The effects of water deprivation on the hypothalamic-hypophysial neurosecretory system of the

black-throated sparrow, Amphispiza bilineata

Authors Poore, John Thomas, 1943-

Publisher The University of Arizona.

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THE EFFECTS OF WATER .DEEB1FAT10M ON THE HYPOTHALAMIC-HYPOPHYSIAL NEUROSECRETORY SYSTEM OP THE

BLACK-THROATED SPARROW:, A1PHXSP1ZA BXLINEATA

Johm Thomas Poore

A Thesis Submitted to the Fpoulty of the.. DEPARTMENT, O-P BIOLOGICAL SCIENCES -

In Partial Fulfillment of the Requirements For the Degree ofMASTER OF 'SCIENCE . ,

WITH A MAJOR .IN ZOOLOGYIn the Graduate" College

THE' UNBtERSITY OF ARIZONA

STATEMENT BY AUTHOR

This thesis has been sittaiitted In partial fulfill­ment of requirements for an advanced degree at The University of Arizona and is deposited in the University Library to be made available to borrowers under rules of the Library.

Brief quotations from this thesis are allowable without special permission, provided that accurate ac­knowledgment of source is made. Requests for permission for extended quotation from or reproduction of this manu­script in whole or in part may be granted by the head of the major department or the Dean of the Graduate College when in his judgment the proposed use of the material is in the interests of scholarship. In all other instances, however, permission must bo obtained from the author.

This thesis has been approved on the date shown below:

SIGNED:

APPROVAL BY THESIS DIRECTOR

B. ChiassonRobert B. Chiasson Professor of Zoology

TABLE OP CONTENTS

o o o o o « 0 e o ^ o e ' o o & oLIST OP .ILLUSTRATIONSABS XBAC X e o e c e oo. o e o e o o o o e o e ©o e » "V*INTBODUCTION \ . 1;METtoX)S AND MATERIALS..................... . . . . 3RE SUL1 S o o o s- c c e o <> o e e e e ® » e e o o o e e 3DISCUSSION. O 0 . c o o . o c o o . o o o o o o . o . 1?LITERATURE CITED 19

111

LIST OF ILLUSTRATIONS 'Pi gtare , Page -

1» Supraoptic median nucleus*' Granular ■■■neurosecretory material apparent* Two days . dehydratiop . ... . » . »;.. . .. . 6 .

. 2. ' Supra.optie-dorso^lateral and ventro-^lateral.Two days dehydration. »' . ♦' ♦' . ?

3«- Median eminence . .N©:; dehydration . • . . . .. . . 8 '4. Median eminence. Three days dehydration . . . . 95« Heurohypophysts. evaglnating from infundibular

stem In unstressed .bird® 106. Pineal gland, with heavily stained ependymal

layer fibers. Three days dehydration. . . . . . 121 7« Neurohypophysis. No dehydration . . . . . . . . . . . 13 .8. Neurohypophysis, Three days dehydration . , , . 14

ABSTRACT

'Osmotic stress^ either by water deprivation or hypertonic saline solution administration has a noticeable effect on the neurosecretory content of the neurohypophysis ©f several avian species®

The content of neuroseeretion in the neurohyp©-* physis has been shown to be affected differently in-birds inhabiting arid environments compared to those Inhabiting moist environments,. The Black^throated Sparrow„ although Inhabiting arid environments,, displays a neurohypophysial neurosecretory reaction similar to that of moist environ'” meat birds. Laboratory conditions were somewhat more stressful in this study than in others'cited, so any •conclusion's must be judged In-view of this fact.

INTRODUCTION

Early studies by Oksehe et al. (1963) on the Zebra Plneh, Taenlopygia-eastanotls* indieated that osmotic stress, by means of hypertonic ad libitum water solutionse had a less marked effect on. the neurosecretory content of the hypothalamic"hypophysial neurosecretory.system than it had had in his previous experiments with the White^crowned Sparrow6 Zonotriehia leucophrys gambelll» That Is, the .neurohypophysis, of the Zebra Finch did not lose Its apparent content of neurosecretory material as rapidly as did the White-crowned- Sparrow, Likewise, various nuclei of the hypothalamus did not begin their apparent increase of neurosecretory material as early in the Zebra Finch as they did in the White-crowned Sparrow under similar stress conditions® This led.Uemura (1964), MatsuI (1964) and Kripalani» Ghosh, and Rahman (196?) to suspect an ecological adaptation of the hypothalamic-hypophysial neurosecretory system In response to stressful ©somotic situations that occur periodically within the range of the Zebra Finch.

Uemura used the Grass Parakeet,. Melopsittaeus undulatus, as an .experimental animal and obtained results similar to those of Oksehe et al. (1963) with the Zebra Finch. The Grass Parakeet inhabits the same arid parts ofAustralia occupied by the Zebra Finch®

.'. 1

. 2Matsui (1964)$ working with the European Tree

Sparrowo Passer .raontaniis s&turatus„ a bird not found in arid environments s, found that its hypothalamic “hypophysial neurosecretory system had a rapid decrease of neurosecretory, substance In the neurohypophysis with a corresponding increase of neurosecretory material in the hypothalamic nuclei when subjected to dehydration.. ■ ' .

Kripalani. et al. (196?) performed dehydration experiments on three birds of -the Family Ploceidae* from several environments* ranging from swampy to semi«>arlde The ploceids from swampy areas-had hypothalamic“hypophysial responses similar to the European Tree and White-crowned Sparrows. The ploceids from semi-arid regions were more like the Zebra Finch and -Grass Parakeet under conditions of stress.

The Black-throated Sparrow* Amohisolza bilineat-a-. inhabits arid- regions of the-western United States and therefore might be expected to have hypothalamic-hypophysial responses similar to the above mentioned desert inhabiting birds. The following study was designed to deprive the birds of water for a period of days and to subsequently analyze their hypothalamic-hypophysial neurosecretory systems histologically*., to determine if water deprivation affected the neurohypophysial neurosecretory'content In the same, way as other desert birds.

METHODS AND MATERIALS

. . Ten Black-throated Sparrows used in this study were ■caught in mist nets near'-Nogales„ Arizona» on 6 January 1 9 68. Pairs of "birds .were placed indoors in 9nx9n^ ^ t, wire cages soon after capture and -given food consisting of flaxseed, various millets, and groat. Tap water was- administered via L-shaped.drinking tubes on 9 January,On 13 January the birds were- placed in a Scherer controlled,, ■temperature chamber set at 22©C ambient temperature, 39% relative humidity, and a 16 hour photoperiod, Oksehe et- al. (19 63)» working with the Zebra Finch, ran his experiment for. several weeks at temperatures ranging from 22 to 3̂ °C«, Uemura . (196^) .cites no ambient temperature and deprived his birds of water for 5 days,' Matsuies (1964) work ■■ , extended;over three days, ©gain with no temperature specified, Kripalani et .al, (196?), although citing no temperature,. • found that few of the birds he studied-could survive dehydration for more than 5 days so he limited the dehydration time to 3 days, Smyth-and Bartholomew (1966) report that Black-throated Sparrows could survive indefinitely on a diet of dried seed and without free water under normal.laboratory conditions.

After acclimatizing the birds, at 22°C for twoweeks, and at 26', 5°C for 10 days, it was decided to- - V : 3 ' V ,.-,. 'v '■ ..

at 32c2°C the .pairs of .birds were separatedtap water was removed9 and.. disttiled'water was administered from graduated cylinders instead, of from unmarked bottles*After seven days acclimation.at' 32o2°C<, two birds were sacrificed and the other eight birds were deprived of " water„ Two birds were sacrificed after one day of dehydration r three, after, two days of dehydration and? three after three days ©f dehydration*

■ The birds were killed by decapitation, at the end of the dark perled. Most of the skull was chipped away except a portion of the basisphenoid which completely encloses the distal portion of the pituitary* The brain, with, the ■ small' port!on of the- skull attached, was placed in Boutn,9 s under' vacuum' for several seconds to facilitate the penetra­tion of fixative into the ventricles* The tissue was.then left in the fixative for several days. All tissues were' paraffin embedded through xylene, cut at 10 microns, and stained with aldehyde =»thionin. Mallory9 s triple' stain was used as a counterstain.

RESULTS

•The topography of the hypothalamus' 'Of the 'Black--throated Sparrow is similar-to that of the other passerinesstudied. With few exceptions^ Matsui^s (196^) terminology•is used in this study.

The supraoptic nueleus of .the-BlB:ek<»throatedBparrow may be 'divided into femr divisions.; the medial(Se Fig, 1)$, the Intermediate (Si)'$ and the yentro-lateral(Slv) and dorso-lateral (Sid).supraoptic groups (Fig, 2),The paraventricular nucleus may be divided into anterior(Pa), anterio-medial (pam), and: poster!o-medial (ppm)groups. Other aldehyd@=thionin positive cell groups arefound associated with the hypothalamus but their functionwas not determined in this study.

The median eminence.of the Black-throated Sparrowis quite similar.to•that of the other passerines studied(Figs, 3 and 4).

The lobes of the neurohypophysis branch laterally •from a relatively long, stylous infundibular stem (Fig, 5)-'•which may or may not 'be-'l-dbed.'-at''"-the distal end.

Nerve cells with large aldehyde-thlonin positivegranules in a paranuclear arrangement occur lateral to thefirst three ventricles and anterior to the pineal gland.These granules are most prominent:.along- blood vessels,

5

6

Figure 1: Supraoptic median nucleus. Granularneurosecretory material apparent. Two days dehydration. -Sm = Supraoptic median nucleus; ns = neurosecretory granules; It = lamina termlnalls; V = third ventricle. Bird #2. 64X.

7

Figure 2: Supraoptic dorso-lateral and ventro-lateral.Two days dehydration,- Sid = Supraoptic dorso­lateral nucleus; Slv = Supraoptic ventro­lateral. Bird #5B. 64X.

8

Figure 3$ Median eminence. No dehydration. - me = median eminence; pt = pars tuberalls; V * third ventricle. Bird #4. 64X.

9

Figure 4: Median eminence. Three days dehydration. -me s median eminence; A = adenohypophysis. Bird #4B. 64X.

10

Figure 5$ Neurohypophysis evaglnatlng from infundibular stem In unstressed bird.-Is = Infundibular stem; A = adenohypophysis; N = neurohypophysis; ca = carotid artery. 25X.

; 11These positively stained, eellular areas, are continuous with the supraoptic and paraventricular.nuclei (Fige.l).

As reported by Laws (1 9 6 1) and verified in this study* aldehyde-fuehsin ■ prominently stains, certain ependymal areas of.the brain. The.pineal* the posterior end of the corpus callosum below the tela ehoroidea, and the lamina terminalis of the. preoptie recess are particularly well .stained in this manner. These areas contain stringy* uniformly heavily "Stained fibers going to the outer margin of the'pineal'body (Fig, 6) and the medial margin of the preoptie recess and at times * looping back into - the Interior of - the organ, . lt: is •Interesting • to note that these fibers are almost completely absent from the inner.layer of the median eminence where they were originally described,. . • "

A reduction of aldehyde^thionln positive material was evident in the neurohypophysis after only one day of water deprivation. After two days even less neurosecretory ■material was apparent, ■ After three days without water* the neurohypophyses of the three Blaek-»throated ■ Sparrows had a considerable reduction■of'stainable material (compare Figs, 7 and 8 ), ■ The median eminence had a relatively constant supply of aldehyde-thlonin positive material throughout the experiment (Figs, 3 and 4).

Deprivation effects were'- -characterized in the hypothalamus, by an increase of staS,nable material in the

X > 1 > V

Figure 6: Pineal gland with heavily stained ependymallayer fibers. Three days dehydration.- pg = pineal gland; tc = Tela Choroldea;V s third ventricle. Bird #1. 64X.

13

Figure ?: Neurohypophysis. No dehydration. -N = neurohypophysis; ca = carotid artery; V = third ventricle. Bird #2B. 64X.

14

Figure 8: Neurohypophysis. Three days dehydration. -N m neurohypophysis; ca = carotid artery;V s third ventricle. Bird #4B. 64X.

15supraoptic and paraventricular nuclei» The cells of these nuclei became evident through staining after two days of water deprivation and after three days were seen to be filled with particulate accumulations of aldehyde=>thi©nin positive material*

As mentioned - earlier$ - cells that lie lateral to the third ventricle and lateral ventricles and contain heavy paranuclear deposits of ..aMehy4©<»thionln positive material were not noticeably affected during th,® deprivation experiment* - . . .

Table 1 is simply a record of additional data obtained during the .experiment®' No attempt has been made to draw any conclusions from this data because ©f the small ..sample size Involved®

TABLE' I

A B C D E . F G • H1 O* 15.5 9 ,2 3 49,2 7.2? 14.19IB (f 15 „ 3 1 2.? 1 33,2 4.2? 7 .84

2 ? 1 2 .0 9.3 ; 2 8 5 .1 10.63 0

2B g 14.6 . 14.3 0 23.8 3.70 3.423 $ 12.6 9 .4 3 105.3 13.23 gain (2.0 3 8)3B $ 1 1 .0 9.5 i 6 0 .2 6 .2? 1 .8 1

4. : cT 12.8 12 .1 0 260.4 33.35 7.03

4B. 16,9 1 0 .8 .. 3 2 3 .6 3.30 13.60

5 $ 12.'5 1 0 .0 2 28,5 3.52 5.22'5B 13.6 9 .9 2 3 0 .6 3.4? 8.08

Legend: .A e Bird identlfieation - B e Sex' ' ’ .C e Initial body weight at beginning of J2.2°C ©oolimatization D ^ Weight at death E s Days dehydratedF = Per cent body weight drunk per day.at '32.2°C G sa. Average ml. water eonstmed' per day at 32.2°C .H s Per cent body weight lost during 6 day acclimatization

/ at 32.2°p.

DISCUSSION

Munsiek*- Sawyere. and Van Dyke (1960) have shorn that the factors present In the avian neurohypophysis. are, physiologically similar to arginine vasotocin and oxytocin if they are not $ in fact, these substance s«> The former substance is thought to be the anti diuretic hormone*' similar to arginine vasopressin found In mammals. These _ substances are also found to;be present' in the median eminence but in differing proportions. It has not -been definitely shorn that these'substances are those which stain . positively with aldehyde«=fuehsin or aldehyd@=thioniri but neuronal1 pathway tracings by Uesura and Kobayashi (1963) indicate that the stalnable material ©f the -median eminence and neurohypophysis has its origin in the nuclei of the hypothalamus. The amount of this stalnable. material in both the -'median eminence and neurohypophysis and apparently in the cells of the hypothalamic nuclei6 varies as the external factors of photoperiodg estrogen administration or osmotic balance are varied,

Stalnable material in the neurohypophysis-began its apparent- decrease as soon as one day. .after water was removed. These results essentially agree with these- of Oksehe et aI, (1959)9 Matsui (1964) and Kripalani et al. (196?)» all. of whom worked with, birds-from moist environments.

18Information gained through" this experiment in regard

to hypothalami© nuclei;response to deprivation of water is not.as clear as that of the neurohypophysis. It seems evident though6 from the limited information available in this study* that the supraoptic and paraventricular nuclei of the hypothalamus require.’a certain amount of time following the initiation of the stimulus* to show a significant accumulation of stainable material regardless of the -environmental''factors to which they are subjected.

. It does not' appear however * that Blaek-=»throat@d ■Sparrows have adapted their hypothalamic •"hypophysial neurosecretory system to their arid existence in the same way as have the birds studied by previous investigators (Oksche et -al. 1963» Uemura 1964, Kripalani et al. 196?).

LITERATURE CITED

> .K„.$ -A, Ghosh and He Rahmane 196?« Hypothalamic. . rietirdseeretion In relation to water deprivation .in :>'s-RidceidS'.,-of arid and swampy zones. J. Morph.;f23$3 5 ^ 4 1e -

Laws, D. P., 1961. Hypothalamic nenroseeretion in the -refractory and post-refractory periods and its

. relationship to the rate of photoperiodieally Induced ■'testicular growth in Zonotriehia leuepphrys

- ze Zellfprsoh. 54t275^3$87=̂ "Matsuie'' T. >. 1964. Effect of water deprivation on the

lalamie.neurosecretory system of the tree Passer.mantanus saturatus. J. F&e. Set.

Univ.'Tokyo, See. IV 16:355»365#f -•-Mmi'giek, R-.-.-Ae:, ¥11 bur H. Sawyer and H. B. Van Dyke* i9 6 0.

properties and tentative identification.. -/.''Endocrinology 66;860-8 7 1.

Gksehe * A.» D. P. Laws, P. I. Kamemote and D. S. Earner *19 59. the hypothalamic-hypophysial neurosecretory system of the■white-crowned sparrow. Zonotriehia ■leucophrys. gambelii. Z. Zellforseh., D. S. Earner, D, L. Serventy* P. Molff and C.- A. Mieholls* 1 9 6 3. The hypothalamic-hypophysial neurosecretory system of the zebra finch* TaenioWgia eastanotis. Z. Zellforseh. 58;846-9l4

Smyth* M. .and G. A. Bartholomew, 1 9 6 6. The water economyof the black-throated sparrow, Amphispiza bilineata and the rook wren. Condor 68:4^7=^59*

Uemura* -H. and H., Kobayashi * 19 63. Effects of prolongeddaily photoperiods and estrogen, on the hypothalamic neurosecretory system of the passerine bird, Zosterpps palpebrosa iaponica. Gen. & Comp. Endocrinology 3i253^2(

=., 1964. Effects of water deprivation on thehypothalamic-hypophysial neurosecretory system of grass parakeet* Melopsittaeus Undulatus.Gen® & Comp. Endocrinology 4:193=198.