The Snowy Owl 9781472597557, 9780713688177

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List of Figures CHAPTER 1 Figure 1.1.

Female Snowy Owl satellite-tagged on Bylot Island, Nunavut, Canada.

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Figure 1.2.

Three consecutive secondary feathers of an adult female Snowy Owl.

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Figure 1.3.

A general model of the possible age- and sex-related variation in spottiness of Snowy Owls.

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Figure 1.4.

S4 feather of a young Snowy Owl (male and female).

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Figure 1.5.

Wing loading (g/cm2) plotted against body mass (g).

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Figure 1.6.

Differences between tarso-metatarsus of Eurasian Eagle Owl and Snowy Owl.

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Figure 1.7

Differences between the skulls of the Eagle Owl, Snowy Owl and Great Horned Owl.

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Figure 1.8

Brain volume of the Strigiformes.

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Figure 1.9.

Reflectance of black and white patches of feathers from different plumage 43 regions in males and females.

Figure 1.10.

Mean (±SD) of total brightness (above) and VIS-Chroma (400–700nm) (b) of white and black patches of Snowy Owls in feathers from different body regions.

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Figure 1.11.

Snowy Owl as seen by conspecifics and by UV-VIS sensitive birds.

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Figure 1.12.

Left: Reflectance of snow (measurements taken at Svalbard). Right: Reflectance of the winter coat of the Arctic Collared Lemming Dicrostonyx torquatus.

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Figure 4.1.

Snowy Owl nest on bare ground amidst snow cover, Lower Kolyma, Russia.

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Figure 4.2.

Territories of the Snowy Owls in the southern part of the Lower Konkovaya Study Area.

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Figure 4.3.

Typical alas at Malaya Konkovaya in the Kolyma lowlands.

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Figure 4.4.

Aerial view of the Kolyma delta.

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Figure 4.5.

Willow shrub along a river.

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CHAPTER 4

CHAPTER 5 Figure 5.1.

Left: Spectrogram of a hooting male, Lower Konkovaya, north-east Siberia. Right: Cackling ka-ka-ka-ka call of a female, northern Taymir (Veprintsev 2008).

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Figure 5.2.

Displaying male, Malaya Konkovaya River, Lower Kolyma, Siberia.

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Figure 5.3.

Snowy Owl nest scrape.

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Figure 5.4.

Increase of the egg laying interval with the number of eggs produced.

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Figure 5.5.

Hypothetical egg laying sequence of a clutch of 8 eggs.

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Figure 5.6.

Latitude .v. date of laying of first egg.

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Figure 5.7.

Clutch size of the Snowy Owl from all available sources.

Figure 5.8.

Egg weight during incubation in two nests.

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Figure 5.9.

Female Owl returning to her nest.

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Figure 5.10.

Activity pattern of observed Snowy Owl pairs during the incubation period.

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CHAPTER 6 Figure 6.1.

Body weight growth in male and female Snowy Owl chicks.

Figure 6.2.

Tarsi growth in Snowy Owl chicks.

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Figure 6.3.

Skull growth in Snowy Owl chicks.

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Figure 6.4.

Beak growth in Snowy Owl chicks.

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Figure 6.5.

Wing growth in Snowy Owl chicks.

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Figure 6.6.

Changes in wing loading in Snowy Owl chicks.

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Figure 6.7.

Growth of rectrices in Snowy Owl chicks.

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Figure 6.8.

Asymptotic growth of Snowy Owl chicks.

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Figure 6.9.

Speed of growth of Snowy Owl chicks.

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Figure 6.10.

Chick during ‘white mask’ stage of development.

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Figure 6.11.

A. Maximum difference in body weight (in grams) between broods plotted against age of the oldest chick. B. Maximum difference in body weight (in grams) of broods plotted against brood size.

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Figure 6.12.

Temperature of Snowy Owl chicks after 5–15 minutes’ exposure to ambient temperatures ranging from 5–10.5°C.

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Figure 6.13.

Oxygen consumption of chicks of different ages at different temperatures. 130

Figure 6.14.

A: Changes of BMG and B: Variation of Lower Critical Temperature with age in Snowy Owl chicks.

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Figure 6.15.

Gross Energy Intake, Metabolised Energy, BMG, and Excretory Energy at different ages (kJ/day).

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Figure 6.16.

Consumption rate of a chick (males and females averaged). A: of a single chick. B: for brood sizes 2–14.

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Figure 6.17.

Total number of lemmings needed for a brood of various sizes.

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CHAPTER 7 Figure 7.1.

Skull dimensions used to calculate the weight of rodents eaten by the owls using formulae given in Table 7.2.

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Figure 7.2.

Winter runs of the Siberian Lemming revealed after snow melt.

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Figure 7.3.

Distribution of body weights of Siberian Lemmings in the diet of parents and chicks, Konkovaya study area, 1987.

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Figure 7.4.

Snowy Owl with captured Peregrine Falcon, Logan International Airport. 155

Figure 8.1.

Snap traps on lemming runs.

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Figure 8.2.

Cotton-grass tussocks on a gentle slope.

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Figure 8.3.

Cotton-grass tussock and tussock formation.

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Figure 8.4.

Location of cotton-grass beds in the study area in the year of their maximum seed-dispersal period.

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Figure 8.5.

Numbers (N) of seed heads and wintering flower buds in a sample plot of 11.82m2.

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Figure 8.6.

Average body weight of Siberian Lemmings in the Malaya Kolyma study area.

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Figure 8.7.

Body weight variation of the Siberian Lemming during a summer.

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Figure 8.8.

Distribution of Siberian Lemming body weight during a summer.

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Figure 8.9.

Distribution of the body weight of Siberian Lemmings in the Lower Kolyma over the study years.

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Figure 8.10.

Relationship between age and body weight in Siberian Lemmings.

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Figure 8.11.

Age of Siberian Lemmings in the Konkovaya study area.

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Figure 8.12.

Age distribution of Siberian Lemmings during a summer.

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Figure 8.13.

Survival of Siberian Lemmings in different years.

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Figure 8.14.

A 3D plot of survival rates of Siberian Lemmings in the Lower Kolyma study area.

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Figure 8.15.

Population Density of Siberian Lemmings at the study areas.

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Figure 8.16.

Feeding places for Siberian Lemmings under snow, as revealed by their melted tracks and runways.

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Figure 8.17.

Schematic representation of winter habitat quality and lemming abundance. Arrows show seed dispersal events.

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Figure 8.18.

Population density of Narrow-skulled Voles and Siberian Lemmings in different years.

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Figure 8.19.

Mean body weight of Narrow-skulled Voles during successive years.

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Figure 8.20.

Distribution of body weights of Narrow-skulled Voles during the summer months.

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CHAPTER 8

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Figure 8.21.

Breeding intensity in Narrow-skulled Voles as observed in body weight distribution of the population.

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Figure 8.22.

Variation of mean body weight of Middendorff ’s Voles during successive years.

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Figure 8.23.

Population density of Middendorff’s Voles during successive years.

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Figure 8.24.

Population density of Collared Lemmings during successive years.

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Figure 8.25.

Population density of small mammals during successive years.

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Figure 8.26.

Fluctuations of population density in all mammals of Lower Kolyma tundra in successive years.

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Figure 8.27.

Fluctuations in biodiversity index resulting from population changes of Figure 8.26.

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Figure 8.28.

Average body weight of all small mammal species in successive years.

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Figure 8.29.

Distribution of body weight of all small mammal species in successive years.

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Figure 8.30.

Numeric response of the Snowy Owl to lemming density.

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Figure 8.31.

Average brood size reduction.

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CHAPTER 9 Figure 9.1.

Percentage of study skins procured within the Snowy Owl breeding range by month.

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Figure 9.2

Snowy Owl at Logan International Airport.

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Figure 9.3.

Migration patterns of tracked birds from Logan International Airport.

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Figure 9.4.

Migration patterns of all tracked birds.

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Figure 9.5.

Latitude of migrating Snowy Owls equipped with satellite monitors.

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CHAPTER 10 Figure 10.1.

Species diversity index for small mammal species and their predators.

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Figure 10.2.

Relative abundance of small rodents by weight cohort, and breeding of most abundant avian predators in the Lower Kolyma study area.

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Figure 10.3.

Distribution of body weight of Siberian Lemmings consumed by the three co-existing predator species in the Konkovaya study area in 1987.

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Figure 10.4.

Body weight distribution of lemmings eaten by parents and chicks of Short-eared Owls, Snowy Owls and Rough-legged Buzzards co-existing in the Malaya Konkovaya study area in 1987.

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Figure 10.5.

Snowy Owl attacking an Elk (moose).

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Figure 10.6.

Snowy Owl chick pestered by mosquitoes.

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Figure 10.7.

Female Snowy Owl in distracting posture.

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Figure 10.8.

Remains of a male Snowy Owl killed by either a Golden Eagle or a Gyrfalcon.

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CHAPTER 11 Figure 11.1.

Figure of a Snowy Owl from Le Portel Cave, France.

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Figure 11.2.

The Sorcerer, a figure from the Trois-Frères Cave, France.

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Figure 11.3.

Position of caves in south-west France with Snowy Owl remains.

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Figure 11.4.

Number of live Snowy Owls exported. All countries combined.

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Figure 11.5.

Female Snowy Owl confiscated at Customs at Magadan, Russia.

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List of Tables CHAPTER 1 Table 1.1

Snowy Owl dimensions (lengths in mm, weights in g).

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Table 3.1.

Comparison of the characteristics of Bubo and Nyctea.

Table 6.1.

Growth parameters of the Snowy Owl.

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Table 6.2.

Daily time and energy budgets of Snowy Owls.

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Table 7.1.

Percentage of damaged bones in the pellets of captive Snowy Owls.

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Table 7.2.

Regression equations for calculating body weight from dimensions of skull bones and other skeleton elements.

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CHAPTER 3 61

CHAPTER 6

CHAPTER 7

CHAPTER 8 Table 8.1.

Patterns of productivity of cotton-grass in the Malaya Konkovaya study area.

Table 11.1.

The distribution of Snowy Owl bones on Magdalenian sites in South-west France.

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CHAPTER 11 242

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Introduction The Snowy Owl (Nyctea scandiaca) is a mysterious bird, a large (wingspan to 1.8m in adult females, 1.6m in adult males, weights to almost 3kg in adult females) Arctic dweller, one of the very few avian species which regularly overwinters in the area. Though many Snowy Owls head south from their Arctic breeding grounds, some remain throughout the winter, surviving temperatures which drop below -40°C and hunting during the darkness of the Arctic winter as efficiently as they did during the 24 hour day of the Arctic summer. The enigmatic nature of the species has resulted in almost every bird enthusiast who has encountered it feeling obliged to write a short note on that encounter. As a result, the literature has thousands of references, all of which have to be read and reviewed so that precious drops of information can be extracted. In particular, the process of extracting data from accounts, often small accounts, on winter sightings of the owl in the temperate zone has resembled gold panning: it has taken us more than two years to do so, and we wonder whether, in the absence of internet technologies, the task would have been possible at all. But not all accounts are the result of chance encounters; important work carried out on the native grounds of the species has resulted in good records of the owl’s biology. Given the difficulties of reaching, and the problems of working in, the remote, climatically harsh areas where Snowy Owls reside, we consider it essential that we place on record our debt to those we consider the more important of these workers.

THOSE WHO HAVE STUDIED SNOWY OWLS Oleg Vasilievich Egorov (1921–1971) was a legendary figure in the study of northern zoology. He was head of the Zoology Department of the Yakutian Institute of Zoology and while there he carried out the first aerial surveys of Snowy Owls across a land area exceeding the size of western Europe. He was first to give quantitative data on the distribution of the owls on continental and island tundras, and was first to conclude that the island population of the species was 20 times more dense than that of the continental tundras (Egorov 1971). This conclusion had previously been suspected by Leonid Portenko (1972a), who studied the species on the Wrangel Island and wrote numerous publications on Arctic birds including a book on the Snowy Owl (Portenko 1972). Portenko’s research (1896–1972) was aided by the observations of Aref Ivanovich Mineev (1900–1973), second Director of the newly established settlement on Wrangel Island, who spent five years on the island (1929–1934). In 1979 two scientists from the Institute of the Biological Problems of the North, Arseniy Krechmar and Igor Dorogoy initiated studies of Snowy Owls, these studies becoming the longest (although not continuous) monitoring within a guaranteed breeding range of the species (Krechmar and Dorogoy 1981). The interaction of lemmings and rodent-eating animals on Wrangel Island was the PhD project of Igor Dorogoy, and resulted in a book (Dorogoy 1987). His studies ended in 1983, but the work was taken over by the Science Department of the Wrangel Island Zapovednik (Strict Nature Reserve). This Nature Reserve was established in 1976 due to the efforts of the Magadan Institute of the Biological Problems of the North (IBPN). Later, the studies of Wrangel’s Snowy Owls were continued by K. Litvin and V. Baranyuk (1989), and from 1986 to the present day by Irina Menushina (Menushina 2003, 1997, 2007).

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The Snowy Owl

Through to the first decade of the 21st century Menushina has amassed data on around 1000 nests (and counting) – an unheard of achievement! It is to be hoped that the studies on Wrangel will long continue. While a student at McGill University financed by the Carnegie Arctic Program, Adam Watson (born 1930) – a Scottish ornithologist and environmentalist with an enormous spread of expertise – provided a splendid account of Snowy Owl breeding at the Baffin Island, Canada. Watson’s expedition to the island lasted four months. Camping and travelling by dog sled with Samo, an Inuit trapper, in an area now known, thanks to their journey, as Owl Valley, at Paddle Fjord. Watson observed 11 Snowy Owl pairs (with 8 nests discovered and further information on 10 more nearby nests) during the peak lemming year of 1953 (Watson 1957). Watson’s eight studied nests are probably the most famous and best studied Snowy Owls in the world (due in large part to the obscurity of Russian studies), and the impact of his study on the scientific community cannot be overstated: no major book on owls can be completed without a reference to Adam Watson’s seminal paper. The famous naturalist, ornithologist and conservationist Robert Tulloch found a Snowy Owl nest on Fetlar, a rather small island in the Shetland Islands off Britain’s northern coast. Fetlar was the first, and to date the only, known breeding place of the species in the British Isles, the owls’ successful breeding over a short number of years putting the island on birdwatcher’s and ornithologist’s maps forever. The discovery generated huge publicity: a Nature Reserve was set up around the nest and the UK’s Royal Society for the Protection of Birds (RSPB) organised round-the-clock watches of the nest, which were maintained by more than 30 recorders who monitored the activity of the owls from a hide at a distance of 100m as well as protecting the nest from would-be egg collectors. The records of these ‘nest guards’, as well as Tulloch’s own thorough observations were incorporated into a paper (Tulloch 1967) which generated considerable interest and was cited by many authors (including the present ones). Later, Robinson and Becker (1986) summarised all records for the entire breeding event (1967–1975). The paper offered one of the great ironies of Snowy Owl research: that the most unusual and southerly of Snowy Owl nests is the most thoroughly observed and described nest in the world, and the one for which there is the longest continuous (and published) record of observations. The prominent US ornithologist and artist George Sutton (1898–1982) studied Snowy Owls at Baffin Island’s Frobisher Bay in the peak lemming year of 1953 (Sutton and Parmelee 1956) in the same year Adam Watson made his studies on the island. Sutton’s list of publications is enormous, with many interesting references to the species. For example he was the first to note that cars might pose a danger to the owls (Sutton 1927), well before the numbers of cars had reached the present dangerous levels. The University of Oklahoma named its centre of avian research in his honour. Besides his own publications on Arctic birds, George Sutton was also the supervisor of David Parmelee (1924–1998) who was equally interested in the species, and was the sole author of the Snowy Owl entry in ‘Birds of North America’ (Parmelee 1992), one of the foremost accounts of the species. In 1992 Denver Holt, a noted owl biologist, initiated a Snowy Owl Project at Barrow, Alaska and this ongoing work has resulted in several publications, covering not only the Arctic breeding grounds, but also the wintering owl population in Montana. In comparison to the research of the Snowy Owl pioneers mentioned above, our own research in the field is limited, though it has been gathered during Arctic trips and seasons which cover a combined total of around 30 years. Eugene Potapov (EP) worked in the field between 1982 and 1992 at several sites in the Lower Kolyma River area of north-east Siberia, all of them very similar ecological entities, namely typical tundra subzones. Snowy Owls bred in the study area in 1983 and 1987 when there were major population peaks of lemmings and

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Introduction

other small rodents. EP’s primary study area was the lemming cycle and the relationship of the rodents to their main predators. Information gathered in the field studies was later developed into a DPhil thesis at Oxford University’s Edward Grey Institute for Field Ornithology. Space limitations required the thesis to concentrate on a single species (the Rough-legged Buzzard), but other raptors, including Snowy and Short-eared owls, Gyrfalcons and Peregrine Falcons were also studied and the work led to numerous relevant publications, as mentioned in the text and bibliography. Richard Sale’s (RS) PhD is in a different field altogether (physics) but since transferring to the study of the Arctic and its species he has produced the first field guide to birds and mammals of the area (Sale 2006) and a complete guide to the Arctic (Sale 2008). The shared interest of the authors in the Gyrfalcon led to an earlier joint monograph on that species (Potapov & Sale 2005). Besides their own interest in the Arctic and its species, this book was also influenced by the enthusiasm of the Norwegian Snowy Owl team (Roar Solheim, Karl-Otto Jacobsen and Ingar Øien) whose research in Scandinavia was instrumental in the understanding of many features of the Snowy Owl’s biology. Production of this book has been an enormous pleasure for both authors, allowing them to relive moments of magic on the tundra when the Snowy Owl, that most magnificent of owls (indeed that most magnificent of birds), was in view. A bird adapted to survive not only the harshness of the Arctic summer – which though more hospitable than many imagine, can still be bleak on occasions – but also the frequently pitiless Arctic winter. But the production would not have been possible without the help of many people, too many to mention them all by name, particularly as the risk of omitting someone by accident is too high. We wish to thank them all. However, it is essential that we thank certain individuals whose help was instrumental in making this book possible. Dr S. Zimov and Dr S. Davydov of the Cherskiy Research station of the Pacific Institute of Geography, Russian Academy of Sciences, and Mr S. Kasyanenko and Yu.Vlasenko, topographers of the tundra who were instrumental for the field studies at the Kolyma Lowlands. Dr Alexander Andreev of IBPN, Magadan, was a mentor of one of the authors, and is thanked for his advice. Valentin Khlestkin assisted one of the authors in raising Snowy Owl chicks in the field camp and subsequently looking after them in captivity. We also thank Igor Dorogoy, Irina Menushina, Nikita Ovsyannikov, Vladimir Pozdnyakov, Arseniy Krechmar, Alexey Estafiev, Maria Gavrilo, Per Michelsen, Karl-Otto Jacobsen, Tom McDonald, Dan Zazelenchuk and other members of the Saskatchewan Snowy Owl trapping team. Jevgeni Shergalin was extremely helpful with obtaining some obscure literature. David H. Johnson, the Director of the Global Owl Project supplied a superb collection of papers on Snowy Owls and was kind enough to find some important and rare papers for us. Roald Potapov was very kind in helping us with certain Russian literature. We thank Olga Potapova for her very considerable help with the section of the book dealing with the palaeobiogeography of the Snowy Owl, Anne Eastham for the box on the Magdalenians and Snowy Owls, Gary Bortolotti and Marten Stoffel for the box on plumage coloration, and Norman Smith and Mark Fuller for the box on the Bostonian Snowy Owl migrations. We thank Andy Bennett (then at Bristol University, UK) and his colleagues for the opportunity to study UV/VIS reflectance of the Snowy Owl plumage, the Royal Society of London for financing a Visiting Fellowship at Bristol for EP, and the faculty of the Bryn Athyn College, Pennsylvania for their assistance to EP also. Thanks too Robert Prys-Jones and his colleagues of the Bird Group of the Natural History Museum at Tring, UK. Finally we thank Jim Martin at T&AD Poyser and Lisa Carden for their patience and perseverance, and Helen Knight for her meticulous editing.

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The Snowy Owl

Very special thanks go to Gary Bortolotti whose untimely death was announced as the final manuscript of the book was being prepared. Gary organized a meeting of the Snowy Owl Research Group in Saskatoon, 16–21 Feb which greatly aided the authors. He also co-authored the Box on Snowy Owl plumage in Chapter 1 of the book. We thank Alexey Berzukov, Igor Dorogoy, Olivier Gilg, Karl-Otto Jacobsen, Per Michelsen, Irina Menushina and Roar Solheim for the use of photographs. All unattributed photographs in the book were taken by the authors.

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CHAPTER 1

What makes a Snowy Owl? The Snowy Owl was undoubtedly known to early humans living in the high latitudes of the northern hemisphere. It had local nicknames – the Scandinavian Nightbird, the Highland Tundra Owl, Ghost Owl, Ermine Owl, Tundra Ghost, and the White Terror of the North – and occasionally these names can be picked out of old literature, folk tales and songs. The Inuit called it Ookpik, the Yupiks Anipa and the Kuskovim dialect name is Yismo with the Sámi calling it the Skuolfi. In Russia it was the Belaya sova (white owl), in Norway the Snøugle, in Iceland Snæugla and in Sweden it was known as the Fjälluggla. Further south it was the Comhachag gheal in the Gaelic language of Scotland, Sowa s´niez´na in Poland and, in Denmark, it was the Sneugle. South again the Dutch called it the Sneeuwuil, the Germans the Schnee-Eule, the Spanish the Búho Nival and the French the Harfang des Neiges. In Finnish the name of the Snowy Owl is Tunturipöllö; in Welsh Tylluan yr Eira; in Hungarian Hóbagoly; in Irish Ulchabhán Sneachtúil; in Portuguese Bufo-branco. To the east it was the xue˘-xia¯o to the Chinese and the shiro-fukuro¯ to the Japanese. Most of the names translate simply as Snow or Snowy Owl, and it is by that name it is now most commonly known across the world. The English name is believed to refer, not to the Arctic habitat of the bird, but to its colour (Roads 1912). Among the owls, the Snowy is the only one with a predominantly white plumage: unlike some other Arctic birds it does not moult to follow the changing background coloration of the tundra, having, as do all other owls, just a single plumage type.

FIELD CHARACTERISTICS AND APPEARANCE The Snowy Owl is a bird like no other: it is both a typical and an atypical owl. Originally considered to have been autochthonous for the Arctic (i.e. to have evolved there), it did not: it is large, yet r-selected (i.e. opportunistic breeder capable of taking advantage of increases in prey number); it is both cryptic and conspicuous; it has the rather slow life-style of other owls, yet it is capable of deadly, falcon-like, stoops; it is both shy and fearless; it can eat greedily or it can fast for long periods. The Snowy Owl is the owl of extremes. Among the world’s bird species

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The Snowy Owl

there are few which cannot be mistaken for another species. The Snowy Owl is close to the top of that list. It is so recognisable that people living in the tropics, as well as in sub-tropical islands, have no problem in identifying it (though, it has to be admitted that recognition is aided not only by its coloration, but to the success of the Harry Potter films which have made the bird among the most recognisable species on the planet). Yet, in its native Arctic habitat in winter, thanks to its coloration, the visual limitations of humans and the darkness of the polar night, it is one the world’s most mysterious species.

GENERAL DESCRIPTION Plumages, ageing and sexing Snowy Owls are robust, with a more or less sleek plumage, not the fluffy feathering of some other Strigiformes. On the tundra the bird spends most of its time perched on flat ground, usually at the boundary of a tundra polygon (i.e. the patterned ground formed by annual freeze-thaw of soil) or on a gentle slope. It is then a typical owl, the head held high, the body straight, the tail down, so that, as Holland (2004) noted, it looks rather like a Russian doll. When incubating, that shape disappears with only the top of the head visible, the eyes watching you, like a brave soldier in a trench. Ear-tufts can be added to each picture, though these are not visible at all times. Each ear-tuft consists of 10–12 tough feathers and is occasionally erected while the bird is flying, something almost unknown in other eared-owl species, e.g. the European Eagle Owl Bubo bubo and the Great Horned Owl Bubo virginianus. On the perched bird the ear-tufts are clearly visible only when the head is brought close to the body. If alerted and in visual contact with the source of danger (e.g. a human), the ear-tufts are not visible, the feathers on head and body being sleek and tight. Most owls have special adaptations for silent, stealthy flight, particularly the serrated fringes along the front vanes of the primaries that have comb-like structures. These are present in some places on the outer primaries of Snowy Owls, but they are much less developed than those of Eagle and Great Horned and the Long-eared Asio otus owls. A carpet of extended barbules on the upper surface of the primaries and some other vaned feathers is also present, but these are evidently not as well developed as those of forest-dwelling species. This carpet, extending along the top of the vane, damps the flapping noise of the vanes touching each other, and is unique to owls, nightjars and harriers. However, in Snowy Owls the carpet is apparent only on the primaries, and only where the primaries overlap, a significant difference from Great Grey Strix nebulosa, Eagle and Great Horned owls. The fact that the noise-reduction serrations on the leading edge of the primaries are so greatly reduced means that a Snowy Owl stooping on a human is audible as a ‘flat’ noise due to the turbulence around the wings: the noise can be heard most clearly during the attacks of a male. Snowy Owl plumage is generally white, but this statement has to be treated with caution as it is a subjective definition based on human perception as we shall see when we deal with plumage coloration in detail later. There are varying degrees of the black barring on this overall white ground colour. In general it is considered that pure white, or mostly white birds are males, while heavily barred individuals are females. Although the majority of the world’s owls do not display sexual dimorphism in plumage, Snowy Owls are an exception, with differences between the sexes in both overall coloration and the amount of barring. Occasionally almost totally white males are seen, these having just a few dark spots. One such, white apart from a few dark spots, is in the collection of the British Museum of Natural History, Tring.

20

What makes a Snowy Owl?

Out of 129 adult male specimens at the Zoological museums of St Petersburg and Moscow University, and the collection at Russia’s Oka Nature Reserve, there are only three pure white individuals (‘pure white’ here meaning an insignificant number of black spots). A further 19 birds have some black spots (up to 10% of the surface), 48 individuals have a large number of black spots, while 17 individuals with a very large number of black spots appear similar to female owls. However, only 2% of this sample of Russian specimens were older adults (Gavrilov et al. 1993). The majority of males have a limited amount of barring on the wing coverts and the breast. Females have significantly more barring on the head, tail, breast, and wing coverts, and in general look very spotted. Females usually have four to six bars on the tail, whereas the males have from none to three (Mikkola 1987; Portenko 1972, 1972a). The fine bars on the male underparts are narrower than 3mm, but in females they are much wider (Portenko 1972, 1972a). Josephson (1980) reviewed these measurements and found that the width of ventral barring was less than 2.5mm (mean 1.6mm) in adult males; 1.8–2.8 mm (mean 2.2mm) in first year males; 2.8–3.6 mm (mean 3.2mm) in adult females; and 2.8–4.5mm (mean 3.8mm) in first year females. The density of ventral barring measured as the number of bars per ventral feather also showed statistically significant differences between the sexes. In adult males it varied from 0–1.3 (mean 0.8); in first year males the range was 2.4–4.5 (mean 3.3); in adult females it was 3.1–5.4 (mean 4.1); and in first year females 4.0–5.9 (mean 4.8). The age of the owls was determined by the measurements of the Bursa of Fabricius (see Box). There was an overlap between first year males and adult females, and adult females and first year females in this trait. However, later data on the ageing of Snowy Owls, from ringed individuals, have contributed some new insights (see Box by Bortolotti and Stoffel). Portenko (1972a) noted that in worn plumage the barring faded significantly due to bleaching.

THE BURSA OF FABRICIUS The Bursa of Fabricius (also known as Bursa cloacalis or Bursa fabricii) is a specialised epithelial and lymphoid organ found only in birds. It is believed to play a very important role in the development of B-cells (bursa-derived cells). It comprises a dorsal diverticulum of the proctadael region of the cloaca. In the bursa, stem cells acquire the characteristics of mature, immuno-competent B-cells. With age, the Bursa of Fabricius retracts. The rate of retraction was considered to be constant and was widely used in wildlife management of some species (mostly waterfowl) to age the birds, but is now less often used as it requires the bird to be in the hand, and remote or non-invasive techniques are preferred. Keith (1960) measured the length of the Bursa of Fabricius in 13 young Snowy Owls trapped during the winter of 1957/58 at Delta, Manitoba, Canada. He found that the Bursa of Fabricius shrank at a rate on 0.28mm per day. With such a rate of regression the Bursa of Fabricius would be completely resorbed by the end of April. Josephson (1980) wrote a detailed account on the ageing and sexing of the Snowy Owls based on the bursal lengths and the results of the anatomical dissections of 33 specimens. Bursa length was used as an indication of first year status. Wing cord and tail length proved to be a reliable way of sexing Snowy Owls as long as the measurements did not fall between 398–404mm and 219–221mm for wing and tail respectively. If the measurements fall into these categories, other methods of sexing should be used.

21

The Snowy Owl

THE COLORATION OF SNOWY OWLS IS NOT SO BLACK AND WHITE by Gary R. Bortolotti and Marten Stoffel Can a leopard change its spots? Perhaps not, but new evidence suggests a Snowy Owl can. Snowy Owls are an unusual species compared to other owls in that they are extremely variable in coloration. They may be absolutely white or have as much black in their feathers as white (Plate 1.1). Most species of owls show very little difference in appearance between the sexes, or between young and old birds, whereas it is generally accepted that male Snowy Owls are less spotted than females and adult birds are less spotted than juveniles (Josephson 1980; Parmelee 1992; Pyle 1997). Some authors have claimed that four unequivocal age/sex classes exist (Kerlinger and Lein 1986), but it is more correctly acknowledged that the darkest males and the lightest females cannot be distinguished (Parmelee 1992). In fact the problem of ageing or sexing the birds is much more complicated. Snowy Owls of any age show substantial individual variation in the proportion of black spots or bars in the plumage. Only the Barn Owl Tyto alba shows noticeable sex dimorphism in addition to conspicuous variation among individuals in degree of spotting and amount of white on the body. However, the variation in Barn Owls is known to be genetic (Roulin et al. 1998), whereas in the Snowy Owl there is proof that individual coloration is not so fixed and is influenced by the environment. It is also commonly believed that Snowy Owls become whiter as they age, so that only the oldest males can be pure white. While this may be true, it is actually more speculation than scientific fact. Our ten-year study of capturing wintering Snowy Owls in Saskatchewan, Canada, has shed some light on the question of factors influencing coloration in the species. The prairies of western Canada hold the densest winter population of Snowy Owls in North America (Kerlinger et al. 1985). Together with Dan Zazelenchuk, we captured 222 owls: roughly 60% were females, and 75% of the birds were older than one year. First we made sure we could sex the owls correctly on size (sex confirmed by analysis of DNA from 70 feather samples by Juan J. Negro at the Doñana Biological Station in Seville, Spain). We then determined that the birds could be aged to at least their first few winters from patterns of wing moult. It is not uncommon for three years to pass before all the feathers of a wing are replaced. It was not a surprise to find that males did indeed have fewer spots than females, and juveniles were more heavily marked than older birds (Plate 1.1). However, the large degree of overlap in spottiness means that many individuals cannot be aged or sexed with certainty. Fortunately, the sexes appear to differ in the shape of the brown dots on the wings, which might be useful in birds at close range and in the hand. Denver Holt (USA) and Irina Menyushina (Russia) have developed promising sexing criteria by identifying that males have spot-shaped and females more bar-shaped pigmented areas. We found that the extent of the terminal brown/black band on the tail differed consistently between males and females: the brown always extended from edge to edge of the feathers in females, whereas in males it always stopped short of the edges. Documenting differences in plumage of the age classes (juvenile v. adult) and sexes only takes us so far in explaining the colour variation in the species. Is variation within an individual bird over time also a factor? Do individuals get whiter with age as is generally believed? We explored this in two ways. First we had the good fortune of recapturing or recovering birds that had been ringed in a previous year and so had replaced feathers during moult. Using photos, we compared the tail, wing and body spotting of the birds in the current year to those from

22

What makes a Snowy Owl?

Figure 1.1. Female Snowy Owl satellite-tagged on Bylot Island, Nunavut, Canada in 2007 as seen in late winter of 2008 and 2010 (photographs by M. Stoffel). up to five years previously. For four males, three had wings, two had tails and one had a body somewhat more spotted in the most recent plumage. In one male the body was deemed to be slightly less spotted and all other comparisons were said to have about the same number of spots. For five females, the changes over time were much more noticeable. One set of wings, one tail and three bodies were conspicuously more spotted in the most recent moult compared to the one before. Only one set of wings and one tail showed a minor degree of whitening over time. Another clear example of a bird’s ability to become darker over time was provided by a female Snowy Owl marked with a satellite transmitter by Jean-François Therrien of Laval University, Quebec, and Marten Stoffel in the summer of 2007. The bird was breeding on Bylot Island, Nunavut, Canada. Figure 1.1 shows that she was much darker in the winter of 2010 than in the winter of 2008. This observation shows the futility of assigning an age class to Snowy Owls based on spottiness: on that basis in 2010 the bird could have been mistaken for a young bird and definitely not one which had bred at least twice. We also assessed how individuals might change over time by examining the number of spots on a wing or tail feather in comparison to the number on feathers from a previous moult. When we examined birds at least three winters old, approximately a third of males displayed more wing spotting, with another third showing less, and the final third staying the same. For the tail, approximately half became more spotted or stayed the same, but none became

23

The Snowy Owl

less spotted. For female owls, most wing feathers (66%) stayed the same, while all of the rest became darker. Furthermore, 50% of the tails of females stayed the same, while the remainder were equally likely to have become more or less spotted. Figure 1.2 shows three consecutive secondary feathers of an adult female Snowy Owl. Two feathers are from the most recent moult, with one from a previous year’s moult. One feather from the current moult shows a noticeable decrease in spotting, while the other shows that pigmentation was the same as before. More commonly one sees stripes or rows across these feathers with about the same number of spots. Clearly conventional wisdom is not correct – Snowy Owls do not become whiter with age: indeed, we find considerably more evidence for the opposite! Results showing individuals that changed with age prompted us to design a graphic model to explain plumage variation (Figure 1.3). We propose that birds may follow different trajectories of coloration over time, perhaps contingent on their physiological condition. There are separate lines for males and females to illustrate the real situation. Moreover, there is very likely an ontogenetic trend for decreased spottiness to the point where some males have the potential to be pure white. However, the new findings presented above suggest that an individual may depart from that ontogenetic pathway and increase in pigmentation in a subsequent year, or may stay the same. This graphically illustrates how birds of any one age can appear very different, and how birds of any degree of spotting can be variable with respect to both age and sex. Figure 1.2. Three consecutive secondary feathers of an adult female Snowy Owl, satellite-tagged in July 2007, which died in December 2008. By comparing photographs from 2007 and the carcass in 2008, and the different ages of feathers at any one time, we determined that the number of spots can indeed change over time for a feather of a particular position. The old (O) worn feather grown in 2007 had four brown spots. One of the two new (N) secondaries grown in 2008 showed no change, having four spots; another of the new secondaries, however, had only one spot and was less spotted than the feather it replaced.

24

What makes a Snowy Owl?

Heavily Spotted

A

B1

a

b

Spottiness

C1

B b

Pure White

C

c 1

2

x

Age

Figure 1.3. A general model of the possible age- and sex-related variation in spottiness of Snowy Owls. The line marked by capital letters represents potential pathways for females; the line with lower case letters is for males. It is likely that many owls become less spotted with age, e.g., moving from point A to B to C for females and a to b to c for males. However, some individuals stay the same, e.g. going from A to B1 or a to b1, or can even get more spotted with age, e.g. B to C1. All these changes are known to occur for both sexes and help explain how various individuals can be of the same age but look very different (compare B1 to b1 to B to b), and how birds that appear the same can in fact be of a different age or sex (e.g. compare A to B1 to C1). As if the coloration of Snowy Owls was not complicated enough, there is yet another factor that influences the appearance of the birds – spots can fade considerably. More than for any other species we have examined, the colour can fade from a blackish-brown to a very pale brown that is hardly visible at all. In part this is due to wear, but bleaching or other changes are also likely. Fading was particularly noticeable when we compared the females trapped in winter to breeding (i.e. summer) birds in the Arctic in a study with Jean-François Therrien, Joël Bêty and Gilles Gauthier. From this study summer birds appear whiter, though we must stress that only female owls were captured in the north, so this may not apply to males. In winter, and at the start of summer breeding, the study indicated that females had fewer, and paler, spots, than they did after breeding. The newer moulted feathers seen towards the end of the summer had more, and darker, spots: the more advanced the moult (by counting the number of primaries replaced), the darker the overall appearance of the body. Determining all the factors that influence coloration has been an enormous challenge, but we consider that may be the easy part of investigating plumage variation in Snowy Owls. Finding out why they are so variable is the next challenge. It is likely that as with many other birds, colour is a sexually selected trait in Snowy Owls. However, the mechanisms of determining colour variation may very well be different, and could involve body condition and stress

25

The Snowy Owl

Mikkola (1987) has explained the differences in barring density as an adaptation to the breeding period. In his opinion the presence of barring on females serves to camouflage the nesting female. In our opinion the trait has not evolved sufficiently to serve such a purpose. Nesting females in summer are very conspicuous and can easily be seen at a distance. Furthermore, there are no avian predators on the tundra capable of killing a female on the nest. By size the Snowy Owl is the largest local predator and can usually protect its breeding territory from intruders (see Chapter 10). We consider the small amount of plumage pigmentation in both sexes as a trade-off between summer handicap and winter adaptation, or near-adaptation. In winter the pigmented spots have no role except signalling to conspecifics (i.e other Snowy Owls), but pigment production costs energy. In summer the lack of pigmentation makes it more difficult to catch prey. Individual plumage variations would then advertise good genes to potential partners, indicating that even with such a handicap the individual is still a good hunter. Despite these plumage generalisations, as noted in the Box, there remains a group of intermediately barred birds which cannot be sexed from a distance on the basis of coloration. However, when the birds are in the hand, the sexing of young owls is possible thanks to a method developed recently after field studies in 2002–2006 at Barrow, Alaska. The study (Seidensticker et al. 2011) used genetic methods to determine the sex of the young owls and then, with the help of the elaborate statistical method known as the ‘random forest model’ identified important predictors of sex. The best of these was the number of irregular bars (IB) on the left fourth secondary feather (S4) (Figure 1.4). If a young bird has zero or one IB it is likely to be a male: if it has more than one IB it is likely to be a female. Seidensticker et al. confess that the method occasionally ‘misclassified males as females’, but the use of multiple characters, such as the presence of more than one IB on secondaries S1– S5, the accuracy of prediction increased. In view of the new outlook on plumage variation (see Box), it would be very interesting to repeat such a study in a different area, under different ecological conditions (e.g. lower or higher abundance of lemmings) which would, therefore, include differing levels of stress in the chicks. We think such a study might reveal interesting surprises. Figure 1.4. S4 feather of a young Snowy Owl male (left) and female (right). The arrows indicate spots on the male feather and ‘Irregular Bars’ on the female feather.

26

What makes a Snowy Owl?

Adult owls have an annual moult which starts in mid-June and ends in early September. Initially the moult is not intensive, but almost every nest with a clutch will have one or two moulted feathers even if there is still snow cover. The intensity of moult increases significantly when the chicks have hatched (July), at which time both parents will usually lack one or two primaries on both wings. Non-breeding birds start to moult later and the intensity of moult in such individuals is the heaviest. At no point during the moult do the birds lose the ability to fly. Beaks and talons are uniformly black. Thick bristles around the beak and the feathers of the facial disk almost bury the black beak, and in the cold the posture is such that the beak sinks into fluffy feathers on the front of the neck. In such conditions the owls also partially close their bright yellow eyes. As a consequence, in murky conditions, the snow scooter driver may have the heart-stopping vision of an insignificant tussock-looking bump on the tundra spreading its wings and gracefully flying away. As noted earlier, first-year birds differ significantly from adults in the amount of barring, such plumage differences also being rare in other owls. First-year birds have much heavier barring; barring being present on the feathers of all the pterilia except the facial disk, tarsi, feet, and the white bib (if present). Males also have barring on almost all parts of the body, and have a white bib which is larger than that of females. First-year males have the same distribution of barring as females, but the coloration is browner and less distinct (Mikkola 1987). A few species of owls have feathered tarsi, some of these also having feathered toes, e.g. Great Grey, Eagle and Great Horned owls, and the Hawk Owl Surnia ulula. Both Eagle and Great Horned owls have feathers covering only the upper part of the toes, while Great Grey and Hawk owls have feathers surrounding the toes, as if the bird is wrapped in the stiff feathers (König et al. 1999). The Snowy Owl’s toes resemble those of the latter two species, except that the feathers are almost pure white, and the layer of feathers is much thicker. Snowy Owls do not have black wing tips, despite the presence of black spots on the plumage. Most other species of white birds do have black wing tips, and as it is believed that melanistic keratin makes the feather tips more resistant to abrasion (Boser 1995), the absence in Snowy Owls has puzzled ornithologists for many years. According to Averill (1923), the black wing tips seen in many gulls, and most notably in the Gyrfalcon Falco rusticolus, reinforce the barb structure and reduce the wear and tear of the wingtips. Averill explains the absence in Snowy Owls by noting that large birds fly more slowly, in a ‘soft and easy flight’, than smaller birds and therefore beat the air less rapidly. This explanation is probably correct, but further studies and experiments are required to confirm the hypothesis. Those who have handled live owls will know that Snowy Owls appear heavier and have denser (less soft) plumage than, say, Great Grey or Eagle owls. However, by comparison to other diurnal birds of prey, the Snowy Owl does have a softer plumage. Snowy Owls have a distinct facial disk and very well developed rictal bristles around the eyes and beak. The bristles serve the same purpose as vibrissae in mammals. Since Snowy Owls are long-sighted (see section on vision below), they cannot see or assess the shape of their prey all that well once they have caught it – so they test it with the bristles. From a distance this makes it look as though the bird is licking its prey, particularly if the eyes are shut, as they occasionally are. The wing is relatively long, and is perhaps the feature which aligns the species most closely to falcons and buzzards rather than to owls. The reason is that Snowy Owls stoop and therefore have morphological adaptations to stooping as well as to long-distance flights. There are large notches on the primary flight feathers, the largest of any owl. This feature was first noted by Averill (1927) who attributed their presence to Snowy Owls’ (relatively) long-distance migration as well as their (relatively) rapid wing movements. He related the presence of the

27

The Snowy Owl

pointed wing to the northerly distribution of the species. The overall flight pattern is direct and steady, appearing to some as a slow falcon flight. The body undulates during wingbeats. Gliding is used occasionally, but we have never seen a Snowy Owl soaring and circling high in the sky: most flights are at altitudes of no more than 150m. The birds are very agile in stooping: one male managed to put a deep scar into the skull of one of the authors by stooping on it. While stooping the male folded its wings to avoid a high-speed collision with a 2m stick placed above the author’s head while he was measuring a chick, but skilfully recovered and gained height after striking the head.

MORPHOLOGY AND MEASUREMENTS The Snowy Owl is the second largest extant owl, the largest being the European Eagle Owl. The latter’s mean weight is 2,416g for males and 3,164g for females (Mikkola 1987). The Great Horned Owl is a contestant for second place if the weight of 2,503g (Parmelee 1992) is accepted. However, no other details of this large individual are given, nor is there information regarding how the weight was measured. We believe this could have been an obese individual from a zoo. Houston et al. (1998) also state that the Great Horned Owl could be as large as the Snowy Owl, but the reality is that the mean weights of 895 male and 772 female Great Horned Owls were 1,304g and 1,706g respectively. The accepted average weight of male Snowy Owls is 1,600g, and that of females is 2,100g. These averages mean the Snowy Owl is larger than its Great Horned cousin; this is consistent with the view of Kerlinger and Lein (1988a) who recommended that the weight of a Snowy Owl before release from rehabilitation centres should be not less than 1,800g for males and 2,020g for females. Each weight is greater than the means for adult Great Horned Owls. We did not find any statistical differences in wing lengths across the entire species range (analysis of variance – ANOVA – Males, F=1.51, P=0.21, N=63, Females, F=0.36, P=0.78, N=74), though small differences, mainly attributed to the abundance of food in particular regions, are seen. Dimensions are given in Table 1.1. Table 1.1 Snowy Owl dimensions (lengths in mm, weights in g).

Wing Wing Wing Wing Wing Wing Wing Tail

28

Males 380.1±15.2 (351–410), N=16 405.4 (384–423), N=86

Females 416.2±16.8 (380–446), N=17 437.9 (428–462), N=63

412±8.8, (395–430) N=68 409 (395.3–439.7), N=34 408.2±16.7, (385.7– 439.7), N=8 406.6 (380–433), N=116 393.6 (383–408), N=22 209.6±7.4, (194–221), N=16

445 (430–471), N=62 437.4 (414.0–477.3), N=40 442.6±21.1, (414.9– 477.3), N=8 449.7 (400–468), N=86 420 (397–446), N=18 228.5±6.6 (216–239), N=15

References Josephson 1980 Dementiev & Gladkov 1951 Portenko 1972a, Portenko 1972 Eckert 1987 Calculated from Parmelee 1992 Priklonskiy 1993 Earhart & Johnson 1970 Josephson 1980

What makes a Snowy Owl?

Tail Tail Tail Tail Tail Tail Beak (from cere) Beak Beak (from back of cere) Tarsi Tarsi Longest toe (3rd) Body length Body length Body length Body length Body length Wingspan Wingspan Wingspan Wingspan Body weight Body weight Body weight Body weight

Males 233.6±17.6, (210-261), N=8 223 (188–252), N=113 233.7 (230.4–240.3), N=34 223 (188–252), N=113 233.7 (230.4–240.3), N=34 235.4 (231–240), N=5 26.1±0.93 (25.5–27.5), N=4

Females 241.3±19.0, (214–275), N=10 247.4 (205–288), N=110 250.3 (248.3–261.7), N=40 247.4 (205–288), N=110 250.3 (248.3–261.7), N=40 254.4 (251–261), N=8 27.9±0.67, (27–29), N=6

References Calculated from Parmelee 1992 Priklonskiy 1993 Eckert 1987 Priklonskiy 1993 Eckert 1987 Keith 1960 Calculated from Parmelee 1992

26.5 (24.6–25.7), N=34 27.9 (26.7–28.2), N=40 36.9 (25–42), N=89 34.3 (24–41), N=87

Eckert 1987 Priklonskiy 1993

64.825 (61.65–68), N=2 66.375 (64.75–68), N=2

Calculated from Parmelee 1992 Priklonskiy 1993 Calculated from Parmelee 1992 Keith 1960

62.4 (53–72), N=97 34.6, (32.3–37), N=2

65.6 (54–74), N=94 39.9, (36,7–43.0), N=2

582.6 (553–622.3), N=5 602.3 (579.1–647.7), N8 678 (647–710), N=2 579 (558–600), N=2 579.6 (560–610), N=5

650, N=1

592.8 (531.1–707.2), N=34 594 (530–640), N=9

663.4 (629.9–766.9), N=40 604.6 (540–660), N=11

(N=1, i.e. no range) 1496 (1485–1540), N=5 1610 1577.4 (1316.7–1656.4), 1643.8 (1567.5–1816.5), N=40 N=34 1575 (1520–1830), N=5 1360 (1160–1490), N=4 1551.3 (1460. –1600.2), 1432.0 (1384–1506), N=8 N=5 2153± 358.3 (1770– 1615±237.9 (1350– 2480), N=3 2000), N=5 1806±30 (1606–2043), 2279±57 (1838–2951), N=21 N=21 1706.7 (1593.0–2002.6). 1612.9 (1448.0– N=40 1839.9), N=34 2083 (1330–2560), 1465 (1300–1590), N=8 N=4

Calculated from Parmelee 1992 Dementiev & Gladkov 1951 Eckert 1987 Priklonskiy 1993 Dementiev & Gladkov 1951 Eckert 1987 Priklonskiy 1993 Keith 1960 Dementiev & Gladkov 1951 Kerlinger & Lein 1988a Eckert 1987 Priklonskiy 1993

29

The Snowy Owl

Body weight Body weight

Males 1808.3 (1617–1936), N=4 1642.4 (1320–2013), N=27

Females 2426 (2154–2934), N=8

References Keith 1960

1962.9 (1550–2690), N=30

Earhart & Johnson 1970

There is a tendency for the birds to accumulate fat prior to winter, a wise precaution as the hunting ground may be covered by thick snow which makes hunt outcome somewhat unpredictable. Fat accumulation depends on autumnal hunting success: given the opportunity, the birds accumulate fat extremely fast – in captive birds such rapid fat increases are not uncommon. There are also records of extremely lean birds being shot on wintering grounds, though such body conditions may indicate a dying bird. That said, Snowy Owls have been known to lose a great deal of weight. Ryabitsev (2001) mentions that the weight of some owls can fall to 700g. Golovatin & Paskhalniy (2005) reported spotting a bird at the Erkuta-yaha River in the Yamalo-Nenets District of western Siberia in 1989 which allowed very close human approach, then took off and crashed into the river. When caught it was extremely lean. Similar reports exist in old literature. In Virginia there was a report of an owl which had almost completely lost its muscles, but nevertheless was still alive (Shufeldt 1914). The bird was captured simply by being picked up. Shufeldt reported: ‘The stomach was entirely empty, and all the organs and viscera of the thoracic cavity and abdomen were reduced almost to a state of atrophy. There was no adipose anywhere, but the most remarkable sight was the muscles. These were all flabby and of a very pale flesh-colour; and the entire system was reduced almost to its tendons and fascia.’ However, it was later found that the bird had been wounded by lead shot. Pitelka et al. (1955a) reported an emaciated Snowy Owl found in snow at Barrow, Alaska, in 1951, a year when the birds did not breed there. It was a male with a weight of 1185g. Another report of a starving Snowy Owl exists from Tatoosh Island, Washington, USA; a barren piece of land overlooking Vancouver Island. There, one owl was found dead, and another was reported to be so weak that it was caught by hand (Levin et al. 1977). The ability to consume body tissues in the hope of better days to come is remarkable: not many birds can survive merely by digesting themselves. Perhaps such extreme adaptation – hoping for the best in a bad situation – has allowed Snowy Owls to survive severe snowstorms. That said, it is not clear whether such a tremendous weight loss is reversible. Snowy Owls, as with all other owls, demonstrate reverse size dimorphism, i.e. males are smaller than females. Indeed, size dimorphism in Snowy Owls (+22%) is one of the most pronounced amongst owls, cf. +30.5% for the Eagle Owl, the most dimorphic of all owls and +25% for Blakiston’s Fish Owl Bubo blakistoni (Potapov unpublished data). Smaller owls, e.g. the Short-eared and Long-eared owls show lower figure (+12.7% in both cases). (All data from Korpimäki 1986). There is a plethora of hypotheses seeking to explain reverse sex dimorphism in owls. One, which covers both owls and diurnal birds of prey, states that it results from the evolution of a reduction of competition between members of a pair as they have different optimal prey sizes. The ‘female dominance hypothesis’ suggests that large females play an important role in the functioning of the pair, being capable of dominating the male such that he provides enough food for the family. This hypothesis was very popular among researchers of diurnal birds of prey (Cade 1960; Smith 1982). The ‘intra-sexual selection hypothesis’ implies that the larger birds compete for the smaller sex, so that large size confers greater competitive ability (Newton 1986; Olsen & Cockburn 1993). The ‘reproductive effort hypothesis’ postulates that larger females produce more and larger eggs (Olsen & Cockburn 1993), while the ‘female

30

What makes a Snowy Owl?

supplementary feeding hypothesis’ (Korpimäki 1985), states that the female size is profitable since larger females are capable of hunting and delivering larger prey than males. The ‘small male hypothesis’ suggests that smaller males have lower energy expenditure during hunting than larger males and thus increase their foraging efficiency (Hakkarainen et al. 1996). The ‘intersexual selection hypothesis’ expands this idea by implying that females would select small males and, as a consequence, amplify ‘small male’ selection by sexual selection (Safina 1984). Wiklund and Stigh (1983) constructed a hypothesis explaining reverse size dimorphism specifically in Snowy Owls. In their view, as the male Snowy Owl delivers most of the food, smaller size is an adaptation towards agility during hunting and nest protection. The large size of females would then be an adaptation for egg production (i.e. large clutches) and for brooding the young. Lundberg (1986) suggested that reverse sexual dimorphism reduces temporary food shortages during the breeding period as the females can cope with longer periods of starvation, an idea (later named the ‘starvation hypothesis’) that was widely discussed. In June 1988 during a deep lemming depression EP spotted a female Snowy Owl on the side of a hillock in the Konkovaya Study Area in Russia’s Kolyma Lowlands. After his initial approach the owl took off, clearly carrying something heavy. The flight was so heavy that; EP was able to follow at a run. After about 2km the near-choking ornithologist forced the owl to release its load. It was a heavily decomposing and partially eaten Snowy Owl male. Clearly this episode supports Lundberg’s ‘starvation’ hypothesis, which, in this instance, should be extended to the non-breeding period. In conclusion, sexual dimorphism has been discussed extensively in the literature (see Massemin et al. 2000 and references therein) with many opinions and no consensus. As such, the discussion is likely to continue into the future and will not be considered further here. The Snowy Owl has one of the highest owl wing loadings (0.55g/cm2), cf. 0.21g/cm2 for the Long-eared Owl and 0.48g/cm2 for the Great Horned Owl (Johnson 1997; Potapov unpublished data). The relationship between wing loading and the body mass of various bird species is shown in Figure 1.5. The Snowy Owls fall just above the general line for diurnal birds of prey, who, at this body mass range, are soarers. The wing loading of smaller birds of this class indicates that they can lift a significant weight, but are still able to fly. The wing-loading of Galliformes does not allow them to carry extra loads, and they are constrained to use only flapping power-flight. Figure 1.5. Wing loading (g/cm2) plotted against body mass (g). Note the logarithmic scale. The filled squares are Galliforme birds; the filled triangles are Anseriformes; the open circles are Accipitridae; the closed circles are owls. The regression line for Galliformes is shown dotted, for Accipitridae dashed, for Anseriformes dash-dotted, and for Strigiformes solid. Data from Potapov (unpublished).

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The Snowy Owl

EGG SIZE The number of measured Snowy Owl eggs outnumbers that of other birds, perhaps reflecting the fact that Snowy Owls produce large clutch sizes and, if they breed, they breed in abundance. Alternatively, of course, it could merely reflect the deep interest egg collectors had in the species with large collections of eggs now available in museums. A consequence of the abundance of research material is the number of papers where egg dimensions are given with high accuracy. In all the following, measurements, in millimetres, are minimum–maximum length x minimum– maximum breadth, followed by means. Bent (1938) measured 56 eggs from North American nests: 50.6–60.0 x 41.7–47.5, mean 56.4 x 44.8. Krechmar and Dorogoy (1981) measured 86 eggs from Wrangel Island: 51.0–62.2 x 48.2–48.4, mean 56.6 x 44.6. Later, Dorogoy (1987) measured 265 eggs on Wrangel Island and gave mean of 56.4 x 45.0. Another 117 eggs measured in 1986 on Wrangel Island gave 50.0–58.9 x 42.3–47.0, mean 54.7 x 44.6 (Stishov et al. 1991). In the following year 43 eggs at the same location were 52.0–60.0 x 43.3–47.2, mean 55.8x44.8. Mean measurements given by Harrison (1984) were 57.4 x 45.2. Portenko (1972) measured 332 eggs, giving 50.6–70.2 x 41.7–49.3, mean 51.1 x 44.9. The famous handbook of oology by Schönwetter (1960) gives results from 300 eggs: 50.5–62.8 x 42.0–47.1, mean 57.0 x 45.0. Wasenius (1930) gives 54.6–61.2 x 41.0–48.1, mean 56.4 x 44.7. Hagen (1960) measured 16 eggs in 1959 in Hardangervidda, Norway: 55.8–60.0 x 43.2–46.5, mean 57.1 x 45.2. A sample of 21 eggs measured by Lid in the same place in 1963 (Portenko 1972) had dimensions 51.2–58.9 x 44.5–47.1, mean 55.7 x 45.8. From a total of 66 eggs measured at the Chroma River mouth, Yakutia, north-east Siberia the mean was 57.0 x 45.2 (Uspenskiy and Priklonskiy 1961). Nearby, at the Lena Delta, eggs measured in 1982 gave 51.8–60.6 x 41.7–46.5, mean 56.4 x 44.4 (Blokhin 1987), and at the same location in 1995 gave 51.5–59.8 x 42.7–46.1, mean 57.1 x 44.9 (Solovieva 1996), and in 2000 gave 53.6–61.1 x 42.8–47.1, mean 57.5 x 45.7, and in 2004 gave 53.6–60.4 x 42.3–46.4, mean 56.9 x 44.5 (Posdnyakov and Safronov 2005). Finally, Makatsch (1976) measured 21 eggs from ‘Lappland’ giving a mean of 57.4 x 45.2 and 73 eggs from Sweden and Finland with a mean of 65.6 x 45.0. Because of the difficulty of reaching the tundra during spring (see Chapter 5) and the difficulty in locating new clutches once there the freshly laid egg mass is difficult to determine in the field. Consequently, the majority of the egg mass records in the literature refer to incubated eggs. Since an embryo breathes within the eggshell, it reduces its mass – at a rate of 0.3±0.16g/ day, N=17 – as well as thinning the egg shell, so quoted masses refer to egg mass less mass respirated by the embryo (see Figure 5.8 – Chapter 5). Watson (1957) reported the mean mass of eight eggs as 58g, Uspenskiy and Priklonskiy (studying eggs in the Indigirka Lowlands, of Yakutia, north-east Siberia) measured 47.5–68.0g, mean 60.3g. Solovieva (1996) gives the weight of the eggs in the middle of the incubation period at the Lena Delta,Yakutia as 57–65.5g, mean 60.6±0.14g. Schönwetter (1960) gives a mean mass of 63.5g. Parmelee (1992) reported a variation of mass in an eight-egg clutch as 58.1–64.5g, mean 62.1g. A sample of 15 eggs studied by Hagen (1960) gave 50–59g, mean 53.3g. The eggshell of a just-hatched egg in the Konkovaya Study Area in the Kolyma Lowlands, weighed 5g. The inner eggshell membrane was thick and, together with chorion fluid, weighed 4g. The egg weight before hatching was 52g; the newly hatched chick weighed 40g, including a 3g externally protruding yolk sac. The chick, the first to hatch from the clutch, successfully fledged. The quoted measurements are interesting for displaying a clear lack of geographic variability in egg size. The average egg (i.e. the average of means) is 56.7 x 45.0mm. The volume was estimated as 57.0cm3 (Worth 1940), the eggshell thickness as 0.36mm (Schönwetter 1960).

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What makes a Snowy Owl?

Snowy Owl eggs are pure white or creamy white (Bent 1938; Harrison 1984; pers. obs.), but become stained by the faeces of hatched siblings or by the remains of the food delivered to the nest. The eggs are elliptical and are 20% smaller than the eggs of the Eagle Owl, and 8% smaller than those of the Great Horned Owl (Voous 1989).

SKELETON The Snowy Owl skeleton is similar to that of the Eagle Owl, but smaller. However, there are significant differences. The tarso-metatarsus is much shorter than that of the Eagle Owl (Figure 1.6) and the crests of the medial condylus in the Eagle Owl are very pronounced, suggesting that the second toe does much more work than the second toe of the Snowy Owl, which has no groove at this condylus. In the past a popular study topic included the measurement of the circumference of the tarsi as this was important in establishing the necessary size for rings. For the Snowy Owl the tarsus circumference was measured as 50mm (Stabler and Hoy 1942). Ford (1967, p68) indicates that the Snowy Owl has a distinct downward direction of the trochlea of the 4th digit, a trait which is very different from members of the Bubo family. Figure 1.6. Differences between tarso-metatarsus of Eurasian Eagle Owl, left, and Snowy Owl, right. The bones are from the collection of the Zoological Institute, RAS, St Petersburg, Russia (N2963 and 3035).

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The Snowy Owl

Figure 1.7. Differences between the skulls of A) Eagle Owl, B) Snowy Owl, and C) Great Horned Owl. Photographs of the skulls by Wouter van Gestel and Jan Jansen of Wageningen University, the Netherlands. Note the slight asymmetry in the position of paraoccipital processes (6) in the Eagle and Great Horned owls. There are significant differences in the skulls of the large owls. Figure 1.7 shows the skull of the Snowy Owl and those of Eagle and Great Horned owls. These large owls have the most symmetrical skulls among all owls. The most pronounced asymmetry in owls is that noted in the Great Grey Owl and Tengmalm’s Owl Aegolius funereus (Norberg 1977), the least being seen in the Great Horned and Eagle owls. In the latter two species the position of the external ear opening led Norberg (1977) to suggest that the ear, and therefore the skull, asymmetry in owls is linked to vertical directional hearing. In woodland, and especially at short range, such an adaptation makes perfect sense. In flat areas of the tundra, almost a two-dimensional hunting space, there is no need for such adaptation. In general, the neurocranium is narrower and longer in the Snowy Owl than in the other two large owls, and the orientation of the eye sockets is also different: in Snowy Owls these are aimed above the beak in comparison to the other two. Pterigoid’s proximal epiphyses are similar in shape across the Bubo species, but have an additional curved knob in Nyctea (Figure 1.7:1). Details of the palate are different, though the overall shape is similar. However, the mesethmoideum is drastically different (Figure 1.7:2); both in shape and in the way it contacts the nasal-frontal hinge and lacrimal region in the Snowy Owl, though these contacts are similar in B. virginianus and B. bubo. The postorbital processus of the quadrate bone (proc. orbitalis ossis quadrati) is different (Figure 1.7:3), mostly because of the different orientation of the eye sockets. The shape of the interorbital septum is also different in shape between the Snowy Owl and the other two species, the latter two being similar. Ford (1967) also noted that the septum

34

What makes a Snowy Owl?

Brain volume (sq. mm)

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Figure 1.8. Brain volume of the Strigiformes (derived from Iwaniuk & Wylie, 2006). Note the logarithmic scale. Note also that the volume relates to brain size only, i.e. excludes the eyes. is different between the Bubo group and Nyctea: the latter has a thicker septum. The place of attachment of the supraorbitalis processus in the Snowy Owl is much more caudal when compared to the other two owls (Figure 1.7:4) – this trait was also noted by Ford (1967) – while the sutures between the dentale, angulare and supra-angulare bones looks different in the Snowy Owl compared to the other two (Figure 1.7:5). In addition the paraoccipital processus (Figure 1.7:6) are thin and elegant in the other two large owls (using the terminology of Ford (1967)), but much blunter in the Snowy Owl. The Snowy Owl brain mass was reported by (Iwaniuk & Wylie 2006) as being 15,870mm3 in a bird weighing 1,894g. Owls possess the largest relative brain size relative to body mass of all birds, and the Snowy Owl has the second largest brain size (relative to body mass) after the Eagle Owl (Figure 1.8). From Figure 1.8 it is obvious that the size of the brain in owls is a simple result of the intercorrelation between body size and the size of the skull. The notion that a larger brain means a more intelligent bird has been rejected, both by numerous studies and by common sense. A simple explanation of why the volume of the brain increases with body size is that a larger owl has more sensory nerve fibres feeding in and out of the brain from the bird’s larger body, and the larger skull can dock larger eye sockets, allowing for the larger eye size. Consequently the graph shows that, as regards brain size, Snowy Owls are no different from other owls. Recent studies (Garamszegi et al. 2001) suggested that the eye and brain size co-evolved in response to nocturnality and, at least partly, to the requirements of catching moving prey.

WHAT THEY SEE, AND HOW THEY ARE SEEN – THE ‘TRUE COLOURS’ OF THE SNOWY OWL Eyesight Snowy Owls do not have extremely large eyes in comparison to other owls, though they are, comparatively, larger than those of other Arctic birds. Even in the temperate zone, where the owls occasionally over-winter, there are few bird species with larger eyes. The eyes are bright

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The Snowy Owl

yellow, with black pupils. A third eyelid is present, as in other owl species, and probably plays a very important role in lubricating the eye surface, which, due its large size, is prone to drying. Veterinary scientists have reported two cases of young, captive Snowy Owls which had protrusions of the third eyelids covering the entire eye, effectively blinding the birds (Williams and Flach 2003). Surgical procedures were performed to remove these third lids, and severe microbial infection was named as the cause. Similar cases of such severity have not been reported among other bird species causing us to suspect that the owls, effectively an Arctic species, and therefore adapted to a habitat where microbes are not abundant in comparison to temperate latitudes, could be susceptible to microbe infections in zoos at a higher rate than for other owl species. The vision of Snowy Owls is probably not significantly different from that of the closely related Bubo owls. The spectral sensitivity of the Great Horned Owl was studied in detail in the 1980s (Jacobs et al. 1987) using non-invasive methods. It appears that the optic cones of these owls are most sensitive to wavelengths of 555–556nm (about the mid-point of the visual spectrum). Previously Bowmaker & Martin (1976) reported that the cones in the Tawny Owl Strix aluco also showed a peak at 555nm, with a small number of cones sensitive to 463 and 503nm. The findings suggest that the owls have very weak colour vision, with the most acute vision achieved by black-and-white sensitive rods. Whether this is also true for the Snowy Owl remains unclear as studies on the vision of the species are not numerous. Of all birds, owls in general have relatively large eyes, those of the larger species being almost the same size as those of humans (Gill 2007). All nocturnal birds, owls included, have higher light sensitivity compared to diurnal birds. Martin (1977) reported that the eyes of the Tawny Owl are 2.2 times more sensitive than human eyes. The vision of Snowy Owls is probably less sensitive in the dark, despite that ability being useful in the dull light of the polar night, but given the size of their eyes their night vision is probably better than humans. While this is speculative, it is supported by the experience of the authors with captive owls which suggests that the species’ eyes are roughly 1.5 times more sensitive than those of humans. It was once assumed that an owl’s eyes were also telescopic, i.e. able to zoom in onto distant objects (Sparks & Soper 1989). However, original views on the structure of owl eyes were either highly anthropomorphic or mechanistic with owl eye structure simply being modelled on the human eye and/or a photographic camera. But an owl’s eyes are not well modelled by either, and because of its morphology, a Snowy Owl’s eye is one of the most highly developed of any owl, and, indeed, of any bird, needing to be capable of tracking distant objects in the extremes of the polar night and the low sun of a polar spring day. Indeed, these conditions make the Snowy Owl’s eyes one of the most ecologically adapted of any bird. Given the huge variations in lighting that the owl faces we were surprised to discover that, to date, no studies of comparative anatomy existed to allow a comprehensive view, a ‘big picture’ if you will, of the structure and function of the owl’s vision. We therefore set down here our own ‘big picture’. The shape and length of the owl’s eye prohibit usage of the term ‘eyeball’. The eyes of owls, and some eagles, are not balls: the eye’s horizontal axis is longer than the vertical, a shape occasionally referred to as tubular eyes. Snowy Owls have the most extreme horizontal to vertical length ratio, the length so large it requires a special set of bone elements to keep it in place – the sclerotic ring: a set of tiny overlapping ossicles surrounding the eye’s cylinder. The sclerotic ring is not a unique feature of birds, the trait being shared by reptiles, but its complexity makes the Snowy Owl very special, no other birds have such pronounced and tall sclerotic ossicles (Curtis & Miller 1938). Ford (1967) reported that Snowy Owls have the longest sclerotic ring, 1.2 times the diameter of the posterior opening, of any owl: in members of the Bubo family the sclerotic ring is 0.7 times the diameter of the posterior opening.

36

What makes a Snowy Owl?

The ossicles are operated by a series of muscles, termed the ciliary muscles, comprising (Sivak et al. 1999) three muscle groups: Brucke’s Muscle, contraction of which causes an annular pad to press against the lens, increasing its convexity; Crampton’s Muscle, (a muscle unique to birds) contraction of which increases curvature of the cornea; and Müller’s Muscle (sometimes referred to as a sub-division of Crampton’s muscles) which squeezes the sclerotic ossicles and so changes the focal length of the eye’s optical system. Owls have extremely welldeveloped Crampton’s Muscles, in sharp contrast to aquatic birds in which the muscle is much less developed, or sometimes even absent (Walls 1963). Both the anterior and posterior surfaces of the owl’s eye lens are convex (in contrast to, say, those of parrots which have flat anterior and convex posterior surfaces). The eyes of owls also have only a single fovea fixed at the centre of the retina (in contrast to Galliformes, which have no fovea, and the bifoveal raptors, swallows, hummingbirds and swifts, which have both central and temporal fovea). These morphological features suggest to us that the Snowy Owl has an eye with variable focus, i.e. the owls have telescopic vision as well as telephoto vision. In their 1983 paper, Murphy and Howland reported that the focal distances of eyes at rest, the ability to change focus (accommodation) and corneal curvature in 15 species of owls, including the Snowy Owl. They measured these parameters using corneal topography (also known as photokeratoscopy or videokeratography), a non-invasive imaging technique for mapping the surface curvature of the cornea, and the outer structure of the eye. The cornea curvature measured in the Snowy Owl was 37.5 dioptres, compared to 24.0 dioptres in the Eagle Owl, 25.0 in the Great Horned Owl, 49.0 in the Short-eared Owl (Asio flammeus) and 53.0 in the Saw-whet Owl (Aegolius acadicus). These figures compare to 40.0 dioptres in humans (Davison 1962). The dioptre is a unit of the optical power of a lens or curved mirror, or the retina, and is equal to the reciprocal of the focal length measured in metres (that is, 1/metres). For example, a 37.5 dioptre lens brings parallel rays of light to focus at 1/37.5 = 0.0267m, or 2.67cm. One of the interesting results of this study was that various species of owl differ in their ability to focus on close objects. In general, the smaller the owl is, the closer it can focus on an object. The Snowy Owl’s near-focus is 1.66m, the longest amongst the studied species, compared to 0.55m for the Great Horned Owl, 0.9m for the Eagle Owl, and 6 dioptres); and Barn Owl (>10 dioptres). This probably means that the eyesight of the Snowy Owl, as well as the Eagle and Great Grey Owl, is tuned to long-range, and is not adapted to hunting over short or variable long-short distances. The resting focus as measured by retinoscopy was -0.12 (emmetropia or balanced vision), while measured by photo-refraction was +0.3 (myopia, or slight near-sightedness). The difference between the methods is explained by the fact that the retinoscopic procedure did not stimulate accommodation as much as did photo-refraction. In accommodating, many but not all owls, showed a near-pupil response. The greatest change in pupil diameter was found in the Screech Owl Megascops asio –13mm to 3mm – but a similar test in Snowy Owls reveals that its pupils do not change, maintaining a diameter of 12mm. It is generally accepted that a change in pupil diameter increases the depth of field of the

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The Snowy Owl

eye and helps accommodation by sharpening the retinal image of a near object at the expense of image brightness. The results of the study suggest that Snowy Owls possess a relatively small depth of field. Many birds have very little area of binocular vision. However, in owls it is evident that the frontal position of the eyes allows a large zone of overlap, i.e. a large zone of binocular vision, although this is at the expense of rather obscured total vision, i.e. owls lack a high degree of peripheral vision (Gill 1994, 2007; Martin 2009). In Tawny Owls the region of binocular vision (48°) is considerably smaller (Martin 1984) than appears from a casual observation: if full use were made of the optical field of each eye, the Tawny Owl’s maximum binocular field width would be 111º. Nevertheless, the owls are unique amongst birds in their binocular vision; their visual system in that respect (i.e. their stereopsis) is very similar to that of primates, including humans (Iwaniuk & Wylie 2006; van der Willigen et al. 1998). In addition to a large area of frontal binocular vision, the owls have a seriously hypertrophied visual Wulst (Iwaniuk and Hurd 2005); the putative homolog of the mammalian primary visual cortex. Recordings from the owl Wulst reveal that it is functionally like the primary visual cortex: Wulst neurons are selective for orientation, movement direction, spatial frequency and binocular disparity (Iwaniuk & Wylie 2006 and references therein). In other words, this means that stereopsis-driven neurons (which are manifested in the overall size of the owl brain), and the presence of large telencephalon (the equivalent of the cerebrum in mammals) and Wulst portions of brain seem to be unique to owls, and have huge ecological and evolutionary significance. Later studies (Martin 2009), suggest that the apparent ‘optical’ zone of overlap might not be supported by the presence of the retina in the visual fields of the frontal vision, as was the case for the Short-toed Eagle Circaetus gallicus. In other words, the lateral parts of the optical front field are not served by sensors. Whether this is true for the owls in general or the Snowy Owl in particular is not known at this stage, but evidently the optical overlap cannot serve as an argument for a large area of the binocular vision in Snowy Owls. The current paradigm is that binocularity in owls is not primarily concerned with having two eyes looking at the same scene in order to extract higher order information from their disparate images, but is simply either a consequence of placing each eye so as to have a portion of its field facing forward for the extraction of information from an expanding optical flow field (Martin 2009), or as a consequence of the necessity to accommodate large and asymmetrical ears (though, of course, asymmetry in the ears of Snowy Owls is, as we have seen, minimal). It appears that in the owls (as was shown in the example of the Tawny Owl (Martin 1984)), the uniocular retinal field is highly asymmetrical. The maximum field width of 124° is less than that recorded in any other vertebrate. The maximum retinal binocular field width equals 48° and the optic axes diverge by 55°. Maximum binocularity occurs above the beak, whose tip lies outside the visual field. The cyclopean retinal field has a maximum width of 201°. Limited data on the visual fields of the pigeon are also presented in Martin’s study. All these data are compared and discussed with regard to visual field widths in other species and the significance of the owl eye’s tubular shape, its nasal asymmetry and the possible factors influencing binocular field width. This means, that the actual binocular vision of owls is much less than has been supposed, and that the primary reason for the eyes being set at the front of the head, pointing forward is to accommodate large ears rather than to give acute binocular vision. Because of the asymmetry of the skull, the binocular vision is also asymmetric. Overall, owls have similar eyesight to humans, although with a more limited field of view, but an increased ability to see in low light levels. As with other owls, Snowy Owls were found to have a multifocal optical system in their eye (Lind et al. 2008), very different from the eyesight of many bird species, most of which are largely monofocal. In multifocal systems, the crystalline lens has concentric zones of different

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What makes a Snowy Owl?

refractive powers generated by a non-linear gradient of refraction. Each zone focuses light of a narrow band of wavelengths. Therefore, it is believed that the multifocal system in owl eyes is a trade off, the gain in image quality across the visual spectrum coming at the cost of lower spatial resolution at a single wavelength. Owls are believed to have all three kinds of cone visual pigment (Bowmaker and Martin 1978) and colour vision (Martin 1974), but, to date, no ultraviolet (UV) sensitive visual pigments have been found (Lind et al. 2008). The reason for the presence of multifocal optical systems in owls may therefore not be their sensitivity to UV light but the relatively low minimum f-number of their eyes. As is the case in other nocturnal vertebrates, increased chromatic blur (aberration) because of short depth of focus seems to make multifocal systems advantageous for owls (Lind et al. 2008). Although Lind et al’s discovery of multi-focal ability in owls went almost unnoticed in the scientific community, its importance can be seen after evaluation of the very new, and equally rapidly developing, area of ‘light field’ photography. Michael Faraday (1846) set down a theory of a light field, seeing it as analogous to a magnetic field. This theory was adapted for vision by Adelson and Bergen (1991) who suggested an approach they called ‘early vision’ which consists of a set of parallel pathways in the retina, each analysing some particular aspect of the visual stimulus; such as motion, colour, binocular disparity, orientation etc. These stimuli are then processed by the brain. The practical realisation of interpreting all this information from a single retinal snapshot has become evident only with the recent invention of plenoptic photo-cameras, some of which are already available (e.g. the ‘Lytro’ – Ng 2005, 2006). Instead of capturing a 2D picture (as in conventional photography), plenoptic cameras capture the ‘light field’, a 3D snapshot being delivered to the viewer, allowing re-focusing of the image after it has been shot, and allowing creation of 2D cross sections of the 3D image. Therefore, based on the information above we believe that the Snowy Owl’s eye has a lens with variable focal distance at one end, high resolution (at least twice the ‘megapixels’ of the human eye), and a curved sensor with flexible geometry at the other end. The eye has a variable overall focal length thanks to the workings of Müller’s Muscle which moves overlapping sclerotic ring ossicles. The existence of multi-focal capability (Lind et al. 2008) implies the owls have the ability to read N-dimensional signals from the retina, and are thus able to derive many more cues from their eyes than we can possibly imagine. (The possible higher dimensions include time, wavelength and polarisation). Although how many parameters an owl reads from its eye is not presently clear, the structure of the eye’s optical elements suggests not only the existence of an almost aberration-free system, but the presence of a sophisticated refractor-based light-field imaging (plenoptic) device. In plain English, owls in general can probably see more than just a 3D image, while the Snowy Owl has this capacity for 3+ vision at the longest distance of any owl. Given this ability, it is little wonder they have difficulty in seeing close objects.

Plumage coloration For a long time, studies of animal coloration assumed that animals see colours as humans do. Scientists used general terms when describing the colours, and sometimes tried to use colour tables in order to give the descriptions of animals in general, and the Snowy Owl in particular, a more objective basis. This assumption is now known to be flawed; experiments conducted at Bristol University, UK (Bennett et al. 1997) showing that UV wavelengths (in the range 300– 400nm, to which humans are blind) are used when birds are hunting for prey, and when they are choosing mates. Furthermore, the Bristol group has demonstrated previously unnoticed avian sexual dimorphism when considering the UV part of the spectrum (Hunt et al. 1999).

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The Snowy Owl

The ability to see UV is thought to be common to most bird species, with the exception of owls (e.g. Cuthill et al. 2000; Mullen and Pohland 2008 and references therein). Some bird species have a distinct UV reflection which has been proved be important for sexual selection and mate choice (e.g. Bennett et al. 1997, Hunt et al. 1999). Birds of prey, and in particular those preying on rodents (e.g. the Eurasian Kestrel Falco tinnunculus, as well as the Common, Buteo buteo, and Rough-legged, Buteo lagopus, buzzards), have the ability to see at UV wavelengths and use UV cues in their foraging activity (Vitala et al. 1995; Koivula and Vitala 1999). The ability of birds to see in the UV part of the spectrum was initially difficult to establish. At first micro-spectrophotometry was used to examine the composite sensitivity of various cones in the retina. To do this live birds have to be kept in darkness for some time, then sacrificed (also in darkness), their eyes being removed (again in darkness) and subsequently dissected (Hart et al. 1999). Clearly the procedure was very laborious, and it is little wonder that only a few species of birds were processed, and the sensitivity of their eyes established, by the end of the millennium. A number of these were passerines, with some Galliformes, but no owls. There was, though, circumstantial evidence based on experiments with Tengmalm’s Owl in Finland (Koivula et al. 1997) to suggest a lack of UV sensitivity.

The colour sensitivity of eye pigments was directly measured in the Great Horned Owl (Jacobs et al. 1987; Crescitelli 1958), using elaborate physiological methods of electroretinogram (ERG) measurements. The ERG was recorded from a corneal contact lens electrode placed on the eye of an anesthetised owl. A flicker flashed light of the particular spectrum part (20nm wide) into the eye, while the response from the optical nerve was measured by the electromagnetic potential read by a recording device. The conclusion was that the Great Horned Owl has a maximum sensitivity to the 555–556nm light, which is close to the value of 503nm given by Crescitelli (1958) by measuring the absorption of the extracted pigment. Unfortunately these measurements were performed before the knowledge of the UV sensitivity of birds was established, so that the experiments only investigated the visual part of the spectra, 460–640nm. Other species of owls, the Snowy Owl among them, were assumed to have no UV sensitivity (Cuthill et al. 2000). To date, experiments with Rough-legged Buzzards, which often occupy habitats close to Snowy Owls, have demonstrated that they detect the UV-visible scent marks of voles (Koivula and Vitala 1999), and are therefore able to detect the small mammal density on arrival on the tundra in spring, and to take a breeding decision based on that information. In contrast, Snowy Owls, which make their breeding decision almost a month before the buzzards, must do so without such visual clues, as it cannot see the trails which are both invisible to it and, in any case, are hidden beneath the snow. So, despite its earlier arrival and the ability to take the best breeding spots before a close avian competitor arrives, the Snowy Owl is gambling on the pre-snow-melt small mammal density, and therefore might demonstrate a different breeding output in comparison to the Rough-legged Buzzard. The breeding success, or lack of it, for the Snowy Owl is therefore a direct consequence of its vision, which results from the morphological differences between itself and other predators occupying the same ecological niche. We will return to these differences in Chapter 10. The plumage colour of Snowy Owls is derived from a schemochrome feather structure which possesses little or no pigment, light reflecting within the feather to produce the coloration (Holt et al. 1995). In general the coloration of feathers is predetermined by the presence of biochrome pigments in their keratinised structures. Inheritance, the presence of the pigments, and natural selection are the most important factors in the coloration of a particular species. There are only three major groups of pigments present in bird feathers: melanins, porphyrins and carotenoids. Of these, Snowy Owls have only melanin, this being concentrated in the

40

What makes a Snowy Owl?

brown or black patches on the owl’s feathers. The obvious question is whether the owls lost the other pigments due to albinism – defined as a condition in which there is marked deficiency of pigmentation – or if there is a genetic switch which turns the pigment formation in the feathers on and off. Since palaeontological evidence (see Chapter 3) suggests that the Snowy Owl once had a much more southerly distribution than now, in areas where there was a marked seasonal climate it is possible to suggest that the birds lost their coloration as an adaptation for winter in a zone free of trees. This idea is reinforced by the fact that the plumage shows distinct adaptations towards a cold climate, e.g. the unavoidable necessity to stand on snow. Tickell (2003) speculated that if white is the structural colour of feathers and there is no selective advantage to being coloured, then natural selection will cease to maintain pigmentation, plumage becoming white by default, which is the case of the Snowy Owl. This statement has some credibility in contrast to the often-repeated mantra that the white plumage of Snowy Owls is the perfect example of ‘cryptic coloration’ (Cott 1940). The mantra raises the immediate question – cryptic for what? In summer there is no other bird on the tundra as conspicuous as the Snowy Owl. The white colour could be an adaptation to the snowy background of the Arctic winter (though bear in mind that the plumage appears white to humans, and so may not be the entire story as far as the species which share the owls’ habitat), but such coloration would then be a handicap in summer. The presence of dark spots in females and young could be an adaptation to mitigate the white colour when seen against the tundra background. But there appears to be no assortative mating based on coloration: barred and striated first-plumage young are able to mate in captivity (Flieg and Meppiel 1972). Our aim here is to re-assess the coloration of the Snowy Owl using methods that detect hidden UV colours in an objective way, independent of human colour vision. We describe the coloration of the white and black patches in the feathers using reflectance spectrophotometry and look to see if there is any hidden sexual dimorphism in coloration, as well as comparing the plumage coloration in both the visual (for humans) and UV parts of the spectrum. There is a strong case for completely reassessing the coloration of birds, and, indeed, other animals such as small mammals that signal to avian predators, using methods that are independent of human colour vision, and which incorporate the UV waveband. Since Snowy Owls spend much of their lives literally sitting in the snow against a uniform white background, it is very important how they are seen through the eyes of, say, an Arctic Fox, their prime predator, or a Willow Grouse (Lagopus lagopus), their prime prey during winter. White Arctic animals are interesting because, to date, there have been very few objective studies of their coloration. This has presumably arisen because, historically, it has seemed obvious why they are white – it camouflages the animal against a white, snow, background (e.g. Cott 1940). Such conclusions, however, assume that birds and other predators see colours as humans do. Not only is this assumption unjustified, but recent work by Koon (1998) shows that the white fur of the Polar Bear (Ursus maritimus) is highly UV absorbing, so the animal will be very conspicuous to UV sensitive animals. This finding confirms unpublished work by Professor Burkhardt of Regensburg, Germany, one of the pioneers of work on UV sensitivity in birds. Burkhardt not only found such effects in Polar Bears, but in the white plumage of various bird species. Taken together, these results indicate that it is erroneous to assume that plumage that appears white to humans will necessarily offer camouflage to Arctic animals. Rather, some white plumage and fur can be UV absorbing and thus more conspicuous, and may play a role in sexual signalling or as warning coloration. The results also raise interesting questions as to whether UV absorption in plumage facilitates protection from mutagenic UV radiation. In our study modern scientific instruments were used to assess colours objectively. These were spectrophotometers of two types – one was a Zeiss MCS 501 Diode Array

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The Snowy Owl

spectrophotometer, the other a Zeiss CLX 500 light source located at Bristol University, UK. This instrumentation was building-bound and so delivery of the Snowy Owl skins from the British Museum of Natural History, Tring had to be carefully orchestrated as most of the skins of this species are irreplaceable, and some are very old. With the arrival of a new generation of portable spectrophotometers, such as Ocean Optics S2000, we were able to take measurements in remote field locations, even of distant objects. The cosine adapter of the Ocean Optics S2000 spectrophotometer also allowed measurements of sky emissions. Coloration was assessed using reflectance spectra which incorporate the near ultraviolet and near infrared (300–800nm). Reflectance spectra are the invariant coloured features of objects, and thus the best way to measure colour. The light of the Zeiss CLXIII Xenon bulb was beamed at 45° onto a feather section and the reflected light was captured with a sensor at 90° to normal. Measurements were taken from a 2mm diameter area, recorded in 1nm steps from 300 to 700nm, and expressed relative to a Spectralon 99% white reflection standard (Labsphere, Congleton). Each spectrum consisted of 400 reflectance measurements for every 1nm step. Individual feathers were placed on black velvet during spectroradiometry to eliminate stray reflection from the background. Dark current and white standard reference measurements were taken immediately before measuring each piece to minimise any error associated with drift of the light source or sensor. The location of the measurement was chosen at random, as was the order in which the parts of the feathers from individuals were measured. We measured plumage of males and females separately, sampling five white and five dark (i.e. black or brown) regions of their feathers. We sampled the head (at the top), the back, primaries, rectrices, tail-coverts, wing-coverts, and the back of the neck. In all, a total of 240 spectral measurements were taken from 10 Snowy Owl specimens (five adult males and five adult females from Greenland, Norway and Canada) with five replications for every region and with measurements made separately for each sex. The resulting spectra were averaged, compiling five spectra taken for black bars/spots and white spaces for 12 plumage regions. We used the following regions: primaries above, primaries under vanes, rectrices above vanes, and rectrices’ reverse side, tail-coverts, upper wing-coverts, back (meaning feathers between scapulae), breast, flanks, top of the head, back of the neck, down parts of the head feathers, and reverse parts of the tail-coverts. Then this massive data set was subjected to a number-crunching session. The resulting spectra are shown in Figure 1.9. We also calculated total brightness (i.e. the sum of reflectance between 300 and 700nm) and VIS-Chroma, represented as a sum of reflectance between 400 and 700nm divided by total brightness (Figure 1.10). The VIS-Chroma was subjected to ANOVA. All the figures given below in respect of statistical significance are the results of the analysis of variance between male and female VIS-Chroma. The first striking result of this study is that the white areas of the Snowy Owl feathers are not white at all. The more-or-less white, or close-to-white lines can be seen only from wavelengths greater than 500nm, i.e. in the green and red parts of the spectrum. But even there the reflectance curve is not horizontal, and steadily increases towards the near-infrared, meaning that the feathers are more reflecting of long light waves than short waves. The white parts of the Snowy Owl feathers are not reflecting in the UV and near UV part of the spectrum. This means that for those birds which can see in UV, e.g. Willow Grouse or Ptarmigan Lagopus lagopus the Snowy Owl appears as a grey spot against a white background (Figure 1.11). Also, the dark spots do not reflect UV, but peak in the near infrared part of the spectrum (c. 1050nm). This latter peak is not shown on the graph, but there is some evidence that a very similar peak occurs in other ‘brown’ looking birds of prey such as the Eagle Owl and the Black Vulture Coragyps atratus.

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What makes a Snowy Owl?

Figure 1.9. Reflectance of black (upper curves) and white (lower curves) patches of feathers from different plumage regions in males (thick line) and females (thin line).

Figure 1.10. Mean (±SD) of total brightness (above) and VIS-Chroma (400–700nm) (b) of white and black patches of Snowy Owls in feathers from different body regions. Black: Males; Grey: Females. 3000

Total brightness of black spots 2500

2000

1500

1000

500

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The Snowy Owl

6000

Total brightness of black spots 5000

4000

3000

2000

1000

0

VIS-Chroma of black spots 0.88 0.86 0.84 0.82 0.8 0.78 0.76 0.74

VIS-Chroma of white spots 0.900.88 0.86 0.84 0.82 0.8 0.78 0.76 0.74

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What makes a Snowy Owl?

Figure 1.11. Snowy Owl as seen by conspecifics (left) and by UV-VIS sensitive birds (right). The spectrum of the snow is not affected, whereas UV absorption by the owl’s feathers was shown by shifting the reflectance spectrum 100nm towards the infrared (e.g. 300–400nm reflectance into 400–500nm zone and so forth). The resulting false colours will be a 3-dimensional cross section of the 4-dimensional vision of the birds, adapted to human eye. Another striking result from this study was the discovery of hidden dimorphism in reflectance of the feathers. In some regions of the plumage, males reflected significantly more light than females (Figure 1.9), the differences being in the visual part of the spectrum (Figure 1.10). The immediate question is, why had such a remarkable trait not been reported before? We believe this comes from the tenacious assumption that our senses are objective. In fact our eyes accommodate for white, and so we do not notice such changes. Variation in the ‘degrees’ of white in Snowy Owl skins were probably attributed to other factors, such as ageing, plumage deterioration, etc. However the UV-VIS spectrophotometer picks up the difference without difficulty and in the most objective way. Significant sexual differences in reflectance was evident in both dark and white patches at the following plumage regions: back (white, ANOVA, F=12.29, P=0.00009; black, F=31.28, P