289 Int. J. Biometeor. 1975, vol. 19, number 4, pp. 289-303

The Pineal Gland and Geographical Distribution of Animals by C.L.Ralph*

ABSTRACT.- A detailed analysis of the o c c u r r e n c e of parietal eye component of the pineal complex in families of lizards has revealed that those in which the parietal eye is absent in most genera (e. g. Gekkonidae, Teiidae) tend to be r e s t r i c t e d to low latitudes, whereas families in which the parietal eye is present in most of the genera (e. g. Agamidae, Iguanidae) extend to higher latitudes. Those few genera which lack parietal eyes in the families where the v e r y great majority have parietal eyes are confined to ranges r a t h e r close to the equator. The parietal eye may be important in t h e r m o r e g u l a t o r y or reproductive adaptations at higher latitudes where seasons a r e m o r e s e v e r e l y varied than at lower latitudes. A pineal body is reported to be absent in crocodilians, edentates and, perhaps, dugongs. All these animals tend to inhabit tropical regions. In contrast, seals and walruses have remarkably large pineal glands and are found at v e r y high latitudes. These few fragments of information cannot be used to support any conclusions, but they do suggest that it might be productive to consider the pineal complexes of animals in the context of their geographical distribution. INTRODUCTION The brain wall of v e r t e b r a t e s can develop a v a r i e t y of enlargements, invaginations, evaginations, or areas of vascular specialization, which collectively are called " c i r e u m v e n t r i c u i a r organs" (Weindl, 1973). Pineal bodies, dorsalprojecting structures on the dienoephalon, are among the m o r e constant of these, being found in some f o r m in almost all v e r t e b r a t e s that have been examined. However, comparative morphological studies have r e v e a l e d a r e m a r k a b l e range of variation in pineal structure. Considered phylogenetioally, pineal bodies are probably unique organs in t e r m s of the extent of their diversity in form and cytological differentiation (Oksehe, 1965). The pineal body or e~physis cerebri of fishes, amphibians and laeertilian reptiles is p r i m a r i l y a photoreeeptor organ. This is also true for certain " a c c e s s o r y pineal organs", including the frontal organ or Stirnorgan of anuran amphibians, the parietal eye of lacertilians, and the parapineal organ of Petromyzontidae (Kappers, 1965). In snakes, turtles, birds and mammals, a c c e s s o r y pineal s t r u c t u r e s are absent and direct photoreceptive responsiveness presumably has disappeared; their epiphyses a r e glandular bodies. F u r t h e r m o r e , whereas the n e u r o s e n s o r y cells of the pineal complexes of lower v e r t e b r a t e s send bundles of afferent fibers to the brain, in birds and mammals the principal innervation of the pineal gland is efferent autonomic fibers originating in the superior c e r v i c a l ganglia of the sympathetic chain (Ralph, 1975a). *) Department of Zoology/Entomology, Colorado State University, Ft. Collins, CO 80523, USA. Studies by the author supported by NIH grants NS-08554 and NS-12257. Preser~ted during the Seventh International Biometeorological Congress, 17-23 August 1975, College Park, Maryland, USA.

290 T h i s g r e a t v a r i a t i o n m a y l e a d one to q u e s t i o n t h e c o n s t a n c y of f u n c t i o n of t h e p i n e a l a p p a r a t u s . E s p e c i a l l y , one m i g h t q u e s t i o n w h e t h e r o r not t h e p h o t o r e e e p t ive p i n e a l of l o w e r v e r t e b r a t e s i s s e r v i n g t h e s a m e r o l e a s t h e n o u - p h o t o r e e e p t i v e g l a n d u l a r p i n e a l of b i r d s and m a m m a l s . It is l i k e l y t h a t c l o s e r a t t e n t i o n to t h e d i f f e r e n c e s in p i n e a l m o r p h o l o g y and cytology m a y lead u s m o r e r a p i d l y to a b e t t e r u n d e r s t a n d i n g of w h a t f u n c t i o n s t h i s o r g a n r e g u l a t e s in t h e v a r i o u s g r o u p s of v e r t e b r a t e s . E v e n w i t h i n s o m e c l o s e l y - r e l a t e d g r o u p s , i n t r i g u i n g v a r i a t i o n s in p i n e a l m o r phology c a n be found. One s u c h i n s t a n c e t h a t h a s held s p e c i a l i n t e r e s t f o r u s i s t h e v a r i a t i o n in o c c u r r e n c e of t h e p a r i e t a l eye in l i z a r d s . P A R I E T A L EYES IN LIZARDS AND Z O O G E O G R A P H Y In a d d i t i o n t o t h e i r l a t e r a l e y e s , m a n y l i z a r d s h a v e a s m a l l " t h i r d eye" o r p a r i e t a l eye on t h e d o r s a l s u r f a c e of t h e h e a d . In i t s fully d e v e l o p e d f o r m , t h e p a r i e t a l eye h a s a c o r n e a , l e n s , and r e t i n a . T h e p a r i e t a l r e t i n a of s o m e l i z a r d s h a s b e e n d e m o n s t r a t e d to c o n t a i n p h o t o r e c e p t o r c e i l s , as well a s s u p p o r t i v e and g a n g l i o n c e i l s . In a few l i z a r d s a t r a c t l e a d i n g f r o m t h e g a n g l i o n c e l l s h a s b e e n t r a c e d ir~to t h e h a b e n u l a r g a n g l i o n . R e c o r d i n g s of e l e e t r o r e t i n o g r a m s h a v e p r o v i d e d c o n v i n c i n g e v i d e n c e f o r t h e view t h a t t h e p a r i e t a l eye i s f u n c t i o n a l (Eakin, 1973). As a p r e d o e t o r a l s t u d e n t in m y l a b o r a t o r y , Gundy b e g a n a s t u d y of t h e o c c u r r e n c e of t h e p a r i e t a l eye a m o n g t h e s e v e r a l f a m i l i e s of l i z a r d s and r e l a t e d t h e r e s u l t s to t h e i r g e o g r a p h i c a l d i s t r i b u t i o n . Some v e r y i n s t r u c t i v e f i n d i n g s h a v e e m e r g e d f r o m h i s s t u d i e s (Gundy, 1974). F i r s t , t h e o c c u r r e n c e of p a r i e t a l e y e s i s r e l a t i v e l y n o n - v a r i a b l e a m o n g g e n e r a of a f a m i l y ; all o r a l m o s t all e i t h e r h a v e o r do not h a v e a p a r i e t a l eye ( T a b l e 1). T A B L E 1.

P a r i e t a l eye o c c u r r e n c e in l i z a r d s (Gundy, R a l p h a n d W u r s t , 1975)

Infraorder

Family

P a r i e t a l eye (% g e n e r a in w h i c h v i s i b l e )

Gekkota

Gekkonidae Pygopodiae Dibamidae

Scineomorpha

Xantusiidae Anelytropsidae Seincidae Cordylidae Lacertidae Teiidae

100 0 91 - 95 100 90 0 - 3

Anguinomorpha

Va r a n i d a e Helodermatidae Lauthanotidae Anniellidae Anguidae Xenosauridae

100 0 0 100 100 100

Iguania

Iguanidae Agamidae Chameieoutidae

96 - 98 83 100

0 0 0

1

291 T h i s p a t t e r n s e e m s s t r o n g l y r e l a t e d to e v o l u t i o n a r y l i n e s at t h e f a m i l i a l l e v e l , w i t h o u t r e g a r d to t h e v a r i e t y of life m o d e s r e p r e s e n t e d w i t h i n e a c h f a m i l y . Second, t h e r e i s a d e f i n i t e r e l a t i o n s h i p b e t w e e n l a t i t u d i n a l d i s t r i b u t i o n of l i z a r d s and p a r i e t a l eye o c c u r r e n c e (Gundy, R a l p h a n d W u r s t , 1975). V i r t u a l l y all Gekkonidae and T e i i d a e , two of t h e l a r g e s t and m o s t s u c c e s s f u l l i z a r d f a m i l i e s , lack p a r i e t a l e y e s . C e n t e r s of a b u n d a n c e - g e o g r a p h i c a l l o c a t i o n s w h e r e t h e g r e a t e s t n u m b e r of g e n e r a o v e r l a p - and r a n g e s w e r e p l o t t e d f o r t h e two f a m i l i e s . G e c k o s a r e m o s t a b u n d a n t w i t h i n 10 d e g r e e of t h e e q u a t o r ( F i g . 1). F o r t e i i d s , t h e e q u a t o r i a l c o n c e n t r a t i o n i s e v e n m o r e p r o n o u n c e d ( F i g . 2).

60 ...... -,a_ ~.JSO ,o

30 20

lO

10 20 30 40

50 F i g . 1.

The new w o r l d d i s t r i b u t i o n of t h e F a m i l y G e k k o n i d a e . L a r g e n u m b e r s i n d i c a t e c e n t e r s of a b u n d a n c e a n d the n u m b e r of g e n e r a o v e r l a p p i n g t h e r e . Shaded a r e a i n d i c a t e s o n e - h a l f of m a x i m u m o v e r l a p . Heavy l i n e s i n d i c a t e r a n g e of t h e f a m i l y (Gundy, 1974).

F o r c o m p a r i s o n , Gundy d e t e r m i n e d t h e g e o g r a p h i c a l d i s t r i b u t i o n of two l a r g e and s u c c e s s f u l f a m i l i e s in w h i c h the p a r i e t a l eye i s p r e s e n t in a l m o s t all g e n e r a ; t h e A g a m i d a e and I g u a n i d a e . T h o s e a g a m i d s p o s s e s s i n g p a r i e t a l e y e s a r e m o s t a b u n d a n t 2 0 - 3 0 ° f r o m t h e e q u a t o r . T h e y r a n g e f r o m a b o u t 50ON to 45°S l a t i t u d e ( F i g , 3). L i k e w i s e , t h e i g u a n i d g e n e r a w i t h p a r i e t a l e y e s r a n g e f r o m 48ON to 55os and h a v e c e n t e r s of a b u n d a n c e at 21 ° a n d 32ON l a t i t u d e (Fig. 4). E v i d e n c e t h a t p a r i e t a l - e y e l e s s l i z a r d s a r e r e s t r i c t e d to low l a t i t u d e s i s found in t h e f a c t t h a t t h e 5 a g a m i d and one iguanid g e n e r a w h i c h l a c k p a r i e t a l e y e s a r e q u i t e e q u a t o r i a l ( T a b l e 2). All of t h e 5 a g a m i d g e n e r a h a v e t h e i r c e n t e r of a b u n d a n c e on t h e e q u a t o r and 4 of t h e 5 r a n g e no f a r t h e r t h a n 9 ° f r o m it. T h e one iguanid g e n u s h a s i t s c e n t e r of a b u n d a n c e 1 o f r o m t h e e q t m t o r . F u r t h e r m o r e , t h e c e n t e r s of a b u n d a n c e of t h e p a r i e t a l - e y e l e s s S c i n c i d a e and L a c e r t i d a e a r e c o n f i n e d to w i t h i n 10 ° of t h e e q u a t o r ( T a b l e 2).

292 60 >50 40 30 20 10

0 10 20 30

40 50

Fig. 2.

The geographical distribution of the Family Teiidae. See Fig. 1 for interpretation (Gundy, 1974). 6o

Fig. 3.

The geographical distribution of the genera of the Family Agamidae witl~ parietal eyes. See Fig. 1 for interpretation (Gundy, 1974).

293 6O

2O

10 2O 3O 40

Fig. 4.

TABLE 2.

The geographical distribution of the Family Iguanidae. See Fig. 1 for interpretation (Gundy, 1974). Latitudinal distribution of parietal eyeless genera of lizards north (+) or south (-) of the equator (Gundy, Ralph and Wurst, 1975) Group

Center of abundance (degrees)*

Range (degrees)

Parietal-eyeless Agamidae (n=5)

0

+24, - 8

Parietal-eyeless Iguanidae (n=l)

-1

+10, -12

Parietal-eyeless ScinCidae (n~--3)

-6

+13, -25

Parietal-eyeless Lacertidae (n=2)

+9.5

+10, - 4

*) Does not conform precisely with center of abundance as defined in Gundy, Ralph and Wurst (1975). In Iguanidae, indicates center of range of only one genus. In Scinidae, indicates latitudes around which the three ranges cluster, since they do not overlap. The 6 families analyzed in Gundy's study: Gekkonidae, Teiidae, Agamidae, Iguanidae, Scincidae and Lacertidae, account for nearly 2500 of the 3000 species of lizards. Thus, ig seems probable that the sample examined can be relied upon

294 t o p r e d i c t g e n e r a l t r e n d s f o r l i z a r d s a s a g r o u p . Gundy c o n c l u d e d t h a t a b s e n c e of a p a r i e t a l e y e r e s t r i c t s l i z a r d s t o low l a t i t u d e s w h i l e p o s s e s s i o n of a p a r i e t a l eye f a c i l i t a t e s s u r v i v a l at h i g h e r l a t i t u d e s . T h e t r u e s i g n i f i c a n c e of t h e s e r e s u l t s r e m a i n s to be u n d e r s t o o d , but we h a v e s p e c u l a t e d t h a t t h e p a r i e t a l e y e m a y p l a y a n i m p o r t a n t r o l e in t e m p e r a t u r e t o l e r a n c e and t h e r m o r e g u l a t i o n (Gundy, R a l p h and W u r s t , 1975). S e a s o n a l s y n c h r o n i z a t i o n of r e p r o d u c t i o n and t h e r m o r e g u l a t i o n a r e esser~tial f o r h e t e r o t h e r m s , s u c h as l i z a r d s , l i v i n g in h a r s h c l i m a t e s a t h i g h e r l a t i t u d e s . P e r h a p s t h e i n c l u s i o n of t h e p h o t o r e c e p t i v e p a r i e t a l c o m p o n e n t in t h e p i n e a l c o m p l e x f a c i l i t a t e s s u r v i v a l at h i g h l a t i t u d e s by a l l o w i n g g r e a t e r p r e c i s i o n in r e p r o d u e t i v e t i m i n g o r t h e r m o r e g u l a t o r y m o d u l a t i o n , o r both, t h u s p r o v i d i n g a c c e s s to a v a r i e t y of temperate habitats. VARIATION IN P I N E A L MORPHOLOGY The i n s i g h t p r o v i d e d by t h e z o o g e o g r a p h i c a l s t u d y of l i z a r d s h a s p r o m o t e d o u r i n t e r e s t in t h e p o s s i b i l i t y that e x a m i n a t i o n of t h e m o r p h o l o g y of t h e p i n e a l s t r u c t u r e s in o t h e r g r o u p s m a y r e v e a l c o r r e l a t i o n s w i t h c e r t a i n f e a t u r e s of t h e i r natural history. M o r p h o l o g i c a l and h i s t o l o g i c a l s t u d i e s of p i n e a l b o d i e s h a v e b e e n p u b l i s h e d f o r s e v e r a l a n i m a l s . However, t h e s e a r e , at b e s t , a v e r y s m a l l s a m p l i n g and t h e y g e n e r a l l y fail to p r o v i d e a d e q u a t e s e r i e s f o r c o m p a r i s o n s w i t h i n o r d e r s , f a m i l i e s o r o t h e r p h y l e t i c g r o u p s . F u r t h e r m o r e , t h e r e p o r t s a r e c o m m o n l y b a s e d on one o r a few s p e c i m e n s of u n s t a t e d a g e and t h e s e a s o n of t h e y e a r i s u s u a l l y not r e c o r d e d . N e v e r t h e l e s s , u s i n g p u b l i s h e d r e p o r t s , I h a v e a t t e m p t e d to c a t e g o r i z e t h e p i n e a l s of s e v e r a l d i f f e r e n t k i n d s of o r g a n i s m s by s u c h t e r m s a s r e l a t i v e l y s m a l l o r l a r g e , and r e l a t i v e l y c o m p l e x v e r s u s s i m p l e . Such a c l a s s i f i c a t i o n is r a t h e r u n s a t i s f a c t o r y b e c a u s e t h e r e a r e no a b s o l u t e s t a n d a r d s f o r c o m p a r i s o n . Some kind of r a t i o of p i n e a l to b r a i n v o l u m e would be u s e f u l in e x p r e s s i n g c o m p a r a t i v e s i z e of p i n e a l s , but t h i s c a n n o t be done on t h a b a s i s of w h a t is a v a i l a b l e in m o s t H t e r a t u r e d e s c r i p t i o n s . However, it is g e n e r a l l y a g r e e d t h a t t h e r e a r e s o m e p i n e a l b o d i e s t h a t a r e q u i t e l a r g e , and t h e r e a r e o t h e r s t h a t c e r t a i n l y m u s t be c o n s i d e r e d v e r y s m a l l . Indeed, t h e r e a r e s o m e v e r t e b r a t e s , w h i c h I will m e n t i o n l a t e r , t h a t h a v e e i t h e r a m i c r o s c o p i c a l l y s m a l l p i n e a l o r lack t h e o r g a n altogether. E s t i m a t i n g c o m p l e x i t y is e v e n m o r e d i f f i c u l t . If t h e r e i s a w e l l d e f i n e d e p i p h y s i a l body t h a t i s w e l l v a s c u l a r i z e d and shows s o m e obvious r e g i o n a l d i f f e r e n t i a t i o n o r d i s t i n c t p a r t s , e s p e c i a l l y a c c e s s o r y p a r t s s u c h a s a n end v e s i c l e f o r m i n g a n eye, I would r e g a r d it as a c o m p l e x p i n e a l . If it e x h i b i t s no u n u s u a l f e a t u r e s and a p p e a r s f a i r l y u n i f o r m t h r o u g h o u t I would c o n s i d e r it a s i m p l e p i n e a l . U s i n g t h e s e c r u d e c r i t e r i a , I h a v e ver~tured to s e e if t h e r e a r e any a p p a r e n t r e l a t i o n s h i p s b e t w e e n t h e m o r p h o l o g y of t h e few p i n e a i s t h a t h a v e b e e n d e s c r i b e d and t h e life s t y l e o r g e o g r a p h i c a l p l a c e a n d d i s p e r s i o n of o r g a n i s m s * . What will be p r e s e n t e d m u s t be r e g a r d e d a s t e n t a t i v e , fragmer~tary, and h i g h l y s p e c u l a t i v e . N o n e t h e l e s s , I hope it m a y l e a d to a c o n s i d e r a t i o n of p i n e a l o r g a n s in t h e b r o a d e r c o n t e x t of t h e p h y l e t i c a r r a y of v e r t e b r a t e s , beyond t h e f a v o r e d l a b o r a t o r y s p e c i e s w h i c h now hold a l m o s t a l l i n t e r e s t , and, e s p e c i a l l y , t o c o n s i d e r a t i o n of the p i n e a l in t h e c o n t e x t of t h e a d a p t a t i o n s t h a t o r g a n i s m s have m a d e to g e o g r a p h i c a l , c l i m a t o l o g i c a l , and m e t e o r o l o g i c a l c o n d i t i o n s .

*) T h e n a t u r a l h i s t o r y i n f o r m a t i o n and g e o g r a p h i c r a n g e s i s l a r g e l y b a s e d on : G r z i m e k ' s A n i m a l Life E n c y c l o p e d i a , Van N o s t r a n d R e i n h o l d Co:, 13 v o l s , 1972.

295 FISH In t h e c y c l o s t o m e Lampetra (Petromyzon)fluviatilis , t h e r e i s a p i n e a l c o m plex c o n s i s t i n g of p i n e a l and p a r a p i n e a l . o r g a n s . T h e 2 o r g a n s a r e s i m i l a r in structure, appearing as irregular flattened sacs with a narrow lumen. Both u p p e r and l o w e r w a l l s of e a c h o r g a n c o n t a i n p h o t o r e c e p t o r c e l l s w h o s e o u t e r s e g m e n t s p r o j e c t into t h e l u m e n . T h e r e a r e a l s o s u p p o r t i n g and p i g m e n t c e i l s m t h e r e t i n a . Young (1935) h a s s p e c u l a t e d , on t h e b a s i s of s o m e e x t i r p a t i o n e x p e r i m e n t s , t h a t t h e p i n e a l of t h e l a m p r e y i s i n v o l v e d in t h e d a i l y r h y t h m of c o l o r c h a n g e . T h u s , t h e p i n e a l c o m p l e x in t h i s a n i m a l m a y b e a m e c h a n i s m t h a t is r e s p o n s i v e to d i u r n a l light c h a n g e s . A n o t h e r c y c l o s t o m e , t h e h a g - f i s h Myxine glutinosa , is r e p o r t e d to h a v e no p i n e a l o r g a n at all ( T i l n e y and W a r r e n , 1919). Myxine is, in s e v e r a l r e s p e c t s , c o n s i d e r e d to be a v e r y d e g e n e r a t e a n i m a l . Its e y e s a r e f u n e t i o n l e s s r u d i m e n t s , a l t h o u g h ~t i s r e s p o n s i v e to c h a n g e s of i l l u m i n a t i o n . Its blood is i s o s m o t i e to s e a w a t e r . Hag'fish b u r r o w in mud, s a n d o r into t h e b o d i e s of d e a d o r dying f i s h . T h u s , t h e y would s e e m to h a v e no n e e d f o r d e t e c t i o n of d i u r n a l c h a n g e s , in c o n t r a s t to ~he m o r e f r e e - l i v i n g and a n a d r o m o u s Larnpetra . Elasmobranchii (sharks, rays, holocephalians) usually have well-developed p i n e a l s , as judged f r o m 15 s p e c i e s t h a t h a v e b e e n e x a m i n e d ( T i l n e y and W a r r e n , 1919). , Squalus acanthias h a s a t u b e - s h a p e d p i n e a l body in t h e w a l l s of w h i c h a r e s e n s o r y c e l l s ( K a p p e r s , 1965). H o w e v e r , it i s r e p o r t e d t h a t t h e r e i s a c o m p l e t e a b s e n c e of t h e p i n e a l in 2 e l e c t r i c r a y s , Torpedoocellata and T. marmorata ( T i l n e y and W a r r e n , 1919). Why t h e d i f f e r e n c e is a n i n t r i g u i n g q u e s t i o n . The T o r p e d i n i d a e a r e i n h a b i t a n t s of w a r m s e a s . Teleost fishes generally have well-developed pineal organs, commonly with t e r m i n a l v e s i c u l a r s t r u c t u r e s , p h o t o r e c e p t o r s , and c r a n i a l a n d skin m o d i f i c a t i o n s to p r o v i d e a p i g m e n t - f r e e " w i n d o w " o v e r t h e o r g a n ( B r e d e r and R a s q u i n , 1950; Murphy, 1971; O m u r a and Oguri, 1969; R i v a s , 1953). Some adult t e l e o s t s a p p a r e n t l y a l s o r e t a i n a s m a l l p a r a p i n e a l o r g a n w i t h r e c e p t o r s like t h o s e in t h e p i n e a l o r g a n (Rtideberg, 1969). R a t h e r r e m a r k a b l e d i f f e r e n c e s h a v e b e e n n o t e d in

296 It is c o m m o n l y i m p l i e d that the frontal o r g a n is a constant s t r u c t u r e in frogs and toads. Two of m y c o l l e a g u e s and I have examined, with the aid of a l o w - p o w e r m i c r o s c o p e , the d o r s u m of the head of 110 s p e c i e s f r o m a total of 13 f a m i l i e s of anurans* and, to the c o n t r a r y , we found that the frontal organ is apparent in only a v e r y few a n u r a n s . A w e l l m a r k e d pineal f o r a m e n is found in the skulls of both b r a n c h i o s a u r s and lepospondyls, indicating that the a n c e s t o r s of m o d e r n Amphibia w e r e equipped with functional t h i r d eyes (Noble, 1931). T h e r e a p p e a r s to be a c u r i o u s t r e n d toward l o s s of the frontal organ in anurans, since our s u r v e y found it p r e s e n t c o n s i s t e n t l y only in one f a m i l y : Ranidae. It was p r e s e n t in two out of the four Pipidae e x a m i n e d . In only one o t h e r family, the Rhacophoridae, r e p r e s e n t e d by a single s p e c i e s ( R]wzopk0rusleucomystax ) in our s u r v e y , did we find a frontal organ. Some a u t h o r i t i e s do not r e c o g n i z e this family, placing ~t in the Ranidae. In none of the s p e c i e s of the o t h e r ten f a m i l i e s of A n u r a did we find a frontal organ (Table 3). TABLE 3.

Distribution of pineal frontal o r :an in s o m e f a m i l i e s of Anura* No. s p e c i e s examined

Suborder I (Xenoanura) F a m i l y Rhinophrynidae (Archaic)** F a m i l y Pipidae (Archaic)

1 4

Suborder II (Soptanura) F a m i l y M i c r o h y l i d a e (Advanced)

3

Suborder IH ( L e m m a n u r a ) F a m i l y D i s c o g l o s s i d a e (Archaic) F a m i l y Ascaphidae (Archaic)

3 1

Suborder Family Family Family Family Family Family

IV (Aeosmanura) Pelobatidae (Transitional) Leptodactylidae (Advanced) Bufonidae (Advanced) Hylidae (Advanced) Ranidae (Advanced) Hyperoliidae ( s o m e t i m e s included in Ranidae) F a m i l y Rhacophoridae ( s o m e t i m e s included in Ranidae) F a m i l y Atelopodidae ( s o m e t i m e s included in Bufonidae e x c e p t genus Brachycephalus)

3 8 33 41 24

F r o n t a l organ P r e s e n t (+) o r Absent (-)

+-

+

6 1

+

5

*} C l a s s i f i c a t i o n m a i n l y based on Savage (1973). **) C a t e g o r i e s of a r c h a i c , t r a n s i t i o n a l , and advanced based on Lynch (1973). Our findings a g r e e with s o m e of the few s c a t t e r e d r e p o r t s on frontal o r g a n s in f r o g s and toads. Although a frontal organ is p r e s e n t in the l a r v a e of Hyla arborea (de Graef, 1886) and H.re~//a (Eakin, 1973}, the o r g a n is absent in the adults *) The c o l l e c t i o n at the Natural H i s t o r y Museum of the U n i v e r s i t y of Colorado, Boulder was kindly m a d e a v a i l a b l e to m e for this s u r v e y .

297 ( T i l n e y and W a r r e n , 1919). It a l s o a p p e a r e d to be a b s e n t in all of t h e 41 s p e c i e s of h y l i d s we e x a m i n e d . T h e f r o n t a l o r g a n is s a i d to be a b s e n t in Pipa snethlageae(=americana) (Pipidae) ( T i l n e y and W a r r e n , 1919). We found it m i s s i n g ih a n u n i d e n t i f i e d s p e c i e s of Pipa , but a f r o n t a l o r g a n w a s p r e s e n t i n Hemipipa carvalhoi . Both t h e s e g e n e r a a r e South A m e r i c a n . In t h e two A f r i c a n pipids e x a m i n e d , we found a f r o n t a l o r g a n in Xenopus laeves , but n o t in X.tropicalis . T h u s , in t h e a r c h a i c f a m i l y , P i p i d a e , t h e r e a p p e a r s to be l o s s of t h e t h i r d eye in s o m e genera, b o t h in t h e A f r i c a n and South A m e r i c a n s u b f a m i l i e s . A f r o n t a l o r g a n a l s o i s a p p a r e n t l y m i s s i n g in t h r e e o t h e r f a m i l i e s t h a t a r e r e g a r d e d a s a r c h a i c : R h i n o p h r y n i d a e , D i s c o g l o s s i d a e , and A s c a p h i d a e . Yet it i s p r e s e n t in t h e R a n i d a e , a n a d v a n c e d f a m i l y , but a b s e n t in all o t h e r t r a n s i t i o n a l a n d a d v a n c e d f a m i l i e s (if R h a c o p h o r i d a e is not r e c o g n i z e d ) . It i s difficult to d i s c e r n h e r e any e v o l u t i o n a r y t e n d e n c i e s . De G r a a f (1886) r e p o r t s a n e x t r a c r a n i a l e p i p h y s i a l p i e c e in two s p e c i e s of R a n i d a e , in a g r e e m e n t w i t h o u r findings, but one a l s o w a s found in two d i s c o g l o s s i d s ( Alytes obstetricans and Bombinator igneus ) and a bufonid ( Bufo dnereus ). We h a v e not e x a m i n e d t h e s e t h r e e s p e c i e s . H o w e v e r , if a f r o n t a l o r g a n is p r e s e n t in t h e s e two f a m i l i e s , it m u s t be q u i t e i n c o n s p i c u o u s e x t e r n a l l y f o r we f a i l e d to s e e a n y s i g n of it in t h e t h r e e s p e c i e s of D i s c o g l o s s i d a e and 33 s p e c i e s of B u f o n i d a e e x a m i n e d in o u r s u r v e y . We w e r e hoping t h a t t h e d i s t r i b u t i o n of t h i r d e y e s a m o n g a n u r a n s would r e v e a l s o m e z o o g e o g r a p h i c a l p a t t e r n like t h a t found by Gundy f o r l i z a r d s . Such d o e s not a p p e a r to be t h e c a s e , f o r t h e two m o s t c o s m o p o l i t a n and p o l e w a r d - e x t e n d i n g f a m i l i e s a r e B u f o n i d a e and R a n i d a e . Both f a m i l i e s a r e w i d e l y d i s t r i b u t e d f r o m c o l d to t r o p i c a l r e g i o n s . Bufonids a r e found on all m a j o r land m a s s e s e x c e p t M a d a g a s c a r , New Guinea, and A u s t r a l i a . R a n i d s a r e on all land m a s s e s e x c e p t New G u i n e a and A u s t r a l i a . The B u f o n i d a e give no i n d i c a t i o n of a f r o n t a l o r g a n ; t h e R a n i d a e h a v e a p r o m i n e n t one. T h e Hylidae, c o n t a i n i n g 33 g e n e r a , a r e w i d e l y d i s t r i b u t e d , e s p e c i a l l y in N o r t h and South A m e r i c a , and t h e y do not h a v e a f r o n t a l o r g a n . Most o t h e r f a m i l i e s a r e m o r e r e s t r i c t e d in d i s t r i b u t i o n , but s e v e r a l r a n g e to r a t h e r h i g h l a t i t u d e s , a p p a r e u t l y w i t h o u t t h e b e n e f i t of a t h i r d eye. Obviously, t h e s i g n i f i c a n c e of t h e f r o n t a l o r g a n in A n u r a r e m a i n s to be d i s c o v e r e d . It c e r t a i n l y a p p e a r s to be s e r v i n g u s e s t h a t a r e d i f f e r e n t f r o m t h e h o m o l o g o u s p i n e a l c o m p o n e n t in l i z a r d s . P e r h a p s t h i s r e f l e c t s t h e m a r k e d d i f f e r e n c e b e t w e e n t h e c o m p l e t e t e r r e s t r i a l i z a t i o n of l i z a r d s and t h e a q u a t i c d e p e n d e n c y of m o s t a n u r a n s . RE P T I L E S In a d d i t i o n to t h e v a r i a t i o n s in o c c u r r e n c e of p a r i e t a l e y e s in l i z a r d s , d e s c r i b e d above, Gundy and W u r s t (in p r e p a r a t i o n ) n o t e d s e v e r a l d i f f e r e n c e s in t h e m o r p h o logy of p i n e a l c o m p l e x e s in l i z a r d s . T h e s e i n c l u d e v a r i a t i o n s in d e g r e e of i n f o l d ing of t h e i n t r a c r a n i a l pineal, s i z e of the p a r i e t a l f o r a m e n , r e l a t i v e a m o u n t of c a r t i l a g e d e p o s i t e d o v e r t h e pineal, and p i n e a l e x t e n s i o n s t o w a r d t h e p a r i e t a l eye. T h e s e f e a t u r e s m a y be shown, t h r o u g h m o r e d e t a i l e d a n a l y s i s , to h a v e z o o g e o graphic correlations. It is c o m m o n l y a g r e e d t h a t t h e C r o c o d i l i a ( G e n e r a Crocodilus and Alligator ) h a v e no p i n e a l o r g a n (Tilney and W a r r e n , 1919; Oksche, 1965). N o t e w o r t h y is t h e f a c t t h a t t h i s o r d e r is c o n f i n e d to t r o p i c a l r i v e r s and s e a c o a s t s . T u r t l e s and s n a k e s h a v e a c o n s p i c u o u s , g l a n d u l a r p i n e a l (Oksche, 1965) and r a n g e to f a i r l y high latitudes.

298 BIRDS The pineal gland of birds is generally a relatively large structure, commonly extending dorsad from the roof of the diencephalon and expanding at its distal end just beneath the skull (Ralph, 1970). However, in two groups, the Stringiformes (owls) and Proeellariiformes (shearwaters, petrels), the pineal is notably atrophic (Quay, 1972a). These groups contain the most nocturnal avian species known. Within each of the two groups, species with the largest pineals are those that are more diurnal and those with the most atrophic pineals are the more nocturnal. Furthermore, the owls display the greatest variation among birds in pineal size or morphology, both as a group and individually. However, Quay (1972a) points out that the relation of pineal atrophy in birds with noeturnality is not obligatory, for nocturnal genera such as Apter)/x (kiwi) and Burhinus (thickknee) have large and active-appearing pineal glfinds. The pineal of the King penguin ( Aptenodytespatagonica ) is quite large - about 6 mm long- and shows cytological indications of active secretion (Breueker, 1967), but the largest known avian pineal occurs in the emu of Australia (Cobb and Edinger, 1962). It is 10 mm long and weighs i00 rag. Even on the basis of body size, the emu's pineal must be considered quite large. Emus maintain a steady body t e m p e r a t u r e (about 38°C), are seasonal b r e e d e r s and a r e diurnal foragers. MAMMALS Mammals as a group present a confusing and confounding situation with respect to pineal morphology. In Prototheria, t h e r e is the echidna ( Taehyglossus aculestus ) with a large pineal (Krabbe, Cited by Tilney and Warren, 1919) and the platypus ( Ornithorynchus ) with a v e r y small pineal (Smith, 1896). Both maintain a body t e m p e r a t u r e around 30-32oc. The echidna hibernates, but regulates body t e m p e r a t u r e fairly well when ambient t e m p e r a t u r e is between 0 and 25°C (Schraidt-Nielsen, Dawson and Crawford, 1966). The opposum (Metatheria) has a r e l a t i v e l y small, thin-walled pineal body (Jordan, 1911). This animal is commonly active after dark and may become inactive for several days during a cold period in the northern part of its range. A pineal organ is reported to be absent in several Edentata (anteater, sloth, armadillos) (Oksche, 1965; Quay, 1965). The m e m b e r s of this o r d e r tend to be nocturnal, are limited to tropical o r subtropical parts of North and South A m e r i ca, and have variable and, for a mammal, low body t e m p e r a t u r e s . The same conditions prevail for the pangolin (Pholidota) (Oksche, 1965). Very small pineals are found in Insectivora (hedgehogs and shrews) (Hillsemann, 1967; Oksche, 1965; Quay, 1965), which tend to be nocturnal. Some (especially hedgehogs) hibernate in colder parts of their range, and s e v e r a l breed throughout the year in w a r m regions. The body t e m p e r a t u r e of hedgehogs v a r i e s diurnally between 34.8 and 36.8°C. Chiroptera (bats) have r a t h e r small pineals (Quay, 1965). Many t e m p e r a t e species are hibernators and their body t e m p e r a t u r e may be highly variable. The rodents (Order Rodentia) display a remarkably great range of adaptations for many kinds of niches and should provide some v e r y interesting possibilities for study of pineal c o r r e l a t i o n s . We know m o r e about rodent pineals than for any other group, through numerous laboratory studies employing rats and h a m s t e r s ; but extremely little is known of the pineal for the multitude of rodents that are not common laboratory subjects. The common dormouse ( Glisglis ) has a v e r y small pineal body (Hiilsemann, 1967), hibernates readily, is nocturnal and has a

299 variable body t e m p e r a t u r e , The Sciuridae (squirrels) should be especially i n t e r esting in t e r m s of trying to r e l a t e hibernators v e r s u s non-hibernators, diurnal v e r s u s nocturnal behavior, or a r c t i c v e r s u s s u b - a r e t i c habitat to pineal f o r m and function. They exhibit great differences in such p a r a m e t e r s and are a diverse, numerous group with widespread geographic distributions at high latitudes. The somewhat related rabbits COrder Lagomorpha), with r a t h e r large pineals (Wartenberg and Gusek, 1964), are among the most successful of m a m m a l s , especially in the holarctic region. They are strongly diurnal and good t h e r m o regulators. The rhinoceros COrder Perissodactyla) has a v e r y small pineal (Oksche, 1965). It is mainly nocturnal, breeds throughout the year, and is confined to South Asia and parts of southern and central Africa. The horse ( E q u ~ ) , a m e m b e r of the same order, has a large pineal (Fassbender, 1962), is strongly diurnal, and is a good t h e r m o r e g u l a t o r . The Artiodactyla (pigs, camels, deer, giraffes, sheep, bovids), based on a sampling mainly of domesticated ruminants, appear to have quite large, welldeveloped pineal organs (Cutore, 1910; Tilney and Warren, 1919). This group is c h a r a c t e r i z e d by being seasonally-timed breeders, and excellent t h e r m o r e g u l a t o r s . The bovids are strongly diurnal. Many m e m b e r s of this o r d e r ( e . g . , Cervidae) are holarctic, ranging to v e r y high latitudes, as well as high altitudes. Based on a v e r y small sample, the pineal organ apparently is v e r y small or absent in the three extant o r d e r s of the Superorder Paenungulata: Hyracoidea ( Procavia=tlyrax ), l>r0boscidae (elephants), and Sirenia ( Dugong ) (Hill, 1945; Oksche, 1965). All these groups are confined to w a r m regions. Proca~a occurs in Arabia, Palestine, Syria and Africa. It has a labile body t e m p e r a t u r e and "suns" in the morning to i n c r e a s e its body t e m p e r a t u r e . Elephants are limited to Africa and tropical Asia and have a core t e m p e r a t u r e of about 20-30°C. Dugongs are r e s t r i c t e d to tropical, coastal w a t e r s . Elephants and dugongs a r e reputed to have no definite breeding season. S t e l l a r ' s sea cow (Hydromalisgig~ =H.stelleri ), an extinet m e m b e r of the Sirenia, o c c u r r e d only around certain islands in the Bering Sea. It is unfortunate that we cannot know if it had a well-developed pineal organ or not. (The same can also be said for mammoths and mastodons.) Whales (Cetaeea) either have rudimentary pineals or no deteetable pineals (Oksche, 1965). The m a r i n e environment of these wide-ranging, often m i g r a t o r y animals may net impose on them some of the thermal or hydrological limits that are encountered by t e r r e s t r i a l f o r m s . It would appear that possession of a pineal organ is not a requisite for penetration into cold marine environments, for many whales ply the arctic w a t e r s . However, the largest pineals known in m a m m a l s occur in the Pinnipedia (sea lions, seals, walruses) (Tilney and Warren, 1919). These polar m a m m a l s have a high resting metabolism - about ten t i m e s higher than manatees (Sirenia) (Scholander et al., 1950). The pineal body of the Weddell seal is differentiated into cortical and medullary regions, is highly v a s c u i a r i z e d and shows great biochemical responsiveness to v a r i e d daylength (Cuel[o and Tramezzani, 1969). The northern fur s e a l ' s large pineal is s i m i l a r l y biochemically v e r y aetive (Elden, Keyes and Marshall, 1971). GENERALIZATIONS AND SUMMARY There has been the tacit assumption throughout the foregoing that g r e a t e r size or complexity indicates g r e a t e r " i m p o r t a n c e " of the pineal organ in a functional sense. Such, of course, may not be the case, certainly not in a direct relation-

300 ship. However, it is probably sound t o assume that v e r y large pineals, or ones that c l e a r l y have differentiated component parts, have l a r g e r physiological roles than those pineals that are e x t r e m e l y small and cytologically uniform. The ext r e m e cases, where some species appear to have no pineal body, certainly must be considered as somehow functionally different f r o m those in which there are large and, apparently, vigorously active pineals. Although the correlation is obviously not a simple, straight-forward one, it appears from the survey presented here that m o r e prominent or complex pineal organs tend to be c h a r a c t e r i s t i c of v e r t e b r a t e s at higher latitudes (certain lizards, penguin pinnipeds, eervids) and small or absent pineals are m o r e c h a r a c t e r i s t i c of lower latitudes (crocodiles, endentates, pangolin, rhinocerous, elephants, dugong). There are other approximate c o r r e l a t i o n s that are not n e c e s s a r i l y related to geography. In general, s m a l l e r pineals tend to be c o r r e l a t e d with nocturnality (owls, shearwaters, petrels, edent~tes, inseetivores, bats, dormouse, rhinoceros) and l a r g e r pineals with diurnality (lizards, most birds, rabbit, horse, bovids). There is another fairly good correlation, it would seem, between pineal size and degree of homeothermy in m a m m a l s . Many of the heterothermie endotherms have ~trophic pineals (edentates, some insectivores, some bats, some rodents). There r e m a i n certain groups of animals that do not conform with these c o r r e l a tions. At present, we can f o r m no conclusions about the role of the anuran frontal organ in geographic distribution. Pineal elaboration in amphibians may be strongly influenced by their aquatic beginnings. Perhaps it is adaptive for them not to be reproductively timed p r i m a r i l y by season or t e m p e r a t u r e , but to be opportunistic in relation to the appearance of water pools. The whales and their relatives, with quite atrophic pineals, also defy Categorization. Perhaps m i g r a t o r y habits should be considered as another possible variable for c o r r e l a t i o n with pineal development. Also, the m a r i n e environment, providing t h e r m a l and hydrologic buffering, may not demand full pineal developmerit in whales. With a few troublesome exceptions such as cetaceans, it would appear that those endothermic v e r t e b r a t e s which exist in the m o r e harsh thermal environments, that maintain a constant, w a r m body t e m p e r a t u r e , and, by necessity, have a s e a s o n a l l y - l i m i t e d and synchronized reproductive pattern, tend to have welldeveloped pineal organs. Of course, a causal relationship is not proven. However, t h e r e are indications of some kind of association of thermal conditions in birds and m a m m a l s with the pineal. The pineal gland of rats exposed to low t e m p e r a ture show cytological changes indicative of stimulated activity (Miline et a l . , 1970), and that of rats exposed to high t e m p e r a t u r e s have d e c r e a s e d RNA and protein content (Nir, Hirschmann and Sulman, 1972). Pinealectomized rats are m o r e sensitive to cold than normal rats (Miline, 1969). The pineal gland of a hibernating bat is hypertrophied compared to the pineal in s u m m e r (Miline, 1971). Pinealeetomy of house sparrows results in abolition of the normal circadian rhythm of body t e m p e r a t u r e in constant darkness (Binkley, Kluth and Menaker, 1971). These few but striking observations, along with the temperature-modifying effects of melatonin, a pinea l hormone (Ralph, 1975b), c l e a r l y suggest a basic role for the pineal in adjustment of body t e m p e r a t u r e . But what of the ectotherms in such a s c h e m e ? Steyn (1961, 1966) has proposed that in lower v e r t e b r a t e s the pineal system, in conjunction with the subeommissural organ, may act as a mechanism sensing thermal and desiccation conditions, light acting as a token stimulus for both. Thus, according to Steyn, the photoreceptive pineal of lower v e r t e b r a t e s , which s e r v e s to monitor heat accumulation and w~ter loss, by token light, becomes the non-photoreeeptive, glandular pineal of the t e r r e s t r i a l v e r t e b r a t e which retains a role in th~rmoregulation and, through the subeommissural organ, in osmoregulation.

301

The pineal apparatus also may s e r v e as a biological clock, controlling diurnal rhythms, as most c l e a r l y demonstrated in the studies of house sparrows by Menaker and colleagues (Binkley, Kluth and Menaker, 1971; Menaker, 1975). A s i m i l a r role may prevail in rats, as shown by Quay (1972b). The pineal gland of hamsters, as r e v e a l e d by Reiter et al. (1975), and of f e r r e t s , as shown by Herbert (1971), plays a role in seasonal rhythms of reproduction. Thus, the pineal organ appears to s e r v e s e v e r a l different functions in different organisms. In reality, it might be acting in s e v e r a l functions in all organisms, and certain ones a r e m o r e emphasized in different organisms, depending upon the r e l a t i v e importance of the function. The pineal may somehow provide g r e a t e r precision in thermoregulation, osmoregulation, chronometry of dally or seasonal events, and other central regulatory functions. Thus, in the interpretation I am propQsing, the pineal is an evolutionarily labile organ, participating in adap-rations to environmental conditions. By being responsive, either directly by photoreception or indirectly by monitoring sympathetic nervous activity, the pineal provides g r e a t e r precision, where demanded, in detecting or anticipating environmental changes. The g r e a t e r the integrated sum of the number and degree of regulations demanded, the m o r e sophisticated will be the pineal apparatus. Where change is small and demand for adaptation is low, the pineal becomes proportionately reduced, and even eliminated. Thus, where an animal lives, how c r i t i c a l its chronometry and how highly homeostatic it is, all would be reflected in the size and complexity of its pineal apparatus, if my hypothesis has validity. ACKNOWLE DGE ME NT I thank Jan Roth, Gary Packard and Bruce Wunder for the c r i t i c a l and helpful consideration they gave to my ideas during the formulation of this work. REFERENCES BINKLEY, S., KLUTH, E. and MENAKER, M. (1971): Pineal function in sparrows: circadian rhythms and body t e m p e r a t u r e . Science, 174: 311-314. BREDER, C.M. and RASQUIN, P. (1950) : A p r e l i m i n a r y r e p o r t on the role of the pineal organ in the control of pigment cells and light reactions in recent teleost fishes. Science, 111 : 10-12. BREUCKER, H. (1967) : Vergleichende histologische Studien an der Zirbel der V'6gel. Verh. Anat. Ges. E r g . Anat. Anz., 120: 177183. COBB, S. and EDINGER, T. (1962) : The brain of the emu ( Dr0m0reusnovaehollandiae , Lath). I. Gross anatomy of the brain and pineal body. B r e v i o r a (Camb.), 170: 1-18. CUELLO, A . C . and TRAMEZZANI, J . H . (1969): The epiphysis c e r e b r i of the Weddell seal: its r e m a r k a b l e size and glandular pattern. Gen. comp. E n d o e r . , 12: 154-164. CUTORE, G. (1910) : I1 corpo pineale di alcuni m a m i f e r i . Arch. ital. Anat. E m b r i o l . , 9 : 402 and 599. De GRAAF, H.W. (1886) : Zur Anatomie und Entwicklung der Epiphyse bei Amphibien and Reptilien. Zool. Anz., 9: 191-194. EAKIN, R.M. (1973) : The Third Eye. University of California P r e s s , Berkeley. ELDEN, C . A . , KEYES, M.C. and MARSHALL, C . E . (1971): Pineal body of the northern fur seal ( Callorhinus ursinus ) : a model for studying the probable function of the mammalian pineal body. A m e r . J. vet. R e s . , 32: 639-647.

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