialization have an advantage that is manifested in a stable and expanding range and growing or stable population size, whereas a variable environment gives an advantage to species with strong adaptive abilities (Greenberg, 1990; Rautian and Zherikhin, 1997; Rozenfeld and Sheremetyev, 2013). We believe that the insignificant role of adaptive abilities in Arctic geese and brants in a dynamic environment must show a high degree of anthropogenic impact and need for nature-conservation efforts. Otherwise, changes in ranges and population sizes are more likely to have natural reasons, and nature-conservation efforts can only have a local effect. The major goal of the study is to ascertain which of the factors chosen for the analysis determines the population size, range, and trends of their change in geese and brants, and to determine the extent and means of its effect. The absence of significant correlations between the studied characteristics, on the one hand,

438 ROZENFELD, SHEREMETYEV and population size, range extent, and trends of their change, on the other, will allow the supposition of a significant anthropogenic impact on the populations of geese and brants. MATERIALS AND METHODS To date, a significant array of information has been accumulated on the ranges, population size, and properties of feeding, migration, and breeding in Artic geese and brants. Here, we consider that it is first appropriate to summarize the published data, despite the fact that many of the field study materials that are their basis were obtained and processed by one of the authors himself. All of the sources of data compared in the work are presented in the list of references. The main task of the methodological approach is to group and/or rank geese and brants that nest in the north of Eurasia by the extent of the range, global population size, and trends in their changes, to rank goslings by their feeding properties and adult birds by their habitat ranges and nesting properties. The compared data are subdivided into those that enable comparison of the sizes of the populations (abundance) and territories occupied by them (ranges) and those that can explain the trends in changes in the abundance and ranges. The growth in population sizes, and probably the range extents, are based on the number of offspring that survives and takes part in the next breeding cycle (Rautian and Zherikhin, 1997). The data on the trends in changes in the population sizes and range extents were assessed with respect to their possible contribution to breeding success, independently of whether this contribution is manifested directly or indirectly. The data on the properties of nesting, behavior, etc. were analyzed in order to estimate the possible effect of the considered characteristics on the trophic properties of goslings and adult geese. In this paper, we use the conventional division of the range of geese and brants into nesting areas (territories in the Artic and Subarctic) and wintering areas (territories in the temperate and/or subtropic zone of Eurasia and North America). The distinctions in living conditions for species, subspecies, and populations of geese and brants that use the European, North American, and east Asiatic wintering areas made it necessary to use the following concepts: the Asiatic part of the range (to the east from the Yenisei River), European part of the range (the west from the Yenisei River), and American part of the range (for circumpolar and amphiberingian species). The contribution of the following characteristics was estimated (table): feeding type, body weight, body length, ratio of body length to beak length, degree of coloniality, nesting habitats, confinement to seacoasts, duration of the nesting period, duration of goslings development, number of food types and share of animal foods in different periods of ontogeny, duration of the gosling transition to the feeding range of adult birds. The relationship of all characteristics was quantified by nonparametric correlation analysis (the Spearman coefficient, SR) due to their different quality and nonnormality. The volume of the compared sets (n) is eight in each case according to the number of species and subspecies of the studied geese and brants; the SR values were recognized to be reliable at a significance level p < 0.05. The calculations were all made with the Statistica 10 software package (Stat- Soft, Inc., 2011). The food resources of geese were distributed by their feeding qualities into the following groups: herbs, rushes, sedges, willows, horsetails, legumes, grasses, mosses, aquatic plants, halophilic plants (grasses, sedges, and some herbs), and insects. The classification of legumes,, as well as aquatic and halophilic plants into a discrete group is due to their exceptionally high food qualities. Legumes are very rich in protein; aquatic and halophilic plants contain a smaller amount of silicon and lignin (Kondratyev, 2002; Graaf et al., 2004; Rozenfeld, 2009). DATA: RANGE, POPULATION SIZE, NESTING PROPERTIES, AND TROPHIC CHARACTERISTICS Brent Goose A very large circumpolar breeding range covers the entire Arctic coast and islands and remains stable. The species hibernates at the seacoast of North America, western Europe, and the Far East (China, Korea, and Japan) (Syroechkovskii, 2011a; BirdLife International, 2014a). Except for the Netherlands, where the black brant has adapted to agricultural lands (Koffijberg et al., 2013), this species prefers to hibernate at coastal marshes (Clausen et al., 2013; Elkinton et al., 2013). The causes of the decreased population size of the black brant in western Europe are now usually attributed to the decrease in eelgrass areas (Zostera sp.) in many wintering places (Dalloyau, 2012; Clausen et al., 2013). As a result, the wintering area has abruptly diminished, and most of it is currently in France (Valery and Schricke, 2013). In the middle of the 20th century, the population size of the black brant in Eurasia was in a deep depression (less than 150000); it then grew to about 300000, but it began to decrease again in the early 1990s. The population size in America remained stable. The world population is currently estimated at 465000 (Ebbinge, 2009; Fox et al., 2010; Syroechkovskii, 2011a; Waterfowl..., 2012). The brent goose is penetrating into the most northern latitudes, where other geese do not already nest. This species is closely confined to seacoasts throughout the life cycle. Its colonies usually nest near water bodies (at a distance of not more than 10 km from the seacoast), in islands or near nests of predator birds, or in colonies of large gulls (Syroechkovskii, 2011a,

ARCTIC GEESE (ANSER) AND BRANTS (BRANTA) OF EURASIA 439 1.0 0.8 0.6 0.4 0.2 Browsers Grazers Mixed feeders 1 2 1 2 1 2 1 2 1 2 1 2 1 2 1 2 Insects Legumes Grasses Aquatic plants Halophilic plants Mosses Rushes Horsetails Willows Sedges Herbs 0 Brent goose Barnacle goose Red-breasted goose Tundra bean goose Greater White-fronted goose Lesser snow goose Lesser white-fronted goose Emperor goose Fig. 1. Distribution of adults (1) and gosling of geese and brants at the age of 7 14 days (2) by feeding types and ratio of their feeding ranges according to the number of plant species of major groups. 2013). As in many small-size brant species, the typical biological characteristic of the brent goose is its later arrival at and earlier departure from nesting sites than other species (Syroechkovskii, 1978). This contributes to its nesting in large areas that are located much farther to the north than those occupied by other geese and brants; the pressure of competition and predation is smaller. In unfavorable years, brent goose may not nest at all. By feeding type, this species is a browser; the beak index is 0.28. It feeds in nesting areas, mainly with dominant plants since there is no opportunity to spend much effort on a long search for high-calorie food. It feeds on 77 plant species from 22 families (Rozenfeld, 2009). The preferred foods are herbs and, in the case of their shortage, grasses and sedges (Fig. 1). In the most northern nesting areas, the species can eat all available plant species, including mosses (Madsen et al., 1989). As the species diversity grows to the south, selectivity increases and the number of eaten species decreases. It is believed that brent geese are more inclined than all other geese and brants to eat animal foods, mainly invertebrates (Rozenfeld and Syroechkovskii, 1998; Syroechkovskii, 2013). Some authors point to the active eating of fish eggs by brent goose (Cottam et al., 1944; Reed et al., 1998). In wintering areas, the species feeds on eelgrass, algae, the vegetation of coastal salty marshes, and, when the reserves of these foods are exhausted, it eats sprouts of winter crops (Krechmar et al., 1991; Rozenfeld and Syroechkovskii, 1998). The ration of brent goose gosling aged 1 3 days may consist of animal foods by 70% or more (Kiera, 1984; Spilling and Stock, 1995), or their ration is based on aquatic and halophilic plants (Volkov and Rozenfeld, 2008). The share of animal foods then decreases, and herbs start to dominate in the diet (Rozenfeld and Syroechkovskii, 1998). In Artic tundras, most of the ration in goslings is formed by sprouts of herbs and motley grass; gosling eat horsetails, sedges, and willows to a much lesser extent (Fig. 1). The full transition of goslings to the adult diet takes place at the age of 2.5 weeks.

440 ROZENFELD, SHEREMETYEV Barnacle Goose Since the middle of the 20th century, the range and population size of the barnacle brant have been characterized by rapid growth. Since the early 1970s, the barnacle brant started nesting in the Gotland, Saaremaa, Hiiumaa, and Muhu Islands; since the 1980s, they began nesting in the Kolguev Island, Yugorskii and Kanin Peninsulars, and the Timan Coast of the Malaya Zemlya tundra, whereas they had previously nested only in Greenland, in the Spitsbergen Islands, Yuzhnyi Island of Novaya Zemlya, and Vaigach Island. Since the late 1980s, barnacle geese began nesting in the Netherlands and they appeared in recent years on the islands of the Gulf of Finland (Ganter et al., 1999; Feige et al., 2007). Barnacle geese wintering in western Europe (Gurtovaya, 2011). The growth in abundance can be characterized by the following ciphers: the world population in the early 1950s was estimated at about 65000 70000 (Boyd, 1961; Owen and Black, 1991; Ganter et al., 1999; Ogilvie et al., 1999); in the late 1990s, the population grew to 330000 (Ganter et al., 1999) and in the late 2000s it was already 770000 (Fox et al., 2010); to date, the population is estimated at about 1 mln individuals (Jeugd, van der, personal report). The barnacle goose is one of the largest brants. Their nesting colonies have a size of from several dozen to several thousand nests. The first nests of a colony are usually formed near nests of predator birds, but the protection of predators loses its value as the colony grows (Kondratyev et al., 2012). As the range increased, they adapted to new habitats: barnacle goose initially nested only on rocks of arctic islands and then adapted to coastal meadows (laidas) and tundras, having successfully survived the competition with other geese and brants. They also adapted to many other types of habitats in places where they had previously only wintered (Feige et al., 2007). By feeding type, the barnacle goose is a browser; the beak index is 0.4. The species has a large rate of plant browsing among geese (Black et al., 2007). The typical property is its ability to completely transform vegetation in large feeding areas, not only eating the tips of sprouts but also digging over the ground in search of the underground parts of plants. As a result, high-grass and hummocky areas are transformed into areas with low vegetation, which are of little use for the feeding of large goose species. The barnacle goose uses 45 plant species from eight families as food (Fig. 1). In coastal meadows, the species for the most part feeds on halophytes: herbs, sedges, and grass types that form a marshy carpet (Black et al., 2007; Rozenfeld et al., 2011). The background plant species of coastal meadows contain much protein and little lignin and silicon (Graaf et al., 2004) and are easily transformable by the barnacle brant, which gives it a large advantage over other goose species (Rozenfeld and Karagicheva, 2010). During nesting in the tundra, the barnacle goose uses almost all types of food plants (Rozenfeld and Sheremetyev, 2013). A large role in the feeding of barnacle goose goslings is played by the vegetation of coastal marshes, which does not undergo xerophytization under a high grazing load of brants (Graaf et al., 2004). This circumstance provides favorable feeding conditions for goslings for a long period. At the age of 1 3 days, barnacle goose goslings mainly feed on animal foods (75 98%), which they get in vast silty areas with sparsely growing alkali grass and saltwort. These are the first plant foods for goslings, which begin to eat them at the age of 3 days, and for adult birds, which are forced to use the same feeding habitats in this period (Fig. 1). The broods then move to areas with a large foliage cover, where the consumption of animal foods by goslings falls and the consumption of halophilic plants rises (Rozenfeld et al., 2011). In tundra habitats, where the feeding conditions are worse, goslings, on the contrary, have fewer distinctions in feeding from adult birds in the first days of life than at the age of three weeks (Rozenfeld and Sheremetyev, 2013). The transition to the adult diet may last from four to five weeks. Red-Breasted Goose The breeding range includes the Taimyr Peninsular (80% of the population), Gydanskii and Yamal Peninsulars; nesting was recorded in Yakutia. Before the 1970s, the species hibernated mainly at the southern coast of the Caspian Sea; then, due to the replacement of cereal fields by cotton plantations in this region, the wintering areas moved to the PreCaucasus and Black Sea Region (Vangeluwe and Stassin, 1991). The species singly wintering in western Europe. Both the breeding and wintering parts of its range show a trend towards expansion. A significant decrease in abundance (to 25000 individuals) has been recorded since the early 1960s. Since the 1980s, thanks to the protective measures undertaken, the population increased to 90000 and continues growing; according to our data, it came to 130000 150000 in 2012 2013 (Rozenfeld et al., 2012). The red-breasted goose is the smallest and most specialized species among Arctic brants. The nesting colonies are placed only near nests of predator birds for protection from terrestrial predators. This species is a browser; the beak index is only 0.23. The red-breasted goose specializes in the nesting period is dicotyledonous plants, mainly legumes. The species uses no less than 28 plant species from nine families as food (Rozenfeld, 2009). The category of major foods includes herbs and horsetails, and sedges are eaten as a substituting food. The share of willows in the diet is always small, with the exception of the years when willow buds are a food of all goose species in the tundra due to the late spring (Rozenfeld and Volkov, 2001). Their specialization in feeding with nonrenew-

ARCTIC GEESE (ANSER) AND BRANTS (BRANTA) OF EURASIA 441 able dicotyledonous plants, the meristem of which suffers during browsing (due to which their further growth is impossible (Kondratyev, 2002) (Fig. 1)), allows this species to obtain food with a high protein content, which is very important for small species. Their individuals are forced to spend much time on feeding during incubation but must not go far from nests. The confinement to nests of predator birds limits the number and size of nesting colonies in the brant and corresponds well to food specialization, which ensures the necessary amount of nutrients in grasslands with a limited size. This nesting strategy is only available to species with small sizes and small abundance (Kondratyev, 2002). In contrast to other species, the goslings of redbreasted goose eat few insects; their share is not more than 5% in the first days of life (Rozenfeld, 2009). They use the same food groups as adult birds but show a greater selectivity to the flowers of legumes. A characteristic difference from the nutrition of adult birds is the greater consumption of willows (up to 5%) and horsetails and smaller consumption of rushes, herbs, and sedges (Fig. 1). The transition to the adult diet ends at the age of two weeks and is manifested in an increased number of eaten plant species in these food groups and by equalization of their ratio (Rozenfeld and Volkov, 2001). Tundra Bean Goose The nesting range includes the tundra and areas of the forest-tundra zone of northern Siberia from the Kanin Peninsular in the west to the northwestern part of Yakutia, Chukotka, and Kamchatka in the east. The eastern part of the nesting range is strongly reduced and fragmented. The tundra bean goose wintering in western and central Europe, sometimes reaching Morocco and Algeria, in Japan, the southern part of the Korean Peninsular, and southeastern regions of China (Scott and Rose, 1996; Krechmar and Kondratyev, 2006; Litvin, 2011a). In the western part of the range, the tundra bean goose population is growing and currently is about 630000. The population of the eastern subspecies until the 1980s was about 1 mln; in the mid-1990s it was only 40000 (Syroechkovskii, 2006; Krechmar and Kondratyev, 2006; Andreev, 2009; Fox et al., 2010; Litvin, 2011a). The tundra bean goose is a very large goose with masked solitary nesting in pairs. Its nests and feeding habitats are not always on banks of water bodies (Kondratyev, 2002). The tundra bean goose shows features that are typical for large-size goose species: a long period of egg formation, incubation, and brood rearing; lower energy expenses for migration; a less intense metabolism; and larger fat deposits, which allow this species to eat very little in the incubation period (Syroechkovskii, 2013). The large size of the tundra bean goose also involves the early nesting, which starts as early as before the snow disappears (Drent, 2006). The large, long beak (the beak index is 0.48) and large size also increase the ecological plasticity, enabling the use of a greater number of food plants and habitat types in the Arctic. The ability to extract the roots of sedges and cotton grasses from the soil with the beak makes it possible to get food in the case of early arrival at the nesting areas. The species is a grazer by feeding type. It eats 20 plant species from eight families (Rozenfeld, 2009). One of the necessary conditions for living is a dense high grass cover, in which feeding requires much lower energy expenditures (Krechmar et al., 1991; Rozenfeld et al., 2011). The tundra bean goose occurs rarely at coastal marshes, but, going into their territory, it can normally feed only in areas with high vegetation (Rozenfeld et al., 2011). In summer, the major food groups for the tundra bean goose are herbs, rushes, horsetails, sedges, and buckwheats (Fig. 1). Tundra bean goose broods at coastal regions stay in the first days of life at the tundra lakes, where goslings feed mainly on nonhalophilic herbs, horsetails, and willow leaves. According to observations of goslings kept in captivity, feeding on insects ends at the age of 4 days. At the age of 7 10 days, broods move to rivers, which they do not leave for the entire moulting period in parents, i.e., until rising on wings. The basis of nutrition in goslings until the age of two weeks is horsetails (Fig. 1). The transition to the adult diet in these habitats ends within three weeks. Goslings from the broods that stick to the boundary of tundra and coastal marshes feed on plants of coastal meadows. During feeding at coastal marshes in families with goslings aged 7 20 days, alkali grass and halophilic plants are prevalent in the diet of adult birds and goslings, and the share of herbs, sedges, rushes, and horsetails is also high in the ration of nestlings (Rozenfeld et al., 2001). The transition to the adult diet in these habitats takes place later than in tundra and lasts more than three weeks. Greater White-Fronted Goose The greater white-fronted goose is the most widespread goose species in the Northern Hemisphere, the only goose with a circumpolar distribution (Mooij and Zöckler, 2000): it nests in the tundras of Europe, Asia, and North America, including many islands of the Arctic Ocean. In Russia, it is widespread from the Kanin Peninsular to the east of Chukotka; some nesting centers are in the taiga zone of eastern Yakutia and the region of the Sea of Okhotsk (Litvin, 2011b). The species wintering in western and eastern Europe and eastern Asia (China, Japan, and Korea).

442 ROZENFELD, SHEREMETYEV The greater white-fronted goose is one of the most numerous geese in Eurasia, where the total population has already been growing for a long period and is currently about 1.2 mln. The population in the Asiatic part of the range has been decreasing since the 1980s. In America, the population is relatively stable. The global population in the 1990s was estimated at about 1150 000 and is currently estimated at 2.5 mln (Fox et al., 2010; Litvin, 2011b; Waterfowl..., 2012). The species nests in single pairs but sometimes nests with a very high density in all types of tundras and forest tundra, entering the taiga zone. It shows a large plasticity in the use of nesting and feeding habitats. As in other geese, the late spring can force a significant part of individuals to avoid breeding. The greater white-fronted goose is a grazer by feeding type; the beak index is 0.47. Its ration was noted to include 36 plant species from ten families. The basis of nutrition is sedges and herbs (Fig. 1). In the nesting period, horsetails, pendant grass and dupontia, aquatic plants, and near-root parts of sedges are prevalent in the diet (Rozenfeld, 2009). The diet of greater white-fronted goose goslings within the first 3 5 days of life predominantly includes animal foods. Within 2 weeks, the consumption of sedges grows, horsetails start to be eaten, and the share of herbs almost changes little (Fig. 1). Insects disappear from the diet of goslings under the age of four weeks, and the transition to the adult diet ends within these terms (Rozenfeld, 2009). At coastal marshes and watershed lakes, the diet of goslings initially does not strongly differ from that of the parents (Kondratyev and Rozenfeld, 2004); Rozenfeld et al., 2011). Here, the timing of the final transition to the adult diet is from 1 3 weeks. Lesser Snow Goose The nesting range includes the tundra and forest tundra of North America from Alaska to the Hudson Bay, Yakutia, the Wrangel Island, and the New Siberian Islands (Litvin, 2011c). In the 19th century, the small white goose nested in the mainland tundras of Eurasia but was extirpated. Now, the small white goose nests in the mainland part of Eurasia only to the east from the mouth of the Kolyma River. The species wintering at the western coast of North America (Syroechkovskii, 2000; Baranyuk, 2007; Litvin, 2011b; BirdLife International, 2014b). The current size of the American population is exponentially growing and is the largest among geese and brants. In the 1980s, the population was about 5 mln (Madge, 1987); by 2010, the population grew to 7 10 mln individuals (Litvin, 2011c). In the Wrangel Island, the population has varied within a range of 60000 150000 during the last forty years (Baranyuk, 2007). In the area from the New Siberian Islands to the Uelen Cape, the species occurs regularly in single pairs or in small groups (Krechmar and Kondratyev, 2006). The lesser snow goose is characterized by a medium size. The species nests in large (up to several hundreds of thousands of pairs) colonies. In all parts of the range, the geese usually do not go more than 40 50 km from the seacoast during nesting (Syroechkovskii, 2013). Due to the late spring, most pairs may avoid breeding. The choice of nesting and feeding habitats is due to the sequence of snow melting rather than the amount of food or shelters; therefore, most nests usually get into areas that have scarce food but thaw earlier (Baranyuk, 2007; Syroechkovskii, 2013). The typical feature of this species is its departure from colonies and massive displacement with broods to habitats with favorable feeding conditions. In the Wrangel Island, the broods immediately move from its central part to tundras in the north of the island and to the coasts. The lesser snow goose is a grazer; the beak index is 0.50. This species eats 44 plant species from 14 families (Rozenfeld, 2009). The major food plants in the territory of a colony are herbs, sedges, legumes, and grasses, and, after having left, herbs (Fig. 1). After migration to the seacoast, the share of grasses, sedges, and horsetails decreases, and halophilic plants become major foods. The feeding range of goslings in the first day consists of animal foods, the share of which can reach 94%. A large part of the ration is made up by the flowers of grasses and legumes and the sprouts of herbs and sedges (Fig. 1). The share of animal foods then decreases, and the share of grasses among plant foods decreases; meanwhile, the share of herbs grows in both the species number and quantitatively. At the age of 2 weeks, goslings eat a smaller amount of herbs and more willows and horsetails than adults; the selectivity and number of species eaten decrease (Rozenfeld et al., 2010). Transition to the adult diet lasts from 1 3 weeks depending on a type of habitat. Lesser White-Fronted Goose The nesting range previously extended from the Scandinavian to the Chukotka Peninsular and reached the taiga zone of eastern Siberia in the south. At the present moment, the range has broken into a number of small fragments, the majority of which have remained in the northern Ural Region, in the southern Yamal, Taimyr, and Putorana Plateau (Romanov, 2001, 2003), in northeastern Yakutia and Chukotka (Morozov and Syroechkovskii, 2002); 99.9% of the range is in Russia. The lesser white-fronted goose wintering in the Black Sea region, southeastern Europe, Greece, the southern coast of the Caspian Sea, Iraq, Iran, Syria, Turkey, and China (Aarvak and Øien, 2000; Tolvanen, 2000; Markkola, 2000; Markkola et al., 2000; Morozov, 2012).

ARCTIC GEESE (ANSER) AND BRANTS (BRANTA) OF EURASIA 443 At present, this is the rarest goose in Eurasia; it is on the verge of extinction. The population of the lesser white-fronted goose decreased from 100000 in the 1940s to 50000 in the second half of the 1970s. The current population is estimated at 35000 40000 (Morozov and Syroechkovskii, 2002; Rozenfeld et al., 2012; A.D. Fox, personal report). The lesser white-fronted goose is one of the smallest representatives of the Anser genus. Its small size allows it to arrive at the Arctic later, since small-size species (brants) have shorter periods of incubation and goslings development (Syroechkovskii, 2013). Although the lesser white-fronted goose is a small-size representative of the geese genus, it is much larger than brants. The period of goslings development in the lesser white-fronted goose is longer, and their growth is much less intensive. That is why the lesser whitefronted goose has not managed to penetrate into the high Arctic, and most of its range is confined to subarctic tundras and forest tundra, which are less rich in food, since plant xerophytization occurs faster here. Its relatively short neck and beak do not allow it to use the habitats that are suitable for larger species. The tendency to use natural feeding habitats in the greater part of the wintering area and at the migration route makes the lesser white-fronted goose dependent on their degradation and deprives it of the opportunity to use cultural plants in full measure. The lesser white-fronted goose nests in single pairs at fresh ponds with dense shrub thickets and sometimes in tundra. Solitary nesting increases the risk of nests being plundered by predators, so the lesser white-fronted goose tends to nest near the nests of predator birds (Morozov and Syroechkovskii, 2002), sometimes in the territory of red-breasted goose colonies (Rozenfeld, 2014). By feeding type, the lesser white-fronted goose is a mixed feeder; the beak index is 0.30. It eats 22 plant species from 11 families. Most of the ration consists of herbs, sedges, and horsetails (Fig. 1); grasses and willows are also consumed (Rozenfeld, 2009). The share of herbs, grasses, and horsetails in the ration of breeding birds is comparatively low, and its majority is constituted by sedges, including their previous-year stems, previous-year crowberries, and willows. Nonbreeding birds prefer herbs and grasses, and the consumption of sedges and crowberries is much lower in them. In the middle of summer, the lesser white-fronted goose turns to feeding on horsetail, pendant grass, dupontia, and grasses, which replace the sedges. The lesser whitefronted goose starts to breed, using a coarse nonnutritious food and with smaller fat deposits that accumulate in spring. The early plant xerophytization in the Subarctic determines the need for a constant change of feeding habitats in the period of brood rearing. Goslings of the lesser white-fronted goose eat a large amount of animal foods in the first days of life in suboptimal habitats, and horsetails account for a significant share among plant foods (Rozenfeld, 2002). As in adult birds, the basis of goslings feeding is herbs and sedges, and the major distinction is the larger consumption of horsetails and grasses by goslings (Fig. 1). In some regions, the share of willows in the ration of goslings is significant (Rozenfeld, 2009). The consumption of grasses grows in the third week and then decreases. The share of herbs constantly grows and they become the major food by the age of 4 weeks. The feeding ranges in adult birds and goslings at the age of 5 6 weeks already completely coincide (Rozenfeld, 2009). In optimal habitats, the diets of goslings and adults may be similar as early as a few days after hatching, and the diet of goslings differs only in the share of consumed groups of foods. At the age of 3 weeks, goslings completely turn to the adult diet (Rozenfeld, 2009). Emperor Goose The greater part of the range is in North America. The breeding range is represented by small fragments at the western and eastern coasts of the Bering Sea, at the coast of the Chukotka and East Siberian Seas to the west to the lower reaches of the Kolyma River, in the St. Laurence and Nunivak Islands. The species hibernates at the coast of North America from Alaska to California, in the Aleut, Kuril, and Komandor Islands and near the coast of eastern Kamchatka (Kondratyev, 1997; Syroechkovskii, 2000; Belobrov and Artyukhin, 2008). The winter part of the emperor goose range is located farther to the north than that of all other geese and brants, so the conditions of its wintering are notable for their severity and food poverty. The range shows a trend towards reduction. The population size has been decreasing in recent decades. It diminished in America from 139 000 in the mid-1960s to 42000 in the mid-1980s. The current population of emperor goose is estimated at 80000 90000. The summer population of emperor goose in Russia is 20000 30000, and the winter population is only several hundred (Syroechkovskii, 2011b; Waterfowl..., 2012). The emperor goose is a middle-size goose with a relatively short beak and short neck. The beak index is 0.40. As in the lesser white-fronted goose, these morphological properties determine an intermediate type of feeding. Its entire life cycle is confined to the seacoast; it is the only goose species that does not penetrate agricultural landscapes (Syroechkovskii, 2011b). In the winter feeding, including the period of arrival, a large role is played by the marine algae sought at silty shoals (Bailey, 1948; Fay and Cade, 1959). In wintering areas in the Komandor Islands, the emperor goose feeds exclusively with three types of algae. The emperor goose nests in single pairs at a large distance from each other in places with a good field of vision (Eisehauer and Kirkpatrik, 1977; Petersen, 1990). The nesting properties result in low breeding

444 ROZENFELD, SHEREMETYEV success: the absence of a male in the second half of incubation leads to the death of clutches and goslings due to predator attacks and unfavorable weather (Krechmar and Kondratyev, 2006). The feeding range is not plastic and is limited to several background plant species of coastal meadows and river valleys (Fig. 1). The species can feed on up to eight resource items (Rozenfeld, 2009). Goslings of the Emperor goose feed at saltish and fresh lakes at river mouths and coastal marshes. At coastal marshes goslings eat exclusively alkali grass, like adult birds. At fresh tundra lakes, the feeding range of goslings and adult birds is identical. At saltish lakes, the feeding basis of adult birds and goslings is formed by sprouts of pendant grass and dupontia, horsetails, and halophilic plants (Fig. 1). Here, goslings consume seven plant species up to the age of 2 weeks, i.e., more plant species than adult birds (Rozenfeld, 2009). Therefore, in optimal feeding habitats at coastal marshes, the diets of goslings and adult birds coincide, and transition to the adult diet in emperor goose goslings takes 2 weeks, at most, 2.5 weeks, in suboptimal tundra habitats. RESULTS AND DISCUSSION Anthropogenic Impact on Population Size and Range We should recognize that the considered characteristics make up a not very large number of the wellknown characteristics of geese and brants. Access to new data can change the idea of the variability of their population size and range. Analysis of the presented data and identified regularities lead to a conclusion about the large contribution of the anthropogenic factor to the variability of range and population size in the studied species. Its impact is so strong that it almost deprives us of the opportunity to reveal the true value of natural factors for the dynamics of population size and range. Over thousands of years, geese and brants were objects of hunting. Human influence in the past led to significant changes in the structure of ranges in some goose species. Thus, it resulted in the disappearance of the wintering areas of the red-breasted goose in the lower reaches of the Nile; its existence is witnessed by famous frescoes in the Meidum of the fourth dynasty (about 2720 B. S.) (Vinokurov, 1987); by the middle of the last century, the lesser snow goose populations in the tundras of northeastern Asia were completely extirpated; due to hunting in the period of moulting, the brent goose population on Kolguev Island was completely extirpated (Trevor-Battye, 1895); by the middle of the 20th century, the giant population of Baikal teal (Anas formosa) was almost reduced to zero. The currently observed expansion of the barnacle goose range is probably not a colonization of new habitats but a restoration of previously extirpated populations in this part of the range. Geese and brants were and are extirpated throughout their life cycle: nesting, autumn migration, wintering, and spring migration. In addition to direct extirpation, geese and brant populations suffer from a decrease in areas of safe habitats. In the breeding period, geese and brants usually occupy large territories in the regions of the north that are hard to access for people. In this period, the influence of extirpation is comparatively low, with the exception of some particular cases; for example, the emperor goose was extirpated during moulting (N.G. Ovsyannikov; E.E. Syroechkovskii, personal communication). In the regions where the local population practices the mass collection of eggs, breeding success has abruptly decreased in many colonial species. Father to the south, as early as during migration stops, geese and brants become more vulnerable. In the migration period, bird hunting, which is concentrated on a significant part of the population or the entire global population during migration stops in a limited territory (lesser white-fronted goose, red-breasted goose), can abruptly reduce their total population for only one season (Rozenfeld, 2010). Shooting deaths due to shooting among the species that migrate along seacoasts (barnacle goose? brent goose, emperor goose, snow goose, individual populations of Greater whitefronted goose and tundra bean goose) and/or within a small number of countries are much lower than in the species that make intracontinental migratory flights for several thousands of kilometers over the territory of the states, where hunting is permitted (lesser whitefronted goose, red-breasted goose, greater whitefronted goose, tundra bean goose). The greatest damage is done by hunting during spring migration, when many birds of reproductive age perish. The mortality caused by hunting in many cases supplements natural mortality rather than replaces it (Klaassen et al., 2005). The effect of the death of adult birds during spring migration is strengthened by the monogamy of geese and brants. Anxiety hinders the accumulation of fat, which is necessary for further migratory rushes (Mainguy et al., 2002; Klaassen et al., 2005). The influence of extirpation during autumn migration on population sizes is the weakest statistically: in autumn, the population size is usually higher, and damage to the reproductive part of the population is lower. The extirpation of geese and brants in wintering areas and/or a decrease in the area of suitable habitats are so significant that they cannot but affect population sizes. First, the area of habitats that are able to provide feeding resources to wintering geese and brants is initially much smaller than the area of habitats in nesting sites and continues to decrease. Second, wintering habitats are less safe, which is primarily due to the greater density of human population in the countries where they are located. In addition, wintering areas have, for the most part, been transformed and are used for agricultural purposes. Therefore, in

ARCTIC GEESE (ANSER) AND BRANTS (BRANTA) OF EURASIA 445 Population, thous 7500 5000 2500 750 500 250 75 50 25 1950 1970 1990 2010 Brent goose Barnacle goose Red-breasted goose Tundra bean goose Greater White-fronted goose Lesser snow goose Lesser white-fronted goose Emperor goose Fig. 2. Population size in arctic geese and brants and trends in its change. order to increase the population of geese and brants, it is necessary to raise the capacity of the environment in wintering places, whereas it is sufficient in nesting sites and at migration stopovers to stop extirpation. In theory, this can be done either by enlarging the area of natural habitats (creation of reserves), where geese and brants can safely feed in winter, or by increasing the specific amount of feeding resources. The former is hard to imagine in the densely populated regions of Eurasia and North America. The latter, as one might expect, has taken place on its own due to the transition to feeding on cultural plants in most goose and brant species. Agricultural landscapes in wintering places have large reserves of standing food plants with a high nutrient value or remains of gathered harvests. The populations and species as a whole that can turn to these new resources are relatively safe and growing in abundance (Europe, America), but those that do not have this opportunity are in decline (Asia). However, independently of the regional situation in the protection of geese and brants, there are the species that have completely (emperor goose) or partially (lesser whitefronted goose, brent goose) failed to turn to feeding on cultural plants in wintering areas (Sterbetz, 1978; Fox et al., 2008; Panagiotopoulou, 2009; Syroechkovskii, 2011a; Dalloyau, 2012; Clausen et al., 2013; Elkinton et al., 2013; Wang et al., 2013). Their relatively small population size is partially explained by this confinement to natural habitats and feeding resources during wintering. Comparison of Population Size and Range Extent The ratio of the studied geese and brants with respect to their current abundance corresponds to the concave distribution curve. The variance in the abundance of the studied geese and brants has been significant in recent decades (Fig. 2). The trends in these changes for the considered period show that they cannot be explained in most species, even by very prolonged population fluctuations. In monitoring the abundance of geese and brants, the dynamics of population size are usually characterized by long-term trends (Scott and Rose, 1996; Baldassarre and Bolden, 2006; Fox et al., 2010; Waterfowl..., 2012). The scheme of collected variables is described in the table. The lesser white-fronted goose and emperor goose populations and the total population of western and eastern tundra bean goose are characterized by a well-marked trend towards reduction; for most of other species, there is a trend towards growth (Syroechkovskii, 2006). The growth is the most intensive for the populations of lesser snow goose and barnacle goose, whereas the increase in the red-breasted goose and greater white-fronted goose populations is less noticeable. The abundance decreases mainly at the expense of Asiatic populations and, to a lesser extent, western populations, whereas the abundance in North America is growing (Waterfowl..., 2012). The growth in western populations in Eurasia since the middle of the 20th century is due to the combination of stringent protective measures and new agricultural technologies of western Europe, which have largely heightened the yield and food value of agricultural crops. On the one hand, the amount of food resources for wintering geese and brants has largely grown, and, on the other, protection has increased their availability (Ebbinge, 1985; Fox et al., 2010; Johnson et al., 2014). Before this, the European populations for the most part showed a trend towards reduction, which became more noticeable in the middle of the 19th century (Mooy, 2010). In the United States, Canada, and Mexico, the action of special state population management programs and projects with a use of a flyway as a territorial management unit has provided an even greater effect (Baldassarre and Bolden, 2006; Waterfowl..., 2012). The Asiatic populations on the contrary have been experiencing decline, which has become catastrophic for many species, since the 1980s (Syroechkovskii, 2006; Andreev, 2009). Among the major causes, we can mention the agricultural development of water and marsh habitats in the countries with wintering areas and barbaric hunting at migratory routes and wintering areas. To the east from the Yenisei, a large number of birds are killed at places of stops during spring migration (Syroechkovskii, 2006; Andreev, 2009), at wintering areas and along migratory routes to China, where meshes, poisons, explosives, and electricity are used (Syroechkovskii, 2006; Cao et al., 2008). The size of populations is largely related to the extent of nesting range. We believe that the extent of