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Post-hatching thyroid development and body growth in precocial vs altricial birds
Camp. Biochem. Physiol. Vol. 18A, No. 4, pp. 629-635, Printed in Great Britain
1984 0
0300-9629/84 $3.00 + 0.00 1984 Pergamon Press Ltd
POST-HATCHING THYROID DEVELOPMENT AND BODY GROWTH IN PRECOCIAL vs ALTRICIAL BIRDS F. M. ANNE MCNABB, FRANCIS W. STANTON* and SAMUEL G. DICKEN Department
of Biology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, U.S.A. (Received 8 December 1983)
Abstract-l. Thyroid growth, thyroid function and body growth are markedly different in developing precocial Japanese quail and altricial Ring doves despite comparability in incubation period, hatchling size, adult body weight and adult serum thyroid hormone concentrations. 2. In quail thyroid activity is high during the perinatal period, declines shortly after hatching, then gradually attains adult function. 3. In contrast, in doves, there is no perinatal peak of thyroid activity. Thyroid function is low at hatching and increases steadily during the first week. Serum hormone concentrations vary around a mean similar to that of adults during the remainder of the nestling and fledgling periods.
INTRODUCTION
development of thermoregulatory control in homeothermic animals proceeds by two types of pattern. Precocial animals are born/hatched at a reIatively advanced stage of development, show endothermic responses to cold and develop good thermoregulatory control relatively early. Altricial species are born/hatched in a less advanced condition, require complete parental care, remain essentially ectothermic for some time and acquire thermoregulatory control and the ability to respond endothermically to cold at a later stage. The thyroid gland is known to play an important role in growth and development and in governing the intensity of metabolic activity. Thyroid function during development has been studied in a number of species of birds and mammals. However, there have been no studies that have compared thyroid development in a precocial and an altricial species that are metabolically similar as adults and are from the same vertebrate class. Our objective in this study was to compare the pattern of thyroid growth and function in precocial vs altricial development. We chose two avian species with approximately the same adult body size and the same length (16.5 day) incubation period. Japanese quail were used as the example of a precocial species; Ring doves were used as the altricial species. The patterns of growth in altricial and precocial birds have been compared by Ricklefs (1973, 1979) but species of equal body weight (W,) have not been studied. The ontogeny of thermoregulation has been described for quail by Freeman (1967) and Spiers et al. (1974); for Mourning doves by Breitenbach and The
*Present address: Department of Medical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 32610, U.S.A.
Baskett (1967). The development of thyroid function in quail, during embryonic life, has been described (McNabb et al., 1981) but post-hatching thyroid function has not. The development of thyroid function in doves has not been described, although histological evidence suggests very low activity during the embryonic period (McNabb and McNabb, 1977a). MATERIALS AND METHODS Fertile eggs from Japanese quail (Coturnix coturnix juponica) werebtained from the Poultry Science Department, VP1 & SU. and incubated at 38 i 1°C. Chicks were housed in plastic ‘cages. Maintenance temperatures were varied accbrding to the scheme of thermoregulatory development indicated bv Freeman (1967): 35 + 1°C for the first 8 davs ~ and 32 f: 1°C for 8-21 days. At 21 days, chicks were transferred to large wire cages and maintained at room temperature (18 + 2°C). A 14L: 10D photoperiod was used throughout the study. Food (Purina Game Bird Startena for 21 days, then Purina Layena) and water were provided ad I.
libitum.
Adult Ring doves (Streptopelia risoria) were obtained from game breeders and housed in individual pairs in wire cages 8 x 20 x 13 inch or larger. The photoperiod used was 14L: 10D. Food (Purina Pigeon Checkers) and water were provided ad libitum. Glass dishes or clay flowerpot saucers (4-5 inch diameter) were provided as nest bowls. Shredded paper (i x @inch) was provided as nest material. Young doves were reared by the adults. Young were observed daily to provide descriptive information about their development. Thyroid weights (W,; to 0.01 mg) and W, (to 0.1 g) were obtained during both the lzsI uptake and serum hormone studies. Thyroidal uptake of “‘1 in qu$l and doves was assessed using intraperitoneal injections of 2 pCi/bird of carrier-free Na’*‘I in 25 pl of 0.9% NaCl. To assess potential differences in constant dose vs weight-specific radioiodine uptake experiments a second developmental sequence of quail were investigated using a weight-specific lZsI dose of 2.OpCi/lOOg body weight. Injection time was between 8 and 10:00 a.m. EDST in all uptake experiments. During the experiments, water but no food was available.
629 C.&P.7*,4*-a
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Fig. 1. Body growth and plumage development in Japanese quail and Ring doves. Values for quail (H) are the mean + SE (N = IO); in some cases error bars are within the size of the symbols. Values for doves (e) are individual measurements; the solid line is described by the equation Y = 6.97~O.~‘,J = juveniles, A = adults. Quail plumage data are from McNabb and McNabb (1977b). The results, for quail, of Duncan’s new multiple range test (ages joined by solid lines do not differ significantly) are: H -
4 6 8 9 11 12 16 15 20 21 28 22 A
The quail were held at their previous maintenance temperatures. For young doves, heat lamps were used to provide temperatures comparable to those provided by brooding adults. The uptake period was 6 hr for quail so the results would be comparable to our previous study with embryos (McNabb et al., 1981). Two-hour uptake periods were used for the nestling doves because longer experiments would have required feeding by the parents. At the end of the uptake period each bird was killed by decapitation and the thyroids were removed, weighed, placed in 1.0 ml of 0.9% NaCl and counted in a Beckman 5500 gamma counter (Beckman Instruments, Silver Spring, MD). All counts were made to 399% confidence and corrected for background radiation and coincidence losses. Serum hormone values for quail are from McNabb and Hughes (1983). Blood from doves was collected from the jugular vein/carotid artery after decapitation, in all age groups except adults, where blood was collected from the brachial vein. Concentrations of serum T3 and T4 were measured using a double antibody RIA (McNabb and Hughes, 1983) verified for use on dove serum as described by McNabb et al. (1981). For the data on quail, statistical comparisons were made by Student’s t-test or Duncan’s New Multiple Range Test. P values of GO.05 were considered indicative of statistically significant differences. Data for doves are presented as scatter diagrams because of the highly variable sample numbers due to the lack of synchronony of breeding times in the dove colony.
RESULTS Body growth and development
The Japanese quail and Ring doves used in this study had similar IV, at hatching (6-8 g) and as adults (130-160 g), but exhibited very different growth rates during the first 3 weeks after hatching (Fig. 1). Quail chicks remained at their hatching weight for 4 days, then W, increased until day 22. The growth rate of doves during this period was considerably faster than that of quail. For example, in the first 20 days doves increase in W, 14.3 x while quail increase in W, only 6.6 x . The developmental pattern of body growth and feathering of quail used in this study was characteristic of that previously described @piers et al., 1974; McNabb and McNabb, 1977b). Quail chicks are hatched covered with down which persists until it is replaced by juvenile plumage. Juvenile contour feathers emerge from day 5 onward and unfurl from days 12-17 (Fig. 1). In contrast, hatchling doves were naked, unfeathered and lacking in physical coordination. Feather shafts had emerged and were beginning to open by day 7, most feathers were unfurled by day 10 and the juvenile plumage was fully developed by days 1618 (Fig. 1). The nestlings were
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Fig. 2. Thyroid weight (a) and thyroid weight/body weight ratios (b) in Japanese quail and Ring doves. Values for quail (M) are the mean I SE (N = 5-17); in some cases error bars are within the size of the symbols. The results, for quail, of Duncan’s new multiple range test are presented above each graph. Ages joined by solid lines do not differ significantly. Values for doves (0) are individual measurements; the solid line in (a) is described by the equation Y = 0.63x’@‘, in (b) by Y = 0.01 +4.23x. J = juveniles, A = adults.
brooded almost continuously by the adults for the first 6 days but by day 8 the parents spent most of the day off the nest. The nestlings were fed by the parents through day 10, after which there was a steady increase in feeding self-sufficiency of the young. Locomotor activity of the nestlings was very limited until days 8-10, but improved steadily between days 10 and 16. By day 18 the young were hopping onto perches and fluttering down from them. Fledging occurred between days 20 and 22. Thyroid growth The pattern of thyroid growth and its relationship to body growth differs in the two species. In quail, the thyroid grows relatively slowly compared to the body (Fig. 2a); the W,/W, ratio at hatching is greater than twice that of adults and declines markedly during the first three weeks (Fig. 2b). In doves, post-hatching thyroid growth is rapid and parallels body growth (Fig. 2a); the W,/ W, ratio at hatching is not
significantly different from that of adults. F?, and the W,/ W, ratio are highly variable from days 9 to 19 (Fig. 2b). Thyroid function In quail chicks, 6 hr thyroidal lz51 uptakes decreased between the end of the perinatal period (day of hatching and day 1) and day 4, then increased steadily to peak at day 21 (Fig. 3a). In this constant dose experiment (2 pCi/bird), thyroidal ‘25I uptake of 12-28 day chicks was significantly greater than that of adults. A second experiment, in which the ‘25Idose was scaled to W,, showed the same pattern of results. Weight-specific iodine uptake (%lz51 dose/mg thyroid weight) was variable but generally remained at the same level throughout the development range studied. In nestling doves, thyroidal “‘1 uptakes increased in the first few days after hatching and showed a peak of activity on days 7-9. The values were variable, but
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Fig. 3. Thyroidal radioiodine uptakes of Japanese quail. Values are the mean + SE (N = 5-17) of the thyroidal “‘1 content 6 hr after injection of a 2 pCi dose. The results of Duncan’s new multiple range test are presented above each graph. Ages joined by solid lines do not differ significantly. A = adults.
tended to be above adult or juvenile values, for the remainder of the nestling period (Fig. 4). Weightspecific, 2 hr iodine uptakes decreased exponentially (Y = 3.78 e”.o’x) from hatching (3.37% of dose/mg thyroid, 8 g bird) through to adult body size (0.29% of dose/mg thyroid, 180 g bird).
DISCUSSION
This study revealed striking differences in the ontogeny of thyroid function and circulating thryroid hormone concentrations during post-hatching development in precocial vs altricial birds. Growth patterns were also different and were consistent with published descriptions of these developmental modes (Ricklefs, 1973, 1979). In precocial species, such as chickens and quail, there is a period of rapid thyroid maturation just prior to hatching. Thyroid hormone concentrations peak during the perinatal period with the initiation of pulmonary respiration, the overt activity of hatching and the initiation of endothermic responses to cooling (chickens: reviews by Freeman, 1971a, 1974;
Serum concentrations of both thyroid hormones, in quail, were high during the perinatal period, decreased in the early post-hatching period, then changed gradually to reach adult levels (Figs 5 and 6). In contrast, in doves, serum concentrations of both hormones were low at hatching, rose during the nestling period and stabilized several days before fledging. Fledgling serum T, concentrations were similar to those of adults (Fig. 6); serum T, concentrations were about 70% those of adults (Fig. 5).
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Fig. 4. Thyroidal radioiodine uptakes of Ring doves. Values are individual measurements of thyroidal tz51content 2 hr after injection of a 2 PCi dose. J = juveniles, A = adults.
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Fig. 5. Serum T4 concentrations in Japanese quail and Ring doves. Values for quail (a) are from McNabb and Hughes (1983) and are expressed as the mean + SE (iv = 612); in some cases error bars are within the size of the symbols. The results, for quail, of Duncan’s new multiple range test are presented above each graph. Ages joined by solid lines do not differ si~i~~tly. Values for doves (0) are ~ndi~dual measurements; the solid line is described by the equation Y = 3.39x0,53.A = ad&s.
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Fig. 6. Serum T, concentrations in Japanese quail and Ring doves. Values for quail (m) are from McNabb and Hughes (1983) and are expressed as the mean + SE (N = 6-12); in some cases error bars are within the size of the symbols. The results, for quail, of Duncan’s new multiple range test are presented above each graph. Ages joined by solid lines do not differ si~ificantly. Values for doves (@) are in~vidual meas~ements; the solid line is described by the equation Y = 0.98x0.@. A = adults.
634
I;. M. ANNE MCNABBer al
Thommes and Hylka, 1977; quail: McNabb ed al., 1981; McNabb and Hughes, 1983). The present study shows that in quail thyroid activity (as indicated by thyroidal “‘1 uptakes, serum T4 and serum T, concentrations) decreased in the first few days after hatching. Concurrently there is yolk sac resorption and an increase in metabolic mass without a concomitant increase in Wa (Freeman, 1967). The W,/ W, ratio decreases rapidly during this time and continues to decrease slowly for the remainder of the juvenile period. This contrasts with the embryonic period when W,/ W, is essentially constant (McNabb et al., 1981). Serum thyroid hormone concentrations have reached a plateau by the time quail chicks first regulate their body temperature (at levels less than those of adults} at 13-15 days of age @piers et aZ., 1974). However, thyroidal ‘*‘I uptakes continue to rise until day 21. This is the time at which the coefficient of temperature regulation reaches an asymptote indicating juvenile temperature regulation equivalent to that of adults (Ricklefs, 1979). It is also the period of juvenile plumage growth. The increasing thyroidal radioiodine uptakes but stable serum hormone levels between days 13 and 21 could indicate either (I) a change in thyroid gland dynamics resulting in net iodine accumulation (hormonal plus non-hormonal), or (2) increased hormone turnover/excretion with high thyroid hormone production. Serum concentrations of thyroid hormones in juvenile quail do not differ si~ificantly from those of ad&s. Studies of hormone turnover and thyroid gland hormone content are needed to evaluate these possibilities. Altricial doves contrast with precocial quail in essentially all aspects of the ontogeny of thyroid function and general growth and development. Doves have low serum thyroid hormone concentrations on the day of hatching (this study) and in late embryos just prior to hatching (unpublished results, our laboratory) as predicted by our earlier study of thyroid histology (McNabb and McNabb, 1977a). Thus they appear to lack a perinatal thyroid hormone peak as seen in precocial species. Of the perinatal events, doves differ from quail only in the absence of endothermic responses to cooling. This suggests that early thermoregulatory responses are of primary importance in the perinatal burst of thyroid activity in precocial species. However, in quail, thyroid hormones rise well before external pipping, the first stage when cooling is likely to elicit a metabolic response. In chickens, roles for thyroid hormones in readiness for hatching, initiation of pulmonary respiration (see review by Freeman, 1974) and thermogenic responses (Freeman, 1971b) have been demonstrated. Detailed investigations of thyroid hormones during the perinatal period are needed in altricial birds to determine whether there are smaller, more transient hormone peaks. The general pattern of growth and development in doves in our study corresponded closely to that described for Mourning doves by Breitenbach and Baskett (1967). Body and thyroid growth were in parallel and rapid in comparison to those of quail. Thyroid functional activity (as indicated by thyroidal lz5T uptake and serum thyroid hormone concen-
trations) increased relatively rapidly during early post-hatching life. Thyroidal radioiodine uptakes are highest at about 6-8 days coincident with the beginning of coordinated locomotor activity and a rather abrupt decrease in parental brooding and feeding of the nestlings. Few of the feathers have unfurled by this time so the vascular feather quails may actually increase the surface area available for heat loss. Breitenbach and Baskett (1967) describe doves at this stage as “precarious homeotherms” that are just beginning to develop temperature control. Serum thyroid hormone concentrations of doves reach a plateau by about 12 days, although a number of developmental changes significant to energetics are still occurring (completion of juvenile plumage, increasing locomotor capability, decreasing parental care and brooding). The attainment of stable hormone concentrations coincides with the beginning of homeothermy as indicated by body temperatures of 3941°C in non-brooded nestlings after 12 days of age (unpublished preliminary data, our laboratory). As in the case of quail, additional information about thyroid gland function and hormone turnover rates during the period through fledging is needed to understand the roles of the thyroid in this developmental stage. Acknowledgements-This study was supported by NIH grant No. ROI AM28216 to F.M.A.M. and a Virginia Academy of Sciences grant to F.W.S. We thank T. E. Hughes for technical assistance and S. Ngo, M. Daly, M. Urbane and H. McCusker for help with animal care. The Department of Poultry Science kindly provided fertile quail eggs for use in this study. REFERENCES Breitenbach R. P. and Baskett T. S. (1967) Ontogeny of the~ore~ation in the Mourning dove. Physiol. Zooi. 40, 207-2 17. Freeman B. M. (1967) Oxygen consumption by the Japanese quail (Coturnix coturnix japonica). Br. Poult. Sri. 8, 147-152. Freeman B. M. (1971a) Body temperature and thermoregulation. Chapt. 48 in Phy~jo~og~~and ~~oc~erni~tr_~ of the ~orne~t~c Fowl (Edited by Bell D. J. and Freeman 3. M.). Academic Press, London. Freeman B. M. (1971b) Imnaired thermoreguiation in the thiouracil-treated nednate~fowl. Comp. B&hem. Physiol. 40A, 5.53-5.55. Freeman B. M. (1974) Hormones in Development. Chapt. 13 in Deuelopment of the Avian Embryo (Edited by Freeman B. M. and Vince M. A.). Chapman & Hail, London. McNabb F. M. A. and Hughes T. E. (1983) The role of serum binding proteins in determining free thyroid hormone concentrations during development in quail. Endocrinology 113, 957-963. ^ _ McNabb F. M. A. and McNabb R. A. (1977a) Thvroid development in precocial and ahricial a&n embryos. The A& 94, 736-742. McNabb F. M. A. and McNabb R. A. (1977b) Skin and plumage changes during the development of thermoregulatory ability in Japanese quail &ricks. Comp. Biothem. Phvsiol. 58A. 163-166. McNabb F.-M. A., W&rich R. T. and McNabb R. A. (1981) Thyroid function in embryonic and perinatal Japanese quail. Gen. camp. Endocrinof. 43, 218-226. Ricklefs R. E. (1973) Patterns of growth in birds. II. Growth rate and mode of development. The Ibis 115, 177-201.
Thyroid development and body growth in birds Ricklefs R. E. (1979) Patterns of growth in birds. IV. A comparative study of development in the Starling, Common tern and Japanese quail. The Auk 96, 10-30. Spiers D. E., McNabb R. A. and McNabb F. M. A. (1974) The development of thermoregulatory ability, heat seeking activities, and thyroid function in hatchling Japanese
635
quail (Coturnix coturnix japonica). J. camp. Physiol. 89, 159-174. Thommes R. E. and Hylka V. W. (1977) Plasma iodothyronines in the embryonic and immediate post-hatch chick. Gem. camp. Endocrinol. 32, 417-422.
1984 0
0300-9629/84 $3.00 + 0.00 1984 Pergamon Press Ltd
POST-HATCHING THYROID DEVELOPMENT AND BODY GROWTH IN PRECOCIAL vs ALTRICIAL BIRDS F. M. ANNE MCNABB, FRANCIS W. STANTON* and SAMUEL G. DICKEN Department
of Biology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, U.S.A. (Received 8 December 1983)
Abstract-l. Thyroid growth, thyroid function and body growth are markedly different in developing precocial Japanese quail and altricial Ring doves despite comparability in incubation period, hatchling size, adult body weight and adult serum thyroid hormone concentrations. 2. In quail thyroid activity is high during the perinatal period, declines shortly after hatching, then gradually attains adult function. 3. In contrast, in doves, there is no perinatal peak of thyroid activity. Thyroid function is low at hatching and increases steadily during the first week. Serum hormone concentrations vary around a mean similar to that of adults during the remainder of the nestling and fledgling periods.
INTRODUCTION
development of thermoregulatory control in homeothermic animals proceeds by two types of pattern. Precocial animals are born/hatched at a reIatively advanced stage of development, show endothermic responses to cold and develop good thermoregulatory control relatively early. Altricial species are born/hatched in a less advanced condition, require complete parental care, remain essentially ectothermic for some time and acquire thermoregulatory control and the ability to respond endothermically to cold at a later stage. The thyroid gland is known to play an important role in growth and development and in governing the intensity of metabolic activity. Thyroid function during development has been studied in a number of species of birds and mammals. However, there have been no studies that have compared thyroid development in a precocial and an altricial species that are metabolically similar as adults and are from the same vertebrate class. Our objective in this study was to compare the pattern of thyroid growth and function in precocial vs altricial development. We chose two avian species with approximately the same adult body size and the same length (16.5 day) incubation period. Japanese quail were used as the example of a precocial species; Ring doves were used as the altricial species. The patterns of growth in altricial and precocial birds have been compared by Ricklefs (1973, 1979) but species of equal body weight (W,) have not been studied. The ontogeny of thermoregulation has been described for quail by Freeman (1967) and Spiers et al. (1974); for Mourning doves by Breitenbach and The
*Present address: Department of Medical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 32610, U.S.A.
Baskett (1967). The development of thyroid function in quail, during embryonic life, has been described (McNabb et al., 1981) but post-hatching thyroid function has not. The development of thyroid function in doves has not been described, although histological evidence suggests very low activity during the embryonic period (McNabb and McNabb, 1977a). MATERIALS AND METHODS Fertile eggs from Japanese quail (Coturnix coturnix juponica) werebtained from the Poultry Science Department, VP1 & SU. and incubated at 38 i 1°C. Chicks were housed in plastic ‘cages. Maintenance temperatures were varied accbrding to the scheme of thermoregulatory development indicated bv Freeman (1967): 35 + 1°C for the first 8 davs ~ and 32 f: 1°C for 8-21 days. At 21 days, chicks were transferred to large wire cages and maintained at room temperature (18 + 2°C). A 14L: 10D photoperiod was used throughout the study. Food (Purina Game Bird Startena for 21 days, then Purina Layena) and water were provided ad I.
libitum.
Adult Ring doves (Streptopelia risoria) were obtained from game breeders and housed in individual pairs in wire cages 8 x 20 x 13 inch or larger. The photoperiod used was 14L: 10D. Food (Purina Pigeon Checkers) and water were provided ad libitum. Glass dishes or clay flowerpot saucers (4-5 inch diameter) were provided as nest bowls. Shredded paper (i x @inch) was provided as nest material. Young doves were reared by the adults. Young were observed daily to provide descriptive information about their development. Thyroid weights (W,; to 0.01 mg) and W, (to 0.1 g) were obtained during both the lzsI uptake and serum hormone studies. Thyroidal uptake of “‘1 in qu$l and doves was assessed using intraperitoneal injections of 2 pCi/bird of carrier-free Na’*‘I in 25 pl of 0.9% NaCl. To assess potential differences in constant dose vs weight-specific radioiodine uptake experiments a second developmental sequence of quail were investigated using a weight-specific lZsI dose of 2.OpCi/lOOg body weight. Injection time was between 8 and 10:00 a.m. EDST in all uptake experiments. During the experiments, water but no food was available.
629 C.&P.7*,4*-a
-
F. M. ANNE MCNABBet al.
630
. .. .
AGE
(doyr)
Fig. 1. Body growth and plumage development in Japanese quail and Ring doves. Values for quail (H) are the mean + SE (N = IO); in some cases error bars are within the size of the symbols. Values for doves (e) are individual measurements; the solid line is described by the equation Y = 6.97~O.~‘,J = juveniles, A = adults. Quail plumage data are from McNabb and McNabb (1977b). The results, for quail, of Duncan’s new multiple range test (ages joined by solid lines do not differ significantly) are: H -
4 6 8 9 11 12 16 15 20 21 28 22 A
The quail were held at their previous maintenance temperatures. For young doves, heat lamps were used to provide temperatures comparable to those provided by brooding adults. The uptake period was 6 hr for quail so the results would be comparable to our previous study with embryos (McNabb et al., 1981). Two-hour uptake periods were used for the nestling doves because longer experiments would have required feeding by the parents. At the end of the uptake period each bird was killed by decapitation and the thyroids were removed, weighed, placed in 1.0 ml of 0.9% NaCl and counted in a Beckman 5500 gamma counter (Beckman Instruments, Silver Spring, MD). All counts were made to 399% confidence and corrected for background radiation and coincidence losses. Serum hormone values for quail are from McNabb and Hughes (1983). Blood from doves was collected from the jugular vein/carotid artery after decapitation, in all age groups except adults, where blood was collected from the brachial vein. Concentrations of serum T3 and T4 were measured using a double antibody RIA (McNabb and Hughes, 1983) verified for use on dove serum as described by McNabb et al. (1981). For the data on quail, statistical comparisons were made by Student’s t-test or Duncan’s New Multiple Range Test. P values of GO.05 were considered indicative of statistically significant differences. Data for doves are presented as scatter diagrams because of the highly variable sample numbers due to the lack of synchronony of breeding times in the dove colony.
RESULTS Body growth and development
The Japanese quail and Ring doves used in this study had similar IV, at hatching (6-8 g) and as adults (130-160 g), but exhibited very different growth rates during the first 3 weeks after hatching (Fig. 1). Quail chicks remained at their hatching weight for 4 days, then W, increased until day 22. The growth rate of doves during this period was considerably faster than that of quail. For example, in the first 20 days doves increase in W, 14.3 x while quail increase in W, only 6.6 x . The developmental pattern of body growth and feathering of quail used in this study was characteristic of that previously described @piers et al., 1974; McNabb and McNabb, 1977b). Quail chicks are hatched covered with down which persists until it is replaced by juvenile plumage. Juvenile contour feathers emerge from day 5 onward and unfurl from days 12-17 (Fig. 1). In contrast, hatchling doves were naked, unfeathered and lacking in physical coordination. Feather shafts had emerged and were beginning to open by day 7, most feathers were unfurled by day 10 and the juvenile plumage was fully developed by days 1618 (Fig. 1). The nestlings were
631
Thyroid development and body growth in birds
24
8
22 t
.
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5 cl
12
H
.
2
4
6
8
IO
12
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16 AGE
18
20
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J
A
(days)
Fig. 2. Thyroid weight (a) and thyroid weight/body weight ratios (b) in Japanese quail and Ring doves. Values for quail (M) are the mean I SE (N = 5-17); in some cases error bars are within the size of the symbols. The results, for quail, of Duncan’s new multiple range test are presented above each graph. Ages joined by solid lines do not differ significantly. Values for doves (0) are individual measurements; the solid line in (a) is described by the equation Y = 0.63x’@‘, in (b) by Y = 0.01 +4.23x. J = juveniles, A = adults.
brooded almost continuously by the adults for the first 6 days but by day 8 the parents spent most of the day off the nest. The nestlings were fed by the parents through day 10, after which there was a steady increase in feeding self-sufficiency of the young. Locomotor activity of the nestlings was very limited until days 8-10, but improved steadily between days 10 and 16. By day 18 the young were hopping onto perches and fluttering down from them. Fledging occurred between days 20 and 22. Thyroid growth The pattern of thyroid growth and its relationship to body growth differs in the two species. In quail, the thyroid grows relatively slowly compared to the body (Fig. 2a); the W,/W, ratio at hatching is greater than twice that of adults and declines markedly during the first three weeks (Fig. 2b). In doves, post-hatching thyroid growth is rapid and parallels body growth (Fig. 2a); the W,/ W, ratio at hatching is not
significantly different from that of adults. F?, and the W,/ W, ratio are highly variable from days 9 to 19 (Fig. 2b). Thyroid function In quail chicks, 6 hr thyroidal lz51 uptakes decreased between the end of the perinatal period (day of hatching and day 1) and day 4, then increased steadily to peak at day 21 (Fig. 3a). In this constant dose experiment (2 pCi/bird), thyroidal ‘25I uptake of 12-28 day chicks was significantly greater than that of adults. A second experiment, in which the ‘25Idose was scaled to W,, showed the same pattern of results. Weight-specific iodine uptake (%lz51 dose/mg thyroid weight) was variable but generally remained at the same level throughout the development range studied. In nestling doves, thyroidal “‘1 uptakes increased in the first few days after hatching and showed a peak of activity on days 7-9. The values were variable, but
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tended to be above adult or juvenile values, for the remainder of the nestling period (Fig. 4). Weightspecific, 2 hr iodine uptakes decreased exponentially (Y = 3.78 e”.o’x) from hatching (3.37% of dose/mg thyroid, 8 g bird) through to adult body size (0.29% of dose/mg thyroid, 180 g bird).
DISCUSSION
This study revealed striking differences in the ontogeny of thyroid function and circulating thryroid hormone concentrations during post-hatching development in precocial vs altricial birds. Growth patterns were also different and were consistent with published descriptions of these developmental modes (Ricklefs, 1973, 1979). In precocial species, such as chickens and quail, there is a period of rapid thyroid maturation just prior to hatching. Thyroid hormone concentrations peak during the perinatal period with the initiation of pulmonary respiration, the overt activity of hatching and the initiation of endothermic responses to cooling (chickens: reviews by Freeman, 1971a, 1974;
Serum concentrations of both thyroid hormones, in quail, were high during the perinatal period, decreased in the early post-hatching period, then changed gradually to reach adult levels (Figs 5 and 6). In contrast, in doves, serum concentrations of both hormones were low at hatching, rose during the nestling period and stabilized several days before fledging. Fledgling serum T, concentrations were similar to those of adults (Fig. 6); serum T, concentrations were about 70% those of adults (Fig. 5).
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Thyroid development and body growth in birds
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Fig. 5. Serum T4 concentrations in Japanese quail and Ring doves. Values for quail (a) are from McNabb and Hughes (1983) and are expressed as the mean + SE (iv = 612); in some cases error bars are within the size of the symbols. The results, for quail, of Duncan’s new multiple range test are presented above each graph. Ages joined by solid lines do not differ si~i~~tly. Values for doves (0) are ~ndi~dual measurements; the solid line is described by the equation Y = 3.39x0,53.A = ad&s.
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Fig. 6. Serum T, concentrations in Japanese quail and Ring doves. Values for quail (m) are from McNabb and Hughes (1983) and are expressed as the mean + SE (N = 6-12); in some cases error bars are within the size of the symbols. The results, for quail, of Duncan’s new multiple range test are presented above each graph. Ages joined by solid lines do not differ si~ificantly. Values for doves (@) are in~vidual meas~ements; the solid line is described by the equation Y = 0.98x0.@. A = adults.
634
I;. M. ANNE MCNABBer al
Thommes and Hylka, 1977; quail: McNabb ed al., 1981; McNabb and Hughes, 1983). The present study shows that in quail thyroid activity (as indicated by thyroidal “‘1 uptakes, serum T4 and serum T, concentrations) decreased in the first few days after hatching. Concurrently there is yolk sac resorption and an increase in metabolic mass without a concomitant increase in Wa (Freeman, 1967). The W,/ W, ratio decreases rapidly during this time and continues to decrease slowly for the remainder of the juvenile period. This contrasts with the embryonic period when W,/ W, is essentially constant (McNabb et al., 1981). Serum thyroid hormone concentrations have reached a plateau by the time quail chicks first regulate their body temperature (at levels less than those of adults} at 13-15 days of age @piers et aZ., 1974). However, thyroidal ‘*‘I uptakes continue to rise until day 21. This is the time at which the coefficient of temperature regulation reaches an asymptote indicating juvenile temperature regulation equivalent to that of adults (Ricklefs, 1979). It is also the period of juvenile plumage growth. The increasing thyroidal radioiodine uptakes but stable serum hormone levels between days 13 and 21 could indicate either (I) a change in thyroid gland dynamics resulting in net iodine accumulation (hormonal plus non-hormonal), or (2) increased hormone turnover/excretion with high thyroid hormone production. Serum concentrations of thyroid hormones in juvenile quail do not differ si~ificantly from those of ad&s. Studies of hormone turnover and thyroid gland hormone content are needed to evaluate these possibilities. Altricial doves contrast with precocial quail in essentially all aspects of the ontogeny of thyroid function and general growth and development. Doves have low serum thyroid hormone concentrations on the day of hatching (this study) and in late embryos just prior to hatching (unpublished results, our laboratory) as predicted by our earlier study of thyroid histology (McNabb and McNabb, 1977a). Thus they appear to lack a perinatal thyroid hormone peak as seen in precocial species. Of the perinatal events, doves differ from quail only in the absence of endothermic responses to cooling. This suggests that early thermoregulatory responses are of primary importance in the perinatal burst of thyroid activity in precocial species. However, in quail, thyroid hormones rise well before external pipping, the first stage when cooling is likely to elicit a metabolic response. In chickens, roles for thyroid hormones in readiness for hatching, initiation of pulmonary respiration (see review by Freeman, 1974) and thermogenic responses (Freeman, 1971b) have been demonstrated. Detailed investigations of thyroid hormones during the perinatal period are needed in altricial birds to determine whether there are smaller, more transient hormone peaks. The general pattern of growth and development in doves in our study corresponded closely to that described for Mourning doves by Breitenbach and Baskett (1967). Body and thyroid growth were in parallel and rapid in comparison to those of quail. Thyroid functional activity (as indicated by thyroidal lz5T uptake and serum thyroid hormone concen-
trations) increased relatively rapidly during early post-hatching life. Thyroidal radioiodine uptakes are highest at about 6-8 days coincident with the beginning of coordinated locomotor activity and a rather abrupt decrease in parental brooding and feeding of the nestlings. Few of the feathers have unfurled by this time so the vascular feather quails may actually increase the surface area available for heat loss. Breitenbach and Baskett (1967) describe doves at this stage as “precarious homeotherms” that are just beginning to develop temperature control. Serum thyroid hormone concentrations of doves reach a plateau by about 12 days, although a number of developmental changes significant to energetics are still occurring (completion of juvenile plumage, increasing locomotor capability, decreasing parental care and brooding). The attainment of stable hormone concentrations coincides with the beginning of homeothermy as indicated by body temperatures of 3941°C in non-brooded nestlings after 12 days of age (unpublished preliminary data, our laboratory). As in the case of quail, additional information about thyroid gland function and hormone turnover rates during the period through fledging is needed to understand the roles of the thyroid in this developmental stage. Acknowledgements-This study was supported by NIH grant No. ROI AM28216 to F.M.A.M. and a Virginia Academy of Sciences grant to F.W.S. We thank T. E. Hughes for technical assistance and S. Ngo, M. Daly, M. Urbane and H. McCusker for help with animal care. The Department of Poultry Science kindly provided fertile quail eggs for use in this study. REFERENCES Breitenbach R. P. and Baskett T. S. (1967) Ontogeny of the~ore~ation in the Mourning dove. Physiol. Zooi. 40, 207-2 17. Freeman B. M. (1967) Oxygen consumption by the Japanese quail (Coturnix coturnix japonica). Br. Poult. Sri. 8, 147-152. Freeman B. M. (1971a) Body temperature and thermoregulation. Chapt. 48 in Phy~jo~og~~and ~~oc~erni~tr_~ of the ~orne~t~c Fowl (Edited by Bell D. J. and Freeman 3. M.). Academic Press, London. Freeman B. M. (1971b) Imnaired thermoreguiation in the thiouracil-treated nednate~fowl. Comp. B&hem. Physiol. 40A, 5.53-5.55. Freeman B. M. (1974) Hormones in Development. Chapt. 13 in Deuelopment of the Avian Embryo (Edited by Freeman B. M. and Vince M. A.). Chapman & Hail, London. McNabb F. M. A. and Hughes T. E. (1983) The role of serum binding proteins in determining free thyroid hormone concentrations during development in quail. Endocrinology 113, 957-963. ^ _ McNabb F. M. A. and McNabb R. A. (1977a) Thvroid development in precocial and ahricial a&n embryos. The A& 94, 736-742. McNabb F. M. A. and McNabb R. A. (1977b) Skin and plumage changes during the development of thermoregulatory ability in Japanese quail &ricks. Comp. Biothem. Phvsiol. 58A. 163-166. McNabb F.-M. A., W&rich R. T. and McNabb R. A. (1981) Thyroid function in embryonic and perinatal Japanese quail. Gen. camp. Endocrinof. 43, 218-226. Ricklefs R. E. (1973) Patterns of growth in birds. II. Growth rate and mode of development. The Ibis 115, 177-201.
Thyroid development and body growth in birds Ricklefs R. E. (1979) Patterns of growth in birds. IV. A comparative study of development in the Starling, Common tern and Japanese quail. The Auk 96, 10-30. Spiers D. E., McNabb R. A. and McNabb F. M. A. (1974) The development of thermoregulatory ability, heat seeking activities, and thyroid function in hatchling Japanese
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quail (Coturnix coturnix japonica). J. camp. Physiol. 89, 159-174. Thommes R. E. and Hylka V. W. (1977) Plasma iodothyronines in the embryonic and immediate post-hatch chick. Gem. camp. Endocrinol. 32, 417-422.