The endocrine control of reproduction and molt in male and female emperor (Aptenodytes forsteri) and adelie (Pygoscelis adeliae) penguins

CENERALANDCOMPARATIVEENDOCRINOLOGY

The Endocrine

62,43-53

(1986)

Control of Reproduction and Molt in Male and ~ern~~~ Emperor (Aptenodytes forsferi) and Adelie (Pygoscelis adeliae) Penguins

I. Annual Changes in Plasma Levels of Gonadal Steroids and LW RENI? GROSCOLAS,

Laboratoire

de Physiologie Dijon, France; 34060 Montpellier,

MONIQUE JALLAGEAS,” ARTHUR AND IVAN ASSENMACHER”

GOLDSMITW,~

Anirnale et de la Nutrition, Facalt@ des Sciences Mirartde, B.P. 138, F-21004, *Laboratoire de Newoendocrinologie, Universitk de Montpellier Ii, France; and +ARC Research Group on Photoperiodism & Reproduction, University of Bristol, Bristol BS 8 1 UG. United Kingdom

Accepted September 30, 1985 Changes in plasma LH, testosterone, and estrogens were investigated throughout reproduction and molt in free-living male and female emperor (Aptenodytes forsteri) and adelie (Pygoscelis adeliae) penguins. In both sexes and species, plasma LN and gonadai steroids were severalfold above basal level at the time of arrival on the breeding grounds, suggesting that environmental cues (especially decreasing daylength in emperors) rather than mating and courting primarily stimulate gonadal development and reproduction. In both species a marked increase in plasma LH (both sexes), testosterone (males), and estrogens (females) corresponded with the time of maximum gonadal size, and peak values were obtained at the time of copulation, i.e., in emperors about lo-15 days prior to egg laying. In femaies, plasma LH and estrogens dropped to low levels between copulation and egg laying. Similarly, following copulation in males plasma testosterone fell to lower levels that in emperors were maintained during incubation and brooding of the non-thermally emancipated chick. Plasma LH levels followed the same trend as testosterone, falling after copulation and falling further prior to molt. Though lower than at copulation, plasma LH was higher in incubating (males) and brooding (males and females) emperors than during rearing of the thermally emancipated chicks, suggesting that plasma LH might be related to incubating, brooding, and territorial behavior. In male and female emperors and in male adelies, plasma gonadal steroids and LH were at basal levels throughout molt. o 1986 Academic PESS, IIIC.

Recent studies on the endocrine control of avian annual cycle have been mainly devoted to domesticated or captive terrestrial species of temperate and tropical regions (for review see Lofts and Murton, 1973; Follett, 2973; Farner, 1975; Assenmacher and Jallageas, 1978, 1980a, b). Some investigations have been made on wild populations of temperate-zone birds (Wingfield and Farner, 1978a, b, 1979; Lincoln et al., 1980; Schwab1 ef al.,. 1980; Dawson and Goldsmith, 1982; Silverin and Wingfield, 1982; Dawson, 1983; Silverin and Goldsmith, 1983; review by Silverin, 1984), but very little is known of the endocrinology of

birds living in polar regions. This would be of interest because of their unique environmental and biological characteristics (see below). Among polar sea birds, antarctic penguins (emperor and adelie penguins) that breed in the vicinity of the French Antarctic Station (Dumont d’urville, Adefie Land, 66” 40’S, 140” 01’ E) offer an exceptional opportunity for the study of the endocrine control of reproduction, and molt in free-ranging wild birds in their natural environment, Indeed, these large birds don’t fly and are not afraid of man. Moreover, they cancentrate on smah terrestrial 43 0016~6480186 $1.50 CopyrightQ 1986byAcademicPress,Inc. All rights ofreproduction in "ny form reserved,

44

GROSCOLAS

areas during breeding, and to a lesser extent molting, and spend a large part of the year ashore so that they can be conveniently and repeatedly caught and sampled. Emperor and adelie penguins also display unusual or even exceptional ecological and behavioral features. For instance, the emperor penguin breeds during the antarctic winter and is therefore one of the few bird which gonadal growth is coincident with short days (see Fig. 1). The emperor penguin has neither nest nor territory and the single egg, and later the young chick, is kept on the feet and warmed in a brood pouch. The male emperor performs incubation and feeds the newly hatched chick with an esophageal “curd” secretion (PrC-

Wlnterlng / ulm”

ET AL.

vost, 1961; Prevost and Vilter, 1963). The adelie penguin is a summer breeder; it builds a stony nest and lays 2 eggs at a 3-day interval, and the male performs the first shift of incubation (Sapin-Jaloustre, 1960). As other penguin species, these two antarctic penguins show a remarkable association of reproduction and molt with proLonged periods without feeding, for as long as 4 months in the breeding male emperor penguin! The process of the annual postnuptial molt is also unique in penguins in that it is of short duration-about 1 month -and that all the feathers, the short tail excepted, are simultaneously replaced. This heavy molt is therefore metabolically characterized by a high rate of feather (ker-

at sea

Male

-

i

AC

Em”

-

H

Chicks 12. 3

q.d4ilma

DAY LENGTH

L

Female

(H)

Ta (%I

JFMAMJJASONDJFM

1. Annual changes in day length, ambient temperature (Ta), extent of sea ice, and activity of emperor and adelie penguins at Dumont d’urville (66” 40’S, 140” Ol’E). Black and white strips show presence of adult birds in the colonies (fasting periods) and at sea (foraging periods), respectively; vertical and slanting hatchings indicate brooded and thermally emancipated chicks, respectively. Numbers show times of blood sampling as described in Table 1 for emperors and in Table 2 for adelies, and as used in Figs. 2 and 3. Abbreviations: A, arrival on the breeding area; C, copulatory period; L, laying for females and beginning of incubation for males; H, hatching; CRl, brooding of the chicks; CR2, feeding of the emancipated chicks. The climatic data were kindly supplied by the weather station of the Dumont d’urville Station. FIG.

REPRODUCTIVE

HORMONES

atin) synthesis and of heat production because of reduced thermal insulation, in association with complete fasting (Groscolas, 1978, 1982a). A description of the seasonal changes in environmental conditions and of the annual pattern of activity of both species appears in Fig. 1. The objective of this study was to get insight on how reproduction and molt are controlled in these two so remarkably adapted birds. The plasma levels of some major reproductive hormones (testosterone, estrogens, and LH) were presently measured during the terrestrial phases of the annual cycle. Information on circulating plasma thyroid hormones should appear in an upcoming paper (Groscolas and Leloup, 1986). MATERIALS

AND METHODS

Animals. The field part of this study was carried out in adelie and emperor penguin colonies situated 100 and 700 meters far from the Dumont d’urville Station and containing 50 and 5000 pairs, respectively. Breeding was studied in free-living birds, while molting birds were kept in a pen in their natural climatic environment. Only a limited proportion of the population molts on the breeding areas-most birds molt on the pack-ice -so that molting penguins are too scattered and cannot be conveniently and regularly sampled in free-living conditions. Since molting penguins are very inactive, confinement probably has no profound effects on their behavior. Breeding penguins were caught on the day of their arrival in the colony and identified by banding and painting marks; adelie penguin nests were also marked. Additional birds were marked at other typical stages of breeding such as laying and the beginning of incubation. Daily visual observation provided information on the breeding status of each bird at the time of blood sampiing (see Table 1). Molting penguins were marked and penned under natural climatic conditions when first sighted ashore, within 1 day after their arrival in most cases. The molt process was followed by daily visual observations of the appearance of the old plumage and by the measurement of the length of the new feathers. In male emperors, four characteristic stages of molt were recogniied according to Groscolas (1978) (see Table 1). Blood was drawn from the marginal vein of the flipper into heparinized tubes, the bird being gently kept lying down on its back with its neck and its head seized between the knees of the kneeling operator.

45

IN PENGUINS

The choice of well-experienced (aggressive) brooders allowed blood sampling in incubating male emperors without loss of the egg from the brood pouch. Routinely, blood was collected between 1400 and ,I700 hr at ambient temperature (+ 5 to - 30”) and immediately centrifuged. Plasma was stored at -20” until hormonal assays were performed in France or England. According to the “Agreed Measures for Native Fauna” recommended under the Antarctic Treaty, a very limited number of penguins were killed at typical stages of the annual cycle for various measurements. including testicular and ovarian weights. Hormonal measurements. Plasma hormone concentrations were measured, in duplicate, on samples from individual animals by radioimmunoassays previously validated for birds. Testosterone measurements were made on lOO- to 45Oql plasma samples (depending on the concentration) as described in Jallageas et nl. (1978). Preliminary tests performed on penguin samples have shown that chromatographic steps following extraction were not necessary; 5 pgitube was the lowest amount of testosterone detectable with this assay. Intra- and interassay variability was 5.5 and 9.6%, respectively. Estrogen levels were determined on IOO- to 300~~1 plasma samples as described in Barbanel and Assenmacher (1980). The sensitivity limit ~2s 10 pg and the intra- and interassay variability was 7 and 8.5%, respectively. Luteinizing hormone was measured using a homologous chicken EH assay (Follett ef al., 1972). Penguin ,plasma samples gave dilution curves parallel to that of the standard curve (chicken kH fraction IRC2), and the experimental samples were run in a single assay in duplicate at two dilutions (20, 10 ~1 plasma). The data were analysed statistically by anaiysis of variance and by the Newman-Keuls multiple range test.

RESULTS Male emperor penguin

(Fig. 2). The

sexual cycle of the male emperor penguin was characterized by marked peaks of both plasma testosterone (13.4 t 4.4 ngiml) and LH (3.4 + 0.3 n&ml> at the time of copulation. The levels of plasma hormones was already significantly (P < 0.001) above basal 1 month before when birds arrived on the breeding area (LH = 2.1 2 0.3 ng/mI, testosterone = 2.3 t 0.7 ngiml). The concentration of both .hormones fell presipitously after copulation and was only 2.6 2 1.0 (P < 0.05) and 1.3 t 0.2 (F < u.001) ngiml for testosterone and LH, respec-

46

GROSCOLAS ET AL. TABLE STAGES OF BLOOD

Stage

SAMPLING

IN BREEDING

1 AND MOLTING

EMPEROR

PENGUINS

Dates of sampling”

Description

Males 2 3 4 6

8 9 10

11 12 13 14 15 Females 1 to 3 4 5 6 7 8 9 10

One hour to 3 days after arrival from the sea on the breeding area, searching for a mate 15 + 3 days after arrival; paired; courting Within minutes following a copulation First 10 days of incubation 30 & 5th day of incubation 50 f. 5th day of incubation 1 to 5 days after hatching, feeding the chick with the esophageal “curd” secretion Departing to the sea after reunion with the female and exchange of the chick 1 to 5 days after coming back from the sea, brooding and feeding the l-month-old chick with the seafood; intensive parental care Feeding the 3-month-old thermally emancipated chick; loose parental bonds Chick rearing achieved, premolting period Beginning of molt, synthesis of the new feathers Molt, synthesis of the new feathers, and loss of the old plumage Molt, loss of the old plumage End of molt, departing to the sea id. males 7 to 12 days after copulation, 3 to 7 days before laying Within the hour following laying, about to leave the male for foraging at sea I to 7 days after laying; kept in a fence instead of travelling back to sea First shift of brooding and feeding the newly hatched chick with seafood after a 2-month sojourn at sea; intensive parental care Feeding the 3-month-old thermally emancipated chick, loose parental bonds Molting, synthesis of the new feathers, and loss of the old plumage End of molt, departing to the sea

Early April Mid-April Early May Late May Mid-June Early July Late July Late July Late August October Late December Late December Early January Mid-January Late January id. males Mid-May Mid-May Mid-May Late July Late October January Late January

a Dates of blood sampling correspond to the period of each stage in the population as a whole, except for molt dates that correspond to early molting birds.

tively, after a few days of incubation. However, while through the incubation period testosterone declined on to a low, but still severalfold more than basal, Ievel (0.3 ? 0.05 rig/ml), plasma LH was maintained at a moderately high level (1.6 2 0.2 rig/ml). This latter level was also maintained in males brooding their young chicks and feeding them with the esophageal secretion, and then with seafood, but plasma LH

declined significantly (P < 0.05) during rearing of the thermally emancipated chick and reached 0.4 _t 0.05 rig/ml at the end of the breeding period. At the same time, plasma testosterone further decreased (P < 0.02) to a very low and often undetectable levels (CO. 1 rig/ml). Plasma LH and testosterone remained at these basal concentrations throughout molt. The few measurements of testicular

REPRODUCTIVE

HORMONES

IN

PENGUINS

Testosterone (rig/ml) COURT

INCUBATION

5

11

\

I

A

I

M

I

J

I

J

t

A

law

p I

J

i

I

L Months

FIG. 2. Annual changes in plasma testosterone (0) and LH (A), and in testicular weight (0) in male emperor penguins. Values are means -C SE and the numbers besides means indicate the sample size. OS, esophageal secretion fed to the chick; BL, beginning of incubation; other abbreviations as in Fig. 1; stages numbered as in Table 1.

OESTROGENS I b-wml)

II COURT

SEA

FIG. 3. Annual changes in plasma estrogens (0) and LH (I) in female emperor penguins. Values are means I? SE and the numbers besides means indicate the sample size. Abbreviations and stages as in Fig. 1 and Table 1, respectively.

48

GROSCOLASETAL.

weight suggest that changes in testes weight run in close parallelism with those in plasma testosterone. Female emperor penguin (Fig. 3). The sexual cycle of the female emperor penguin was characterized by very sharp parallel peaks in plasma LH and estrogens with maximal levels at the time of copulation (LH = 3.5 + 1.2 r&ml; estrogens = 1.19 + 0.05 rig/ml). Plasma levels of both hormones were already significantly (P < 0.001) above basal when females arrived in the breeding colony. They fell dramatically within the week following copulation and were as low as 0.55 4 0.1 (P < 0.05) (LH) and 0.10 +- 0.03 rig/ml (P < 0.001) (estrogens) at the time of laying. This low estrogen level was maintained 2 months later in females brooding their young chicks. By contrast, by this time plasma LH had increased again to a moderately high level (1.4 i: 0.1 rig/ml) identical to that in males at the same stage. Thereafter, plasma hormones decreased (P < 0.02) in a way similar to that in males and were at basal levels (LH = 0.5 2 0.05 rig/ml; estrogens ~0.1 rig/ml) during rearing of the thermally emancipated chick (estrogens) or molt W-U. At the time of copulation, the ovary and the oviduct of one female weighed 181 and 280 g, respectively. Two markedly developed yellow yolky follicles were present (respective weight 91.5 and 54.5 g) together with numerous considerably less developed other ones (total weight ca. 25 g). The respective weights of the ovary and of the oviduct were 28 and 201 g in a second female at the time of laying and 4 and 57 g in a third bird 2 weeks after laying. Adelie penguins (Table 2). In both sexes, plasma gonadal steroids and LH were at their maximal Ievels at the time of copulation. However, in males these maximal levels were only slightly, and nonsignificantly, higher than at the time of arrival in the colony. In males, plasma testosterone was 7-fold less at the onset of incubation

than at the time of copulation, but plasma LH was only 40% lower. In females, plasma estrogens and LH decreased by 5fold from copulation to laying. Plasma testosterone and LH were at very low levels in molting males. Testicular weight was 19.6 t 3.7 g (n = 5) at the time of copulation and only 0.74 _t 0.05 g (n = 10) during molt; no ovarian weights were obtained in females. DISCUSSION

The observation that in both sexes of both penguin species the plasma levels of LH and gonadal steroids, and the testicular size in male emperor penguins, were markedly above basal at the time of arrival on the breeding grounds provides evidence that the initial phase of gonadal development occurred when birds were still at sea. Since courtship and pair-bond formation behavior requires standing on the sea-ice (emperors) or on the nest (adelies), and cannot occur in water (Jouventin, 1978), this is strongly indicative that the initial gonadal growth is not initiated by, or related to, pairing, courting, or territorial behavior. Environmental cues as basic information for the initiation of breeding must therefore be considered. The stimulation of gonadal development and thus of breeding activity, by increasing day length has been widely demonstrated in birds of temperate and tropical regions (see review by Farner, 1975). Since, apart from increasing day length, environmental factors have been steady for several months when adelie penguins began to breed (Fig. l), it is likely that long days are the major, if not unique, information that initiates breeding in this species. On the other hand, the onset of breeding in the emperor penguin is coincident with simultaneous decreases in day length and air temperature, and with formation of sea-ice. Since the breeding cycle of the emperor penguin is tightly bound to that of the sea-ice (Prevost, 1961), the ap-

REPRODUCTIVE

TABLE PLASMA

GONADAL

STEROIDS

AND

LH

2

IN BREEDING

AND MOLTING

ADELIE PENGUINS

Male Stage 1. Arrival on the breeding area 2. Copulation 3. Laying

49

HORMONES IN PENGUINS

Female

Testosterone

LH

Estrogens

LH

(&ml)

tndmi)

(r&ml)

(ngiml)

1.70 -c 0.21a.b (7) 2.32 -c 0.314 (3) -

0.48 (1) 1.06 + 0.214 (4)

1.22 (1) 2.75 I 0.33a (4)

0.19 i 0.026 -

0.50 YZ 0.08” (4) -

-

-

1.77 It 1.310 (7) 9.62 ‘-’ 1.12a (31 -

(6) 4. Beginning of incubation

1.39 t 0.12b (3

5. Molt

0.11 2 0.02c (12)

1.42 + O.lOb (4) 0.26 i 0.07~ (10)

Note. Values are mean i SE; number of individuals shown in parentheses. In a column values with different superscript letters are significantly different (P < 0.05). Stage 1, from 0.5 to 2 days after arrival; 2, within 1 hr after a copulation: 3, 1 day after laying the 1stegg; 4, first day of incubation: 5, from the beginning to the end of molt.

pearance of sea-ice might provide a major visual stimulus for the initiation of gonadal growth. However, the recent success in initiating a complete breeding cycle in emperor penguins held under a constant subfreezing temperature in an U.S. Zoo, but with a lighting system duplicating the light and the dark of the austral summer and winter (Anonymous, 1980), emphasizes the primary role of seasonal changes in day length, though not proving a direct stimulation of gonadal growth by shortening day lengths. According to observations in the spotted munia (Chandola et al., 1983) and to recent suggestions by Sharp (1984) about reproductive activity in birds, it might be hypothesized that in the emperor penguin the shortening of day length phases an autonomous rhythm of reproductive activity into Winter months. This phasing would be of a great adaptative significance since it would lead the maximum food requirement of the chicks (final growth and,fledging) to coincide with the summer peak in antarctic sea productivity. The role @food supply in relation to the onset of breeding activity also merits consideration. Since the fully developed gonads in male and female em-

perors only represent about 0.1 and 0.5% of the body mass, respectively, and since during gonadal development emperors have considerable body reserves (Groscolas, 1982a), food availability appears of any significance in the gonadal grohth. By contrast, it is likely that the deposition of the large body reserves (essentially fat stores) that are required for surviving starvation during courtship and incubation is a prerequisite for the initiation of migratory and reproductive activity. However, whether February and March is the only period during which emperors have sufficient surplus food to rapidly build body reserves is unknown. Plasma LH and estrogens in females increased during courtship, peaked at the time of copulation, and then precipitously fell between copulation and laying. That the increases in plasma LH and estrogens were closely related to the development of the ovarian follicles is indicated by the parallel increase in plasma total lipids, triglycerides, and phospholipids (Groscolas, 1982b and unpublished data) and calcium (Groscolas, unpublished data). Indeed, it is well known that in birds the lipids of the

50

GROSCOLAS

yolk are synthesized in the liver under the stimulating action of estrogens, and then transported in the blood stream to the enlarging oocyte (Sturkie, 1976). Estrogens also cause increased levels of plasma calcium in birds (Gibbins and Robinson, 1982), and have been reported to increase during vitellogenesis in several avian species. The finding that in the only female emperor that was slaughtered at the time of copulation the weight of the more developed ovarian follicle was closed to that of the egg yolk in this species (80- 120 g; Groscolas, unpublished data), together with the observation by Prevost (1961) that ovaries were at their maximum development and copulations at their highest frequency in early May, suggest that copulation and maximum plasma hormone levels were coincident with the maturation of the ovarian follicle. This is in agreement with the finding that in the female whitecrowned sparrow (Zonotrichia leucophrys pugetensis) the plasma concentrations of LH and estrone, and the size of the ovarian follicles are at their maximum at the time of copulation and ovulation (Wingfield and Farner, 1978b). A decrease in plasma LH and/or estrogens has been previously reported at the onset or through the course of incubation in females of several avian species, including white-crowned sparrows (Wingfield and Farner, 1978b, 1979), ring doves (Cheng and Follett, 1976; Goldsmith et al., 1981), mallards (Donhan et al., 1976; Goldsmith and Williams, 1980), turkeys (Burke and Dennisson, 1980), and snow geese (Campbell et al., 1978). These changes were tentatively related to incubation. In female emperors, the fall in plasma LH and estrogen levels occured several days prior to laying and was therefore independent of oviposition, of mate separation that in this species follows laying by a few hours, and of course of incubation because females in this species do not incubate. Though plasma samples have not been obtained between copulation and laying of the first egg in adelie, similar conclusion might

ET AL.

be drawn from the observation that plasma LH and estrogens were deeply depressed before the second egg was laid. A picture of the time relationship between copulation, egg yolk completion, ovulation, fertilization, and oviposition has not been obtained in penguins. However, a study on egg formation by using dye ring experiments has shown that in fiordland crested penguins (Eudyptes pachyrhynchus) yolk deposition lasts 16 days and that there was a lag of 7 days between yolk completion and oviposition (Grau, 1982). Taking account of the lofold larger size of the emperor, and based on changes in plasma lipids (Groscolas, 1982b) suggesting that in this species vitellogenesis lasts at least 1 month, it might be reasonably infered from the above data that in the emperor more than 1 week separates yolk completion from oviposition. Since ovulation obviously takes place between these two events, and since the thecal cells of the growing ovarian follicles are the major source of estrogens (Lofts and Murton, 1973), it is reasonable to suggest that it is the cessation of their secretory activity that at the time of ovulation induces a drop in plasma estrogen levels. Among possible causes for the parallel fall in plasma LH an endocrine feedback mechanism might be hypothesized. In courting male penguins, plasma LH and testosterone levels peaked at the time of copulation. Our few measurements of testicular weight, together with the observations by Prevost (1961) that the maximum development of the testes was coincident with the period of highest frequency of copulation and with the presence of spermatozoa in the lumen of the seminiferous tubes, indicate that in emperors plasma LH and testosterone are at their maximum levels when mature spermatozoa are released. This is consistent with reports of maximal plasma LH and gonadal steroids coincident with maximal gonadal weights and with copulation in other birds, e. g., the white-crowned sparrow (Wingfield and Farner, 1978b). Because no blood

REPRODUCTIVE

HORMONES

samples were taken between copulation md the onset of incubation, the timing of .he fall in plasma LH and testosterone .evels that follows copulation is not conveniently known, and consequently this fall is difficult to explain. However, it could be hypothesized that the decline in plasma LH was the consequence of the reduction of stimuli provided by copulatory and/or mating behavior. More notably, the departure of the female in the hours following laying could remove essential stimuli that induce in males an increase of gonadotropic activity beyond the level reached by the time of arrival in the breeding colony. The association of an elevated plasma LH concentration with low but above basal plasma testosterone, as observed in incubating and brooding male emperors and in earIy incubating male adelies, recalls previous findings in other birds. For example, in the male white-crowned sparrow (Z. leucophvys gambelii) there is a precipitous decrease in plasma testosterone early in incubation .despite a continued high plasma level of LH (Wingfield and Farner, 1978b). Similarly, in Z. leucophrys pugetensis, another race of white-crowned sparrow, nesting’ for the second brood is associated with a second maximum plasma level of LH without a corresponding increase in plasma testosterone (Wingfield and Farner, 1978a). In willow ptarmigan (Stokkan and Sharp, ‘1980) testosterone decreases before plasma LH after seasonal maxima are reached. Since LH has a steroidogenic function in’ birds (Maung and Follett, 1977), such a disparity between LH and .testosterone levels in the plasma is intriguing. In the; duck, a depression of plasma testosterone as a result ,of an increase in metabolic clearance rate caused by a ri!se in the concentration ,of plasma thyroid hormones has been’ demonstrated (Assenmacher et al., 1974). .Though such a metabolic change in incubating male emperors must not be discarded; it,‘cannot be related to ‘changes in Iplasma thyroid hormones whioh do not show any significant change by the same

IN PENGUINS

51

time (Groscolas and Leloup, 1986). The level of testosterone might also fall because of a decrease in the sensitivity of the Leydig cells to LH, perhaps because of a loss of LH receptors (Stokkan and Sharp, 1980). We further hypothesize that in penguins the decreased secretion of testosterone could be related to a decline in the total number of the Leydig cells. It is also noted that in both sexes of emperor penguins a moderately high plasma LH level was associated with brooding behavior (incubation in males, protection of the young chick in males and females), and that this level declined during late chick rearing when the young were no longer protected in the brood pouch, and when the bonds within the pairs and between parents and chicks became weaker. Since brood pouch of the emperor penguin may be considered as its territory (Isenmamr and Jouventin, 1970), a correlation between territorial behavior and plasma LH, as suggested recently in other male birds (Silverin, 8984, might be hypothesized. The plasma levels of LH, testosterone and estrogens were at basal in molting emperor and adelie penguins. Moreover, plasma levels of LH and testosterone did not change through the course of molt in male emperors. Similarly, basal or minimal levels of LH and’gonadal steroids were reported in molting male Peking ducks and teals (Jallageas et ai., 1978) and willow ptarmigans (Stokkan and Sharp, l%(a), and in both se’xes in white-crowned sparrows (Wingfield and Farner, 197&a, b) blackbirds (Schwab1 et al., 1981), and bar-headed geese (Dittami and Hall, 1983). This is in agreement with current ‘opinion that! in many avian species molt and reproductive capability are mutually exclusive and normally separated in time by the Cont.rsl system (e;g., Wingfield and Farnes, 19X%), and with the finding that androgens and estrogens may delay or inhibit molt (Payne, 1972; Assenmacher- and Jallageas, P98Oa). In penguins, this antagonism between reproduction and molt is further suggested by

52

GROSCOLASETAL.

our observation that young birds that have not yet reached the age of sexual maturity molt earlier in the season than successful breeders. In addition to low sex hormones titers, molting was associated in emperors and adelies with a marked increase in plasma T, and T, (Groscolas and Leloup, 1986) conformingat least for T4-to a pattern repeatedly described in molting birds (Assenmacher and Jallageas, 1980a). Thus, the hormonal status of molting emperor and adelie penguins conforms to a very general pattern prevailing in birds and consisting in a temporary imbalance between minimal sex steroid and increased thyroid hormones production. This particular molt promoting ratio between both hormonal compounds appears consistent with earlier demonstration of the protective effect of sex hormones on mature feathers opposed to the stimulating action of thyroid hormones on the early development of new feathers (Assenmacher and Jallageas, 1980a). ACKNOWLEDGMENT This study was supported by grants from Centre National de la Recherche Scientifique (RCP 764) and Terres Australes et Antarctiques Franqaises and received logistic support from ExpCditions Polaires FranCaises.

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docrinology” (A. Epple and M. H. Stetson, eds.), pp. 391-411. Academic Press, New York. Barbanel, G., and Assenmacher, I. (1980). Postnatal development of estradiol receptor in female and male rats. Mol. Cell. Endocrinol. 18, 227-239. Burke, W. H., and Dennisson, P. T. (1980). Prolactin and luteinizing hormone levels in female turkeys (Meleagris gallopavo) during a photoinduced reproductive cycle and broodiness. Gen. Comp. Endocrinol. 41, 92- 100. Campbell, R. R., Ashton, S. A., and Leatherland, J. E (1978). Seasonal changes in plasma concentrations of LH in lesser snow geese (Anser caerulescens). Biol. Reprod. 18, 663-668. Chandola, A., Bhatt, D. 1 and Pathak, V. K. (1983). Environmental manipulation of seasonal reproduction in spotted munia Lonchura punctulata. In “Avian Endocrinology: environmental and ecological perspectives” (S. Mikami, K. Homma, and M. Wada, eds.), pp. 229-242. Japan Sci. Sot. Press, Tokyo/Springer-Verlag, Berlin. Cheng, M. F., and Follett, B. K. (1976). Plasma luteinizing hormone during the breeding cycle of the female ring dove. Harm. Behav. 7, 199-205. Dawson, A. (1983). Plasma gonadal steroid levels in wild starlings (Sturnus vulgaris) during the annual cycle and in relation to the stages of breeding. Gen.

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