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The reproductive biology of the western red squirrel. Millar, John Steven 1968

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THE REPRODUCTIVE BIOLOGY OF THE WESTERN RED SQUIRREL  by  JOHN STEVEN M I L L A R B.Sc, U n i v e r s i t y o f B r i t i s h Columbia,  1965  A THESIS SUBMITTED I N P A R T I A L FULFILMENT OF THE.REQUIREMENTS FOR THE DEGREE OF MASTER OF S C I E N C E  i n t h e Department o f  Zoology We a c c e p t t h i s t h e s i s a s c o n f o r m i n g t o t h e required  standard  THE U N I V E R S I T Y OF B R I T I S H COLUMBIA February,  1968  In  presenting  advanced  Library  agree  this  degree  shall  that  purposes  make  be  tatives.  It  financial  gain  The  the  University  for  granted  is understood  shall  not  of  U n i v e r s i ty of Br 8, C a n a d a  ^^s/V  of  be  f u l f i l m e n t of  British  available  extensive  by  Vancouver  Date  in p a r t i a l  i t freely  permission  may  Department  at  thesis  the  that  Head  of  my  of  this  Department  or  without  requirements  Columbia,  reference  copying  copying  allowed  for  the  and  study.  thesis  or  publication  my  I agree  written  by  of  for  that  I  the  further  for  scholarly  his  represen-  this  thesis  permission.  an  for  ABSTRACT The r e p r o d u c t i v e squirrels  / c o n d i t i o n o f male and female r e d  (Tarn l a s c l u r u s h u d s o n l c u s ) i n s o u t h e r n  British  C o l u m b i a was s t u d i e d i n r e l a t i o n t o a g e , s e a s o n , population level,  and foods u t i l i z e d .  The r e p r o d u c t i v e  c y c l e o f males and females i s d e s c r i b e d gross  relative  on t h e b a s i s o f  anatomy and h i s t o l o g i c a l c h a r a c t e r i s t i c s .  A low  p o p u l a t i o n o n V a n c o u v e r I s l a n d was s t u d i e d i n  and  I967 a n d a h i g h p o p u l a t i o n was s t u d i e d n e a r P r i n c e t o n , B.C. in  I967.  The h a b i t a t s a r e s i m i l a r i n b o t h r e g i o n s .  low  I966 p o p u l a t i o n h a d a l a t e b r e e d i n g  all  f e m a l e s s a m p l e d p r o d u c e d two l a r g e l i t t e r s .  o v u l a t i o n r a t e f o r t h e two l i t t e r per l i t t e r .  season i n which The  s e a s o n a v e r a g e d 5«12  The s e c o n d o v u l a t i o n o c c u r r e d  the b i r t h of the f i r s t  litter,  v a g i n a e came i n t o f u l l  estrus condition.  before  shortly  adults bred  I n 19&7  both Princeton  s e a s o n s when n e a r l y a l l  y e t o n l y one t h i r d o f t h e y e a r l i n g f e m a l e s  participated. areas.  after  t h e u t e r i and  the low Vancouver I s l a n d p o p u l a t i o n and t h e h i g h p o p u l a t i o n had e a r l y b r e e d i n g  The  Only s i n g l e l i t t e r s  The o v u l a t i o n r a t e was ^.11  were produced i n b o t h per l i t t e r  V a n c o u v e r I s l a n d p o p u l a t i o n a n d 3«58 p e r l i t t e r high Princeton population. 11$ w e r e f a i r l y  constant  l o s s e s were n o t p r e s e n t  i n the low i n the  P r e i m p l a n t a t i o n l o s s e s o f about  i n both years.  Postimplantation  i n t h e l o w 1966 p o p u l a t i o n ,  a b o u t 19% I n t h e h i g h 19&7 p o p u l a t i o n , a n d w e r e n o t d e t e r m i n e d i n t h e l o w 19^7 p o p u l a t i o n .  Similarities  were  ill  b e t w e e n t h e h i g h and  l o w 19&7  b e t w e e n t h e l o w 1966  and  p o p u l a t i o n s and d i f f e r e n c e s  l o w 196?  I s l a n d s u g g e s t t h a t d e n s i t y was Influencing productivity.  populations not  on  the primary  food sources.  cones a r e the main w i n t e r food of the r e d  Conifer  squirrel.  L o d g e p o l e p i n e cones were t h e m a i n food s o u r c e the h i g h l y productive breeding  successful breeding  force  Another e x p l a n a t i o n i s found  i n the e v a l u a t i o n of the primary  D o u g l a s f i r c o n e s made up  Vancouver  before  s e a s o n i n I966 w h i l e  the d i e t before  s e a s o n i n 19&7.  o f t h e c o n i f e r s I s d i s c u s s e d and  The  the  less  fruiting  habits  I t appears t h a t i t i s  a d v a n t a g e o u s f o r t h e s q u i r r e l t o f e e d on l o d g e p o l e cones.  A good w i n t e r f o o d s u p p l y  important  is particularly  to the red s q u i r r e l s i n c e i t breeds  t h e l a t e w i n t e r and  during  i t ' s already high metabolic  i n c r e a s e s s t i l l more d u r i n g c o l d w i n t e r w e a t h e r . is  inferred  pine  t h a t t h e w i n t e r f o o d s u p p l y may  rate It  influence  t h e r e l a t i v e c a p a c i t y o f the female t o produce young. The  t i m i n g of the breeding  and  seems t o be a f f e c t e d b y  weather.  season i s q u i t e v a r i a b l e the s e v e r i t y of the  winter  iv TABLE OF CONTENTS page . TITLE PAGE  ...  ABSTRACT  ...................... i  •  ••  TABLE OF CONTENTS  •  i  LIST OF FIGURES  P  L  .......vii A  T  E  S  «  INTRODUCTION **• °  •  «  •  •  »  v  • • • • « e » » « » » « e » » » » »  .  3  «  «  ^  m s t t i o d s « » o o » c « « o « * « e 0 c e o * e e o » o 6 « « o  3  e  e  e  t  f  o  «  *  «  «  e  *  «  «  «  •  3 • *  «  Q  »  •  •  e  a  o  «  e  *  c  .  #  «  0  «  «  * e  «  «  «  o  *  «  «  «  .  o  »  »  «  «  «  c  «  o  o  « 0  «  « «  «  »  o  *  «  o  » o  o  . e  «  «  «  ^  RESULTS The male r e p r o d u c t i v e c y c l e Infantile . Developing Functional Degenerate  9 9 11 1 3 17 20 2 3 2426 28  The female r e p r o d u c t i v e c y c l e Infantile Proestrus Estrus 3? J C * 3 ^ ] Q a r i t Lactating Anoestrus e  •  •  •  e  e  «  o  The b r e e d i n g season •  •  •  •  f  l  o  0 * V * l l l a t i 0*fl X*atO  e  0  «  e  o  0  *  »  f  e  o  0  0  «  c  «  »  t  >  t  e  «  e  o  *  3-1  «  3 3 3 6  -.  3 8  ........ \ 0  « «  1  1  «  •  •  i  •  •  .  i «  MATERIALS A N D METHODS Description of habitats FiGXcL HietllO(3.S Xiaboxa'cory Asj© ciet ©jtmiiiatxon  F©OTJm.(3.it"y"  v  vi  LIST OF TABLES LIST OF  1 1  0  C  9  e  e  o  «  o  «  o  o  «  «  *  e  *  e  0 •  e e  o o  » o  « a  « v  e o  »  c e  c  * a  0 c  O e  * o  * e  « o  »  ^ 3 ^*3  *  Preimplantation losses 4-5 Eoib2?yo conribs Embryo r e s o r p t i o n s 4-7 Frequency of b r e e d i n g females........... 5 0 «  «  o  c  0  *  o  «  t  c  »  *  «  *  »  «  o  e  «  «  o  e  «  o  *  «  Reproduction i n r e l a t i o n t o P o p u l a t i o n L e v e l . 5 2 Reproduction In r e l a t i o n t o food  5 3  V  page , . 58 58 58 58  DISCUSSION The r e p r o d u c t i v e c y c l e , . . The m a l e c y c l e The f e m a l e c y c l e Age  59  at maturity  The b r e e d i n g s e a s o n Timing o f breeding Yearly variations E f f e c t s o f weather Duration of breeding Possible influences of habitat.... Male and female synchrony  0  60 60 60 6l 63 6k 65  Yearly v a r i a t i o n 66 E f f e c t o f d e n s i t y d e p e n d e n t f a c t o r s . . . . . . 66 E f f e c t o f foods 67 N a t u r e o f t h e c o n i f e r cone c r o p s 68 Advantages o f p i n e cone c r o p s o v e r f i r cone c r o p s Possible control of breeding  , 69 71  ACKNOWLEDGMENTS  83  L I T E R A T U R E CITED.  84  vi L I S T C F FIGURES  FIGURE  1.  D r i e d eye l e n s weight-age s c a l e , t a b u l a t e d from 59 animals aged i n d e p e n d e n t l y by t o o t h wear and c l o s u r e o f t h e raidsagittal c r e s t .  2.  S e a s o n a l changes I n t h e mean l e n g t h o f male r e p r o d u c t i v e - organs. Taken d u r i n g (A) t h e 1966 b r e e d i n g season on Vancouver I s l a n d and (B) d u r i n g t h e 19&7 b r e e d i n g season on Vancouver I s l a n d and i n t h e i n t e r i o r o f B r i t i s h Columbia,  >  3.  The d u r a t i o n o f v a r i o u s r e p r o d u c t i v e stages of males and females. P l o t t e d as t h e p e r i o d between t h e c o l l e c t i n g o f t h e f i r s t and l a s t a n i m a l i n each p a r t i c u l a r s t a g e . (A) The I 9 6 7 b r e e d i n g season on Vancouver I s l a n d and i n t h e i n t e r i o r o f B r i t i s h Columbia. ( B ) The I 9 6 6 b r e e d i n g season on Vancouver I s l a n d  h.  The f r e q u e n c y of l a c t a t i o n as i n d i c a t e d by the . c o n d i t i o n o f t h e n i p p l e s i n 1 9 6 6 , 19^7 • and o f p r e v i o u s l y c o l l e c t e d animals i n t h e V e r t e b r a t e Museum a t t h e U n i v e r s i t y o f B r i t i s h Columbia  vii L I S T OP TABLES TABLE I  II  page The o v u l a t i o n r a t e a s i n d i c a t e d bycorpora l u t e a counts of a l l breeding females. Tabulated by age, season, y e a r and l o c a t i o n . . - . P r e i m p l a n t a t l o n l o s s e s as i n d i c a t e d b y t h e d i f f e r e n c e b e t w e e n t h e number o f o v u l a t i o n s i t e s and i m p l a n t a t i o n sites. Tabulated by age, season, year &11GL 1 OGStfc 3. O H ©  III  e  o  «  o  e  e  o  «  »  «  c  o  o  v  o  o  o  e  «  »  e  e  »  «  P o s t i m p l a n t a t i o n l o s s e s as i n d i c a t e d b y t h e number o f v i s i b l e r e s o r b i n g embryos. T a b u l a t e d by age, season,  V  Percent females b r e e d i n g a f t e r the o n s e t o f t h e b r e e d i n g season as i n d i c a t e d by p r o e s t r u s , pregnancy o r lactation. Tabulated by age, year  VII  «  9  0  «  o  o  e  e  o  o  Embryo c o u n t s a s i n d i c a t e d b y v i s i b l e embryos o r i m p l a n t a t i o n s i t e s . Resorbing embryos i n c l u d e d . T a b u l a t e d by age, season, y e a r and l o c a t i o n . . . . . . . . 0 0 0 . 0 . 0 . 0 . . . . .  IV  VI  *l4  R e l a t i v e p o p u l a t i o n l e v e l s as i n d i c a t e d b y t h e number o f c a l l s h e a r d p e r h o u r and t h e number k i l l e d p e r d a y . T a b u l a t e d b y y e a r a n d l o c a t i o n . . ........ Frequency o f g e n e r a l food types found i n s q u i r r e l stomachs. T a b u l a t e d as a p e r c e n t o f t h e t o t a l number o f s t o m a c h s e x a m i n e d  ^4*6  48  54  vlii  L I S T OF PLATES PLATE  page I  IX  Ill  IV  V  VI  VII  73  Vancouver I s l a n d h a b i t a t A. A n o p e n r o c k y s i t e . B. Dense v e g e t a t i o n . l i l t 63?!. O fa&Di fc&*fc «  A. Bo  # "o • • « « « o e » » o o « * o e « « « » e e «  7^  An open s i t e . Dense v e g e t a t i o n .  S e a s o n a l c h a n g e s i n t h e t e s t e s . ............... 7 5 A. Infantile. B. Developing. C. E a r l y f u n c t i o n a l . D. L a t e f u n c t i o n a l . E. Degenerating. S e a s o n a l changes i n t h e e p i d i d y m i d e s . A. Infantile. 3. Developing. C. Functional. D. Degenerating.  76  S e a s o n a l changes i n t h e s e m i n a l v e s i c l e s . A. Infantile. B. Early developing. C. F u n c t i o n a l ( C i , i i , i i i ) C o n s e c u t i v e stages o f e p i t h e l i u m development. D. L a t e f u n c t i o n a l .  77  S e a s o n a l changes i n t h e p r o s t a t e . A. Infantile. B. Early developing. C. F u n c t i o n a l ( i ) e a r l y (ii) late D. Degenerate. S e a s o n a l changes i n t h e v a g i n a A. Infantile. B. Early Proestrus. C. E s t r u s . D. Late Pregnancy. E. Early anoestrus.  «. 7 8  79  ix PLATE  page  VIII  IX  X  S e a s o n a l changes i n t h e u t e r u s , A. Infantile. B. Estrus. C. Early lactation. D. Anoestrus ( i ) winter (ii) summer  80  S e a s o n a l changes i n t h e o v a r y • A. Infantile (i) three to four months o l d (ii) four to five months o l d nearing proestrus (iii) B. Post ovulatory. C. Winter anoestrus  81  Changes i n t h e c o r p o r a l u t e a . . A. P r e g n a n c y and l a c t a t i o n . ( i ) e a r l y pregnancy ( i i ) l a t e pregnancy (iii) lactation. B. Late lactation. C. Early anoestrus.  82  INTRODUCTION The  redsquirrel  (Tamiasciurus hudsonicus) i s  a common i n h a b i t a n t o f t h e c o n i f e r o u s f o r e s t s o f N o r t h America.  Although  i t i s e a s i l y observed  and.generally  a b u n d a n t , much o f i t s b a s i c b i o l o g y i s u n r e c o r d e d . R e p r o d u c t i o n i s one f a c e t o f t h e r e d s q u i r r e l ' s b i o l o g y t h a t i s n o t w e l l documented, p a r t i c u l a r l y i n t h e west. This study concerns hudsonicus  the red squirrels  Tamiasciurus  l a n u g i n o s u s and Tamiasciurus  streatorl.  C o l l e c t i o n s w e r e made o f T . h  hudsonicus a  l a n u g i n o s u s on  s o u t h e r n V a n c o u v e r I s l a n d f r o m O c t o b e r 19&5 *° S e p t e m b e r 1967,,  T o h . s t r e a t o r l was s t u d i e d i n t h e v i c i n i t y o f  P r i n c e t o n , B „ C . f r o m J a n u a r y I967 t o O c t o b e r  1967.  O b s e r v a t i o n s w e r e made o n t h e l i f e h i s t o r y i n o r d e r t o e v a l u a t e t h e y e a r l y and s e a s o n a l r e p r o d u c t i v e changes w i t h p a r t i c u l a r emphasis on t h e v a r i a t i o n i n r e p r o d u c t i v e performance  i n r e l a t i o n t o age, f o o d , season, and  population density.  I n addition, histological preparations  w e r e made o f m a l e a n d f e m a l e  organs  t o determine t h e  y e a r l y c y c l e s as w e l l as t h e e x a c t r e p r o d u c t i v e c o n d i t i o n of  each  animal. Important  of  previous f i e l d  s t u d i e s on t h e r e p r o d u c t i o n  t h i s s p e c i e s a r e t h o s e o f L a y n e (195^) a n d S m i t h  (1965).  Layne*s s t u d y I n c l u d e s t h e g r o s s s e a s o n a l changes i n t h e r e p r o d u c t i v e organs  o f Toh. l o q u a x i n New Y o r k .  s t u d y i n c l u d e s d a t a on l i t t e r  s i z e and b r e e d i n g  Smith s s  seasons  -2-  for  the Douglas s q u i r r e l  red s q u i r r e l  ( T a m i a s c l u r u s d o u g l a s l ) and t h e  (T.h. s t r e a t o r l )  i n B r i t i s h Columbia.  The  anatomy o f t h e male r e p r o d u c t i v e t r a c t has b e e n d e s c r i b e d b y Mossman, L a v x l a h , a n d B r a d l e y  (1932).  MATERIALS AND  Red  METHODS  s q u i r r e l s were c o l l e c t e d monthly,  except  when p r e v e n t e d b y h e a v y snow o r f o r e s t f i r e d a n g e r . a n i m a l s , w i t h the e x c e p t i o n of a few.road o b t a i n e d w i t h a .410  shotgun.  One  kills,  h u n d r e d and  A l l  were sixty-nine  a n i m a l s w e r e t a k e n on V a n c o u v e r I s l a n d d u r i n g 1965-66 and  51  i n 1967.  Two  h u n d r e d and  t w e n t y - t h r e e were t a k e n  from the i n t e r i o r of B r i t i s h Columbia The  i n I967.  a r e a s s t u d i e d on V a n c o i i v e r I s l a n d a r e i n  t h e C o a s t a l Douglas  F i r z o n e ( K r a j i n a , 1965)  c o n s i s t o f open r o c k y b l u f f s where Douglas  and  generally  f i r (Pseudotsuga  m e n z l e s l i ) and l o d g e p o l e p i n e (Pinu£ o o n t o r t a ) a r e dominant t r e e s ( P l a t e I ) . include red alder  O t h e r t r e e s on t h e a r e a  (Alnus r u b r a ) , western hemlock  h e t e r o p h y l l a ) and a r b u t u s  the  (Arbutus m e n z l e s l i ) .  (Tsuga Salal  ( G a u l t h e r i a s h a l l o n ) i s the dominant shrub beneath t r e e c a n o p y and k i n n l k i n n i k h a i r y manzanita  uva-urs1),  ( A r c t o s t a p h yI o s  (Arctostaphy1os  c o l u m b l a n a ) , and  s p r a y ( H o i o d l s o u s d i s c o l o r ) a r e common on o p e n The  c l i m a t e of these areas i s very m i l d .  temperature and  50°F, r a i n f a l l  averages  s n o w f a l l averages The  C o l u m b i a was habitat.  l e s s than  sites.  i s greater than  50"  30". British  f o r I t s s i m i l a r i t y to the  C o l l e c t i n g was  ocean  The mean a n n u a l  study area i n the i n t e r i o r of chosen  the  island  done w i t h i n t h e I n t e r i o r  Douglas  F i r zone n e a r P r i n c e t o n where t h e dominant t r e e s a r e l o d g e p o l e p i n e ( P . c o n t o r t a ) and Douglas a l t h o u g h ponderosa spruce The  f i r (P. m e n z i e s i i ) ,  p i n e ( P i n u s p o n d e r g s a ) a n d Engelraann  ( P i c e a e n g e l m a n n l ) a r e common o n c e r t a i n  sites.  h a b i t a t i s more o p e n t h a n t h a t f o u n d o n V a n c o u v e r  Island  (Plate I I ) .  Soopalallie  r e d - o s i e r dogwood ( C o r n u s (Ceanothus  ( S h e p h e r d l a canadensis)„  s t o l o n i f e r a ) and snowbrush  v e l u t i n u s ) a r e t h e dominant shrubs.  The  c l i m a t e I s d r i e r than Vancouver I s l a n d w i t h an annual p r e c i p i t a t i o n o f l e s s t h a n 22". and  S n o w f a l l I s b e t w e e n 30  70" a l t h o u g h t h e mean a n n u a l t e m p e r a t u r e  i s ^9°P«  Specimens were weighed and measured as soon a f t e r c o l l e c t i n g as p o s s i b l e . animal's a c t i v i t i e s The  A n o t e was made o f e a c h  or l o c a t i o n a t the time o f c o l l e c t i o n .  c o n d i t i o n o f t h e n i p p l e s and v u l v a o f  females and t h e scrotum  o f t h e m a l e s was r e c o r d e d .  Eyeballs  w e r e r e m o v e d a n d s t o r e d i n 10% b u f f e r e d f o r m a l i n f o r u s e as a c r i t e r i o n o f age by eye l e n s e w e i g h t .  The  g e n e r a l c o n d i t i o n o f t h e r e p r o d u c t i v e t r a c t was n o t e d , and  t h e u t e r i , vaginae,, a n d o v a r i e s o f f e m a l e s  measured.  were  The c o r p o r a l u t e a , embryos o r p l a c e n t a l s c a r s  w e r e c o u n t e d when p o s s i b l e .  I n males t h e t e s t e s ,  seminal  v e s i c l e s , and p r o s t a t e g l a n d s were measured. A l l r e p r o d u c t i v e t r a c t s were f i x e d  I n Bouins  fixative for  t h r e e d a y s a n d s t o r e d i h 70^ e t h y l a l c o h o l .  Stomachs  -5.were.noted as f u l l ,  half full,  little  presence of general  food  recorded.  types  o r empty a n d t h e Representative  m o n t h l y s t o m a c h s a m p l e s w e r e s t o r e d i n 10$ f o r m a l i n i n case c l o s e r examination cleaned  became d e s i r a b l e .  S k u l l s were  d u r i n g 1965=66 t o b e u s e d i n e s t a b l i s h i n g a n e y e  lens weight-age s c a l e . S p e c i a l a t t e n t i o n was p a i d t o s i g n s o f s q u i r r e l f e e d i n g such as s t o r e d f o o d s , d i g g i n g s , and cone remains in  middens. The number o f c a l l s h e a r d p e r u n i t t i m e  noted f o r d i f f e r e n t times get a r e l a t i v e  was  d u r i n g t h e day i n order t o  index of population d e n s i t y .  One  hour  was t h e u s u a l t i m e p e r i o d u s e d o n V a n c o u v e r Island„ B e c a u s e o f t h e much g r e a t e r number o f c a l l s h e a r d , m i n u t e p e r i o d s were r e c o r d e d o n l y were used f o r t h i s the breeding  at Princeton.  A p r i l a n d May  i n d e x s i n c e t h e s e months  seasons o f b o t h years, before  15  included  t h e young o f  the y e a r were o u t . I n the l a b o r a t o r y , a r e p r e s e n t a t i v e sample o f each month s c o l l e c t i o n o f r e p r o d u c t i v e 8  embedded all  i n p a r a f f i n and s e c t i o n e d a t 7  o r g a n s was .  trimmed,  The o v a r i e s o f  f e m a l e s i n r e p r o d u c t i v e c o n d i t i o n , as w e l l as a  sample o f a l l other females, order  to get accurate  were s e r i a l l y s e c t i o n e d i n  counts o f corpora  a l b l c a n t i a , and f o l l i c l e s . w i t h D e l a f i e l d s haematoxylin  lutea,  corpora  A l l s e c t i o n s were s t a i n e d and e o s i n .  -6-  Age was d e t e r m i n e d b y t h e u s e o f t h e d r i e d e y e lens weight technique  (1959)*  developed by Lord  f i x e d l e n s .was c l e a n e d  o f a l l v i t r e o u s humor, p l a c e d  a s m a l l v i a l a n d d r i e d f o r 72 h o u r s a t 65°C. l e n s was t h e n w e i g h e d t o t h e n e a r e s t on an e l e c t r i c b a l a n c e .  ,2mg,  In  Each d r i e d  tenth of a milligram  At f i r s t both lenses  were  w e i g h e d , b u t t h e maximum d i f f e r e n c e f o u n d i n 17 o f l e n s e s was  Each  pairs  s o o n l y one l e n s was u s e d t h e r e a f t e r .  S i n c e no known age a n i m a l s w e r e a v a i l a b l e , a n accurate  eye l e n s age s c a l e c o u l d n o t be d e t e r m i n e d .  was p o s s i b l e , h o w e v e r , t o s e p a r a t e  animals greater  It  than  one y e a r o l d f r o m a n i m a l s l e s s t h a n one y e a r o l d t h r o u g h the use of other  c h a r a c t e r i s t i c s ; namely, t o o t h wear and  midsagittal crest closure.  One h u n d r e d a n d f i f t y - o n e  s k u l l s w e r e c l a s s e d a s j u v e n i l e ( l e s s t h a n one y e a r o l d ) or adult Since  ( g r e a t e r t h a n one y e a r o l d ) b y t o o t h w e a r .  t o o t h wear c a n v a r y w i t h f e e d i n g  s k u l l s were a g a i n  conditions the  c l a s s i f i e d as a d u l t s o r j u v e n i l e s by  the degree of c l o s u r e of the m i d s a g i t t a l c r e s t . with fully  c l o s e d c r e s t s were c o n s i d e r e d  w i t h open c r e s t s were c o n s i d e r e d  Those  a d u l t s , and t h o s e  juveniles.  The e y e l e n s  w e i g h t was p l o t t e d f o r 59 o f t h e s e a n i m a l s i n w h i c h t h e a g e was t h e same b y b o t h m e t h o d s the  ( f i g . 2).  Once  e y e l e n s w e i g h t s c a l e was c o m p l e t e d , t h e age was  d e t e r m i n e d on t h e b a s i s o f eye l e n s w e i g h t a l o n e .  In  Figure I.  D r i e d eye l e n s w e i g h t - a g e s c a l e , t a b u l a t e d f r o m 59 a n i m a l s a g e d i n d e p e n d e n t l y b y t o o t h w e a r and c l o s u r e o f t h e midsagittal crest.  -7-  -8-  c a s e s where t h e e y e b a l l s were destroyed.,  the animals  were aged on t h e b a s i s o f s k u l l c h a r a c t e r i s t i c s , size,  w e i g h t and c o n d i t i o n o f t h e r e p r o d u c t i v e  body tract.  RESULTS The M a l e R e p r o d u c t i v e The  Cycle  anatomy o f t h e m a l e r e p r o d u c t i v e t r a c t  Tamiasciurus hudsonicus Lawlah, of  has b e e n d e s c r i b e d b y Mossman,  and B r a d l e y (1932).  permanently  of  B a s i c a l l y the t r a c t  consists  s c r o t a l t e s t e s , a s i n g l e compound t u b u l a r  prostate gland, a p a i r of s a c - l i k e tubular seminal v e s i c l e s and a p a i r o f v e s t i g i a l Cowpers g l a n d s . b u t t h e Cowpers g l a n d s a r e c o n s i d e r e d i n t h e study. and  present  Extreme s e a s o n a l changes b o t h i n g r o s s  size  h i s t o l o g i c a l s t r u c t u r e occur i n the reproductive  organs.  These changes i n v o l v e a l l a c c e s s o r y as w e l l  primary r e p r o d u c t i v e organs. was  A l l  determined  The  as  reproductive condition  by t a b u l a t i n g t h e c h a r a c t e r i s t i c s  r e p r o d u c t i v e organs, r a t h e r than j u s t the testes  of a l l and  epididymides. U s i n g two  independently derived  r e p r o d u c t i v e c o n d i t i o n a n d age are c l a s s i f i e d  criteria,  approximation, the males  i n t o f o u r m a j o r grou.ps;  d e v e l o p i n g , f u n c t i o n a l and d e g e n e r a t e .  infantile, I n f a n t i l e males  a r e t h o s e t h a t were b o r n w i t h i n t h e y e a r ; t h a t i s , t h e y a r e l e s s t h a n one y e a r o l d and  show no s i g n s o f h a v i n g  e x p e r i e n c e d any r e p r o d u c t i v e d e v e l o p m e n t . males i n c l u d e animals of a l l ages,  Developing  i n c l u d i n g young o f  t h e y e a r t h a t show a n i n c r e a s e i n t h e s i z e o f r e p r o d u c t i v e organs  a l o n g w i t h h i s t o l o g i c a l changes, but which are  sexually fully  functional.  F u n c t i o n a l males are  not  animals  -10o f a l l ages t h a t p o s s e s s l a r g e a c t i v e r e p r o d u c t i v e and  a p p e a r t o be c a p a b l e o f b r e e d i n g  includes  only  organs  successfully.  This  those males i n which a l l r e p r o d u c t i v e  organs a r e f u n c t i o n a l .  D e g e n e r a t i n g males i n c l u d e  animals  of a l l ages t h a t have been s e x u a l l y f u n c t i o n a l b u t appear t o have l o s t  the capacity t o breed.  between d e v e l o p i n g , is  often d i f f i c u l t  The d i s t i n c t i o n  f u n c t i o n a l and d e g e n e r a t i n g t o make s o t h a t h i s t o l o g i c a l  males criteria  i n these cases i s p a r t i c u l a r l y u s e f u l . The  general  classification  made f o r t h e f o x s q u i r r e l 1955)  a  n d male a c c e s s o r y  gray s q u i r r e l Kirkpatrlck,  i s similar  (Sciurtis nlger)  to that  testes (Kirkpatrlck,  organs o f t h e f o x s q u i r r e l and  ( S c i u r u s c a r o l l n e n s i s ) (Mossraan, H o f f m a n a n d 1955).  -11Infantile  Males I n f a n t i l e males a r e present  i n the population  f o r most o f t h e y e a r .  They a r e a b s e n t o n l y b e t w e e n t h e  time o f f i r s t breeding  i n t h e s p r i n g a n d t h e t i m e when  the young l e a v e  the nest  a b o u t two m o n t h s l a t e r .  The  young remain i n t h e i n f a n t i l e c o n d i t i o n u n t i l about s i x t o t e n m o n t h s o l d . d e p e n d i n g o n when t h e y w e r e b o r n . They b e g i n  t o come i n t o b r e e d i n g  c o n d i t i o n i n January  o r F e b r u a r y , a l o n g w i t h t h e o l d e r males« T h r o u g h o u t t h e i n f a n t i l e pha.se t h e s c r o t u m i s b a r e l y d i s c e r n a b l e and t h e penis being  l e s s t h a n 40 mm  a b o u t 6 mm although  i n length.  scrotal i n position,  t h e y a r e sometimes found i n t h e i n g u i n a l c a n a l I n texture the testes are firm  smooth, and f i n e s t r a i g h t b l o o d  i n the tunica albuginea. and  The t e s t e s , w h i c h a r e  i n length, are typically  or abdominal c a v i t y . and  i s small, ustially  c a n be seen  The e p i d i d y m i d e s a r e s m a l l  compact, and a l l a c c e s s o r y  inconspicuous  vessels  organs remain s m a l l and  throughout the i n f a n t i l e p e r i o d .  On  each s i d e o f t h e a n t e r i o r u r e t h r a a r e s i t u a t e d t h e small, w i n g - l i k e seminal 3 mm  vesicles„  i n l e n g t h a n d f r e q u e n t l y h i d d e n i n a mass o f f a t .  Just caudal gland  t o these glands l i e s  the prostate, a single  a b o u t 3 mm l o n g a n d 2 mm w i d e t h a t i s i n t i m a t e l y  associated with the ventral urethra. the  These a r e about  Microscopically,  i n f a n t i l e t e s t e s possess c l o s e l y packed  seminiferous  =12=  tubules  averaging  7 0 ^ i n diameter (Plate I I I A).  These  t u b u l e s , w h i c h a r e b o u n d w i t h s m o o t h b a s e m e n t membranes, c o n t a i n l o o s e l y a s s o c i a t e d rows o f s p e r m a t o g o n i a , p r i m a r y s p e r m a t o c y t e s and S e r t o l i  cells.  open l u m i n a i n t h e t u b u l e s , a l t h o u g h tubules  T h e r e a r e no  the centre  of the  f r e q u e n t l y c o n s i s t s of an a c i d o p h i l i c m a t r i x  r a t h e r t h a n c e l l u l a r components.  Between t h e  tubules  there are scattered Leydig  c e l l s , which are generally  l e s s t h a n 9/< i n d i a m e t e r .  These p o s s e s s d a r k  n u c l e i and v e r y l i t t l e  irregular  cytoplasm.  The e p i d i d y m i d e s d u r i n g c o n s i s t o f s m a l l round tubules  the i n f a n t i l e  period  w i t h open l u m i n a  that  a r e l i n e d w i t h c o l u m n a r e p i t h e l i u m a b o u t 12/< i n h e i g h t (Plate IV A).  These columnar c e l l s  contain  oblong  b a s a l n u c l e i w i t h s e v e r a l n u c l e o l i and a v e r y of a p i c a l cytoplasm. in  these c e l l s .  consists c h i e f l y of loose connective  heavily nucleated strips  of the epididymides tissue.  v e s i c l e s of the i n f a n t i l e  possess secretory tubules number ( P l a t e V A ) .  Much o f t h e g l a n d  of collagen f i b r e s  e  consists of  t i s s u e separated  thin lumina  them shows  The s e c r e t o r y c e l l s a r e  t h e i r n u c l e i are large, but l i t t l e  present.  by  Although the tubule  r e m a i n open t h e s e c r e t o r y e p i t h e l i u m l i n i n g  and  male  w h i c h a r e s m a l l and few i n  connective  no s i g n o f a c t i v i t y .  area  No s e c r e t i o n d r o p l e t s ©an b e s e e n  The r e s t o f t h e b u l k  The s e m i n a l  thin  elongate  cytoplasm i s  -13Th e p r o s t a t e a l s o c o n s i s t s m a i n l y o f nucleated connective tissue, ( P l a t e VI A ) . lumina but  A few  along with small tubules .  of these tubules possess  open  i n many t h e r a n d o m l y o r i e n t e d e p i t h e l i a l  occlude the openings. epithelial  cells  a p p e a r t o be a n y tubules.  heavily  cells  I n the la.tter case, I n which  a r e o r i e n t e d randomly, t h e r e does  the not  true s e c r e t o r y e p i t h e l i u m i n the  There i s , however, a d i s t i n c t  row  of o v a l  n u c l e i about the p e r i p h e r y of the tubules t h a t i s p r o b a b l y d e s t i n e d t o become t h e f u n c t i o n a l s e c r e t o r y epithelium. Taken t o g e t h e r , the male r e p r o d u c t i v e organs during the i n f a n t i l e  s t a g e a r e c h a r a c t e r i z e d by  small  t e s t e s p o s s e s s i n g c l o s e l y packed seminiferous tubules t h a t a r e b o u n d e d b y s m o o t h b a s e m e n t membranes and  which  c o n t a i n no n a t u r a l l u m i n a .  i n the  epididymides  and  Open l u m i n a a r e f o u n d  s e m i n a l v e s i c l e s and  occasionally i n  the p r o s t a t e , although the e p i t h e l i a w i t h i n these possess  little  c y t o p l a s m and  glands  show no s i g n s o f s e c r e t o r y  activity. Developing D e v e l o p i n g m a l e s c a n be  found  i n the p o p u l a t i o n  f r o m l a t e D e c e m b e r t o e a r l y M a r c h , d e p e n d i n g on t h e I t p r o b a b l y t a k e s an i n d i v i d u a l male l e s s develop  to the functiona.1 s t a t e .  year.  t h a n a month t o  There appears  to  be  -In-  c o n s i d e r a b l e synchrony among i n d i v i d u a l s i n development d u r i n g t h i s p e r i o d and the j u v e n i l e s , although  they have  not bred b e f o r e , undergo developmental changes a t t h e same time as the o l d e r males. Gross changes d u r i n g the p e r i o d o f development i n c l u d e an Increase  i n s i z e and consplcuousness o f the  scrotum, along w i t h a p a r t i a l shedding o f the s c r o t a l f u r and  a darkening  o f the s c r o t a l s k i n  v a r y from 8 t o 16 mm  In length.  0  The t e s t e s may  Blood v e s s e l s i n the  t u n i c a a l b u g i n e a become conspicuous and the enlarge. at this  Epididymal  epididymides  tubules a r e n o t e x t e r n a l l y conspicuous  time. The  seminal v e s i c l e s , i n which the tubules a r e  evident e x t e r n a l l y , may be as l a r g e as 1? mm l o n g d u r i n g t h i s p e r i o d o f development.  Although q u i t e l o n g ,  they  a r e not as s w o l l e n as those o f f u n c t i o n a l males.  Two  d i s t i n c t r e g i o n s o f the seminal v e s i c l e s become e v i d e n t ; a l a r g e , promlnant p o r t i o n showing d i s t e n d e d  tubules and  a s m a l l e r d o r s o - l a t e r a l p o r t i o n made up o f s m a l l The d e v e l o p i n g  tubules.  p r o s t a t e may be as l a r g e as 6 mm  l o n g and k mm wide and forms a t h i c k , l i g h t c o l o u r e d bulge on the v e n t r a l u r e t h r a .  Because o f i t s compact form, the  gross morphology o f the p r o s t a t e does n o t show any c l e a r cut i n d i c a t i o n o f i t s p h y s i o l o g i c a l s t a t e . accurate determination  A much more  can be made h i s t o l o g i c a l l y .  M i c r o s c o p i c a l l y , the t e s t e s show s e v e r a l d i s t i n c t f e a t u r e s d u r i n g the developmental phase, a l l o f which  -15g e n e r a l l y occur simultaneously. around the seminiferous tubules  The  b a s e m e n t membranes  t u b u l e s become t h i n n e r as  increase i n diameter.  As  the tubules  the  increase,  they a l s o separate, l e a v i n g l a r g e i n t e r t u b u l a r spaces t h a t c o n t a i n d i s t i n c t clumps o f L e y d i g c e l l s  ( P l a t e I I I B)  The  gradually  c e l l s a r e a b o u t 11^  a c q u i r e an  i n diameter  and  they  i n c r e a s i n g amount o f c y t o p l a s m .  seminiferous  Within  the  tubules there i s spermatogenic a c t i v i t y  s p e r m a t o z o a may  be  seen a t the time  t h a t the tubule  and lumina  open. The  increase In the gross  s i z e of the  i s c h i e f l y a r e s u l t of i n c r e a s i n g tubule ( P l a t e IV B ) .  L a r g e open l u m i n a  p a r t i a l l y occluded  by  from the d e v e l o p i n g epithelium.  The  cytoplasmic  intertubular connective  connective in size.  the tubules  increase  t h e t u b u l e s and  vesicles  the connective  compact.  also  tissue,  t i s s u e b e c o m i n g t h i n as t h e t u b u l e s  the  increase  W i t h i n the tubules the p r e v i o u s l y jumbled  (Plate V B).  forms a b a s a l p s e u d o s t r a t i f i e d  F u r t h e r tubule development  i n the f o r m a t i o n of a t h i n l a y e r of a p i c a l and  the  t i s s u e becomes t h i n and  array of e p i t h e l i a l c e l l s layer  of the s e c r e t o r y  is a pseudostratified  Changes w i t h i n t h e s e m i n a l involve both  be  filaments projecting  a p i c a l cytoplasm  As  diameter.  a r e p r e s e n t b u t may  epithelium Itself  columnar c e l l l a y e r .  epldidymid  results  cytoplasm  t h e p r e s e n c e o f s e c r e t i o n d r o p l e t s w i t h i n them.  Most of the gland growth r e s u l t s from the  tremendous  -16Increase  i n the s i z e of the lumina i n c o n j u n c t i o n  the formation  of s e c r e t i o n d r o p l e t s .  During  with  late  d e v e l o p m e n t t h e s e c r e t o r y e p i t h e l i u m becomes t h r o w n i n t o f o l d s and  t h e a p i c a l c y t o p l a s m becomes v e r y  D e v e l o p m e n t a l changes i n the p r o s t a t e from those i n the seminal does not  v e s i c l e s i n t h a t the  form l a r g e lumina ( P l a t e VI B ) .  lumina are  considerably  smaller  a r e much more n u m e r o u s , and  The  are separated  layers.  Within  by  the tubules  t h i n l a y e r s of connective  differ prostate  tubule  i n the p r o s t a t e  the tubules tubules  The  are  but  lobulated.  t h i c k connective and  thick.  tissue  between the l o b u l e s  tissue.  Small  open l u m i n a  o c c a s i o n a l l y seen b u t most l o b u l e s r e m a i n c l o s e d the developmental period. the p r o s t a t e  The  f i r s t forms a p s e u d o s t r a t i f i e d l a y e r  a d e f i n i t e a p i c a l cyroplasmic  occludes  the  It  the b a s i s of gross  cells  r e a d i l y recognized.  spermatozoa.  develop i n the  possess enlarged  tubules  The  seminal  t e s t e s show possess  D i s t i n c t clumps of  i n t e r t u b u l a r spaces.  tubules  b u t no  sperm.  of  developmental  t h a t may  d e v e l o p s an a c t i v e s e c r e t o r y c e l l l u m i n a and  alone  to determine the developmental stage  separating seminiferous l u m i n a and  and  which  organ morphology  M i c r o s c o p i c a l l y , however, the  p h a s e c a n be  in  lumina.  is difficult  the male.  area  are  during  secretory epithelium  acquires  On  are  The  enlarged, open  Leydig The  epididymides  prostate  l a y e r b u t w i t h few  v e s i c l e s p o s s e s s open l u m i n a w h i c h  open are  -17not  greatly distended,  w i t h o n l y a few s e c r e t i o n d r o p l e t s .  T h e r e d o e s seem t o b e a f a i r l y of the t e s t e s , prostate occasion  synchronous development  and s e m i n a l v e s i c l e s b u t on  a l l t h r e e have t o be s t u d i e d  reproductive  t o determine the  state of the animal.  Functional Males with f u n c t i o n a l reproductive may b e t a k e n f r o m J a n u a r y u n t i l A u g u s t .  organs  The s c r o t u m  i s l a r g e , and t h e s k i n i s d a r k and s p a r s e l y The  penis  i s g e n e r a l l y a r o u n d 50 mm  furred.  i n length.  The s i z e  of t h e f u n c t i o n a l male organs v a r i e s c o n s i d e r a b l y some o v e r l a p  occurs between t h e s i z e o f  f u n c t i o n a l and d e g e n e r a t i n g organs. the  gross, s i z e i s n o t an a b s o l u t e  function.  For this  i n d i c a t i o n o f organ  flaccid  and t h i c k prominent b l o o d  s e e n i n t h e smooth, l i g h t  coloured  as t h e s e a s o n  vessels  tunica  that remain dlscernable functional period. large distended  c a n be  albugineae.  l a r g e e p i d i d y m i d e s e x h i b i t a few l a r g e  33 mm.  reason  The t e s t e s a r e u s u a l l y f i r m i n  t e x t u r e , b u t may become s l i g h t l y  The  developing,  T e s t i s l e n g t h v a r i e s f r o m 16 t o 23 mm i n  f u n c t i o n a l animals.  progresses,  and  tubules  t o t h e naked eye throughout t h e  The s e m i n a l v e s i c l e s a r e g e n e r a l l y  glands that vary  i n l e n g t h f r o m 13 t o  The p r o s t a t e , a l w a y s r e t a i n i n g a s o l i d  r e a c h e s a maximum s i z e o f a b o u t 16 b y 11  mm.  texture,  -18M i c r o s c o p i c a l l y , t h e testes possess s e m i n i f e r o u s t u b u l e s a b o u t 200^ i n d i a m e t e r . lumina, which  contain loosely associated  and a l l s t a g e s o f s p e r m a t o g e n e s i s , in and  Their  spermatozoa  appear t o i n c r e a s e  s i z e as t h e f u n c t i o n a l s t a t e p r o g r e s s e s I I I D).  large  (Plate I I I C  L e y d i g c e l l s , w i t h a maximum d i a m e t e r o f  a b o u t 15A o c c u p y a c e n t r a l p o s i t i o n i n t h e l a r g e i n t e r t u b u l a r spaces.  Although the Leydig c e l l s  in diameter through a l o s s  i n cell  cytoplasm  t h e end o f t h e f u n c t i o n a l p e r i o d , s e c r e t i o n remain  evident.  decrease  towards vacuoles  F u n c t i o n a l L e y d i g c e l l s may b e a s s m a l l  a s 11^ i n d i a m e t e r . The  f u n c t i o n a l e p i d i d y m i d e s d o n o t show t h e  same d e g r e e o f v a r i a t i o n a s d o t h e t e s t e s .  A  a p i c a l cytoplasm i s r e t a i n e d by the e p i t h e l i a l  thick cells  of  t h e t u b u l e s and t h e whole e p i t h e l i u m I s m a i n t a i n e d  at  a h e i g h t o f 20 t o 25/< o  of  c y t o p l a s m i c f i l a m e n t s and remain  throughout  The t u b u l e l u m i n a a r e f r e e f i l l e d w i t h sperm  the functional period (Plate IV C).  Changes  i n the i n t e r t u b u l a r connective t i s s u e of the epididymides are not evident during the functional The  phase.  structure of the seminal v e s i c l e s i s  quite v a r i a b l e a t t h i s time.  Various stages of epithelium  development c a n be seen a t a l l times d u r i n g t h e b r e e d i n g s e a s o n a n d I t i s l i k e l y t h a t t h e t u b u l e s go cycles of a c t i v i t y which,  through  i n c r o s s s e c t i o n i s seen as  -19s e v e r a l stages  w i t h i n one g l a n d .  o f one e p i t h e l i u m gland.  However a p r e d o m i n a n c e  t y p e c a n u s u a l l y be s e e n i n a n y one  The e a r l y f u n c t i o n a l e p i t h e l i u m shows a f o l d e d  l a y e r o f a c t i v e columnar c e l l s which possess darkly stained, basal nuclei (Plate V Gi). cytoplasm I n these c e l l s d r o p l e t s a r e common.  time, few  L a t e r stages  possess oval  epithelium  At this  i s uncommon a n d r e l a t i v e l y  s e c r e t i o n droplets are present.  eventually shrinks, there  basal  e v e n t u a l l y becomes a s i n g l e ,  l a y e r ( P l a t e V C i and V C i i ) .  f o l d i n g of.the  epithelium  The a p i c a l  i s w e l l developed and s e c r e t i o n  n u c l e i , and t h e e p i t h e l i u m culoidal cell  elongate,  As t h e t u b u l e  i s a thickening of the  through p s e u d o s t r a t i f i c a t i o n .  The a p i c a l  c y t o p l a s m i s t h i n b u t some s e c r e t i o n d r o p l e t s a r e s t i l l present  (Plate V D). The p r o s t a t e , a l t h o u g h  constituency, the breeding epithelial  retaining i t s solid  a l s o shows e p i t h e l i a l c h a n g e s season.  cell  throughout  The l o b u l e s p o s s e s s a s i n g l e  l a y e r a b o u t 20/, i n h e i g h t  and s e c r e t i o n  d r o p l e t s a r e common n e a r a n d o n t h e s u r f a c e o f t h e l a y e r . During t h e e a r l y stages  the c e l l s possess a t h i c k a p i c a l  c y t o p l a s m w h i c h g r a d u a l l y becomes r e d u c e d i n t h i c k n e s s . In conjunction with this reduction i n c e l l l u m i n a open ( P l a t e V I C i and V I C i i ) .  Late  height the i n the  f u n c t i o n a l p e r i o d t h e c e l l s appear c u b o i d a l , b e i n g as little  as 10^ i n h e i g h t .  even on t h e s e s m a l l c e l l s .  Secretion droplets are present The c o n n e c t i v e  tissue  separating  - 2 0 -  the t u b u l e s and l o b u l e s remains t h i n d u r i n g most o f t h e f u n c t i o n a l p e r i o d , b u t may a p p e a r somewhat t h i c k e n e d a s the gland regresses d u r i n g the l a t e r Despite v a r i a t i o n s i n organ  stages. size,  the functional  s t a t e i s c h a r a c t e r i z e d by s e v e r a l microscopic  criteria.  Spermatozoa a r e present i n both t h e seminiferous tubules and  i n the epididymides.  Seminal  v e s i c l e s possess  open l u m i n a and s e c r e t i n g e p i t h e l i a l a l s o possesses  cells.  large  The p r o s t a t e  an a c t i v e s e c r e t o r y e p i t h e l i u m and open  lumina. Degenerate Once t h e m a l e r e p r o d u c t i v e o r g a n s a r e no l o n g e r f u n c t i o n a l , complete scrotum  becomes f u l l y  degeneration occurs r a p i d l y . furred although the hairs are  g e n e r a l l y t i p p e d w i t h brown and t h e d a r k of t h e integument i s l o s t . o f kO t o 5 0 mm.  The  pigmentation  The p e n i s r e t a i n s a l e n g t h  The t e s t e s s h r i n k , t h e t u n i c a t a k e o n  a b l u e t i n g e a n d t h e s u r f a c e o f t h e t u n i c a becomes wrinkled.  The e p i d i d y m i d e s  tend t o remain  large i n  r e l a t i o n to the testes, but eventually shrink.  The  e p i d i d y m a l t u b u l e s become e x t e r n a l l y i n c o n s p i c u o u s a n d cannot  be seen by t h e naked eye. Consequent t o t h e s e changes i n t h e t e s t e s ,  the accessory organs a l s o degenerate.  Seminal  vesicles  l o s e t h e i r t h i c k t u b u l a t e d a p p e a r a n c e a n d become i n f a n t i l e - l i k e p r o j e c t i o n s a b o u t k mm p r o s t a t e becomes l e s s t h a n 7 b y k mm  long while the i n l e n g t h and w i d t h  -21dark  i n c o l o r , and "rather i n c o n s p i c u o u s . H i s t o l o g i c a l l y , t h e t e s t e s show c l o s e l y  packed  t u b u l e s a b o u t 100^ i n d i a m e t e r w h i c h assume i r r e g u l a r shapes.  B a s e m e n t membranes become t h i c k a n d w r i n k l e d .  Germ c e l l l a y e r s a r e t h i n a n d a l l l u m i n a e v e n t u a l l y become c l o g g e d w i t h d e g e n e r a t e (Plate I I I E). and S e r t o l i  sperm and c e l l u l a r d e b r i s  Only spermatogonia,  c e l l s remain  primary  i n t h e tubules„  l o s e t h e i r v a c u o l a t e d appearance,  spermatocytes  The L e y d i g  cells  t h e i r c y t o p l a s m becomes  s c a r c e , a n d t h e i r n u c l e i become d a r k , g i v i n g t h e I m p r e s s i o n that they are f u n c t i o n a l l y The  degenerate.  e p i d i d y m i d e s g r a d u a l l y assume t h e i n f a n t i l e  form through a t h i c k e n i n g o f the c o n n e c t i v e  tissue,  s h r i n k i n g o f t h e t u b u l e s and c l e a r i n g o f t h e l u m i n a . The  first  sign of nonfunction i n the epididymides  i n v o l v e s a d e g e n e r a t i o n o f t h e sperm and t h e p r e s e n c e o f some c e l l u l a r d e b r i s a n d l e u c o c y t e s ( P l a t e I V D ) . F u r t h e r c h a n g e s show a r e d u c t i o n i n e p i t h e l i u m h e i g h t a n d a b r e a k d o w n o f some o f t h e c e l l s . Degeneration  i n the seminal vesicles  consists  o f s u b t l e changes t h a t e s s e n t i a l l y i n v o l v e a l o s s o f s e c r e t i o n d r o p l e t s and a p i c a l c y t o p l a s m cells,  i n the secretory  t h e b r e a k d o w n o f some e p i t h e l i a l c e l l s a n d a n  accumulation of debris within the shrinking Eventually the seminal vesicles  lumina.  t a k e on t h e i n f a n t i l e  form, showing s m a l l t u b u l e s supported by t h i c k , nucleated connective tissue.  They d i f f e r  heavily  from t h e  i n f a n t i l e a n i m a l m a i n l y I n t h e m a i n t e n a n c e o f more  -22-  a c l d o p h i l i c connective  tissue.  Prostate degeneration o f e p i t h e l i a l c e l l s and  o c c l u s i o n of the lumina  d a r k s t a i n i n g n u c l e i and with this the  cytoplasmic  i s a decrease i n tubule  formation  s i z e and  The  number,  d i s t i n g u i s h e d from the  can  only  m a l e c a n be  a larger  epididymides  i n the complete absence o f sperm.  a d d i t i o n , the seminiferous  tubules  take  on  s h a p e s , w r i n k l e d b a s e m e n t membranes, and  associated  be  characterized  t h e p r e s e n c e o f d e g e n e r a t e sperm i n t h e  open lumina.  degenerate  intertubular tissue.  Thus t h e d e g e n e r a t i n g  resulting finally  Leydig  eventually  Seminal v e s i c l e s l a c k s e c r e t i n g  c e l l s and  t h e p r o s t a t e shows a s l o u g h i n g  loosely  epithelial of the  a l o n g w i t h a l o s s i n number o f l o b u l e s and  epithelium  tubules.  results in infantile-like  organs  t h a t are d i s t i n g u i s h e d from the i n f a n t i l e animals t h e b a s i s o f a s l i g h t l y l a r g e r s i z e and that are not  a few  tubules  and  on  histological  always r e l i a b l e .  d e g e n e r a t e a d u l t t e s t e s show more i r r e g u l a r seminiferous  lose  seminiferous  tubules.  characteristics  In  irregular  c e l l s become s m a l l , f o r m i n g  clumps packed between the  Complete degeneration  the  nucleated  i n f a n t i l e p r o s t a t e by  p o r t i o n of c o l l a g e n i n the  and  Many o f  completely  i n f a n t i l e f o r m and  with  Coincidental  are r e p l a c e d by h e a v i l y  t i s s u e (Place VI D).  p r o s t a t e assumes t h e  by  debris.  o f a h e a v y b a s e m e n t membrane.  l o b u l e s a r e l o s t and connective  begins w i t h a breakdown  The  shaped  more w r i n k l e d b a s e m e n t membranes  -23than the i n f a n t i l e .  The s e m i n a l v e s i c l e s  connective tissue that i s quite thick l e s s so i n the I n f a n t i l e . prominent  possess  i n t h e a d u l t and  Acidiphilic  collagen i s  i n most a d u l t s e m i n a l v e s i c l e s and v e r y s c a r c e  i n the i n f a n t i l e organs.  Similarly,  the adult prostate  shows a much h e a v i e r d e s p o s i t i o n o f c o l l a g e n t h a n t h e infantile. The  Female R e p r o d u c t i v e The  Cycle  female r e p r o d u c t i v e organs undergo  s e a s o n a l changes t h a t a r e a l m o s t as extreme as t h o s e found  i n t h e male.  L a y n e (195^) d e s c r i b e d t h e g r o s s  s e a s o n a l changes I n t h e male and female r e p r o d u c t i v e o r g a n s o f T.h. l o q u a x  i n New Y o r k a n d t h e h i s t o l o g y  o f t h e o v a r i e s h a s b e e n d e s c r i b e d b y Mossman  (1966).  I n t h e p r e s e n t s t u d y , t h e gross and m i c r o s c o p i c changes i n t h e o v a r i e s , u t e r i and v a g i n a e were r e c o r d e d throughout  t h e y e a r so t h a t t h e e x a c t c o n d i t i o n o f any  a n i m a l c o u l d be d e t e r m i n e d . female  c y c l e was d i v i d e d  infantile, and  into s i x functional  lactating.  These phases were d e f i n e d s o t h a t t h e on t h e b a s i s o f g r o s s  i f necessary, confirmed m i c r o s c o p i c a l l y .  determined  phases;  anoestrous, proestrous, e s t r o u s , pregnant,  a n i m a l s c o u l d be c l a s s i f i e d and,  For convenience, the  form  Independently  a g e d a t a a i d e d i n some o f t h e c l a s s i f i c a t i o n . The  I n f a n t i l e females  Include only those that  a r e t h e young o f t h e y e a r and have n e v e r been i n breeding condition. those females  The a n o e s t r o u s  t h a t have produced  stage a p p l i e s t o  young  previously,  -24o r a r e o l d enough t o p r o d u c e y o u n g , b u t w h i c h a r e neither breeding the previous  nor preparing  year  t o breed.  are considered  Young o f  anoestrous i f they  do  n o t b r e e d , o r show s i g n s o f d e v e l o p m e n t a t t h e t i m e when o t h e r s  o f t h e i r a g e g r o u p d o s o , a n d when  reproductive adults. and  their  organs a r e i n s i m i l a r c o n d i t i o n t o anoestrous  A l l other stages  (proestrous, estrous,  pregnant  l a c t a t i n g ) i n c l u d e a l l s e x u a l l y a c t i v e age groups  f o r the purpose o f h i s t o l o g i c a l d e s c r i p t i o n . Infantile  Female The  classified  i n f a n t i l e female c a n f r e q u e n t l y be  on t h e b a s i s o f e x t e r n a l  characteristics,  u s u a l l y by t h e s i z e and shape o f t h e n i p p l e s appear o n l y as p i n p o i n t s o f l i g h t brown on  the skin.  which  pigmentation  The v u l v a i s s m a l l a n d i m p e r f o r a t e a n d  does n o t p r o t r u d e  t o any g r e a t  extent.  external features are not d i s t i n c t , of the reproductive  tract  of the i n f a n t i l e stage.  When  the morphology  i s frequently Indicative The I n f a n t i l e o v a r i e s a n d  u t e r i a r e n o t c o n s p i c u o u s and a r e o f t e n found within the pelvis. mm  these  The u t e r u s  lodged  i s r a r e l y more t h a n 20  l o n g b y 1 mm w i d e a n d i s g e n e r a l l y a r o u n d 1 ? mm  long,  w h i l e the o v a r i e s , which remain hidden w i t h i n the bursa, as  a r e a b o u t 3 nun b y 2 mm  i n s i z e and a r e seen  s m o o t h o v a l s o f opaque t i s s u e .  1 mm  i n width  The v a g i n a ,  about  i s s i t u a t e d almost e n t i r e l y w i t h i n the  p e l v i s and i s s i m i l a r t o t h e u t e r u s  i n appearance.  -25Microscoplcally, a simple layers lies  the i n f a n t i l e vagina i s  t u b e - l i k e s t r u c t u r e made u p o f s e v e r a l  (Plate V I I A ) .  Beneath the t h i c k outer a d v e n t i t i a  a t h i n c i r c u l a r l y o r i e n t e d submucosa t h a t i s  i n t e r s p e r s e d w i t h a few c o l l a g e n f i b r e s . Is  concentric  The s u b m u c o s a  n o t s h a r p l y demarcated from t h e c o l l a g e n l c  lamina  p r o p r i a and no d i s t i n c t g e r m l n a t i v u m c a n be s e e n between it  and t h e e p i t h e l i u m l i n i n g  lining  cells  showing l i t t l e  a rather convoluted The  uterus  up  c y t o p l a s m and l y i n g  lumen.  during  t h e i n f a n t i l e s t a g e shows  several t i s s u e layers i n cross The  The  epithelium consists of a pseudostratified layer  of c u b o i d a l along  t h e v a g i n a l lumen.  o u t e r myometrium, r o u g h l y  section (Plate V I I I A ) . 75# i  n  t h i c k n e s s , i s made  o f muscle c e l l s which possess l i t t l e  dark s t a i n i n g , elongate  nuclei.  c y t o p l a s m and  Two d i s t i n c t  layers  w i t h i n t h e myometrium a r e d i s c e r n a b l e ; a n o u t e r l o n g i t u d i n a l l a y e r and a n i n n e r c i r c u l a r l a y e r .  The e n d o m e t r i u m ,  s i t u a t e d d i r e c t l y b e n e a t h t h e myometrium, i s o f s i m i l a r thickness  a n d c o n s i s t s o f a n u n o r g a n i z e d mass o f h e a v i l y  nucleated  tissue.  A few e n d o m e t r i a l  n e a r t h e i n n e r s u r f a c e and l i k e  g l a n d s c a n be s e e n  the inner surface, are  lined with a d i s t i n c t  single layer of cuboidal  a b o u t 10^ i n h e i g h t .  The e p i t h e l i u m c o n t a i n s  epithelium little  c y t o p l a s m and t h e d a r k s t a i n i n g n u c l e i a r e i r r e g u l a r in  shape.  -26Th e o v a r y o f t h e i n f a n t i l e f e m a l e simple.  I t i s o f t h e t y p i c a l r o d e n t t y p e as d e s c r i b e d  b y Mossman (I966) and  shows a t h i c k c o r t e x h e a v i l y  p o p u l a t e d w i t h naked ova f o r t h e f i r s t months o f l i f e follicles  ( P l a t e IX A i ) .  are f a i r l y  about  three to four  Degenerating  secondary  common i n t h e m e d u l l a r y r e g i o n o f  older i n f a n t i l e animals at  i s quite  ( P l a t e IX A i i ) ,  e i g h t months t h e i n f a n t i l e  and  eventually,  ovary appears  very  s i m i l a r to the anoestrous a d u l t ovary, except f o r a h e a v i e r c o r t i c a l p o p u l a t i o n of naked ova The  (Plate IX A l i i ) .  P r o e s t r o u s Female The  w i t h the f i r s t  p r o e s t r o u s p e r i o d was  considered to begin  s i g n s of c o i l i n g of the vagina  that  accompanied an i n c r e a s e i n s i z e of a l l p a r t s of the reproductive tracts. of  During this period  t h e p r e v i o u s l y i n f a n t i l e and  the  anoestrous  become e n l a r g e d s o t h a t i t i s d i f f i c u l t  nipples  animals  to d i s t i n g u i s h  j u v e n i l e a n d a d u l t a n i m a l s w i t h any d e g r e e  of  certainty.  Development f o l l o w s a v e r y s i m i l a r p a t t e r n whether or n o t t h e a n i m a l s have b r e d b e f o r e .  For t h i s  a l l d e v e l o p i n g females were c l a s s i f i e d  reason  i n one  group.  A t t h e t i m e j u s t p r e c e d i n g e s t r u s , t h e n i p p l e s become conspicuously thicker. Internally, appearance  The  v u l v a remains  t h e o v a r i e s t a k e on a r a t h e r g r a n u l a r but remain hidden w i t h i n the bursa.  u t e r i become t u r g i d and m e a s u r e o v e r 30 mm about degree  3 mi  small.  i n diameter.  The  l o n g and  v a g i n a shows t h e g r e a t e s t  o f change, becoming an e x t r e m e l y e l o n g a t e  highly colled  o r g a n o f up  The  t o 7 mm  and  i n diameter during  proestrus. Microscopically,  the whole v a g i n a  i n s i z e through h y p e r p l a s i a of the s i z e ( P l a t e V I I B).  cell  .shapes and  The  stain lightly.  increases  t i s s u e and  increased  n u c l e i assume r e g u l a r  The  submucosa d e v e l o p s  i n t o b u n d l e s of randomly o r i e n t e d smooth muscle a little The  c o l l a g e n i s present  greatest  between the muscle bundles.  change i n the v a g i n a  i s seen i n the  p r o p r i a w h e r e t h e w h o l e l a y e r becomes e x t r e m e l y O n l y a few  widely  collagen.  As  spaced n u c l e i are present  the lamina  and  p r o p r i a Increases  in  lamina collagen!  the  i n thickness,  t h e g e r m i n a t i v u m becomes a c o n s p i c u o u s l a y e r w h i c h i s heavily nucleated  only  In the b a s a l regions.  indications  of sloughing  be  i s m i n o r when c o m p a r e d w i t h t h a t s e e n i n  seen but  estrus.  As  shows a v e r y cross  w e l l as b e i n g irregular  of the s u r f a c e  Slight  highly coiled  inner surface.  s e c t i o n a l view of the  t i s s u e t o be  Increase  the As  changes i n the u t e r u s  become c o n s p i c u o u s . 400/, i n t h i c k n e s s  and  The  t h e two  Increased  of  are not  There i s a  as general  become  muscle l a y e r s  endometrium i n c r e a s e s  to  about  becomes I n v a d e d i t f i t h many g l a n d s  w h i c h f r e q u e n t l y show o p e n l u m i n a o n l y d u r i n g proestrus.  a  are.  i n myometrium t h i c k n e s s , the c e l l s w i t h c y t o p l a s m and  vagina  t r a c t shows l a y e r s  those seen i n the vagina.  distended  can  a result,  much t h i c k e r t h a n t h e y r e a l l y  Proestrus m a r k e d as  layers  cytoplasm i s evident  late  in a l l cells.  -28-  Although  i tmaintains i t s pseudostratified  the s e c r e t o r y e p i t h e l i u m l i n i n g uterus acquires cytoplasm.  appearance,  t h e lumen o f t h e  Epithelial cell  nuclei  s t a i n l i g h t l y a n d assume r e g u l a r s h a p e s , u s u a l l y  slightly  elongate. The  o v a r i e s d u r i n g p r o e s t r u s show f e w n a k e d  ova  i n the c o r t i c a l  r e g i o n even i n t h o s e females  are  young o f t h e y e a r .  that  The m e d u l l a r y r e g i o n h o w e v e r ,  has many s e c o n d a r y a n d t e r t i a r y f o l l i c l e s ,  although  many o f t h e s e a r e i n v a r i o u s s t a g e s o f d e g e n e r a t i o n . The 3 0 0 ^  active  follicles  remain s m a l l and few l e s s  o v e r 300^ I n d i a m e t e r m e a s u r e d i n f o u r  p r o e s t r o u s a n i m a l s was 6 0 0 * The  The l a r g e s t o f 2 9 d e v e l o p i n g  i n d i a m e t e r show a n t r a .  follicles  largest of  atretic  2 3  , a n d t h e mean s i z e was  follicles  over  3 0 0 * ,  found  w i t h a mean o f 3 8 3 ^ - .  i n t h e same f o u r a n i m a l s was The  than  E s t r o u s Female E x t e r n a l l y t h e e s t r o u s female has n i p p l e s  t h a t a r e e l o n g a t e and pigmented and  but not noticably swollen  t h e v u l v a i s a t h i c k p i n k p r o j e c t i o n about  5 mm  in height. I n t e r n a l l y , t h e v a g i n a remains and b o t h t h e v a g i n a a n d u t e r i a r e t u r g i d . become i r r e g u l a r  coiled  Both ovaries  I n shape through t h e development o f  Graafian f o l l i c l e s lutea.  highly  and, a f t e r o v u l a t i o n , of corpora  Ripe f o l l i c l e s  appear  as v i s c o u s b u b b l e s  on t h e  o v a r i a n s u r f a c e , w h i l e new c o r p o r a l u t e a a p p e a r a s  .  -29-  distlnct  o p s q u e b u l g e s a b o u t 1 mm  i n diameter.  Blood-  c l o t s s o m e t i m e s show as b r o w n s p o t s i n r e c e n t l y  formed  corpora. The distinct,  microscopic features of'estrus are  especially  i n the vagina  v a g i n a l submucosa remains f u l l y  fairly  (Plate V I I C ) .  formed but  the  The  highly  c o l l a g e n i c l a m i n a p r o p r i a shows a l o o s e n i n g o f  the  collagen fibres  s i g n of  t h a t may  collagen degeneration.  be As  t a k e n as t h e f i r s t this degeneration  proceeds  t h e c o l l a g e n t i s s u e n u c l e i become v e r y g r a n u l a r . germlnatlvum,  which  i s very thick during l a t e proestrus,  p r o d u c e s t h e s l o u g h i n g corneum t h a t a l m o s t occludes  the v a g i n a l lumen.  the germlnatlvum  and  The  completely  U n l i k e the lamina  corneum a r e b a s o p h i l i c .  propria, The  I m m e d i a t e p o s t o v u l a t o r y v a g i n a becomes p e r m e a t e d w i t h leucocytes. D e f i n i t e u t e r i n e changes a r e a l s o e v i d e n t during estrus.  P r i o r t o o v u l a t i o n t h e myometrium  shows a n a b s e n c e o f c o n s p i c u o u s middle  c i r c u l a r nmscle l a y e r develops  collagen. The  Endometrial glands  possess  secretory epithelium consists  tall and  b l o o d v e s s e l s and  columnar c e l l s  t h a t possess  of  open l u m i n a .  of a s i n g l e l a y e r elongate basal  a t h i c k a c t i v e a p i c a l cytoplasm.  a r e common on t h e e p i t h e l i a l s u r f a c e . cells  strands  the  of  nuclei  Secretion droplets Those s e c r e t o r y  fo\ind w i t h i n t h e e n d o m e t r i a l g l a n d s a r e more  c u b o i d a l than columnar, but  they too are a c t i v e .  The  -304  internal surface of the uterus i s rough and highly convoluted at this time (Plate VIII B ) . There i s considerable variation i n the ovaries. Some animals show many developing f o l l i c l e s and others shox-7 very few. One juvenile female taken i n May 1966 was i n f u l l estrus by a l l other c r i t e r i a but showed no developing f o l l i c l e s i n the ovaries.  Normally the  f o l l i c l e s that develop large antra assume c o r t i c a l positions while smaller ones continue to develop and degenerate i n the medulla.  Atretic f o l l i c l e s i n four  estrous females varied from zero to eleven i n number, averaged  39^-  i n diameter and had a maximum size of  64o# .  Developing f o l l i c l e s over 300/, i n diameter i n the same four estrous females varied from zero to f i v e i n number, averaged 55^  i n  diameter and had a maximum size  of 880/,. . As noted by Mossman  (I966)  the ripe f o l l i c l e s  possesses a d i s t i n c t thecal glandular layer between the granulosa and I n t e r s t i t i a l c e l l s . the corpora lutea develop rapidly.  Following ovulation, The average diameter  of 21 corpora lutea found i n four females during the preimplantatlon stage was 1036^ . Early corpora lutea possess large central blood clots which are usually gone by the time the embryos are discernable.  A few  females had corpora lutea without blood clots and did not have v i s i b l e embryos.  The corpora lutea showed no  signs of degeneration and i t i s unknown whether or not they would have produced young (Plate IX B ) .  One case  was found where small blood clots were present i n  -31c o n j u n c t i o n w i t h 7 mm  embryos.  The l u t e a l c e l l s  during  t h e p o s t o v u l a t i o n p e r i o d show l a r g e n u c l e i w i t h many nucleoli.  Their cytoplasm  the c e l l s a r e f a i r l y are  appears s l i g h t l y  granular,  r e g u l a r i n s h a p e , and c e l l  boundaries  indistinct.  The P r e g n a n t F e m a l e During  pregnancy t h e n i p p l e s remain conspicuous  but  not p a r t i c u l a r l y distended,  while the vulva  its  conspicuous s w o l l e n appearance.  During  later  p r e g n a n c y , when t h e abdomen becomes n o t i c e a b l y the vagina  loses  swollen,  l o s e s i t s h i g h l y c o i l e d a p p e a r a n c e and  becomes a s h o r t f l a c c i d  t u b e a b o u t 7 mm w i d e .  The  o v a r i e s d u r i n g p r e g n a n c y may be a s l a r g e as 6 b y 4 mm due  t o the presence of corpora  lutea.  r e m a i n c o n s p i c u o u s b u t become d a r k e r progresses.  Corpora l u t e a as p r e g n a n c y  I n l a t e p r e g n a n c y t h e mammary g l a n d s  b e s e e n a s two t h i n w h i t e  sheets  running  can  the f u l l  length  o f t h e abdomen. The m i c r o s c o p i c  p i c t u r e of the vagina  during  p r e g n a n c y shows a g e n e r a l d e c r e a s e i n t i s s u e l a y e r s . The m u s c u l a r s u b m u c o s a r e m a i n s i n t a c t b u t r a t h e r  thin  beneath the a d v e n t i t i a . Greater tissues.  c h a n g e s a r e shown b y t h e  The l a m i n a  p r o p r i a has a f a i r l y  of c o l l s g e n , u n t i l  only a very  associated strands  remains post  and  corneum, o n l y  remaining  rapid  degeneration  t h i n layer of l o o s e l y p a r turn.  Of t h e g e r m i n a t i v u . m  t h e b a s a l g e r m l n a t l v u m r e m a i n s and  -32t h e r e seems t o be no s l o u g h i n g o f c e l l s . remain  Leucocytes  I n t h e v a g i n a l l u m e n f o r some t i m e and  lumen i t s e l f  e n l a r g e s and  eventually develops  w a l l s by the time of p a r t u r i t i o n  changes s i m i l a r  t o those found  smooth  ( P l a t e V I I D).  S e c t i o n s of the u t e r i , beyond or between the embryonic  the  t a k e n where  possible  s w e l l i n g s , show some i n the vagina.  o u t e r l o n g i t u d i n a l l a y e r o f t h e myometrium  The  remains  i n t a c t b u t t h e more c o l l a g e n i c m i d d l e l a y e r a p p e a r s d e g e n e r a t e , d e v e l o p b l o o d v e s s e l s and become loose.  The  endometrium remains  The  relatively  ovary d u r i n g pregnancy  fairly  unchanged.  shows a c o n s t a n t  g e n e r a t i o n and d e g e n e r a t i o n o f f o l l i c l e s ,  although  much o f i t s v o l u m e i s t a k e n up b y c o r p o r a l u t e a . a c t i v e and d e g e n e r a t i n g t e r t i a r y at  a l l times.  t h a n 10 mm  follicles  I n f i v e f e m a l e s c a r r y i n g embryos  follicles  414^  was  .. A t r e t i c  f i v e females averaged  30 mm  .  had  diameter.  38.5^  Four females  follicles  58  i n t h e same  i n d i a m e t e r and  t h e maximum  c a r r y i n g embryos g r e a t e r t h a n  66 d e v e l o p i n g f o l l i c l e s The maximum s i z e was averaged  a v e r a g i n g 501/,  720/,  680/< .  Corpora l u t e a r e t a i n an average d i a m e t e r throughout  pregnancy  seem t o be a s l i g h t d e c r e a s e .  in  Thirty-one  follicles  kZ6ju  , and  .  atretic  a b o u t 900/,  less  i n l e n g t h , the l a r g e s t d e v e l o p i n g f o l l i c l e , w h i l e the average diameter of  600/,  Several  are present  m e a s u r e d 600/,  was  to  the l a r g e s t  being of  a l t h o u g h t h e r e does The  average diameter i n  -33= animals  c a r r y i n g embryos l e s s  9^8^  The a v e r a g e  .  t h a n 10 mm l o n g was  f o r animals  i n t h e embryos  larger  t h a n 30 mra was 888# . The  s t r u c t u r e o f t h e l u t e a l t i s s u e does n o t  change, except pregnancy  f o r the loss of the blood c l o t early i n  ( P l a t e X A l and X A i l ) .  From t h e n  until  p a r t u r i t i o n a t a b o u t t h e 40 mm embryo s t a g e , t h e r e a r e no  g r e a t l u t e a l changes.  are d i s t i n c t l y The  cells  cytoplasm  g r a n u l a r and round  cells  o r o v a l I n shape.  show i n d i s t i n c t b o u n d a r i e s , a l t h o u g h t h e tends  t o p a c k around, t h e n u c l e i , g i v i n g a  relatively distinct Lactating  Nuclei within the luteal  shape t o t h e c e l l .  Females F o l l o w i n g p a r t u r i t i o n t h e r e a r e two p o s s i b l e  p a t t e r n s t h a t may b e f o l l o w e d . of  a l l organs  The f i r s t  i s a degeneration  and r e g r e s s i o n t o t h e anoestrous  stage.  T h i s o c c u r r e d d u r i n g 19&7, b o t h o n V a n c o u v e r I s l a n d a n d in  the Interior.  The s e c o n d  p a t t e r n shows p o s t  partum  e s t r u s o c c u r r i n g s h o r t l y a f t e r p a r t u i t l o n , a s was f o u n d on V a n c o u v e r I s l a n d " d u r i n g 1966. When n o p o s t p a r t u m e s t r u s o c c u r s a f a i r l y s i m p l e p a t t e r n c a n be seen.  The n i p p l e s become v e r y  d i s t e n d e d and t h e f u r around  them i s w o r n away, a n d t h e  v u l v a remains themselves full  flaccid  f o r some t i m e .  The mammary  glands  c a n be s e e n a s two w h i t e pads r u n n i n g t h e  l e n g t h o f t h e abdomen.  Towards t h e end o f l a c t a - t i o n  -34t h e y become f a i r l y  compact and d a r k  In color.  The  v a g i n a and u t e r i a r e s w o l l e n f o r a s h o r t p e r i o d o n l y and  p l a c e n t a l scars a r e conspicuous  lactation. this  f o r some t i m e  The o v a r i e s d o n o t s h r i n k a p p r e c i a b l y d u r i n g  time. Microscopically there i s a general  of  t h e v a g i n a and u t e r u s u n t i l  form.  degeneration  t h e y assume t h e a n o e s t r o u s  The o r g a n s d o n o t a p p e a r t o r e g r e s s f u l l y  the period of l a c t a t i o n . the degeneration The  l u t e a , which  after  The m o s t n o t i c e a b l e c h a n g e i s  of the collagen tissue.  o v a r i e s d u r i n g l a c t a t i o n c o n t i n u e t o show  some d e v e l o p i n g a n d r e g r e s s i n g f o l l i c l e s .  The c o r p o r a  show no a p p r e c i a b l e c h a n g e I n s i z e s i n c e  e a r l y p r e g n a n c y , d o show some s t r u c t u r a l The  after  differences.  i n d i v i d u a l l u t e a l c e l l s appear t o l o s e the f i n e  v a c u o l e s and t h e c y t o p l a s m  c o a l e s c e s around the n u c l e i ,  g i v i n g them a more d i s t i n c t f o r m . tend t o s e p a r a t e from  Some l u t e a l  each other.and  a little  d e g e n e r a t i o n becomes e v i d e n t d u r i n g l a t e (Plate X A l i i The distinguished  cells fatty  lactation  and X B ) . p o s t partura e s t r o u s f e m a l e from  t h e l a c t a t i n g female  cannot  be  on a n e x t e r n a l  basis.  A s w o l l e n v u l v a was n e v e r  female,  a l t h o u g h t h e s a m p l e was t o o s m a l l t o g i v e  conclusive  s e e n on a p o s t  evidence. There a r e a l s o few gross s i g n s o f p o s t  estrous.  partum  Seven post partum females  partum  t h a t had n o t y e t  o v u l a t e d d i d n o t show a n y s i g n o f i n c r e a s e d s i z e o r  -35coiling  of the vagina,  post partum females  L i k e w i s e , none o f t h e t e n  t h a t h a d o v u l a t e d showed a n y s i g n  of v a g i n a l Increase. M i c r o s c o p i c a l l y t h e r e i s no c l e a r p i c t u r e o f t h e p o s t p a r t u m e s t r o u s s i n c e t h e r e w e r e n o t enough animals  taken  t o make a n a c c u r a t e h i s t o l o g i c a l  determination.  Pour o f t h e seven post partum females not  t h a t had  o v u l a t e d showed l a r g e f o l l i c l e s b u t i t i s u n c e r t a i n  whether o r n o t they would have o v u l a t e d . vaginae  of these  four animals  were i d e n t i c a l  i n a normal l a c t a t i n g female. were s t u d i e d i n t h r e e females not possess  U t e r i and t o those  The u t e r i a n d v a g i n a e t h a t had o v u l a t e d b u t d i d  d i s c e r n a b l e embryos.  I n one, b o t h  the uterus  and  v a g i n a were s m a l l and h i s t o l o g i c a l l y  The  o v a r i e s , however, c o n t a i n e d c o r p o r a l u t e a w i t h l a r g e  blood c l o t s , ovulated. clots The 3 mm  i n d i c a t i n g t h a t t h e a n i m a l had r e c e n t l y  I n t h e o t h e r two f e m a l e s  i n the corpora lutea,  vaginae  degenerate.  t h e r e w e r e no b l o o d  s o t h e y had n o t j u s t  were d e g e n e r a t e h i s t o l o g i c a l l y and o n l y about  i n diameter.  The u t e r i ,  Identical histologically Although  however, were t u r g i d and  t o normal estrous  the evidence  animals.  i s scanty, i t appears  t h a t when p o s t p a r t u m e s t r u s o c c u r s  soon a f t e r  parturition  the v a g i n a does n o t have t h e c a p a c i t y t o d e v e l o p initial  ovulated.  estrous condition.  while the vaginae  to the  That i s , o v u l a t i o n occurs  and u t e r i a r e s t i l l  r e c u p e r a t i n g from  t h e e f f e c t s o f p r e g n a n c y and p a r t u r i t i o n . When p o s t p a r t u m e s t r u s o c c u r s  i ti s possible  t o d i f f e r e n t i a t e b e t w e e n t h e two s e t s o f c o r p o r a  lutea.  36 The in  o l d c o r p o r a l u t e a a r e s m a l l e r and more m e d u l l a r y p o s i t i o n t h a n t h e new  cell old  set.  Furthermore,  the  luteal  s t r u c t u r e o f e a c h s e t i s somewhat d i s t i n c t , s e t a p p e a r i n g as c o r p o r a l u t e a o f l a c t a t i o n  t h e new  s e t a p p e a r i n g as c o r p o r a l u t e a o f  Even a f t e r the b i r t h  o f the second  d e g e n e r a t i o n i s more a d v a n c e d Because of t h i s  litter  and  pregnancy. the stage of  i n the o l d e r corpora.  t h e number o f eggs o v u l a t e d a t  e s t r u s c a n be d e t e r m i n e d  the  each  even a f t e r the b r e e d i n g  season  by c o u n t i n g c o r p o r a a l b l e a n t i a . The  Anoestrous The  in  Female anoestrous  f e m a l e shows s e v e r a l f e a t u r e s  i t s g r o s s anatomy t h a t s e p a r a t e s i t f r o m  the  infantile.  A l t h o u g h t h e n i p p l e s c a n o n l y be s e e n u p o n c l o s e e x a m i n a t i o n , t h e y r e m a i n as d a r k t i p p e d about  1 mm  i n l e n g t h and  projections  s e r v e as a f e a t u r e t h a t  d i s t i n g u i s h e s a d u l t s from young throughout w i n t e r season. slightly  The  o v a r i e s , u t e r i and v a g i n a e  l a r g e r than those of the i n f a n t i l e  and a r e u s u a l l y s e e n as f a i r l y organs.  the  conspicuous  The u t e r i m e a s u r e a b o u t  30  by 2 mm  nonbreeding are  females, abdominal in length  and w i d t h , t h e v a g i n a I s g e n e r a l l y g r e a t e r t h a n 2 i n d i a m e t e r , and l e n g t h and w i d t h .  the o v a r i e s a r e about  4 b y 3 mm  During the e a r l y anoestrous  c o r p o r a a l b i c a n t i a may  b e s e e n as l i g h t  on t h e s m o o t h s u r f a c e o f t h e o v a r y .  mm in  period  coloured bulges  Towards l a t e  anoestus,  t h e c o r p o r a a l b i c a n t i a c a n n o t b e s e e n e x t e r n a l l y and  the  -37 ovaries are e s s e n t i a l l y  i n f a n t i l e In  Microscopically, s i m i l a r t o t h a t found only apparent of  appearance.  the anoestrous  vagina Is very  i n the I n f a n t i l e female.  The  d i f f e r e n c e i s i n t h e more d e f i n i t e  the muscular  s u b m u c o s a and  the presence  of  layering  conspicuous  s c l e r o t i c blood v e s s e l s i n the lamina p r o p r i a (Plate. V I I E ) . The  u t e r i a r e a l s o s i m i l a r t o those seen  the I n f a n t i l e stage, although the t i s s u e l a y e r s thicker.  The  r o u g h l y 150*  myometrium remains  remain  i n thickness  w h i l e t h e e n d o m e t r i u m i s m a i n t a i n e d a t a b o u t 130* Little  o r g a n i z a t i o n i s shown b y  s c l e r o t i c blood v e s s e l s remain d u r a t i o n of the anoestrous  t h e myometrium conspicuous  stage  E n d o m e t r i a l g l a n d s a r e s c a r c e and tends cell  The  c y t o p l a s m and  epithelial cells  their nuclei stain  Anoestrous m i c r o s c o p i c a l l y which i n f a n t i l e organs.  f o r the  (Plate VIII D i ) . the s u r f a c e e p i t h e l i u m  seen  single  contain l i t t l e darkly.  o v a r i e s show s e v e r a l  characteristics  s e r v e t o d i s t i n g u i s h them f r o m  the  Corpora a l b l c a n t l a are maintained f o r  many weeks a f t e r t h e end c a n be  .  and  t o r e m a i n p s e u d o s t r a t i f i e d r a t h e r t h a n as a layer.  In  o f l a c t a t i o n and  even I n the p r o e s t r o u s s t a g e  i n some c a s e s ( P l a t e IX C).  Many s i g n s o f d e g e n e r a t i o n , s u c h a s s m a l l s i z e , many fibroblasts,  l a r g e v a c u o l e s between c e l l s ,  s h a p e d n u c l e i and  poorly, d e f i n e d l u t e a l c e l l s  d i s t i n g u i s h these old corpora a l b i c a n t i a . regions possess follicles.  irregularly  relatively  serve  The  few n a k e d o v a and  to  cortical  primary  The m e d u l l a r y r e g i o n shows t h e r e m a i n s  of  -38many r e g r e s s e d f o l l i c l e s  and l i t t l e  s i g n o f antrum  f o r m a t i o n i s seen d u r i n g most o f the a n o e s t r o u s  period.  S m a l l a n t r a do become r e l a t i v e l y common t o w a r d s  the  of  the anoestrous  end  period.  Summer a n o e s t r o u s f e m a l e s , w h i c h h a v e u s u a l l y not bred p r e v i o u s l y , are q u i t e s i m i l a r t o the w i n t e r anoestrous adults  i n e x t e r n a l appearance.  remains  t h e n i p p l e s do become s l i g h t l y  s m a l l and  as s m a l l w h i t e p r o j e c t i o n s about  The  vulva enlarged  and  appear  The  g o n a d s r e m a i n s m a l l and a r e o c c a s i o n a l l y f o u n d  b e as s m a l l a s i n i n f a n t i l e of  females.  There  one mm  long.  i s no  to coiling  the vagina. M i c r o s c o p i c a l l y , h o w e v e r , t h e summer a n o e s t r o u s  f e m a l e s do a p p e a r d i f f e r e n t t h a n t h e w i n t e r a n o e s t r o u s animals.  They a r e h i s t o l o g i c a l l y s i m i l a r t o t h e  early  p r o e s t r o u s a n i m a l s b u t show no s i g n o f r e a c h i n g e s t r u s . F o r t h i s r e a s o n t h e y a r e c l a s s e d as a n o e s t r o u s w i t h t h e r e a l i z a t i o n t h a t some a c t i v i t y  although  occurs i n the  gonads. The B r e e d i n g  Season.  The b r e e d i n g s e a s o n o f e a c h y e a r was  determined  by m i c r o s c o p i c e x a m i n a t i o n o f a l l r e p r o d u c t i v e o r g a n s . As  emphasized  b y L a y n e (195^), t h e a c c e s s o r y o r g a n s  t h e male r e d s q u i r r e l a r e u s e f u l c r i t e r i a by w h i c h judge the s e x u a l c o n d i t i o n .  The  p o i n t a t which  of to  the male  becomes f u n c t i o n a l , o r l o s e s t h e c a p a c i t y t o b r e e d , i s difficult organs  t o a s s e s s and  the c o n d i t i o n of the accessory  can a i d i n t h i s d e t e r m i n a t i o n .  I n o r d e r t o be  sure  -39t h a t only males t h a t v/ere t r u l y f u n c t i o n a l were c l a s s i f i e d as such, males which showed only one f u n c t i o n a l a c c e s s o r y organ v/ere considered sperm was  n o n f u n c t i o n a l , even i f epidldymal  present. The  seasonal r e p r o d u c t i v e changes found i n  1966  on Vancouver I s l a n d a r e presented  3B.  The males came i n t o c o n d i t i o n i n March and remained  so u n t i l the b e g i n n i n g  i n F i g u r e 2A and  of September, although  steady d e c l i n e i n organ s i z e a f t e r May. seminal  there was a  The sharp drop i n  v e s i c l e l e n g t h i n June was not due t o a drop i n  function since microscopic fully functional.  examination showed them t o be  The drop probably  r e l e a s e o f the contents  r e s u l t e d from the  of the gland s i n c e the females v/ere  i n e s t r u s a t t h i s time.  N o second peak i n gland s i z e  v/hen the females came i n t o e s t r u s a g a i n i n August.  occurred  A slight  i n c r e a s e appeared i n the t e s t e s l e n g t h but t h i s w a s . l i k e l y ' due  t o the s m a l l sample s i z e f o r that month. The  females i n 1966 showed no s i g n o f coming  Into r e p r o d u c t i v e c o n d i t i o n u n t i l A p r i l and e s t r u s was not found u n t i l May, a t l e a s t a month a f t e r the males became f u n c t i o n a l .  The females a g a i n came i n t o estrus  a f t e r b i r t h of the f i r s t  litter.  There was a gap d u r i n g  l a t e June and J u l y between the c o l l e c t i n g of the l a s t pregnant female c a r r y i n g the f i r s t c o l l e c t i n g of the f i r s t the second l i t t e r .  and the  v i s i b l y pregnant female c a r r y i n g  Post partum e s t r u s d i d occur  l a c t a t i o n but probably parturition.  litter  n o t immediately f o l l o w i n g  during  F I G U R E 2 -~ S e a s o n a l c h a n g e s i n t h e mean l e n g t h s of male r e p r o d u c t i v e organs, A„  The I966 b r e e d i n g s e a s o n o n Vancouver I s l a n d ,  B,  The I967 b r e e d i n g s e a s o n o n . Vancouver I s l a n d and I n t h e i n t e r i o r o f B r i t i s h Columbia,  -40-  FIGURE 3  -  The d u r a t i o n o f v a r i o u s r e p r o d u c t i v e s t a g e s o f m a l e s and f e m a l e s , p l o t t e d a s the p e r i o d between the c o l l e c t i n g of the f i r s t and l a s t a n i m a l i n e a c h p a r t i c u l a r stage, A  c  B.  The 1967 b r e e d i n g s e a s o n on V a n c o u v e r I s l a n d and i n t h e i n t e r i o r of B r i t i s h Columbia. The I966 b r e e d i n g s e a s o n Vancouver I s l a n d .  on  -41-  MALE Developing Functional  FEMALE <  Proestrus  A.  Estrus Pregnant Lactatlng  D  J  J  _J  L  F  M  A  M  J  J  J  L _  A  S  !  O  MALE Developing Functional  FEMALE Proestrus Estrus Pregnant Post Partum Estrus & Pregnant  w/JM////////m  Lactating  D  J  F  M  l  A  I  M  I  J  L  J  A  J  S  I  O  L  The c y c l e found i n 196? i s shown i n F i g u r e 2B and 3 A .  The s m a l l sample t a k e n from Vancouver I s l a n d  i n I967 showed an i d e n t i c a l p a t t e r n t o those t a k e n  from  t h e I n t e r i o r i n I967 and t h e d a t a were combined f o r t h e purpose o f s e a s o n a l  comparisons.  One male showed e a r l y s i g n s o f development I n l a t e December and a l l were i n f u l l b r e e d i n g c o n d i t i o n by t h e end o f January.  They remained i n b r e e d i n g  c o n d i t i o n o n l y u n t i l t h e end o f March.  The p a t t e r n was  t h e same as found I n 1966 i n t h a t t h e r e was a peak i n organ s i z e , p a r t i c u l a r l y t h e s e m i n a l v e s i c l e s ,  this  time when t h e females were coming i n t o e s t r u s .  The  peak was n o t as h i g h as t h a t I n I966 b u t c o l l e c t i n g was done o n l y once a month and a h i g h e r peak may have been missed by a few weeks.  There was a drop i n male  organ s i z e s i n F e b r u a r y and March w h i c h c o i n c i d e d w i t h e s t r u s i n t h e female.  The drop i n organ s i z e s  following  t h e b r e e d i n g p e r i o d was n o t as pronounced as i n 1 9 6 6 . This i s p o s s i b l y a r e s u l t of the lower p r o p o r t i o n o f females b r e e d i n g t h a t y e a r . The females d u r i n g 1967 came i n t o b r e e d i n g c o n d i t i o n a t t h e end o f January a l o n g w i t h ' t h e males. D u r i n g l a c t a t i o n i n A p r i l and May t h e r e was no post partum e s t r u s .  I f t h e r e had been one i t would n o t have  been s u c c e s s f u l s i n c e t h e males were no l o n g e r c a p a b l e of b r e e d i n g .  Fecundity The  corpora l u t e a proved u s e f u l  the  o v u l a t i o n rates s i n c e they are l a r g e ,  and  a r e m a i n t a i n e d f o r months a f t e r  Even w i t h a p o s t partum  from  easily  seen  the b r e e d i n g season.  e s t r u s , the f i r s t  l u t e a c a n be d i s t i n g u i s h e d  i n determining  s e t of corpora  t h e s e c o n d by  their  s m a l l e r s i z e , more m e d u l l a r y p o s i t i o n and d i s t i n c t cell  morphology.  C o r p o r a l u t e a c o u n t s g i v e a good  i n d i c a t i o n o f o v u l a t i o n r a t e o n l y i f i t c a n be  assumed  t h a t "each c o r p u s l u t e u m r e p r e s e n t s t h e o v u l a t i o n of  one  egg.  Two  luteal  site  f e m a l e s w e r e c o l l e c t e d w h i c h had  Implantation sites  than corpora l u t e a .  I n one  more  case  the  i m p l a n t a t i o n s i t e s v/ere n o t e d f r o m p l a c e n t a l s c a r s a l o n e and  t h e r e may  have b e e n an e r r o r i n c o u n t i n g .  The  other  f e m a l e showed f i v e c o r p o r a l u t e a i n c o n j u n c t i o n w i t h six  embryos.  T h i s d i s c r e p a n c y may  have been caused  t w i n n i n g of the ova or from a p o l y o v u l a r f o l l i c l e .  by No  embryos w e r e s e e n t h a t p o s s e s s e d a common c h o r i o n s o the No  d i f f e r e n c e was follicles  probably the r e s u l t  of  polyovulation.  w e r e s e e n t h a t c o n t a i n e d more t h a n one  ovum.  W i t h t h e e x c e p t i o n o f t h e s e two a n i m a l s , t h e c o r p o r a l u t e a c o u n t s were t a k e n t o be  i n d i c a t i v e of the  ovulation  rate. C o r p o r a l u t e a " c o u n t s were t a b u l a t e d by age, s e a s o n , and T a b l e 1'.  year.  The  On V a n c o u v e r  comparisons Island  area,  are presented i n  i n 19&7»  t  n  e  juveniles  had  TABLE I  -  O v u l a t i o n r a t e s as i n d i c a t e d b y corpora l u t e a counts of a l l breeding females. T a b u l a t e d by age, s e a s o n , y e a r and l o c a t i o n .  Season  . Age  N  Ran,a;e  Mean  May-June  Ad.  16  4-7  5.18  Van. I s .  Juv.  14  4-6  4.85  Tot.  30  4-7  5.03  1966  Ad.  4  6  6.00  Juv.  6  4-6  5.00  Tot.  10  4-6  5.40  May-Aug.  Ad.  20  4-7  5.35  Van. I s .  Juv.  20  4-6  4.90  Tot.  40  4-7  5.12  Mar.-Apr.  Ad.  19  3-5  3.68  Interior  Juv.  15  2-6  3.46  Tot.  34  2-6  3.58  1966 Van. I s .  1966  1967  Mar.-Apr.  Ad.  5  4  4.00  Van. I s .  Juv.  4  4-5  4.25  Tot.  9  4-5  4.11  1967  P=.01 P=.2 J  P=.05  p=.5  P=.OOI  P=.01  P=.3  P=.05  a higher was  not  adults  o v u l a t i o n r a t e than the a d u l t s but significant  showed a h i g h e r  juveniles.  .03).  (P=  the  In a l l other  difference  cases,  the  average o v u l a t i o n r a t e than  the  T h i s d i f f e r e n c e was  significant  f o r the  •partum b r e e d i n g on V a n c o u v e r I s l a n d I n I966 (P= 1966  f o r the not  f o r the  I n the  first  Interior  o f 3.68 the  breeding season i n general  w h i c h was  estrous  I n 1967, not  period adults  .2)  (P= had  significantly  an  .01)  .05)  (P=  season.  ovulation  rate  .5)  (P=  and  but  of that  higher  post  than  3.46.  j u v e n i l e r a t e of  S i g n i f i c a n t d i f f e r e n c e s were found i n o v u l a t i o n rates  i n d i f f e r e n t a r e a s and  i n 1966 than the The  the  years.  o v u l a t i o n r a t e o f 5.12  r a t e o f 4.11  Interior region  f o u n d on I n 1967  was  the  reproductive  necessarily  .01)  (P=  1967.  same a r e a i n  (P=  .001)  was and  o v u l a t i o n r a t e i s an  indication  p o t e n t i a l o f an a n i m a l i t does  show t h e a c t u a l p r o d u c t i v i t y .  o f young b o r n can be ovulated  higher  Island  .05).  (P=  A l t h o u g h the the  Vancouver  w i t h a r a t e o f 3.58  l o w e r t h a n V a n c o u v e r I s l a n d I n 1966 1967  On  The  Preimplantation  losses  not number  r e d u c e d f r o m t h e number o f  through preimplantation  of  eggs  o r embryo r e s o r p t i o n .  l o s e s were d e t e r m i n e d from  the  d i f f e r e n c e b e t w e e n t h e number o f o v u l a t i o n s i t e s and  the  number o f v i s i b l e • i m p l a n t a t i o n s i t e s as embryonic s w e l l i n g s losses are  presented  or p l a c e n t a l s c a r s . i n Table I I .  The  indicated  by  Preimplantation sample  from  TABLE I I -  P r e i m p l a n t a t i o n l o s s e s as i n d i c a t e d by t h e d i f f e r e n c e between o v u l a t i o n s i t e s and e m p l a . n t a t i o n s i t e s . Tabulated b y a g e , s e a s o n , y e a r , and l o c a t i o n .  -46-  Season  Age  N  Ov. Sites  Implant Sites  % Loss  May-June 1966 Van. I s .  Ad.  7  35  34  2.85  Juv.  2  9  4  55.55  Tot.  9  44  38  13.63  Ad.  2  12  11  8.33  Juv.  1  5  5  Tot.  3  17  16  5.88  Ad.  9  47  45  4.25  Juv,  3  14  - 9  35.71  —  Tot.  12  61  5^  11.49  —  Ad.  14  52  49  5.76  Juv.  6  21  18  Tot,  20  73  67  8.21  2  8  5  37.37  2  8  5  37.37  25  107  99  7A7  Juv.  9  35  27  22.85  Tot.  34  142  126  11.26  July-Aug. 1966 Van. I s .  May-Aug. 1966 Van. I s .  Mar.-Apr. 1967 Interior  M a r . -Apr.' 1967 Van. I s .  Ad.  0  14.28  — , P=.05 J  13.2  Juv. Tot.  Total  t . test  Ad.  p=.l  P=.4  -4 7  Vancouver I s l a n d useful.  i n 1967  w  a  n o t l a r g e enough t o b e  s  I n a l l c a s e s t h e j u v e n i l e s showed a h i g h e r  preimplantation significant.  l o s s b u t t h e d i f f e r e n c e was n e v e r  The o v e r a l l p r e i m p l a n t a t i o n  Vancouver I s l a n d  l o s s on  i n 1966 was n o t s i g n i f i c a n t l y d i f f e r e n t  from t h e I n t e r i o r l o s s e s  I n 1967.  The l o s s f o u n d f o r a l l  a n i m a l s was .47 eggs p e r f e m a l e , o r a n o v e r a l l l o s s o f 11.26$ o f eggs o v u l a t e d . . When p r e i m p l a n t a t i o n consideration,  the adults  significant difference  were t a k e n  Into  a n d j u v e n i l e s showed n o  i n t h e number o f embryos c a r r i e d .  A d u l t s on V a n c o u v e r I s l a n d per  losses  i n 1966 a v e r a g e d 5.00 embryos  f e m a l e , w h i c h was n o t s i g n i f i c a n t l y d i f f e r e n t (P= .5)  f r o m t h e 3.75 Adults  embryos p e r f e m a l e c a r r i e d b y t h e j u v e n i l e s .  I n t h e I n t e r i o r i n 1967 c a r r i e d 3.62 embryos p e r  f e m a l e a n d t h i s was n o t s i g n i f i c a n t l y d i f f e r e n t (P= .02) f r o m t h e j u v e n i l e embryo r a t e o f 2.66 p e r p r e g n a n t  female.  When c o m b i n e d h o w e v e r , t h e 4 . 6 l embryos p e r p r e g n a n t female on Vancouver I s l a n d higher  i n I966 was s i g n i f i c a n t l y  (P= .001) t h a n t h e 3.36  f r o m t h e I n t e r i o r i n 1967.  embryos p e r f e m a l e t a k e n  Embryo c o u n t s a r e p r e s e n t e d  i n Table I I I . Embryo r e s o r p t i o n s  a r e recorded i n Table IV.  None was f o u n d i n 13 f e m a l e s f r o m V a n c o u v e r I s l a n d The I n t e r i o r s t u d y a r e a i n 1967, when 11 p r e g n a n t  i n 1966. females  w e r e t a k e n , showed a n o v e r a l l r e s o r p t i o n r a t e o f 18.91$ o f t h e embryos.  Age d i f f e r e n c e s  i n the resorption  loss  TABLE  III -  Embryo c o u n t s a s i n d i c a t e d b y t h e number o f v i s i b l e embryos o r I m p l a n t a t i o n sites, R e s o r b i n g embryos i n c l u d e d . T a b u l a t e d by age, s e a s o n , y e a r and location  -48-  Season  Age  N  Range  Mean  May-June 1966 Van. I s .  Ad.  7  4-5  4.86 -  Juv.  3  1-6  3.33 -  Tot.  10  1-6  4.40  Ad.  2  5-6  5.50  Juv.  1  5  5.00 -  Tot.  3  5-6  5.33  Ad.  9  4-6  5.00  Juv.  4  1-6  3.75  Tot.  13  1-6  4.61  July-Aug. 1966 Van. I s .  May-Aug. 1966 Van. I s .  Mar-Apr. 1967 Interior  "~p2..2  8  3-4  3.62  Juv.  3  2-3  2.66  2-4  3.36  11  PJ.3  I  P=.5  Ad.  Tot.  t . test  —1 P=.02 I  P=.001  TABLE I V  ~  P o s t i m p l a n t a t i o n l o s s e s as i n d i c a t e d by v i s i b l e r e s o r b i n g embryos.  -49-  Season  Age  May-June 1966  Ad.  Van. Is..  Total Embryo  Viable Embryo  % Loss  7  34  34  0  Juv.  2  4  4  0  Tot.  9  38  38  0  July-Aug. 1966  Ad.  2  11  11  0  Van. I s .  Juv.  1  Tot.  3  May-Aug. 1966  Ad.  Van. I s .  Juv.  5  0  16  16  0  9  45  45  0  3  9  9  0  12  54  54  0  Ad.  8  29  22  24.13^  Juv.  3  8  8  37  30  Tot. Mar-Apr. 1967 Interior  N  Tot.  11  5  0 18.91/S  -50-  could  n o t be d e t e r m i n e d b e c a u s e o f t h e s m a l l  sample.  Only three  of the eleven  possessed resorbing  embryos.  pregnant  females  The r e s o r p t i o n s  o c c u r v a r i e d f r o m one o u t o f t h r e e litter  juvenile  that d i d  embryos t o a c o m p l e t e  of three. As  w e l l as d i f f e r e n c e s  i n the productivity of  b r e e d i n g a n i m a l s t h e r e was c o n s i d e r a b l e frequency of breeding females.  v a r i a t i o n i n the  T a b l e V shows t h e  p e r c e n t a g e a n i m a l s b r e e d i n g by age each y e a r . 100$ o f t h e a d u l t f e m a l e s b r e d d u r i n g  Almost  the three  seasons.  I n I966 a l l j u v e n i l e f e m a l e s b r e d o n V a n c o u v e r I s l a n d , but  i n I967, b o t h I n t h e . I n t e r i o r a n d o n V a n c o u v e r  only  one t h i r d  of the juveniles bred.  loss  to the breeding population  a large proportion  since  This  Island,  i s a large  j u v e n i l e s make u p  of the spring population.  a n i m a l s t a k e n betx^reen M a r c h a n d May o f b o t h  Of 160 years,  64$ w e r e j u v e n i l e s . I n summary, t h e r e  was n o s i g n i f i c a n t  between t h e s i z e o f t h e f i r s t  litter  on V a n c o u v e r I s l a n d i n I 9 6 6 .  Age d i f f e r e n c e s  r a t e s were e v i d e n t Preimplantation  only  and t h e second  litter  i n ovulation  on V a n c o u v e r I s l a n d i n I966.  l o s s e s were c o n s t a n t  throughout the study.  difference  a t about  The d i f f e r e n c e b e t w e e n  11$ preimplantation  l o s s e s b y a g e on V a n c o u v e r I s l a n d i n 1966 a r e p r o b a b l y not  r e a l and s i m p l y  a r e s u l t o f s m a l l sample s i z e .  age  d i f f e r e n c e s w e r e f o u n d I n embryo c o u n t s  although  i n 1966  probably  t h e d i f f e r e n c e s on V a n c o u v e r I s l a n d would have been r e a l  No  i f t h e sample s i z e had been l a r g e r .  TABLE V  -  Percent females breeding a f t e r the o n s e t o f t h e b r e e d i n g s e a s o n as i n d i c a t e d by p r o e s t r u s , p r e g n a n c y , or l a c t a t i o n . T a b u l a t e d by age, y e a r , and l o c a t i o n .  -51-  Year-Area  Age  N  No. Breeding  $ Breeding  May-Aug. 1966 Van. I s .  Ad.  21  21  100$  Juv.  18  18  100$  5  5  100$  Juv.  13  4  30.79$  Ad.  23  22  95.59$  Juv.  59  21  35.59$  Apr.-Aug. 1967 Van. I s .  Feb.-July 1967 Interior  Ad.  -52Embryo r e s o r p t i o n s w e r e p r e s e n t o n l y i n 19&7. The  yearly productivity picture i s different  in a l l of the breeding populations studied. Island  I n I966 a l l f e m a l e s b r e d t w i c e , p r o d u c i n g  f i v e young each l i t t e r .  Those females  that d i d breed  t h r e e o r f o u r young.  of the juveniles d i d so.  produced  o n l y one  In the I n t e r i o r  all  a d u l t s b r e d w h i l e o n l y one t h i r d  did  so.  of  about  On t h e same a r e a i n 1967 a l l  a d u l t s b r e d b u t o n l y one t h i r d  of  On V a n c o u v e r  There the b r e e d i n g females  litter  i n 19&7  almost  of the juveniles produced  one  litter  two o r t h r e e y o u n g .  Reproduction i n Relation t o Relative Population Densities In  order t o evaluate the differences i n  p r o d u c t i v i t y o f young i n t h e t h r e e b r e e d i n g  seasons,  t h e r e p r o d u c t i v e s u c c e s s was c o m p a r e d w i t h t h e r e l a t i v e population  densities. That t h e I n t e r i o r r e g i o n supported a h i g h  s q u i r r e l p o p u l a t i o n i n 19^7 was a p p a r e n t began. in  One h u n d r e d a n d f o u r t e e n a n i m a l s w e r e  12 d a y s d u r i n g M a r c h , A p r i l , a n d May.  Island  when  collecting collected  On V a n c o u v e r  i n I966, 35 a n i m a l s w e r e t a k e n i n 20 d a y s  t h e same p e r i o d , w h i l e t h e same a r e a i n 19&7 12 a n i m a l s  i n t e n days.  r e l a t i v e p o p u l a t i o n count an a n i m a l  Such a k i l l  yielded  p e r day i s o n l y a  s i n c e i t took time t o autopsy  immediately a f t e r k i l l i n g ,  and t h i s  reduced  t h e h u n t i n g t i m e a p p r e c i a b l y when s e v e r a l a n i m a l s taken.  within  were  I n a d d i t i o n , c o n i f e r s t a n d s w e r e more o p e n i n  -53t h e I n t e r i o r so t h a t the animals  c o u l d more r e a d i l y  be  seen, A f u r t h e r estimate was  made b y  hour.  Red  t a b u l a t i n g t h e number o f c a l l s s q u i r r e l s are extremely  loud chattering c a l l not  t h a t was  given at a constant  I.965) and  of r e l a t i v e p o p u l a t i o n  g i v e n b y any  one  v o c a l and  recorded.  r a t e summer and  i t i s not u n l i k e l y animal  c o u n t s b a s e d on h o u r l y r e c o r d i n g s  The  (Smith, calls with the  Vancouver I s l a n d  1.16  calls  per  calls  per  I n t e r i o r c o u n t s I n I967 w e r e made  minute periods  s i n c e t h e y w e r e much t o o numerous  check of f o r an hour.  showed a n a v e r a g e o f 30.66 c a l l s From t h e s e d a t a Interior  are  considered  showed I . 7 8 and  the  calls  winter  i s not  h o u r w i t h i n h e a r i n g d i s t a n c e I n 1966  to keep proper  The  For t h i s reason  t o be a n a b s o l u t e p o p u l a t i o n i n d e x .  on 15  i t was  increases considerably  number o f c a l l s h e a r d p e r u n i t t i m e  The  per  t h a t t h e number o f  increasing population density.  hour i n I967.  heard  level  i n I967 had  per  i t c a n be  These hour.  seen t h a t  a h i g h p o p u l a t i o n and  w h i l e the two-year low  recordings  the  low  reproduction,  p o p u l a t i o n on V a n c o u v e r I s l a n d  showed h i g h r e p r o d u c t i o n  i n I966 b u t l o w  reproduction  i n I967 ( T a b l e V I ) . Reproduction Red  i n R e l a t i o n t o Foods  s q u i r r e l s u t i l i z e almost every  v e g e t a t i o n a v a i l a b l e t o them. food  species  study,  Utilized  of s q u i r r e l s  type  of  S m i t h (I965) l i s t s  73  i n B r i t i s h Columbia.  stomach a n a l y s i s i n the f i e l d  revealed  In the  this  TABLE V I  -  R e l a t i v e p o p u l a t i o n l e v e l s as i n d i c a t e d by t h e c a l l s recorded per h o u r a n d t h e number k i l l e d p e r d a y . T a b u l a t e d by y e a r and l o c a t i o n .  -54-  Population '  Hours Rec.  Calls/ Hour  Days Coll.  Coll./ Day , ,  Pop. Level  Reprod.  Vancouver Island 1966  51  .78  20  1.75  low  high  Vancouver Island 1967  25  1.16  10  1.20  low  low  3.75* 30.66  12  9.50  high  low  Interior 1967  * B a s e d on 15 m i n . r e c o r d i n g  periods.  -55o c c u r r e n c e o f v a r i o u s food types such as c o n i f e r f u n g i , greens  o r b e r r i e s and t h e monthly  seed,  average  frequencies o f these g e n e r a l food types a r e presented I n Table V I I .  Further i d e n t i f i c a t i o n of the foods,  particularly  t h e c o n i f e r s e e d s , was made b y o b s e r v a t i o n s o f t h e a n i m a l s and  their  middens. Greens were eaten throughout  the year i n s m a l l  amounts, b e i n g p r e s e n t i n 1 4 . 5 $ o f a l l stomachs B e r r i e s were r e l a t i v e l y u n i m p o r t a n t utilized  h e a v i l y when a v a i l a b l e  t o t h e d i e t b u t were  i n August  and September.  K l n n i k i n n i k and s a l a l were t h e main b e r r i e s The  utilized.  c h i e f components o f t h e y e a r l y d i e t were  seeds  and f u n g i .  throughout 79%.  F u n g i were found  conifer  I n k7% o f a l l s t o m a c h s  t h e y e a r vrhile c o n i f e r seeds were found i n  C o n i f e r seeds were u t i l i z e d  w h i l e t h e f u n g i were n o t u t i l i z e d month and o n l y s l i g h t l y  heavily  i n a l l months  as h e a v i l y  i n any  i n J a n u a r y , F e b r u a r y and March.  Storage caches  on t h e a r e a s s t u d i e d  e x c l u s i v e l y o f c o n i f e r cones.  consisted  A few f u n g i were  d r y i n g on l o g s a n d I n t r e e s b u t t h e s e w e r e f o u n d e a r l y summer a s w e l l a s i n t h e n o r m a l August  and September.  C o n i f e r seeds  w i n t e r foods s t o r e d by r e d s q u i r r e l s . and D o u g l a s caches  studied.  found i nthe  harvest time of are the staple Lodgepole  pine  f i r w e r e t h e c o n e s most a b u n d a n t i n t h e  and I n t h e f e e d i n g m i d d e n s , a l t h o u g h Engelmann  s p r u c e and ponderosa when a v a i l a b l e .  p i n e w e r e t a k e n I n s m a l l amounts  TABLE V I I  -  Frequency o f g e n e r a l food types In s q u i r r e l stomachs. T a b u l a t e d by month a s a p e r c e n t o f t h e t o t a l number o f stomachs examined.  -56-  Month  Contents  No, Stomachs Greens  Berries  Conifer Seeds  Mushrooms  Jan.  15  0.0  0.0  100.0  13.3  Feb.  36  8.3  0.0  100.0  19.4  Mar.  27  3.7  0.0  92.6  3.7  Apr.  19  5.3  0.0  89.5  21.0  May  38  15.8  0.0  84.2  65.8  June  54  18.5  0.0  62.9  68.5  July  50  26.0  6.0  60.0  72.0  Aug.  27  14.8  40.7  85.2  59.2  Sept.  20  20.0  80.0  65.0  15.0  Oct.  8  12.5  0.0  87.5  62.5  Nov.  5  20.0  0.0  80.0  80.0  Dec.  5  0.0  0.0  100.0  80.0  304  14.5  9.7  79.3  47.4  Total  -57Durlng Island,  t h e w i n t e r o f 1965-66 o n V a n c o u v e r  t h e f i r cone crop'was r e l a t i v e l y  l o d g e p o l e p i n e was u t i l i z e d I966 t h e y  almost  poor and  exclusively.  f e d on t h e new c r o p o f g r e e n p i n e c o n e s b u t  d i d n o t s t a r t s t o r i n g cones a t t h a t t i m e . fir  In July  cone c r o p o c c u r r e d  A very  i n I966 a n d b y S e p t e m b e r  were s t o r i n g f i r cones almost  exclusively.  good  squirrels  Throughout  t h e w i n t e r o f 1966-67 b o t h o n V a n c o u v e r I s l a n d a n d i n t h e Interior,  s q u i r r e l s were t a k e n most f r e q u e n t l y i n  a s s o c i a t i o n w i t h Douglas f i r t r e e s , and t h e i r consisted primarily  middens  o f Douglas f i r cone b r a c t s .  I n 19&7  t h e f i r c o n e c r o p was p o o r a n d p i n e c o n e s a g a i n became the prime o b j e c t i v e of the h a r v e s t i n g s q u i r r e l s . The r a t e o f r e p r o d u c t i o n i n t h e r e d s q u i r r e l was h i g h i n t h e b r e e d i n g s e a s o n t h a t f o l l o w e d a w i n t e r d i e t o f p i n e c o n e s , b u t i t was l o w b o t h I s l a n d and i n t h e I n t e r i o r been u t i l i z e d winter.  almost  on V a n c o u v e r  i n 19^7 when f i r c o n e s h a d  exclusively during the previous  -58DISCUSSION  The  Reproductive  Cycle  There i s n o t h i n g p a r t i c u l a r l y unusual about t h e changes i n t h e male r e p r o d u c t i v e organs throughout  the year.  extremely s i m i l a r Kirkpatrick  of the red s q u i r r e l  The h i s t o l o g i c a l c h a n g e s a r e  t o those found  i n t h e f o x s q u i r r e l by  (1955) a n d t h e a c c e s s o r y o r g a n s  t e s t i c u l a r cycle very The  follow the  closely.  f e m a l e s , h o w e v e r , show h i s t o l o g i c a l  that are quite distinct.  changes  The h i s t o l o g y o f t h e o v a r i e s  has b e e n d e s c r i b e d b y Mossman ( i 9 6 0 ) .  Corpora l u t e a a r e  m a i n t a i n e d u n t i l l a t e l a c t a t i o n and t h e e v e n t u a l r e g r e s s i o n i s a s l o w p r o c e s s l a s t i n g s e v e r a l months. Corpora l u t e a a r e also maintained during l a c t a t i o n i n Citellus  t r i d e c e m l l n e a t u s ( D r i p s , 1919K  ( R a s m u s s e n , 1918), C i t e l l u s and  Citellus beldlngi  carollnensls  lateralis  M a r m o t a monax  ( M c K e e v e r , I966)  ( M c K e e v e r , 1966) b u t n o t i n S c i u r u s  ( D e a n e s l y a n d P a r k e s , 1933).  The v a g i n a l  changes, however, a r e v e r y d i s t i n c t i v e o f t h e r e d s q u i r r e l . The  l a r g e c o i l e d and h i g h l y c o l l a g e n i c v a g i n a t h a t  develops  a t e s t r u s i s n o t common among s c i u r i d s .  A  c o i l e d v a g i n a has been d e s c r i b e d d u r i n g e s t r u s i n C i t e l l u s beldingi any  ( M c K e e v e r , 1966) b u t h a s n o t b e e n r e p o r t e d i n  other s c i u r l d .  a colled  The d e v e l o p m e n t o f t h e v a g i n a  s t r u c t u r e o c c u r s a t a t i m e when e s t r o g e n s  are h i g h , which  suggests  t h a t e s t r o g e n may b e  into  -59a casual f a c t o r involved i n the collagen formation, but it  i s very d i f f i c u l t  pattern.  The u s e f u l n e s s  questionable estrous  t o imagine the f u n c t i o n of such a  s i n c e , i n t h e summer o f I966 when a s e c o n d  occurred  breeding  o f such a development Is  without  any a p p r e c i a b l e v a g i n a l growth,  was s t i l l s u c c e s s f u l . I t was n o t p o s s i b l e t o d e t e r m i n e w h e t h e r  ovulation i n the red s q u i r r e l Cl t e l l u s  193*0  a n (  t r i d ec eml I n e a t u s  i Asdell  are a l s o .  ( I 9 6 6 )  i s an induced  suggests  ovulator (Foster,  t h a t many o t h e r  sciur.ids  One f e m a l e t a k e n d u r i n g a m a t i n g c h a s e h a d  a l r e a d y o v u l a t e d and s u g g e s t s squirrel  i s spontaneous o r induced.  that ovulation i n the red  i s spontaneous.  Age a t M a t u r i t y The q u e s t i o n o f a g e a t m a t u r i t y one t h a t i s d i f f i c u l t  to evaluate.  j u v e n i l e s , come i n t o b r e e d i n g and  I s an i n t e r e s t i n g  The m a l e s , a d u l t s a n d  c o n d i t i o n i n synchrony  r e m a i n f u n c t i o n a l f o r t h e same l e n g t h o f t i m e .  In  I967 a l l m a l e s w e r e i n f u n c t i o n a l c o n d i t i o n i n l a t e January.  Of t h e s e ,  t h e m a l e s b o r n i n J u n e 1966 w e r e  s e v e n months o l d when t h e y a t t a i n e d s e x u a l whereas those It  maturity,  i n l a t e A u g u s t w e r e o n l y f i v e months o l d .  i s p o s s i b l e t h a t most o f t h e young b o r n l a t e  y e a r had d i f f i c u l t y h a r v e s t i n g a food thus  less  likely  in' the  i n e s t a b l i s h i n g a t e r r i t o r y and  s u p p l y b e f o r e w i n t e r s e t i n and were to survive.  For this  reason,  a  -60c o n s e r v a t i v e e s t i m a t e o f age a t m a t u r i t y o f males be  would  7 months. The  a g e s t r u c t u r e i n t h e f e m a l e segment o f t h e  p o p u l a t i o n would  be s i m i l a r  t o t h e males,  but maturity  i n r e l a t i o n t o age p r e s e n t s a c o n f u s i n g p i c t u r e .  In  I n 19&7 many  1 9 6 6 a l l f e m a l e s b r e d a t t h e same t i m e .  of t h e young o f t h e p r e v i o u s y e a r d i d n o t b r e e d . about  one t h i r d  o f t h e young females bred  t h e y were p r o b a b l y about  7 months o l d .  a s s u m e d t h a t t h e two t h i r d s young'to  I n 19&7  a n c l  I t cannot be  t h a t d i d n o t b r e e d were t o o  d o s o s i n c e t h e r e was no s i g n i f i c a n t  (P=.5) b e t w e e n t h e e y e l e n s w e i g h t s  of those  t h a t d i d b r e e d and t h o s e t h a t d i d n o t . t h a t age i t s e l f d i d n o t cause juveniles.  Only  difference juveniles  Thus i t a p p e a r s  t h e l a c k o f b r e e d i n g among  The a g e o f m a t u r i t y f o r t h e f e m a l e s a s w e l l  as males c a n be g i v e n a c o n s e r v a t i v e e s t i m a t e o f 7 months. The B r e e d i n g S e a s o n The b r e e d i n g s e a s o n o f t h e r e d s q u i r r e l n o r m a l l y b e g i n s d u r i n g t h e w i n t e r months.  I n New Y o r k  development  o f t h e m a l e o r g a n s b e g i n s i n l a t e November a n d December and b r e e d i n g o c c u r s i n J a n u a r y Columbia  Smith  i n March.  (I965)  ( L a y n e , 195^).  found males i n b r e e d i n g  In British condition  I n the present study, the timing of the breeding  s e a s o n d u r i n g 1966 a n d 19&7 was d e t e r m i n e d b y a s s e s s i n g the monthly  o c c u r r e n c e o f l a c t a t i o n among f e m a l e s .  - 61L a c t a t l o n c a n r e a d i l y be d e t e r m i n e d  on s t u d y s k i n s and  t h e f r e q u e n c y o f t h e o c c u r r e n c e o f l a c t a t i o n was p l o t t e d f o r s p e c i m e n s i n t h e V e r t e b r a t e Museum a t t h e U n i v e r s i t y of B r i t i s h Columbia  i n o r d e r t o g e t some I d e a o f t h e  v a r i a t i o n and l i m i t s Columbia.  o f t h e b r e e d i n g seasons  F i g u r e 4 shows t h e f r e q u e n c y o f l a c t a t i o n f o r  1966 a n d 1967 a n d f o r B r i t i s h C o l u m b i a years. from  in British  The e a r l i e s t  the study skins,  occurrence of l a c t a t i o n , i sApril.  30  determined  I n I967 l a c t a t i o n was  a l s o e v i d e n t i n A p r i l and i t appears 1967 b r e e d i n g s e a s o n  over the past  therefore that the  c a n be r e g a r d e d as a n e a r l y one.  I n 1966 l a c t a t i o n d i d n o t o c c u r u n t i l J u n e a n d was apparently late.  Additional  i n f o r m a t i o n on b r e e d i n g  s e a s o n v a r i a t i o n s was r e c o r d e d b y S m i t h found  l a c t a t i n g females  none u n t i l J u l y  (I965).  i n May o f 1962 and. I963 b u t  i n 1964.  I t appears  likely  that a r i g i d l y  s e a s o n does n o t o c c u r i n t h e r e d s q u i r r e l . opportunistic  timed breedingI t i s extremely  i n i t s c h o i c e o f h a b i t a t and f o o d and i s  a p p a r e n t l y a l s o an o p p o r t u n i s t i c  breeder.  The e x a c t f a c t o r s b e h i n d one s e a s o n  He  t h e t i m i n g o f any  r e m a i n unknown, b u t t h e g e n e r a l w e a t h e r  c o n d i t i o n s do a p p e a r t o be a n i n f l u e n c e on t h e t i m e o f breeding.  The w i n t e r o f 1965-66 was s e v e r e w i t h t h r e e  times t h e normal  s n o w f a l l on t h e a r e a s s t u d i e d , and t h e  b r e e d i n g s e a s o n was l a t e .  The b r e e d i n g s e a s o n  i n 1964  FIGURE 4  -  The f r e q u e n c y o f l a c t a t i o n a s i n d i c a t e d by t h e c o n d i t i o n o f t h e n i p p l e s i n 19&6, 19&7 ^ °f p r e v i o u s l y c o l l e c t e d animals i n the V e r t e b r a t e Museum a t t h e U n i v e r s i t y o f B r i t i s h Columbia, a n c  MONTH  -63was  ( S m i t h , 1965)  also late  average  snowfall.  preceded  could affect it  by a s e v e r e w i n t e r , was  and  is difficult the normal  r e a d i l y burrows  was  above  preceded  S i m i l a r data i n which a delayed  t h e g r a y s q u i r r e l by S h o r t e n It  preceded by an  e a r l y s e a s o n i n 1967  The  by a v e r y m i l d w i n t e r . s e a s o n was  and was  found f o r  (195*0.  to visualize  activities  j u s t how  snowfall  of the s q u i r r e l ,  t h r o u g h t h e snow t o i t s f o o d  caches  t h e snow p r o v i d e s a n i n s u l a t i n g c o v e r f o r t h e  t o work beneath.  A g r e a t d e a l o f snow, h o w e v e r ,  f o r c e t h e a n i m a l t o s p e n d more t i m e d i g g i n g and time eating.  Severe weather  would  t o s p e n d more t i m e h o l e d u p and I t was  would less animal  foraging.  n o t p o s s i b l e t o compare t h e w i n t e r  c o n d i t i o n o f a n i m a l s d u r i n g m i l d and because of s m a l l w i n t e r sample s i z e s . noticeably  animals  a l s o f o r c e the  l e s s time  since  f a t a t any  severe winters No  a n i m a l s were  time of year.  Although there i s c o n s i d e r a b l e synchrony b o t h m a l e s and  f e m a l e s d u r i n g any  one b r e e d i n g  in  season  there i s c o n s i d e r a b l e v a r i a t i o n i n the d u r a t i o n of the breeding season  of d i f f e r e n t years.  I n most y e a r s  f u n c t i o n a l p e r i o d of the males l a s t s about a s was t o 1964  found  i n 1967  by S m i t h  and  (I965).  t h r e e months,  over t h r e e y e a r s from  a b o u t s i x months as f o u n d  i n 1966  l i t t e r was  s i n g l e i n s t a n c e o f an  produced.  The  I96I  O c c a s i o n a l l y the season when a n  the  lasts  additional extended  -64•  b r e e d i n g s e a s o n i n 1966, 1961-64 ( S m i t h ,  1965)  t h a t two l i t t e r s This  out of f i v e years o f records,  a n d 1965-67  (present  study),  a r e r a t h e r uncommon i n B r i t i s h  i s i n sharp contrast  suggests  Columbia, (1954)  t o t h e f i n d i n g s o f Layne  i n New Y o r k w h e r e t h e f u n c t i o n a l s e a s o n f o r t h e m a l e s commonly l a s t s  f o r a b o u t 6 months a n d many f e m a l e s  p r o d u c e two l i t t e r s . is  seen i n t h e males.  reproductive in  An a d d i t i o n a l p o i n t o f c o n t r a s t Two d i s t i n c t p e a k s I n m a l e  organ s i z e a r e found i n t h e east b u t n o t  t h e west.  I t seems u n l i k e l y t h a t l a t i t u d e i s a  dominant i n f l u e n c e i n t h i s d i f f e r e n c e s i n c e only  about  9°  British  of l a t i t u d e separates the areas,  Columbia has a r e l a t i v e l y m i l d Inland  regions  and s o u t h e r n  climate  compared t o more  of s i m i l a r latitudes,  A possible explanation h a b i t a t d i f f e r e n c e s between east  can be seen i n t h e and west.  Coniferous  f o r e s t s dominate t h e western h a b i t a t o f the r e d s q u i r r e l w h i l e much o f t h e e a s t e r n were s t u d i e d  h a b i t a t where r e d s q u i r r e l s  c o n s i s t s o f mixed deciduous f o r e s t s .  d e c i d u o u s f o r e s t s two d i s t i n c t the  first  fruit  f r u i t i n g seasons  involving early spring plants  before  the leaves  of the trees  a closed  Coniferous  form a c l o s e d  t r e e buds, and f l o w e r s  trees i n  forests  c a n o p y y e a r r o u n d a n d o n l y one m a i n  s e a s o n o c c u r s i n l a t e summer.  occur;  t h a t bloom and  canopy; and t h e second i n v o l v i n g t h e f r u i t i n g l a t e summer ( B r a u n , 1950).  In  Early fleshy  present  fruiting fruits,  a r e major s p r i n g foods o f eastern  -65(Layne,195 *') w h i l e  squirrels utilized  i  very It  i n t h e west such foods a r e  little. i s possible that the eastern  red squirrel  responds t o t h e mixed deciduous f o r e s t h a b i t a t by e x h i b i t i n g two d i s t i n c t b r e e d i n g p e a k s , s o t h a t t h e y o u n g are  p r o d u c e d a t t h e two t i m e s when f o o d  In t h e west t h e c o n i f e r o u s provide two  favorable  f o r e s t s do n o t n o r m a l l y  conditions  forsquirrels  t o produce  l i t t e r s and I t I s o n l y under p a r t i c u l a r l y  conditions a  i s most abundant.  s u c h a l a r g e s t o r e o f good w i n t e r  favorable  favorable food and  s p r i n g t h a t t h e y c a n p r o d u c e more t h a n one  litter. Despite duration  yearly variations  of breeding there  i s very  I n t h e time and c l o s e synchrony between  peaks i n t h e male organ s i z e s and t h e o c c u r r e n c e o f estrous  i n the females.  conditions  I t appears that the e x t e r n a l  t h a t o p e r a t e on t h e p o p u l a t i o n  to i n i t i a t e  b r e e d i n g o p e r a t e e q u a l l y o n b o t h s e x e s t o b r i n g them c o n d i t i o n a t a b o u t t h e same t i m e . evident  i n the i n i t i a t i o n  the  same t i m e i n I967.  i n both years coincided  Some v a r i a t i o n i s  of breeding.  i n t o c o n d i t i o n a month a f t e r  The f e m a l e s came  t h e m a l e s i n 1966 b u t a t  The p e a k s i n m a l e o r g a n with  suggests that a synchronizing  into  estrous  size  i n t h e females and  mechanism i s o p e r a t i n g  between t h e sexes. Smith  (I965)  suggests that the anal gland  the vagina might produce o d e r i f e r o u s could  substances  a t t r a c t t h e males and a i d i n s e x u a l  or  that  synchrony.  -66However, t h e g r o s s  appearance o f the a n a l gland  same i n b o t h s e x e s t h e y e a r  i sthe  r o u n d a n d t h e r e v/ere n o  a p p a r e n t h i s t o l o g i c a l d i f f e r e n c e s i n t h e 57 a n a l c o l l e c t e d d u r i n g t h e summer o f I966. probably not  does n o t operate  the vagina  stimulates  glands  Thus t h e a n a l  i n t h i s mechanism.  gland  Whether o r  produces an o d e r l f e r o u s substance  that  t h e male remains t o be i n v e s t i g a t e d .  Fecundity There a r e d i s t i n c t y e a r l y d i f f e r e n c e s i n breeding.  A low population  participating two  i n 1966 showed a l l f e m a l e s  i n an extended breeding  large l i t t e r s .  s e a s o n and  The h i g h p o p u l a t i o n o f t h e I n t e r i o r  i n I967 showed a l l a d u l t f e m a l e s b u t f e w y o u n g i n a short breeding The  season and p r o d u c i n g  participating  one s m a l l  litter.  l o w I s l a n d p o p u l a t i o n I n 1967 showed a s i m i l a r  pattern  t o t h e h i g h I n t e r i o r p o p u l a t i o n o f t h e same PreImplantation all  producing  three  evident  l o s s e s appear constant  instances,  only  been present  year.  a t a b o u t 11% i n  P o s t i m p l a n t a t i o n m o r t a l i t y was  i n the high population  i n 19&7 b u t may h a v e  i n t h e l o w 1967 p o p u l a t i o n a s w e l l .  These changes i n r e p r o d u c t i o n do n o t f i t a p a t t e r n o f an I n t r i n s i c d e n s i t y dependent c o n t r o l system. An  i n d i r e c t measurement o f p o p u l a t i o n l e v e l , based on  rate of calls  and k i l l  p e r d a y shows no c l e a r  relationship  between p o p u l a t i o n d e n s i t y and r e p r o d u c t i v e output. I967 t h e a r e a  t h a t had a p o p u l a t i o n  In  I n d e x much h i g h e r  than  the o t h e r had a v e r y l o w r e p r o d u c t i v e r a t e and d e n s i t y d e p e n d e n t f a c t o r s may h a v e b e e n o p e r a t i n g a t t h a t  time.  -67The  V a n c o u v e r I s l a n d p o p u l a t i o n had a l o w p o p u l a t i o n  Index I n both  y e a r s , b u t showed a c o m p l e t e r e v e r s a l o f  r e p r o d u c t i v e output  i n one y e a r  t h i s case i t i s d i f f i c u l t mechanism i s a p r i m a r y Fecundity type  over the other.  In  t o s e e how a d e n s i t y d e p e n d e n t  factor regulating  reproduction.  d o e s seem t o f l u c t u a t e w i t h t h e  o f food a v a i l a b l e .  Regardless  of population  t h e r e was a h i g h r e p r o d u c t i v e p e r f o r m a n c e a f t e r all  w i n t e r on s t o r e d l o d g e p o l e  low  r e p r o d u c t i v e output  fir  cone c r o p d u r i n g t h e w i n t e r .  level,  feeding  p i n e c o n e s , and a r e l a t i v e l y  a f t e r f e e d i n g on a h e a v y D o u g l a s  shows a s i m i l a r phenomenon.  (I965)  Smith's data  Reproduction  was l o w I n  1962 a f t e r f e e d i n g on D o u g l a s f i r c o n e s a n d h i g h i n 1964 a f t e r f e e d i n g on l o d g e p o l e  pine  cones.  There i s c o n s i d e r a b l e controversy reproduction  i n mammals i s c o n t r o l l e d b y d e n s i t y d e p e n d e n t  f a c t o r s o r through support  t h e amount o f f o o d a v a i l a b l e t o  the r a i s i n g of offspring.  c o n v i n c i n g evidence  L a c k (195*0  for  o f food.  t h a t t h e same m e c h a n i s m o p e r a t e s Although  presents  t h a t t h e c l u t c h s i z e i n some b i r d s  varies d i r e c t l y with the a v a i l a b i l i t y suggests  as t o whether  little  He  i n .mammals'.  c o n c l u s i v e evidence  i s recorded  s c i u r i d mammals, a n a p p a r e n t e f f e c t o f f o o d  on r e p r o d u c t i o n larger l i t t e r s areas  i s seen i n the f o x s q u i r r e l . were f o u n d i n c o r n f i e l d  supply  Significantly  h a b i t a t than i n  o f m i x e d hardwoods (Brown and Yeager,19^5).  Most  -68fox squirrels  o f t h e h a r d w o o d s d i d n o t b r e e d when t h e .  a c o r n crop f a i l e d , b u t a few d i d so i n farmland t h e y had a s u b s i d i a r y food s u p p l y Support  (Allen^19^3).  f o r the p o s s i b i l i t y  • s u p p l y m i g h t be c r i t i c a l  where  t h a t t h e food  f o r breeding red squirrels i s  enhanced by t h e h i g h m e t a b o l i c r a t e o f t h e s p e c i e s . T h e i r b a s a l m e t a b o l i c r a t e i s 80% h i g h e r t h a n t h a t o f other animals increases  o f s i m i l a r s i z e and d u r i n g c o l d weather i t a n d H o n s o n , 1955).  ( I r v i n g , Krog,  p h y s i o l o g i c a l conditions a winter shortage  Under  these  of food  would  be d e t r i m e n t a l t o t h e c o n d i t i o n o f t h e a n i m a l . red s q u i r r e l s begin breeding during the cold months, a food s h o r t a g e  c o u l d be r e f l e c t e d  r e p r o d u c t i v e performance.  Since  winter  i n their  whole  I n t h e p r e s e n t s t u d y a change  i n f o o d s p e c i e s r a t h e r t h a n a n a b s e n c e o f f o o d was f o l l o w e d by a change i n r e p r o d u c t i v e o u t p u t . There a r e s e v e r a l p o s s i b l e f a c t o r s both  involving  t h e h a b i t s o f t h e s q u i r r e l s and t h e f r u i t i n g h a b i t s  of the conifers that could a f f e c t the capacity of the red s q u i r r e l forests.  t o p r o d u c e more y o u n g i n l o d g e p o l e  First,  w e l l adapted  the western  red squirrel  pine  i s particularly  t o i n h a b i t a t i n g open f o r e s t s d o m i n a t e d b y  lodgepole pine.  Both  t h e i r pelage  c o l o r and v o c a l i z a t i o n  are adapted  t o a n open f o r e s t s i t u a t i o n s u c h a s l o d g e p o l e  pine s i t e s ,  and t h e i r  powerful  t o enable  p i n e cones  jaw m u s c u l a t u r e  i s sufficiently  them t o o u e n t h e t o u g h  ( S m i t h , 19'$5).  serotinous  I n these respects i t i s  -69advantageous pine  f o rthe red s q u i r r e l to l i v e  i n lodgepole  habitat. Secondly, there a r e advantages  l o d g e p o l e p i n e cones.  t o f e e d i n g on  Lodgepole p i n e produces a r e l a t i v e l y  s t a b l e c o n e c r o p y e a r a f t e r y e a r , t h e c o n e s r e m a i n on t h e t r e e s f o r many months a n d many o f them d o n o t o p e n u n t i l subjected  t o i n t e n s e h e a t ( C r o s s l e y , 1952).  l o d g e p o l e p i n e cones  the s q u i r r e l i s sure of a r e l a t i v e l y  c o n s t a n t c r o p o f cones needed. all  that r e t a i n  This i s b e n e f i c i a l  t h e i r seeds  until  t o the s q u i r r e l since almost  t h e cones s t o r e d a r e a v a i l a b l e  as f o o d t h r o u g h o u t t h e  Of 93 l o d g e p o l e p i n e c o n e s  winter.  By h a r v e s t i n g  t a k e n from  c a c h e s i n 196? o n l y e i g h t p e r c e n t w e r e open.  squirrel The s e e d s  d r o p o u t o f t h e s e open c o n e s a n d a p p a r e n t l y a r e n o t utilized  b y t h e s q u i r r e l s , f o r my c a p t i v e  which r e a d i l y a t e closed on o p e n c o n e s the  wild  cones  cones, would n o t attempt t o feed  e v e n when no o t h e r f o o d was a v a i l a b l e .  In  no s q u i r r e l s w e r e o b s e r v e d f e e d i n g on o p e n  o r t h e i r i n d i v i d u a l seeds.  t h a t t h e s e e d s c o u l d be r e t r i e v e d conifer  squirrels,  The p o s s i b i l i t y e x i s t s from t h e ground b u t  seeds a r e s m a l l and t h e energy expended i n  s e a r c h i n g f o r them w o u l d p o s s i b l y e x c e e d t h e e n e r g y obtained.  Thus l o d g e p o l e p i n e c o n e s a r e a good  food f o rs q u i r r e l s  winter  since there i s a r e l i a b l e yearly  cone c r o p and most o f t h e cones s t o r e d r e m a i n and c a n b e u s e d b y t h e s q u i r r e l s  closed  throughout the winter.  -70D o u g l a s f i r c o n e s on t h e o t h e r hand s e v e r a l u n c e r t a i n t i e s to the red s q u i r r e l  present  even though  t h e y a r e e a s i e r t o o p e n t h a n l o d g e p o l e p i n e and have a h i g h e r c a l o r i c c o n t e n t (Smith,1965). cone c r o p s  initially  o f s e e d s t h a n do t h e p i n e  Douglas f i r t r e e s have e x t r e m e l y  and i t i s o n l y d u r i n g y e a r s  t h a t the s q u i r r e l harvests  variable  o f good  yield  them i n any g r e a t amount.  D o u g l a s f i r c o n e s open and d r o p t h e i r s e e d s a t m a t u r i t y and, u n l e s s h a r v e s t e d by s q u i r r e l s  i n their closed state  before  this  t i m e , a r e n o t a v a i l a b l e as a s o u r c e  of winter  food.  When D o u g l a s f i r c o n e s a r e a b u n d a n t a l a r g e c a c h e  o f them I s n o t n e c e s s a r i l y i n d i c a t i v e o f t h e amount t h a t w i l l be a v a i l a b l e t o s q u i r r e l s  throughout the winter.  Many f i r c o n e s o p e n i n t h e c a c h e s and t h e i r s e e d s a r e lost. In  Of 94 D o u g l a s f i r c o n e s removed  the I n t e r i o r  Under  from caches  i n I967, kj>% w e r e f o u n d t o be  these circumstances  open.  o n l y about h a l f the s t o r e d  c o n e s w o u l d be a v a i l a b l e f o r f u t u r e u s e . Most o p e n and t h u s  o t h e r c o n i f e r s produce cones t h a t fall  readily  I n t o the poor food category w i t h Douglas  fir. In  t h i s manner a good s t o r e o f l o d g e p o l e  cones i s b e n e f i c i a l t o the s q u i r r e l w h i l e a h a r v e s t fir  c o n e s o n l y a p p e a r s t o be s o .  concentrate During  pine of  The s q u i r r e l seems t o  on w h a t e v e r c o n e s a r e m o s t r e a d i l y  available.  a good D o u g l a s f i r c o n e c r o p t h e h a r v e s t i s  concentrated  on t h a t c o n i f e r s p e c i e s , and t h e s q u i r r e l s  -71l e a v e m o s t o f t h e p i n e c o n e s on t h e t r e e s . known why t h e r e d s q u i r r e l c o n c e n t r a t e s a s t a b l e p i n e cone c r o p  i savailable.  I t i s not  on f i r cones w h i l e T h e y may p r e f e r t h e  s o f t e r f i r c o n e s b e c a u s e t h e y a r e e a s i e r t o open. squirrels  can s t i l l  The  go b a c k a n d c u t t h e p i n e c o n e s , b u t i t  means t h a t t h e e n e r g y e x p e n d e d i n c o l l e c t i n g t h e f i r s t harvest  i s l a r g e l y wasted.  Thus p o o r w i n t e r c a c h e s o f  p i n e c o n e s may p r o v i d e t h e s q u i r r e l s w i t h e n o u g h e n e r g y to  produce a l a r g e l i t t e r ,  litters  o r i n e x c e p t i o n a l y e a r s , two  p e r breeding female.  On t h e o t h e r h a n d , a s u p p l y  o f f i r c o n e s may f u r n i s h o n l y enoiigh e n e r g y t o p r o d u c e a small l i t t e r ,  o r i n t h e case  o f young a n i m a l s  which  need energy f o r growth and development as w e l l as m a i n t e n a n c e , none a t a l l . This,  i n part, Is a possible explanation of  the comparatively g r e a t e r success over I967. for  I n 1966  I t i snot l i k e l y a total  e x p l a n a t i o n , however  t h e r e was a d i f f e r e n c e i n l i t t e r  s i z e between t h e two  p o p u l a t i o n s I n I967. in  of breeding  T h i s may h a v e b e e n d u e t o d i f f e r e n c e s  t h e weather, s p r i n g food supply, o r t h e major h a b i t a t  d i f f e r e n c e s b e t w e e n t h e two a r e a s , found  i n 1967  animals  The r e s o r b i n g embryos  c o u l d have been a n I n d i r e c t r e s u l t o f t h e  b r e e d i n g b e f o r e t h e snow h a d m e l t e d ,  when t h e r e w e r e no f r e s h f u n g i o r g r o w i n g the pregnant-females  could  feed.  a t a time  p l a n t s on w h i c h  Despite success  and f o o d  possibility  the s t r o n g c o r r e l a t i o n between supply  studied, the  of i n t r i n s i c d e n s i t y dependent f a c t o r s o p e r a t i n g  c a n n o t be I g n o r e d . although  i n the populations  breeding  P o p u l a t i o n s do n o t r e m a i n s t e a d y  t h e V a n c o u v e r I s l a n d and I n t e r i o r  were d i f f e r e n t  i t was  and  populations  not determined whether the p o p u l a t i o n s  were i n c r e a s i n g o r d e c r e a s i n g .  Such d a t a would a i d c o n s i d e r a b l y  the e v a l u a t i o n of the r o l e of d e n s i t y dependent f a c t o r s in controlling reproduction. to  Further study  e v a l u a t e more f u l l y t h e e f f e c t s  food supply  i s needed  of the q u a l i t y of the  and o f d e n s i t y d e p e n d e n t f a c t o r s on  breeding  i n the red s q u i r r e l , but i t appears that the food f a c t o r e x e r t s a marked young.  i n f l u e n c e on t h e y e a r l y p r o d u c t i o n  of  PLATE I  The Vancouver Island habitat  A.  An open rocky s i t e . . Arbutus, Douglas f i r and lodgepole pine are the dominant trees and ocean spray and s a l a l are the dominant shrubs.  B,  Dense vegetation, A stand of predominantly Douglas f i r where s a l a l forms a thick understory.  PLATE I I  The Interior habitat  A.  An open s i t e forested with Douglas f i r , lodgepole pine and ponderosa.'pine. Snowbrush is the dominant shrub.  B.  A dense stand of mixed.lodgepole pine and Douglas f i r , Soopalalie i s present in the sparse slirub layer.  -74-  PLATE I I I  -  Seasonal  changes i n t h e t e s t e s .  A.  I n f a n t i l e male. The s m a l l c l o s e l y p a c k e d s e m i n i f e r o u s t u b u l e s a r e b o u n d e d by s m o o t h b a s e m e n t membranes, Mag. X 101.  B.  Developing male. The t u b u l e s , s e p a r a t e and l u m i n a f o r m i n c o n j u n c t i o n w i t h spermatogenic a c t i v i t y . Mag. X 169.  C,  E a r l y f u n c t i o n a l male. L a r g e clumps o f L e y d i g c e l l s a r e p r e s e n t and t h e t u b u l e lumina are packed w i t h spermatozoa. Mag. X I69.  D.  L a t e f u n c t i o n a l male. Leydig c e l l s are s m a l l and t h e t u b u l e s c o n t a i n f e w e r s p e r m a t o z o a . Mag. X 169.  E.  E a r l y degenerate male. L e y d i g c e l l s a r e v e r y s m a l l and t h e t u b u l e l u m i n a are clogged w i t h c e l l u l a r d e b r i s . Mag. X 169.  PLATE IV  -  S e a s o n a l changes i n the e p i d i d y m i d e s  A.  I n f a n t i l e . Very l i t t l e c y t o p l a s m i s p r e s e n i n the e p i t h e l i a l c e l l s l i n i n g t h e t u b u l e s . Mag. X 169.  B.  D e v e l o p i n g . The e p i t h e l i u m o f t h e t u b u l e s forms a p s e u d o s t r a t i f i e d l a y e r and possesse a s m a l l amount o f a p i c a l c y t o p l a s m . Mag. X I69.  C.  F u n c t i o n a l . The i n t e r t u b u l a r c o n n e c t i v e t i s s u e i s v e r y t h i n and the t u b u l e s a r e packed vrith sperm. Mag. X I69.  D.  E a r l y degenerate. The t u b u l e s s h r i n k , the r e l a t i v e amount o f c o n n e c t i v e t i s s u e i n c r e a s e s and l e u c o c y t e s a r e p r e s e n t . Mag. X I 6 9 .  PLATS V  Seasonal changes i n the seminal v e s i c l e s  A.  Infantile. The lumina are open but the secretory epithelium i s disorganized. Mag. X 1 6 9 . "  B.  E a r l y Development, Only the i n i t i a l o r g a n i z a t i o n o f the s e c r e t o r y e o i t h e l i u m is evident. Mag. X 1 6 9 .  C.  Functional. Consecutive stages i n the development of the e p i t h e l i u m from ( i ) a f o l d e d e p i t h e l i u m of elongate c e l l s , to ( i i ) a pseudostratified c e l l l a y e r w i t h o v a l n u c l e i , to ( i i i ) a single cuboidal c e l l layer Mag. X I69.  D.  Late f u n c t i o n a l . The e p i t h e l i u m becomes p s e u d o s t r a t i f i e d and possesses only a small amount o f cytoplasm. Secretion d r o p l e t s a r e s t i l l present. Mag. X 169.-  PLATE V I  -  S e a s o n a l changes i n t h e p r o s t a t e  A.  Infantile. The s m a l l t u b u l e s p o s s e s s no o p e n l u m i n a a n d no o r g a n i z e d e p i t h e l i u m . Mag. X 169  B.  E a r l y Development. I n i t i a l l y the e p i t h e l i u m becomes o r g a n i z e d a n d l u m i n a open b e f o r e t h e e p i t h e l i a l c e l l cyloplasm occludes i t . Mag. X I69.  C.  Functional. The g l a n d s show p r o g r e s s i v e changes from ( i ) t h e e a r l y f u n c t i o n a l s t a t e vrhere t h e l u m i n a a r e l a r g e l y o c c l u d e d by s e c r e t o r y c e l l c y t o p l a s m , t o ( i i ) the l a t e f u n c t i o n a l state-where t h e c y t o p l a s m i s r e d u c e d and t h e l u m i n a larger. Mag. X 169.  D.  Degenerate. The t u b u l e s become h e a v i l y n u c l e a t e d a n d w i t h o u t l u m i n a and a r e supported by c o l l a g e n i c c o n n e c t i v e tissues. Mag. X I69.  PLATE V I I  ~  S e a s o n a l changes i n t h e  vagina.  A.  Infantile. The l u m e n i s c o n v o l u t e d but the e p i t h e l i u m i s organized. The outer t i s s u e layers are heavily nucleated. Mag. X 1 0 1 .  B.  Early Proestrous. The t i s s u e l a y e r s and t h e l u m i n a i n c r e a s e d u r i n g t h e i n i t i a l stages. Mag. X 1 0 1 .  C.  Estrous. The l a m i n a p r o p r i a becomes l o o s e and h i g h l y c o l l a g e n i c , a t h i c k g e r m i n a t i v u m f o r m s and t h e c o r n i u m sloughs heavily. Mag. X 4 0 .  D.  Late Pregnancy. The c o l l a g e n d e c r e a s e s c o n s i d e r a b l y and t h e e p i t h e l i u m r e t u r n s to a t h i n layer. Leucocytes are s t i l l present. Mag. X 4 0 .  E.  E a r l y Anoestrous. A l l tissue layers shrink and become h e a v i l y n u c l e a t e d , and s c l e r o t i c blood vessels develop. Mag, X 1 0 1 .  i  S e a s o n a l changes i n t h e u t e r u s .  PLATE V I I I A.  Infantile. A l l tissues are heavily n u c l e a t e d and e n d o m e t r i a l g l a n d s a r e scarce. Mag. X 1 0 1 .  B.  Estrous. A l l tissue layers are thick. The l u m e n p r e s e n t s a c o n v o l u t e d s u r f a c e and e n d o m e t r i a l g l a n d s a r e open. Mag. X 4 0 .  C.  Recent Post Partum. The t i s s u e a n d e p i t h e l i u m a r e h e a v i l y n u c l e a t e d and s c h l e r o t i c blood vessels develop. Mag. X 1 0 1 .  D.  Anoestrous. Schlerotic blood vessels are present, the t i s s u e s are h e a v i l y n u c l e a t e d , and e n d o m e t r i a l g l a n d s a r e minimal. I n w i n t e r (1) t h e r e i s l i t t l e c o l l a g e n p r e s e n t , b u t i n summer ( i i ) t h e collagen i s distinct. Mag. X 1 0 1 .  PLATE IX  -  Seasonal  changes i n the Ovary.  A.  Infantile. A t h i c k c o r t i c a l l a y e r of naked ova predominates f o r the f i r s t three to f o u r months of l i f e . (i) Then secondary and r e g r e s s i n g f o l l i c l e s appear a t about f o u r to f i v e months of age. Mag, X 68 ( i i ) and changes continue u n t i l near Proestrous. Mag. X 40. ( i i i ) Mag. X 40.  B.  Post O v u l a t i o n . The corpus luteum forms r a p i d l y although the blood c l o t may be v i s i b l e u n t i l a f t e r i m p l a n t a t i o n . Mag. X 68.  .C.  Anoestrous, Naked ova are s c a r c e and corpa a l b i c a n t i a (centre) may remain u n t i l the next b r e e d i n g season. Mag. X 40.  PLATE X  -  Changes I n t h e C o r p o r a  Lutea  A.  P r e g n a n c y and l a c t a t i o n , There i s l i t t l e change i n the c o r p o r a l u t e a s t r u c t u r e from ( i ) e a r l y pregnancy, t o ( i i ) l a t e pregnancy, to (iii) lactation. Mag. X  B.  Late l a c t a t i o n . The i n i t i a l d e g e n e r a t i v e change i s a s e p a r a t i o n of the l u t e a l c e l l s , Mag, X I69.  C.  Early anoestrous. V a c u o l a t i o n and f u r t h e r d e g e n e r a t i v e changes t a k e p l a c e a b o u t t h r e e months p o s t partum. Mag. X 101.  -82-  -83-  ACKNOWLEDGEMENTS  I wish  t o t h a n k my s u p e r v i s o r , D r . J . M . T a y l o r ,  whose s u p p o r t  a n d e n c o u r a g e m e n t made t h i s  D r . C. C. S m i t h species  study  possible.  k i n d l y made h i s u n p u b l i s h e d d a t a on t h e  available  t o me.  D i s c u s s i o n w i t h D r . V. J .  K r a j i n a r e g a r d i n g t h e v e g e t a t i o n and p l a n t were v e r y u s e f u l .  Extremely  v i d e d b y H . D. F i s h e r  helpful  associations  criticism  and D r . I . McT. Cowan.  was p r o M r s . J . D.  Hudson a i d e d i n t h e p r e p a r a t i o n o f t h e m a n u s c r i p t . am g r a t e f u l for  I  t o a l l o f t h e s e p e o p l e , a n d t o many o t h e r s ,  t h e i r help throughout  the course  of this  study.  -84L I T E R ATU RE CITED A l l e n , D.L. 1943. M i c h i g a n f o x s q u i r r e l management. M i c h . D e p t . C o n s . Game D i v . P u b l . 100. 404 p. . A s d e l l , S.A. 1966. P a t t e r n s o f mammalian r e p r o d u c t i o n , Cornstock, I t h a c a , Mew Y o r k . 670 p. Braun,  E.L. 1950. America.  2nd. e d .  Deciduous f o r e s t s of eastern North B l a k l s t o n Co. , P h i l a d e l p h i a . 59'6 P*  B r o w n , L.G. and L . E . Y e a g e r . 1945Pox s q u i r r e l s and gray s q u i r r e l s In I l l i n o i s . 111. N a t . H i s t . Survey 3 u l l . 23: 449-536. Cowan, I . McT. a n d C . J . G u l g u e t . 19&5* mammals o f B r i t i s h Columbia, B r i t i s h C o l u m b i a P r o v . Mus. Handbook 1 1 . 414 p. 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