Stoats

The reproductive cycle in stoats is quite different from those of common and least weasels (Figure 9.4B). First, in both sexes the cycle is strictly controlled by the season, or, more precisely, by the changing ratio of light-to-dark hours (King & Moody 1982; Herbert 1989). This control is fixed, and cannot be overridden even in years when the countryside is teeming with prey. Second, the breeding cycle in stoats includes an obligatory delay in the development of the embryos, which starts about 2 weeks after fertilization. By this stage, each zygote has traveled down the fallopian tube from the ovary, developing as it goes into a hollow ball of 100 to 200 cells, a blastocyst, until it has reached the uterus.

By 38 to 40 days after mating, the tough little blastocysts are visible to the naked eye inside fresh uteri examined via transmitted light (Polkanov 2000). In common and least weasels (and most other mammals) the blastocyst then implants in the wall of the uterus and proceeds to develop to full term. But in stoats and long-tailed weasels, it stops developing and floats freely in the uterus for the next 9 to 10 months. When the days begin to lengthen again in the following spring, it reawakes and continues with its progress as if nothing had happened.

Delayed implantation (also called embryonic diapause) is one of the most fascinating puzzles among the many presented to us by the weasels (Chapter 14).

Immediately after the winter solstice, the first signs of spermatogenesis appear and the males begin to prepare for the spring breeding season. From mid-February to April their testes enlarge rapidly, stimulated by a massive rise in the level of testosterone in their bloodstreams (Gulamhusein & Tam 1974), although they are not yet capable of fertile matings because no spermatozoa have reached the epididymis. In most parts of Europe the fertile season in adults starts in May and lasts until July (in Ireland, March to August: Sleeman 2004). Thereafter, the testes regress, more slowly than they enlarged, and are small from November to early February. The regressed testes of adults in autumn and winter are still distinctly larger than the undeveloped testes of juvenile males at the same season.

The annual cycle in the ovaries (Figure 9.5) is much more complex than that in the testes. Throughout the long period of delay, the corpora lutea are small (0.7 to 0.8 mm across) and produce the small amounts of progesterone needed to maintain the blastocysts. The free blastocysts can be seen in fresh uteri, and there is a 1:1 relationship between the numbers of corpora lutea and of blasto-cysts. If the ovaries and their corpora lutea are removed during delay, the blas-tocysts decay (Shelden 1972).

As the spring days gradually lengthen, the increasing ratio of light-to-dark hours passes some more or less definite threshold, and triggers a response in the pituitary. The pituitary then begins to produce larger amounts of LH, the corpora lutea enlarge to 1.2 to 1.3 mm across, and the level of progesterone in the blood suddenly rises. These changes prepare the uterus for implantation, and also stimulate development of other essential organs, such as the mammary glands. About 10 days later the blastocysts implant, spreading themselves evenly between and along the two horns of the uterus (migrating from one to the other if need be). The embryos complete their long-interrupted growth in another 28 days. The number of implanted embryos is often less than the number of corpora lutea, meaning that some potential young have already been lost (Table 9.2).

The control of delayed implantation in stoats, and in the other mammals that have it, is complex (Mead 1989; Renfree & Shaw 2000), and requires a series of mutual signals between the blastocyst and the uterus that must be sent and received correctly. Conventional descriptions cannot account for all these events in terms of the interactions of hormones, which suggests that the most important role in this physiological drama must be played by some additional, unknown actor. Recent research has identified one gene, encoding for leukemia inhibitory factor (LIF), that has a critical role in the process of embryo implantation in several species.

LIF is most abundantly expressed in the uterus at the time of implantation, on day 4 after mating in laboratory mice and between days 19 and 25 of the menstrual cycle in humans. Genetically modified mice in which LIF is not brain pituitary gland ovary brain pituitary gland ovary

one of the two horns of the uterus

FSH = Follicle stimulating hormone LH = Luteinising hormone one of the two horns of the uterus

FSH = Follicle stimulating hormone LH = Luteinising hormone

(2) Summer: ovulation and fertilization

(3) Autumn and winter: blastocysts in delay

implanted embryos increasing day length

Figure 9.5 Hormonal control of the seasonal reproductive cycle in the female stoat.

increasing day length

implantation and development implanted embryos

Figure 9.5 Hormonal control of the seasonal reproductive cycle in the female stoat.

212 | The Natural History of Weasels and Stoats Table 9.2 Litter Size in Weasels, by Species

Stoat weasel

212 | The Natural History of Weasels and Stoats Table 9.2 Litter Size in Weasels, by Species

Data from

Country

Mean

Range

Reference

CL

Britain

10

6-

17

Rowlands (1972)

New Zealand

10

3-

20

King & Moody (1982)

Sweden

9

5-

15

Erlinge (1983)

Blastocysts

Sweden

7

1-

15

Erlinge (1983)

Embryos

Britain

9

6-

13

Deanesly (1935)

Britain

9

7-

10

McDonald & Harris (2002)

New Zealand

9

6-

13

King & Moody (1982)

Siberia

11

1-

17

Ternovsky (1983)

Births

New York

6

4-

9

Hamilton Jr. (1933)

Germany

6

4-

9

Müller (1970)

Siberia

7

1-

14

Ternovsky (1983)

USSR

9

2-

18

Heptner et al. (1967)

CL

Britain

7

4-

11

Deanesly (1944)

Embryos

Britain

6

6-

7

Deanesly (1944)

Poland

5

4-

7

Jgdrzejwska (1987)

Britain

6

4-

7

King (1980c)

Britain

6

4-

9

McDonald & Harris (2002)

Births

Britain

5

2-

7

East & Lockie (1964, 1965)

New Zealand

5

3-

6

Hartman (1964)

Embryos

Alaska

10

7-

16

Fitzgerald (1981)

Mongolia

12

5-

19

Heptner et al. (1967)

USSR

7

4-

10

Danilov & Tumanov (1975)

Births

Finland

4

4-

5

Blomquistet al. (1981)

Finland

5

1-

14

Sundell (2003)

United States

5

3-

10

Hall (1951)

Michigan

5

1-

6

Heidt (1970)

Births

N. America

7

2-

9

CL, corpora lutea expressed can mate and ovulate normally, but their embryos fail to implant (Stewart et al. 1992). In spotted skunks and in minks, which also delay implantation and are closely related to stoats, maternal expression of LIF is required for successful implantation at the end of diapause (Song et al. 1998; Hirzel et al. 1999). This observation may explain the failure of earlier attempts to induce implantation out of season by hormonal manipulation alone (Mead 1989).

Although no research has yet identified the role of LIF in stoat reproduction, we predict that LIF will be found to be critical. Delayed implantation in stoats is obligate, is prolonged, and shows no apparent natural variation (Chapter 14). Inflexible control of any biological system can only be exerted by a set of genes with almost no variation, like those that govern vital functions such as respiration, because there is never any benefit in behaving differently (Cooper

1999). The virtually zero variance in the normal reproductive cycle of female stoats should make it possible to conduct an experiment and test hypotheses even when sample sizes are small.

The internal coordination of the activities of the reproductive cycle is done by genetically controlled hormones and neurotransmitters, but the external cue that turns the system on and off is day length. Captive stoats can be induced to implant and produce their young at the wrong season by adjusting the ratio of light-to-dark hours in their cages to that typical of spring, but not simply by injecting what appear to be the right hormones (Wright 1963; Mead 1981). Where stoats normally wear a white coat in winter, it is easy to tell when a female is about to produce her young, because the molt and the breeding cycles respond together to changes in day length. Births may be expected some 22 to 25 days after the first brown hairs appear on a female's nose (Ternovsky 1983).

From carcasses, the probable date on which a litter would have been born can be estimated by inserting the average weight of the fetuses into the formula developed by Hugget and Widas (1951):

3Vw = a(t - t0), where W is the average weight of the fetuses of one litter, a is the specific fetal growth constant, t is the age of the fetuses from conception, and t0 is the intercept on the time axis. The original formula applies to all mammals, and can be adapted for any species so long as the weight of the newborn young is known and the value of a can be calculated. For example, young stoats in New Zealand are 3 to 4 g at birth (King & Moody 1982). Substituting appropriate values for a and to, and rearranging the equation, t can be calculated as a negative value, days before birth, as follows:

Stoats vary tremendously in size across their range, and in some of the local races of smaller adult body weight, the newborn young weigh under 2 g (Table 9.3). For them, this equation can be generalized to t = (24^ 3VW /3VW b) - 24, where Wb is the average weight at birth (in grams).

The gestation lengths of stoats and longtails are similar, so this equation applies to longtails as well as stoats.

The critical change in day length, which sets off the processes leading to implantation, is reached earlier in places at lower latitudes than at places nearer to the poles; hence, the young are born earlier in warmer climates. For example, in New Zealand, King and Moody (1982) collected stoats from places spanning a range of latitudes from 38°S, where implantation starts at about the end of August, to 45°S, where it starts about 10 to 15 days later. The estimated range of birth dates was from late September to mid-October (the austral spring) in the North Island, and from mid- to late October in the South Island (Figure 9.6).

The roughly equivalent dates in the northern hemisphere would range from late March or early April in California (from south of 35°N to north of 40°N) and France (south of 45°N) to late April or May in Canada (north of 45°N) and Scotland (north of 55°N). In the former USSR the range of birth dates recorded by Aspisov and Popov (1940) was from late March in the Ukraine (45 to 50°N) to early May in Tatary (55°N). Local variation spans about 3 weeks in any one place, but, compared with many other small animals, including both common and least weasels, the season of births in stoats is closely synchronized.

Day length also controls the seasonal development of the testes, so the spring rise in testis weight is conspicuously later in higher latitude males. Since day length also controls the spring molt, weasels change into their summer coats later at higher latitudes (Chapter 3). In fact, the whole suite of related spring activities is closely coordinated by the neuroendocrine system and adjusted to the expected environmental conditions.

While her young are still suckling, a mother stoat comes into heat again. Estrus normally follows littering in adults, and preparations for it are, therefore, also controlled by day length. When the days reach a certain length, follicle-stimulating hormone (FSH) from the pituitary stimulates the ovary to produce estrogen, which prepares the vulva for mating. An estrous female will not ovulate

30

25

03

20

ro

O

15

si

m

10

5

Oct

Sep

30

25

37 38 39 40 41 42 43 44 45 Degrees South Latitude

Figure 9.6 The date of implantation in stoats is controlled strictly by day length, so the date of birth of the young is significantly related to latitude. (Note: October is spring in New Zealand.) (Redrawn from King & Moody 1982.)

until she has mated, though, and remains in heat (with swollen vulva) until after mating. The pituitary will not release the LH, necessary for ovulation until it receives the nervous signals from the vulva (Figure 9.5).

It is, therefore, easy to tell the state of any given female because, as soon as she has mated, the swollen vulva subsides and a fresh set of corpora lutea appears in the ovaries. The corpora lutea persist for most of the year, whether or not any young are eventually born, and successive generations of corpora lutea cannot overlap, because each set degenerates before the next estrus.

The male who serves the adult female also fertilizes her precocious female young (p. 225). So, by midsummer practically all wild females of all ages (>99%) are pregnant, carrying a new set of blastocysts and showing no signs of recent estrus. If estrus is brief and synchronized by day length, males must be very good at finding receptive females. The proverbial English description of a particularly persistent human suitor as "a bit of a stoat" (Drabble 1977) is obviously quite a compliment. Meanwhile, in adults the postpartum estrus (extended for as long as is necessary to find a mate) and prolonged delay in implantation mean that almost all female stoats are pregnant almost all the year round. If there were a prize for the sexiest animal, the stoat would surely win it.

According to Ternovsky (1983), Amstislavsky and Ternovskaya (2000), and Polkanov (2000), the estrous season of captive Russian stoats can be months long, and individually variable if a female does not mate early in her season. The gestation period is also variable, depending on the date of mating, and is significantly longer in young females (averaging 317 days) than in adults (averaging 298 days). In New Zealand, three captive females kept in isolation by King and Moody (1982) were still in full heat some 3 months after the normal season, and had no corpora lutea.

How is it, then, that in the wild, estrus is brief, and no prolonged estrus season is ever observed? For example, among 46 adult females collected from all over New Zealand in the southern spring months of September and October, 45 were not yet in estrus, five were in the stage immediately preceding estrus, and only one was in full estrus. Not one of 38 newly independent young females collected in early summer (December) showed any sign of recent estrus (King & Moody 1982:117); all had mated and estrus was over. We conclude that the reported cases of lengthy estrus in caged animals are an artifact of captivity; they might extend the opportunities for breeding stoats for research, but they do not reflect the habits of wild females. Only a lone female with no male for miles and miles around (say, isolated on an island) might prolong her estrus in the wild.

Two persistent errors concerning the breeding of stoats have confused people for many years despite a total lack of evidence that either is true. The first is the idea that females ovulate spontaneously throughout the year but do not conceive until the spring. This story arose because Deanesly (1935), who undertook the first intensive study of the reproductive cycle of stoats, did not know about induced ovulation or delayed implantation. She therefore interpreted the corpora lutea of delay as spontaneous infertile ovulations. Alerted by Wright (1942a), she later re-examined her material and published a correction (Deanesly 1943). Nonetheless, the earlier paper was so good in every other respect, so thorough and so much more widely read than the correction, that the mistake was repeated in general reference books for the following 30 years.

The second error is the idea that the few females that do not conceive during the main breeding season get a second chance the following spring, and that litters conceived then develop directly, with no delay in implantation (Watzka 1940; Kopein 1965). There is no empirical support for this interpretation, either from examination of the reproductive state of large samples of wild-caught females or from extensive observation of the mating behavior of stoats in captivity, but it is an understandable mistake. Females that lose their entire litters for any reason do come into estrus earlier than others, and are ready to mate in spring before any young conceived the previous year could have been born. These females can be fertilized as soon as the males are ready, which could be 6 to 8 weeks before the successful breeders reach postpartum estrus. These early-breeding females must, nonetheless, wait until the following year to produce their young, after an unusually long period of delay.

Since shortage of food is a critical factor controlling the survival of young weasels of all species born in the wild, and since every female stoat captured during summer, autumn, and winter is already pregnant, one might expect it to be easy to establish a breeding colony of stoats in captivity, simply by catching females over most of the year and feeding them well. Unfortunately, that is not the case. Although some breeding colonies of stoats have been established (Müller 1970; Ternovsky 1983; DonCarlos et al. 1986), many females fail to produce young when brought into captivity (McDonald & Lariviere 2002; O'Connor et al 2004)). Virtually all wild-caught female stoats of all ages carry fertilized blastocysts, but they seem especially vulnerable to the stress of captivity, especially at first.

What sort of five-star treatment wild-caught females need before they can be persuaded to produce their young in the confinement of a cage is still not entirely clear, although at least one thing seems certain: Female weasels of all species (except, perhaps, the large British stoats) breed best on a diet of small rodents (DonCarlos et al. 1986; Sundell 2003). More important, since well-adjusted and well-fed adult females can live for several years, we need to know how to encourage adults acclimatized to captivity to breed year after year.

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