Comparison of the Ontogenesis of Thyroid Hormones, Growth Hormone, and Insulin-like Growth Factor-I inad Libitumand Food-Restricted (Altricial) European Starlings and (Precocial) Japanese Quail

Comparison of the Ontogenesis of Thyroid Hormones, Growth Hormone, and Insulin-like Growth Factor-I inad Libitumand Food-Restricted (Altricial) European Starlings and (Precocial) Japanese Quail

JOBNAME: GCE 101#3 96 PAGE: 1 SESS: 11 OUTPUT: Tue Apr 30 14:18:31 1996 /xypage/worksmart/tsp000/68045k/27pu General and Comparative Endocrinology 101...

549KB Sizes 0 Downloads 15 Views

JOBNAME: GCE 101#3 96 PAGE: 1 SESS: 11 OUTPUT: Tue Apr 30 14:18:31 1996 /xypage/worksmart/tsp000/68045k/27pu General and Comparative Endocrinology 101, 304–316 (1996) Article No. 0033

Comparison of the Ontogenesis of Thyroid Hormones, Growth Hormone, and Insulin-like Growth Factor-I in ad Libitum and Food-Restricted (Altricial) European Starlings and (Precocial) Japanese Quail William A. Schew,*,1 F. M. Anne McNabb,† and Colin G. Scanes‡,2 *Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104; †Department of Biology, Virginia Tech, Blacksburg, Virginia 24061; and ‡Department of Animal Sciences, Cook College Rutgers—The State University of New Jersey, New Brunswick, New Jersey 08902 Accepted December 20, 1995

In this study, we compare the ontogenic patterns for thyroid hormones, growth hormone (GH), and insulinlike growth factor-I (IGF-I) in altricial European starlings and precocial Japanese quail and examine the effects of feed restriction on these species. The most marked difference in development between the altricial and precocial birds was with respect to plasma thyroid hormone patterns. In the starling, circulating concentrations of triiodothyronine (T3) and thyroxine (T4) were very low in embryos, then increased progressively after hatching to peak at 10–11 days of age. In contrast, in quail, in which other studies have shown that most thyroid maturation occurs during the embryonic and perihatch periods, the circulating concentrations of T3 and T4 showed little posthatch ontogenic change. Plasma concentrations of both GH and IGF-I showed similar patterns in both species with a posthatch rise (peak at 3 days in starlings and 8 days in quail), followed by a decline. Food restriction to maintain body weight resulted in decreased plasma concentrations of T3 and IGF-I in both species. After return to ad libitum feeding,

1

Present address: Physiology Department, UCLA Medical Center, Los angeles, CA 90095-1751. 2 Present address: Department of Animal Sciences, College of Agriculture, Iowa State University, Ames, IA 50011.

304

plasma T3 and IGF-I increased in both early and late restricted starlings and in late restricted quail. Although both species responded to food restriction with similar patterns of endocrine change, age-related differences in the magnitude of hormonal responses were observed. © 1996 Academic Press, Inc.

Avian species with altricial development typically have higher growth rates, differences in the patterns of growth and maturation of individual organs, and later thermoregulatory development than do those with precocial development (O’Connor, 1977; Ricklefs, 1983). The key hormones that are known to be involved in the control of growth, tissue differentiation/ maturation, and metabolism are thyroid hormones [thyroxine (T4) and triiodothyronine (T3)], growth hormone (GH) and growth factors such as insulin-like growth factor-I (IGF-I). To date, comprehensive studies of the ontogeny of these hormones and of hormonal control of avian development have centered on development of precocial galliform species (reviews, Thommes, 1987; Scanes et al., 1992; McNabb and King, 0016-6480/96 $18.00 Copyright © 1996 by Academic Press, Inc. All rights of reproduction in any form reserved.

JOBNAME: GCE 101#3 96 PAGE: 2 SESS: 9 OUTPUT: Tue Apr 30 14:18:31 1996 /xypage/worksmart/tsp000/68045k/27pu 305

Avian Hormone Ontogenesis

1993). Few studies have addressed these aspects of hormonal development in altricial species (doves [Streptopelia risoria] GH: Scanes and Balthazart, 1981; thyroid hormones: McNabb and Cheng, 1985; McNichols and McNabb, 1988). In this present study, the ontogeny of plasma concentrations of thyroid hormones (T3 and T4), GH, and IGF-I was determined in altricial European starlings and precocial Japanese quail to evaluate further the hypothesis that there are general patterns of altricial and precocial hormone development. In precocial birds, nutritional restriction results in marked changes in concentrations of circulating hormones. For instance, fasting or feed restriction reduces circulating concentrations of T3 and IGF-I, whereas it is associated with increases in the plasma concentration of GH (Harvey et al., 1978; Kühn et al., 1985; Hughes and McNabb, 1986; Lauterio and Scanes, 1987; Rosebrough et al., 1989; Kim et al., 1991; Morishita et al., 1993). Recent work by Schew (1995a,b) has shown also that growing altricial European starling (Sturnus vulgaris) and precocial Japanese quail (Coturnix japonica) chicks respond physiologically in very different ways during periods of food restriction. In quail, a weight maintenance food restriction dramatically reduced skeletal growth and resulted in facultative hypothermia and reduced metabolic energy expenditure. In contrast, in starlings on a weight-maintenance food restriction there were relatively high rates of skeletal growth and relatively constant metabolic energy expenditures. These differences in metabolic and growth responses may be mediated by the endocrine system. Thus, by examining differences in endocrinological responses, it may be possible to further our understanding of the hormonal control of development. In this present study, the effects of food restriction and subsequent return ad libitum feeding on plasma hormone (T3, T4, GH, and IGF-I) concentrations were examined in starling and quail chicks and related to the different physiological and metabolic responses of these species. These investigations were conducted using foods that approximated the natural diets of the young of these species (i.e., a high-protein meat-based diet for starling chicks and a lower protein granivorous diet for the quail). The food restriction imposed was sufficient to maintain stable body weight and the ages used were chosen in relation to the growth rate and thermoregulatory development of each species.

METHODS AND MATERIALS Animals Known-age European starling embryos and chicks were obtained from nest boxes at the Bloomfield Farm of the Morris Arboretum, Montgomery County, in southeastern Pennsylvania and transported to the University of Pennsylvania where they were housed. One-day-old Japanese quail chicks were purchased from Truslow Farms (MD) and housed in a 100 × 75 × 150-cm brooding cage with a 12L/12D light cycle at the University of Pennsylvania. Chicks were provided with a heat source suspended 15 cm above the center of the brooding cage. For both species, the day of hatching was considered as Day 0. Beginning in midApril, starling nest boxes at the Morris Arboretum were visited daily and the numbers of eggs and chicks were recorded to ensure that chicks were aged accurately. Once a chick hatched (Day 0) body mass was measured every other day. Because of the temporal variation in hatching of starling chicks, sufficient numbers of age-specific individuals were not always available; therefore, sample sizes for starling protocols ranged from 3–11 individuals.

Food Restriction Experiments Starlings. Two starling chicks of equal age were removed from each nest box between 1100 and 1300 hr, transported to the University of Pennsylvania, and maintained at approximately 33° on a natural light schedule. Chicks removed from each nest were assigned randomly to either a restricted or ad libitum food regimen. Restricted chicks were placed on a weight maintenance diet of a high protein (50.0%) meat-based cat food (Alpo Captain’s Table) for either Posthatch Days 2–5 (early restriction) or Posthatch Days 7–10 (late restriction). Chicks were fed four to five small meals a day and given water approximately six times a day to prevent dehydration. All chicks were weighed before and after each meal to make sure that their body mass remained relatively constant. The nest-mate of equal age was fed ad libitum and given water for the same period to control for handling effects. Ad libitum status was maintained by feeding the

Copyright © 1996 by Academic Press, Inc. All rights of reproduction in any form reserved.

JOBNAME: GCE 101#3 96 PAGE: 3 SESS: 13 OUTPUT: Tue Apr 30 14:18:31 1996 /xypage/worksmart/tsp000/68045k/27pu 306

chicks approximately every 0.5 hr until the chick no longer responded by begging. Following the 3-day restriction, all chicks were fed ad libitum for 2 days then replaced in nest boxes randomly to be fed by adult starlings. At that time all broods were reduced to three chicks. Generally, starlings raise broods of four to six and, therefore, because food did not appear to be limiting during the course of this study, we feel confident that all chicks in the reduced broods were fed adequately. Quail. Chicks assigned to a restricted food regimen were placed on a low-protein (21.6%), weight maintenance diet of Purina Chick Chow (Purina Mills, St. Louis, MO) with access to ad libitum water for Days 3–13 (early restriction) or 20–30 posthatch (late restriction). Restricted chicks were allowed to feed for approximately 2 min three times a day; each chick was weighed before and after each feeding bout to ensure that body weight remained stable. Control chicks had access to ad libitum food and water. After the 10-day restriction chicks were allowed to feed ad libitum.

Blood Collection and Plasma Hormone Measurements For determining the normal ontogeny of plasma hormone concentrations, blood samples were taken by syringe from the jugular vein of starling and quail chicks and transferred to heparinized microcentrifuge tubes. Only one blood sample per bird was taken during the course of this study to avoid possible artifacts due to stress induced by handling. These samples were taken between 1100 and 1300, approximately 3 hr after the chicks were last fed. Embryonic starling blood samples, of sufficient volume for thyroid hormone measurements only, were collected into heparinized capillary tubes, from chorioallantoic arteries. Plasma samples were stored frozen at −20° until analysis. Because of an insufficient number of ad lib quail chicks late in the restriction study, we chose not to sample control individuals on Day 25. Although these control hormone values are not available, we feel that the data from restricted individuals will still provide useful information. Plasma concentrations of T3 and T4 were determined using double antibody radioimmunoassays validated previously for use on quail plasma (McNabb and

Copyright © 1996 by Academic Press, Inc. All rights of reproduction in any form reserved.

Schew, McNabb, and Scanes

Hughes, 1983). For use on starling plasma, the methods were validated by (1) demonstrating parallelism with the standard curve for a series of dilutions of starling plasma with the hormone-stripped chicken plasma used to prepare the standards, and (2) by recoveries of >92% of T3 and T4 spikes added to starling plasma samples. Precision tests indicated intraassay variation of <3%. Samples below the detection limits were assigned values at the respective lower limits (0.125 ng/ml for T3 and 1.25 ng/ml for T4). Plasma concentrations of GH were determined by a homologous chicken GH radioimmunoassay (Harvey and Scanes, 1977). The assay was validated for starling plasma samples based on two criteria. The first was parallel inhibition of binding of 125I chicken GH to the antisera by starling plasma and the chicken GH standards. Second, GH secretagogues injected into the jugular vein significantly increased plasma concentrations of immunoreactive GH in adult starlings [10 min after challenge (mean ± SEM; n = 5 for each group): avian ringers solution, 2.3 ± 0.37 ng/ml, NS; growth hormone releasing factor (2.5 mg/kg), 15.9 ± 4.36 ng/ ml, P < 0.02; in young (14 days) starling: avian ringers, 9.0 ± 3.69 ng/ml, NS; thyrotropin releasing hormone (2.5 mg/kg), 23.6 ± 1.32 ng/ml, (P < 0.05). The lower limit of sensitivity of the GH assay was 5.0 ng/ ml based on a laboratory GH standard. Plasma concentrations of IGF-I were determined by a human IGF-I radioimmunoassay (antisera kindly provided by the National Hormone and Pituitary Program and 125I-human IGF-I obtained from Amersham, Arlington Heights, IL) which has been validated for avian plasma (Huybrechts et al., 1985; C.G. Scanes, L., McCann-Levorse, W.A., Schew, unpublished). All samples for a single experiment were assayed together to eliminate interassay variation.

Statistics Pearson’s product–moment correlation coefficients were calculated to determine age-related changes in plasma hormone concentrations. Differences in hormone concentrations between prerestriction and restriction levels (unpaired observations) and between restricted and control treatments were determined using Student’s t test. All levels of significance were set at P = 0.05.

JOBNAME: GCE 101#3 96 PAGE: 4 SESS: 11 OUTPUT: Tue Apr 30 14:18:31 1996 /xypage/worksmart/tsp000/68045k/27pu Avian Hormone Ontogenesis

307

RESULTS Hormone Ontogeny in Starlings Plasma concentrations of both T4 and T3 were very low in starling embryos; T4 did not change significantly in embryos but there was a small but significant increase in plasma T3 during embryonic life (Fig. 1). It should be noted that these data may overestimate the thyroid hormone concentrations for 6- and 8-day embryos because many of the samples for these ages read at or below the detection limits of the assays, but were recorded as being equal to the detection limit of the assays. If alternatively, such samples were considered to have zero hormone, it would decrease the mean values slightly, but would not alter the pattern presented in Fig. 1. Thyroid hormones remained low during the perihatch period and then increased steadily for the first 10–11 days posthatch. Plasma T4 concen-

FIG. 2. Growth trajectory, daily growth rates, and plasma GH and IGF-I concentrations of nestling European starlings (n = 130). Values represent the means (±SEM) of age-specific cross-sectional measurements.

FIG. 1. Mean plasma thyroid hormone concentrations in embryonic (n = 13) and nestling European starlings (n = 108). Values represent the means (±SEM) of age-specific cross-sectional measurements.

trations increased much more (about 8–10×) between hatch and Days 10–11 than did T3 concentrations (about 3×). After Days 10–11, plasma T4 concentrations decreased but T3 changed relatively little. There was no significant correlation between T4 and T3 during the posthatch period studied (r = 0.07, P > 0.05). Plasma concentrations of both GH and IGF-I increased dramatically during the first 3 days posthatch, then decreased throughout the rest of the growth period (Fig. 2). The initial increase in GH and IGF-I was closely associated with the period of rapid growth prior to the point of inflection of their sigmoidal growth curve. GH and IGF-I plasma concentrations were significantly positively correlated during this period (r = 0.60, P < 0.001).

Copyright © 1996 by Academic Press, Inc. All rights of reproduction in any form reserved.

JOBNAME: GCE 101#3 96 PAGE: 5 SESS: 9 OUTPUT: Tue Apr 30 14:18:31 1996 /xypage/worksmart/tsp000/68045k/27pu 308

Schew, McNabb, and Scanes

Hormone Ontogeny in Quail Posthatch plasma concentrations of both thyroid hormones showed correlated age-related changes through age 60 days (r = 0.32, P < 0.02). Plasma concentrations of both T3 and T4 were low on the first two days posthatch, increased briefly, decreased, and then steadily increased to concentrations in the range characteristic of adult quail (Fig. 3). Quail plasma growth hormone and IGF-I concentrations both increased during the rapid growth period that occurs shortly after hatching, then decreased during the slower growth period during later posthatch life (Fig. 4). Because of insufficient plasma volume, GH concentrations were not determined for the first day posthatch. However, during the rest of the posthatch period, plasma concentrations of GH and IGF-I were positively correlated in quail (r = 0.43, P < 0.01).

Hormonal Responses to Food Restriction European starlings. Early posthatch food restriction (Days 2–5 posthatch) resulted in significantly de-

FIG. 4. Growth trajectory, daily growth rates, and plasma GH and IGF-I concentrations of Japanese quail chicks (n = 35). Values represent the means (±SEM) of age-specific cross-sectional measurements.

FIG. 3. Plasma thyroid hormone concentrations Japanese quail chicks (n = 57). Values represent the mean (±SEM). Values represent the means (±SEM) of age-specific cross-sectional measurements.

Copyright © 1996 by Academic Press, Inc. All rights of reproduction in any form reserved.

creased plasma concentrations of both thyroid hormones compared to controls (Fig. 5). Late food restriction (Days 7–10 posthatch) resulted in only plasma T3 being significantly decreased compared to controls. In the early food restriction, the effect on T4 was to prevent the hormone increase with age that was observed in the controls. In both restriction periods, the effects on T3 were relatively greater than those on T4 and plasma T3 concentrations were significantly decreased not only compared to controls, but also compared to their own values at the beginning of the restriction period (P < 0.01). Realimentation (i.e., return to ad libitum feeding), resulted in rebound of plasma concentrations of T3 to control levels by Day 12 (P < 0.05). T4 did not increase significantly upon refeeding, but by

JOBNAME: GCE 101#3 96 PAGE: 6 SESS: 14 OUTPUT: Tue Apr 30 14:18:31 1996 /xypage/worksmart/tsp000/68045k/27pu Avian Hormone Ontogenesis

309

FIG. 5. Mean (±SEM; n) plasma thyroid hormone concentrations of ad libitum control and early and late restricted European starling nestlings. The horizontal black bar indicates the period of the weight maintenance food restriction and asterisks indicate significant differences between treatment groups (between symbols) or between consecutive mean values (adjacent to the line) within a treatment (* < P = 0.05; ** < 0.01).

Day 12, T4 levels of control chicks had declined and were not significantly different from those of previously restricted chicks. Plasma concentrations of GH were not significantly changed by the early or late posthatch food restriction (Fig. 6). However, after 2 days of ad libitum feeding following the early restriction, the previously restricted chicks had higher plasma GH concentrations than control values (P < 0.05). In contrast to GH, plasma IGF-I concentrations decreased significantly (P < 0.001) during both restriction periods. Plasma IGF-I in control chicks did not change significantly during this time. Japanese quail. Although the timing of the early (Days 3–13) and late (Days 20–30) food restriction periods used for quail differed from those used for starlings, the patterns of thyroid hormone responses to food restriction were similar in both species. In quail, plasma concentrations of T3 were significantly less than those of controls at the end of both restriction

periods and rebounded to control levels within a week of ad libitum feeding (Fig. 7). Plasma T4 was decreased compared to controls in the middle of the early restriction period, but did not differ from controls by the end of the early restriction. There were no significant differences in plasma T4 between restricted and control quail during the late food restriction. Neither early nor late food restriction significantly altered plasma GH concentrations in Japanese quail chicks (Fig. 8), although it should be noted that insufficient plasma volumes were available for measuring GH on the last day of the early restriction period. Plasma concentrations of IGF-I remained unchanged throughout both early and late restriction periods (i.e., food restriction prevented the increases in IGF-I that occurred in controls at this time). Return to ad libitum feeding did not affect plasma IGF-I concentrations in early restricted chicks but did result in a significant increase (P < 0.05) in IGF-I in late restricted chicks. The previously restricted chicks did not differ from con-

Copyright © 1996 by Academic Press, Inc. All rights of reproduction in any form reserved.

JOBNAME: GCE 101#3 96 PAGE: 7 SESS: 11 OUTPUT: Tue Apr 30 14:18:31 1996 /xypage/worksmart/tsp000/68045k/27pu 310

Schew, McNabb, and Scanes

FIG. 6. Mean (±SEM; n) plasma GH and IGF-I concentrations of ad libitum control and early and late restricted European starling nestlings. The horizontal black bar indicates the period of the weight maintenance food restriction and asterisks indicate significant differences between treatment groups (between symbols) or between consecutive mean values (adjacent to the line) within a treatment (* < P = 0.05; ** < 0.01).

trols after 7 days of ad libitum food availability (37 days of age).

DISCUSSION Thyroid Hormone Ontogeny The ontogeny of the thyroid gland, the patterns of circulating T3 and T4, and thyroid hormone roles in the development of thermoregulation offer examples of marked differences in the maturation of control systems and their effects in altricial and precocial species. Specifically, in precocial species such as Japanese quail, thyroid function develops relatively rapidly during the latter half of embryonic life, and peaks of plasma thyroid hormones during the perihatch period are associated with the initiation of thermoregulatory responses at this time (McNabb et al., 1981, 1984). In

Copyright © 1996 by Academic Press, Inc. All rights of reproduction in any form reserved.

contrast, in altricial ringed doves, thyroid development is much slower; plasma thyroid hormones are low in the embryo and during the perihatch period, then rise steadily during the first 8–12 days posthatch when initial signs of endothermy are appearing. Thermoregulatory control then develops fairly rapidly and young are effective homeotherms by the time of fledging at about 21 days posthatch (McNabb et al., 1984; McNabb and Cheng, 1985; McNichols and McNabb, 1988). Although previous studies have suggested that differences in the timing of thyroid development are important in the hormonal control of thermoregulatory development, it is not clear whether these patterns are characteristic of precocial and altricial ontogeny. The thyroid hormone pattern previously observed in precocial quail (McNabb et al., 1981, 1984) is consistent with that of other galliformes (chickens [ Gallus domesticus], Thommes and Hylka, 1977; turkeys [Meleagris gallopavo], Christensen et al., 1982; bobwhite quail

JOBNAME: GCE 101#3 96 PAGE: 8 SESS: 11 OUTPUT: Tue Apr 30 14:18:31 1996 /xypage/worksmart/tsp000/68045k/27pu Avian Hormone Ontogenesis

311

FIG. 7. Mean (±SEM; n) plasma thyroid hormone concentrations of ad libitum control and early and late restricted Japanese quail chicks. The horizontal black bar indicates the period of the weight maintenance food restriction and asterisks indicate significant differences between treatment groups (between symbols) or between consecutive mean values (adjacent to the line) within a treatment (* < P = 0.05; ** < 0.01).

[Colinus virginianus], Spiers and Ringer, 1984) but thyroid development in other precocial birds, particularly from other orders within Aves, has not been investigated. In altricial species, the only published accounts of thyroid development throughout the embryonic and nestling period are for ringed doves (McNabb et al., 1984; McNabb and Cheng, 1985). However, recently we (Schew and McNabb, 1994) and another laboratory (Vyboh et al., in press) have presented preliminary data on posthatch European starlings. The results of our present investigation of embryonic and posthatch thyroid ontogeny in European starlings are consistent with previous observations for ringed doves, suggesting a general pattern associated with altricial development. Data from Vyboh et al. (in press) add further verification to this picture. As in doves, plasma thyroid hormone concentrations in embryonic and perihatch starlings were very low, then both T4 and T3 concentrations rose steadily in posthatch chicks to reach their highest values between 9

and 12 days of age. The timing of these highest thyroid hormone concentrations corresponds to the timing of the attainment of homeothermy, thermal independence, and a period of rapidly rising metabolic scope (Clark, 1982; Choi et al., 1993). Thus, the pattern of thyroid hormones in starlings is like that in altricial ringed doves and differs from precocial species in which thyroid development occurs much earlier. In this current study, plasma thyroid hormones in Japanese quail chicks declined during the first 2 days posthatch, then increased, decreased, and remained subsequently within concentration ranges characteristic of young adult galliform birds. The perihatch peak of plasma thyroid hormones, previously reported in quail and other galliform birds (review, McNabb, 1988), presumably was over before sampling was begun at Day 1 posthatch in the present study. This peak, in which T4 and T3 both rise dramatically (to several-fold those in adults) is thought to be important in the initial thermoregulatory responses during the

Copyright © 1996 by Academic Press, Inc. All rights of reproduction in any form reserved.

JOBNAME: GCE 101#3 96 PAGE: 9 SESS: 13 OUTPUT: Tue Apr 30 14:18:31 1996 /xypage/worksmart/tsp000/68045k/27pu 312

Schew, McNabb, and Scanes

FIG. 8. Mean (±SEM; n) plasma GH and IGF-I concentrations of ad libitum control and early and late restricted European starling nestlings. The horizontal black bar indicates the period of the weight maintenance food restriction and asterisks indicate significant differences between treatment groups (between symbols) or between consecutive mean values (adjacent to the line) within a treatment (* < P = 0.05; ** < 0.01).

perihatch period in galliformes. Posthatch, the highest thyroid hormone concentrations in the present study occurred between Days 7 and 10 and corresponded well with the timing of attainment of homeothermy, high metabolic scope, high basal metabolism (Choi et al., 1993; Schew, 1995b), and thermal independence. At these ages quail are effective homeotherms but have relatively less insulation and less favorable surface to volume ratios for thermoregulation than at later ages. It should be noted, however, that the marked peak of T3 at Day 8 has not been observed in other studies and remains an anomaly.

Growth Hormone and IGF-I Ontogeny In contrast to the differences in development of thyroid function and thermoregulatory ability between developmental modes, the literature on GH in relation to posthatch growth suggests a similar pattern among

Copyright © 1996 by Academic Press, Inc. All rights of reproduction in any form reserved.

altricial and precocial species. Plasma GH concentrations increase and peak during the posthatch period of rapid growth. As the growth rate of a chick slows during the second phase of growth, GH concentrations decline and are low in adult birds. There do not appear to be any major pattern differences in plasma GH between altricial and precocial species although the timing of the peak and subsequent decline are shifted in relation to the body growth characteristics of different species. When age is expressed as a percentage of time from conception to maturity, patterns of posthatch plasma GH in different bird species appear to be synchronized (Scanes et al., 1992). Plasma GH has been studied in a number of precocial species from several orders (chickens, Harvey et al., 1979a,b; Scanes and Harvey, 1981; domestic goose [Anser anser] Scanes et al., 1979; Peking duck [Anas platyrhynchos], Harvey and Phillips, 1980), but only in one altricial species (ringed dove, Scanes and Balthazart, 1981) and one

JOBNAME: GCE 101#3 96 PAGE: 10 SESS: 11 OUTPUT: Tue Apr 30 14:18:31 1996 /xypage/worksmart/tsp000/68045k/27pu Avian Hormone Ontogenesis

semialtricial (American kestrel [Falco sparverius], Lacombe et al., 1993). None of these investigations of altricial species have studied all the developmental stages necessary to provide a complete ontogenic posthatch profile. In this study, plasma concentrations of GH rose to a peak following hatch (starlings: −3 days old, corresponding to the achievement of 20% of maximal/ asymptotic body weight; and quail: −7 days old, corresponding to 9% of asymptotic weight). Previously, Burke and Marks (1984) reported ontogenic changes in circulating concentrations of GH in quail from 7 days of age onward and, as in the present study, GH declined between 7 and approximately 20 days of age when the quail had achieved only approximately 40% of maximal body weight. In contrast, in starlings in this study, plasma concentrations of GH declined steadily between Days 3 and 18. Thus, the decrease in plasma GH in starlings occurred considerably earlier than the age at which maximal body weight was attained (z13 days). In addition to examining the ontogenetic profiles plasma concentrations of GH, those of IGF-I also need to be considered. It is generally accepted that GH exerts its action primarily by stimulating the production and release of IGF-I by the liver. In precocial chickens, posthatch plasma concentrations of IGF-I are similar, but not identical, to the pattern of plasma GH (Huybrechts et al., 1985; Burnside and Cogburn, 1992). A similar situation exists in the domestic turkey (Bacon et al., 1993; McMurtry et al., 1994). Until the present study, there were no published ontogenic profiles of IGF-I in nondomesticated birds of either precocial or altricial species. Our results indicate that the ontogenic patterns of plasma IGF-I are similar in altricial starlings and in precocial quail and correspond to those previously reported for chickens and turkeys (see above). Also, as in species investigated previously, there is good correspondence between GH and IGF-I in the plasma of developing starling and quail. However, although the developmental profiles of these hormones are similar in all species that have been studied, there are differences between species related to chronological age for different parts of the profile. This emphasizes the need to consider the patterns in relation to physiological development (e.g., growth pattern characteristics for each species).

313

Effects of Feed Restriction on Hormone Ontogeny Feed restriction or starvation typically causes marked reductions in plasma T3 concentrations in both birds and mammals (review, Eales, 1988) and the decrease in T3 is generally considered to be due to decreased T4 to T3 59 deiodination (59D) in organs such as the liver and kidney which supply most of the plasma T3 (review, McNabb, 1992). This decrease in production of T3 (the key metabolically active thyroid hormone) is considered to have a sparing effect on body metabolism in general, while developing tissues that are particularly vulnerable to thyroid hormone deficiency (e.g., central nervous tissues) maintain intratissue T3 production (review, McNabb, 1992; studies in birds, Rudas et al., 1993, 1994). In the present study, both starlings and quail showed the expected decreased plasma T3 concentrations, relative to controls of the same age, during both early and late posthatch food restriction. Plasma T4 was decreased during the early food restriction but not during the late restriction in either species. Decreases in plasma hormone concentrations were compensated rapidly when ad libitum food availability was restored. Although dietary differences affected plasma T3 in adult chickens (Klandorf and Harvey, 1985), the similarity in plasma T3 responses to feed restriction and refeeding chicks of both species in this study suggests that dietary composition did not play a role in the pattern of response during development. The T3 decreases that we observed are consistent with reduced hepatic 59D activity as has been observed in response to fasting/starvation in chickens (Decuypere and Kühn, 1984) and quail (Hughes and McNabb, 1986). Because thyroid hormones are important in the control of metabolic rate in homeotherms, the decrease in circulating T3 during fasting might be expected to play an important role in energy partitioning in developing homeotherms. Thyroid hormones are thought to affect primarily that component of metabolism that provides “obligatory heat”, i.e., the component of metabolism that is unique to the maintenance of homeothermy (Danforth and Berger, 1984). Thus, food restriction and its associated decreases in plasma T3 might have different effects on metabolism and body temperature depending on the degree of thermoregulatory development at the time of feed restriction.

Copyright © 1996 by Academic Press, Inc. All rights of reproduction in any form reserved.

JOBNAME: GCE 101#3 96 PAGE: 11 SESS: 11 OUTPUT: Tue Apr 30 14:18:31 1996 /xypage/worksmart/tsp000/68045k/27pu 314

In the present study, the early feed restriction period (Days 2–5 posthatch) used for starlings was prior to the time when the nestlings show endothermic responses to cooling; the late feed restriction period (Days 7–10 posthatch) was during the ages when the nestlings shiver in response to cooling but have limited endothermic capability for maintaining constant body temperature. Neither oxygen consumption nor body temperature are significantly altered in starlings during either the early or late food restriction and concurrent with depression of plasma T3 (Schew, 1995b). This suggests that the cellular mechanisms for thyroid hormone conversions and their control may be present prior to the maturation of metabolic and thermoregulatory control in this species. In contrast to starlings, quail showed significant decreases in both oxygen consumption and body temperature during both the early and late restriction periods (Days 3–13 and 20–30 posthatch; Schew, 1995b). Quail are relatively good homeotherms at these ages, so it seems likely that the decreased plasma T3 during food restriction is an important factor in these metabolic responses and the energy sparing that must result. Restricted Japanese quail failed to show the characteristic increase in plasma GH concentrations observed in other birds during periods of food restriction (e.g., Scanes et al., 1979; Lacombe et al., 1993). Because our first blood samples were taken 5 days after the imposition of the food restrictions, we most likely missed the spike of GH that stimulates lipolysis and is invoked as a protein sparing mechanism following the onset of a period of undernutrition (see Scanes et al., 1984 for a review). Circulating concentrations of IGF-I were reduced during feed restriction in both European starlings and Japanese quail. The only reported studies of the effects of nutritional restriction on circulating concentrations of IGF-I in birds are on the domestic chicken. As in the present study, plasma concentrations of IGF-I have been reported to be decreased in chickens following fasting (Kim et al., 1991), protein restriction (Lauterio and Scanes, 1987), and energy restriction (Rosebrough et al., 1989). This is consistent with the need, during times of energy limitation, for a reduction in hormonal “drive” pushing growth. In the present study, restoring ad libitum feeding increased circulating concentrations of IGF-I relative to

Copyright © 1996 by Academic Press, Inc. All rights of reproduction in any form reserved.

Schew, McNabb, and Scanes

those during both early and late nutritional restriction periods in starlings and during the late restriction in quail. Restoration of circulating concentrations of IGF-I following the removal of nutritional restriction have not been previously observed in birds. Indeed refeeding following fasting in young chickens was reported to be followed by a further reduction in the circulating concentrations of IGF-I (Kim et al., 1991). Although qualitatively the changes in the starling and late restricted Japanese quail were similar, the magnitude of the increase in plasma concentrations of IGF-I following return to ad libitum feeding was much greater in quail. Thus, restoration of ad libitum feeding restored plasma IGF-I concentrations to control values in starlings but resulted in an overshoot; i.e., values above those of controls, in late restricted, refed quail. The elevated circulating concentrations of IGF-I above restriction values may be involved in the phenomenon of so called “catch-up” growth that has been observed in domestic galliform species following food restriction or starvation but this requires further investigation.

ACKNOWLEDGMENTS We thank the American Ornithologists’ Union for supporting this research though a grant to W.A.S. from the Josselyn Van Tyne Research fund and AOU Supplemental Research fund. We thank Steve Kovack, Douglas Thamm, Chick Culp, and the Morris Arboretum for their support in the field and laboratory. We also thank Osama Abed for his technical assistance. This research was also supported by the New Jersey Agricultural Experiment Station, by an NSF grant (DEB90-07000) to Robert E. Ricklefs, and by Hatch and New Jersey State funds.

REFERENCES Bacon, W. L., Nestor, K. E., Emmerson, D. A., Vasilatos-Younken, R., and Long, D. W. (1993). Circulating IGF-I in plasma of growing male and female turkeys of medium and heavy weight lines. Dom. Anim. Endocrinol. 10, 267–277. Burke, W. H., and Marks, H. L. (1984). Growth hormone, thyroxine, and triiodothyronine levels of Japanese quail selected for four week body weight. Poult. Sci. 63, 207–213. Burnside, J., and Cogburn, L. A. (1992). Developmental expression

JOBNAME: GCE 101#3 96 PAGE: 12 SESS: 9 OUTPUT: Tue Apr 30 14:18:31 1996 /xypage/worksmart/tsp000/68045k/27pu Avian Hormone Ontogenesis of hepatic growth hormone receptor and insulin-like growth factor-l mRNA in the chicken. Mol. Endocrinol. 89, 91–96. Choi, I., Ricklefs, R. E., and Shea, R. E. (1993). Skeletal muscle growth, enzyme activities, and the development of thermogenesis: A comparison between altricial and precocial birds. Physiol. Zool. 66, 455–473. Christensen, V. L., Biellier, H. V., and Forward, J. F. (1982). Physiology of turkey embryos during pipping and hatching. III. Thyroid function. Poult. Sci. 61, 367–374. Clark, L. (1982). The development of effective homeothermy and endothermy by nestling starlings. Comp. Biochem. Physiol. 73A, 253–260. Danforth, E., Jr., and Burger, A. (1984). The role of thyroid hormones in the control of energy expenditure. Clin. Endocrinol. Metab. 13, 581–595. Decuypere, E., and Kühn, E. R. (1984). Effects of fasting and feeding time on circadian rhythms of serum thyroid hormone concentrations of glucose, liver monodeiodinase activity and rectal temperature in growing chickens. Dom. Anim. Endocrinol. 1, 251–262. Eales, J. G. (1988). The influence of nutritional state on thyroid function in various vertebrates. Am. Zool. 28, 351–362. Harvey, S., and Phillips, J. G. (1980). Growth, growth hormone and corticosterone secretion in freshwater and saline-adapted ducklings (Anas platyrhynchos). Gen. Comp. Endocrinol. 42, 334–344. Harvey, S., Scanes, C. G., Chadwick, A., and Bolton, N. J. (1978). Influence of fasting, glucose and insulin on the levels of growth hormone and prolactin in the plasma of the domestic fowl (Gallus domesticus). J. Endocrinol. 76, 501–506. Harvey, S., Scanes, C. G., Chadwick, A., and Bolton, N. J. (1979a). Growth hormone and prolactin secretion in growing domestic fowl: influence of sex and breed. Br. Poult. Sci. 20, 9–17. Harvey, S., Davison, T. F., and Chadwick, A. (1979b). Ontogeny of growth hormone and prolactin secretion in the domestic fowl (Gallus domesticus). Gen. Comp. Endocrinol. 39, 270–273. Harvey, S., and Scanes, C. G. (1977). The purification and radioimmunoassay of chicken growth hormone. J. Endocrinol. 73, 321–329. Hughes, T. E., and McNabb, F. M. A. (1986). Avian hepatic T3 production by two pathways of 59-monodeiodination: Effects of fasting and patterns during development. J. Exp. Zool. 238, 393–399. Huybrechts, L. M., King, D. B., Lauterio, T. J., Marsh, J., and Scanes, C. G. (1985). Plasma concentrations of somatomedin-C in hypophysectomized, dwarf and intact growing domestic fowl as determined by heterologous radioimmunoassay. J. Endocrinol. 104, 233–239. Kim, J-W., Fletch, D. L., Campion, D. R., Gaskins, H. R., and Dean, R. (1991). Effect of dietary manipulation on c-myc RNA expression in adipose tissue, muscle and liver of broiler chicken. Biochem. Biophys. Res. Commun. 180, 1–7. Klandorf, H., and Harvey, S. (1985). Food intake regulation of circulating thyroid hormones in domestic fowl. Gen. Comp. Endocrinol. 60, 162–170. Kühn, E. R., Gerheyen, G., Chiasson, R. B., Huts, C., and Decuypere, E. (1985). Ovine growth hormone reverses the fasting-induced decrease in plasma T3 in adult chickens. IRCS Med. Sci. 13, 451– 452. Lacombe, D., Bird, D. M., Scanes, C. G., and Hibbard, K. A. (1993).

315 The effect of restricted feeding on plasma growth hormone GH concentrations in growing American kestrels. Condor 95, 559–567. Lauterio, T. J., and Scanes, C. G. (1987). Time course of changes in plasma concentrations of the growth related hormones during protein restriction in the domestic fowl (Gallus domesticus). Proc. Soc. Exp. Biol. Med. 185, 420–426. McMurtry, J. P., Francis, G. L., Upton, F. Z., Rosselot, G., and Brocht, D. M. (1994). Developmental changes in chicken and turkey insulin-like growth factor-I (IGF-I) studies with a homologous radioimmunoassay for chicken IGF-I. J. Endocrinol. 142, 225–234. McNabb, F. M. A. (1988). Peripheral thyroid hormone dynamics in precocial and altricial avian development. Am. Zool. 28, 427–440. McNabb, F. M. A. (1992). “Thyroid Hormones.” Prentice Hall, Englewood Cliffs, NJ. McNabb, F. M. A. (1995). Thyroid hormones, their activation, degradation and effects on metabolism. J. Nutr. 125, 1773S–1776S. McNabb, F. M. A., and Cheng, M-F. (1985). Thyroid development in altricial doves, Streptopelia risoria. Gen. Comp. Endocrinol. 58, 243–251. 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 King, D. B. (1993). Thyroid hormone effects on growth, development and metabolism. In “The Endocrinology of Growth, Development, and Metabolism of Vertebrates” (M. P. Schreibman, C. G. Scanes, and P. K. T. Pang, Eds.), pp. 393–417. Academic Press, New York. McNabb, F. M. A., Weirich, R. T., and McNabb, R. A. (1981). Thyroid development in embryonic and perinatal Japanese quail. Gen. Comp. Endocrinol. 43, 218–226. McNabb, F. M. A., Stanton, F. W., and Dicken, S. G. (1984). Posthatching thyroid development and body growth in precocial vs. altricial birds. Comp. Biochem. Physiol. 78A, 629–635. McNichols, M. J., and McNabb, F. M. A. (1988). Development of thyroid function and its pituitary control in embryonic and hatchling precocial Japanese quail and altricial Ring doves. Gen. Comp. Endocrinol. 69, 108–118. Morishita, D., Sasake, K., Wakita, M., and Hoshina, S. (1993). Effect of fasting on serum insulin-like growth factor-I (IGF-I) levels and IGF-I-binding activity in cockerels. J. Endocrinol. 139, 363–370. O’Connor, R. J. (1977). Differential growth and body composition in altricial passerines. Ibis 119, 147–166. Ricklefs, R. E. (1983). Avian postnatal development. In “Avian Biology” (D. S. Farner, J. R. King, and K. C. Parkes, Eds.), Vol. VII, pp. 1–83. Academic Press, New York. Rosebrough, R. W., McMurtry, J. P., and Steele, N. C. (1989). Protein and energy relations in the broiler chicken. Chronic or acute effects of alternating protein or intermittent feeding regimens on broiler lipid metabolism. Br. J. Nutr. 61, 223–233. Rudas, P., Bartha, T., and Frenyo, V. L. (1993). Thyroid hormone deiodination in the brain of young chickens acutely adapts to changes in thyroid status. Acta. Vet. Hung. 41, 381–393. Rudas, P., Bartha, T., and Frenyo, V. L. (1994). Elimination and metabolism of triiodothyronine depend on the thyroid status in the brain of young chickens. Acta. Vet. Hung. 43, 218–230. Scanes, C. G., and Balthazart, J. (1981). Circulating concentrations of

Copyright © 1996 by Academic Press, Inc. All rights of reproduction in any form reserved.

JOBNAME: GCE 101#3 96 PAGE: 13 SESS: 9 OUTPUT: Tue Apr 30 14:18:31 1996 /xypage/worksmart/tsp000/68045k/27pu 316 growth hormone during growth, maturation and reproductive cycles in ring doves (Streptopelia risoria). Gen. Comp. Endocrinol. 45, 381–385. Scanes, C. G., and Harvey, S. (1981). Growth hormone and prolactin in avian species. Life Sci. 28, 2985–2902. Scanes, C. G., Harvey, S., Marsh, J. A., and King, D. B. (1984). Hormones and growth in poultry. Poult. Sci. 63, 2062–2074. Scanes, C. G., Pethes, G., Rudas, P., and Murray, T. (1979). Changes in plasma growth hormone concentration during growth in domesticated geese. Acta Vet. Acad. Sci. Hung. 37, 3–184. Scanes, C. G., Radecki, S. V., and Malamed, S. (1992). Mechanism involved in the avian patterns of growth hormone secretion during growth and development. Ornis Scand. 23, 214–221. Schew, W. A. (1995a). The effects of food restriction on the growth of Japanese quail and European starling chicks, submitted for publication. Schew, W. A. (1995b). Metabolic and thermoregulatory responses of European starling and Japanese quail chicks to undernutrition:

Copyright © 1996 by Academic Press, Inc. All rights of reproduction in any form reserved.

Schew, McNabb, and Scanes An example of developmental constraints and adaptive responses, submitted for publication. Schew, W. A., and McNabb, F. M. A. (1994). Thyroid ontogeny of altricial starlings and the effects of food restriction in altricial starlings and precocial quail. Am. Zool. 34, 120A. Spiers, D. E., and Ringer, R. K. (1984). Thyroid hormone changes in the Bobwhite (Colinus virginianus) after hatching. Gen. Comp. Endocrinol. 53, 302–308. Thommes, R. C. (1987). Ontogenesis of thyroid function and regulation in the developing chick embryo. J. Exp. Zool. Suppl. 1, 273– 279. Thommes, R. C., and Hylka, V. W. (1977). Plasma iodothyronines in the embryonic and immediate post-hatch chick. Gen. Comp. Endocrinol. 34, 193–200. Vyboh, P., Zeman, M., Jurani, M., Byuse, J., and Decuypere, E. Plasma thyroid hormone growth hormone patterns in precocial Japanese quail and altricial European starlings during postnatal development. Comp. Biochem. Physiol., in press.