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«ABSTR•CT.Histological criteria indicate that thyroid glands are organized into follicles at about the same time of incubation in JapaneseQuail ...»

THYROID DEVELOPMENT IN PRECOCIAL AND

ALTRICIAL AVIAN EMBRYOS

F. M. ANNE MCNABB AND ROGER A. MCNABB

ABSTR•CT.--Histological criteria indicate that thyroid glands are organized into follicles at

about the same time of incubation in JapaneseQuail (precocial)and Ringed Turtle Dove (altricial) embryos,but dove thyroidsdevelopmore slowly, are much smaller and are much lessactive than quail thyroids by the time of hatching. These resultsindicate thyroid readinessfor participation in early endothermic responses precocial hatchlings, and relative thyroid inactivity in young ecof tothermic altricial nestlings.--Departmentof Biology, Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24061. Accepted 12 April 1976.

THYROID hormonesare known to be important determinants of metabolic rate and heat production in adult birds. In addition, the time course of developing thyroid function closelyparallels developingthermoregulatoryability in precocialyoung that hatch at a relatively advanced stageof development(seeFreeman 1971, for the data on domesticchickens;McNabb et al. 1972 and Spiers et al. 1974 for the data on Japanese Quail [Coturnix coturnix japonica]). These precocial hatchlings exhibit some thermoregulatoryability shortly after hatching although they do not become truly homeothermic severalweeks;the actual time course homeothermic for of development dependson the species.In contrast, altricial birds hatch at a lessdeveloped stageand are dependenton parental care and feedingfor sometime. Altricial hatchlings are ectothermicfor the first few daysafter hatching, but acquire thermoregulatory ability duringthe nestlingperiod, and are homeothermic the time of fledging by (usually at about 2-3 weeks of age, Dawson and Hudson 1970). Using the single criterion of epithelial cell height, Dawson and Allen (1960) concludedthat thyroid function in nestlingVesper Sparrows(Pooecetes gramineus)matchesor exceeds that of adultsand, therefore,anticipatesthe developmentof homeothermy.Rol'nik (1968) stated that the thyroid of altricial birds differentiates into follicles and becomes physiologicallyactive relatively later than in precocial birds, but this comparisonis based on birds that differ markedly in body size and length of their incubation periods.

The objective of this paper is to comparethyroid gland developmentduring the embryonicperiod in a precocialspecies (Japanese Quail), and in an altricial species (Ringed Turtle Doves, Streptopeliarisoria). Although these speciesboth have an incubation period of about 16+ days duration, quail exhibit endothermicresponses to cold shortly after hatching (Spiers et al. 1974) while doves are presumably ectothermic for at least the first few days after hatching (Breitenbachand Baskett 1967 have shown that nestlingMourning Doves are ectothermicfor at least the first 3 days). Our choice of these specieswas determined by the equal length of their incubation periodsplus patterns of developmenttypical of thoseconsidered precocial and altricial.

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of incubation.In dove embryos,similar degrees colloidvacuolizationwere seenin of bothred and bluestainedcolloid; vacuolization waslackingin chromophobic colloid.

In quail thyroidsFD increased significantlyfrom 14.5/• on day 10 to 23.3/• on day 16 (Fig. 3). This change in FD in quail was due to an increase in CD with no significant change in ECH (mean ECH through days 10-16 was 4.5/• with the greatestcell height of 5.7/• 2 days prior to hatching; [Fig. 3]). In embryonicdove thyroids FD did not increasesignificantly(19.6/• on day 16), and ECH decreased significantlyfrom 6.5/• on day 11 to 4.9/• on day 16 (Fig. 3). Follicle diameter was significantlygreater in quail thyroidsthan in dove thyroidson day 16; ECH did not differ significantlybetween the two species (Fig. 3).

–  –  –

thyroid size is considerablysmaller and organization of the gland into follicles is slowerthan in quail embryos(Figs. 1 and 2). Stainingreactionsindicatethat only of the thyroidfolliclesare activein the doveat the time of hatching.In dovethyroids the existence somechromophobic of colloidlate in the incubationperiodparallelsthe conditionin chickenembryos(Romanoff 1960)and is in contrastto the conditionin embryonic quail thyroids.

Colloid vacuolizationdid not appear to be a particularly useful indicator of hormone mobilizationin theseavian embryos.Vacuolizationwas presentin both active and inactivechromophilic colloid,but the degree vacuolization of was not correlated with either changes cell height, or times when hormonereleaseis indicatedby in changesin thyroidal iodine content (McNabb et al. 1972).

Measurementsof follicle dimensionsindicate that quail thyroid growth, after organizationinto completefollicles,occurs increases both follicle number (Fig. 2) by in and FD (Fig. 3). As ECH doesnot increase, but CD does,cell numbersor cell width in the follicle walls must increase.In dove thyroids, FD doesnot changesignificantly during this period. The lack of significantdifferencesbetween species ECH, in although other criteria indicate differencesin thyroid activity, suggests this measurementis poor as a singlecriterionfor comparingthyroid activity betweendifferent avian species, but the generalpattern of ECH changes may be one useful sourceof information. In this study, ECH in quail thyroids showed the same pattern of changes that McNabb et al. (1972) were able to correlatewith the pattern of stable iodine content of the glands. In embryonicdoves, ECH measurements similar to are thoseof hatchling and adult Vesper Sparrows,but lessthan ECH measurements in 2-8-day nestling sparrows (Dawson and Allen 1960).

The histologicalcriteria for thyroid activity usedin this study show good correlation betweenthe time course changes thyroid gland activity, and the patternsof of in developingthermoregulatoryability in theseprecocialand altricial species. Japanese Quail are precocial, and from the time of hatching usemetabolic energyto gain some independence environmental temperature. These quail chickshave active thyroid of glands during most of the latter half of the incubation period. High thyroid hormone secretionoccursjust prior to the initiation at hatching of endothermicresponses to cold (McNabb et al. 1972, Spiers et al. 1974). The patterns of both thyroid gland development and thermoregulatory ability in Japanese Quail are similar to those described chickens,the precocialspecies for that has receivedthe most study (see review by Freeman 1971). The time course of developing thermoregulation in JapaneseQuail is prolonged, relative to that in chickens, as might be expected because of the high rates of heat loss resulting from the quail's small body size.

JapaneseQuail attain thermoregulatoryability more rapidly than do the larger Bobwhite Quail (Borchelt and Ringer 1973), a pattern that is reversedfrom that expected on the basisof body size. Thus while Japanese Quail seeman appropriatechoicefor studyingthe role of the thyroid gland in the thermoregulationof precocialbirds, their rate of post-hatchingdevelopmentis unusually rapid in comparisonto that of other quail.

The altricial pattern of developmentis characterizedby ectothermyin the early hatchling period with high growth efficiency, at least partly becauselittle energy is expendedfor thermoregulation.The thyroid glands of altricial Ringed Turtle Doves showed little evidence of activity by the time of hatching. These resultsare consistent with the low metabolic rates in altricial nestlingsthat remain ectothermicfor at least severaldaysafter hatching (seeBreitenbachand Baskett 1967 for work on Mourning 74-2 McNABBANDMCNABB [Auk, Vol. 94 Doves). The small proportionof active thyroid folliclesduring the embryonicperiod in doves indicates at least some production of thyroid hormones. As thyroid hormonesappear to be necessary normal growth and developmentof avian embryos for (seereview by Betz 1971), the low level of thyroid hormonesmay be sufficientfor this purposebut insufficientto elevatethe metabolicrate to the high levelsrequired for homeothermy. One line of evidence(ECH values in Vesper Sparrow thyroids, Dawson and Allen 1960) indicatesthat the thyroids of altricial nestlingsshow histological evidenceof activity prior to the time when these nestlingsexhibit endothermicresponsesto cold.

Evidence of thyroid hormone production prior to the initiation of endothermic responses cold in both quail and doves indicates thyroid participation in these to metabolic events, but does not reveal the mechanisminvolved in their onset. A marked increasein the release of thyroid hormones could be either the trigger for initiating thermoregulatoryresponses merelypart of the metabolicconditionpreor requisiteto central nervousinitiation of thermoregulatoryresponses.

Distinguishing betweenthesetwo possibilities require neurophysiological will experimentsand measurements circulatingthyroid hormonelevels during the period of developing of thermoregulatory ability.



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