H E L G O L ~ N D E R M E E R E S U N T E R S U C H U N G E N H e l g o l ~ n d e r M e e r e s u n t e r s . 37, 99-112 (1984)
T u m o r f o r m a t i o n s
i n s c l e r a c t i n i a n
c o r a l s
Y. Loya 1, G. Bull 2 & M.
P i c h o n 21 D e p a r t m e n t o f Zoology, Tel A v i v University; Tel A v i v , Israel 2 D e p a r t m e n t o f M a r i n e Biology, J a m e s C o o k U n i v e r s i t y o f N o r t h Q u e e n s l a n d ;
T o w n s v i l l e , Q u e e n s l a n d 4811, A u s t r a l i a
ABSTRACT: A h i g h l y localized i n c i d e n c e of s k e l e t a l m a l f o r m a t i o n s (tumors) in the s c l e r a c t i n i a n corals Ptatygyra pini a n d P. sinensis on a n i n s h o r e f r i n g i n g reef at Cockle Bay, M a g n e t i c Island w i t h i n the G r e a t Barrier Reef p r o v i n c e is reported. T h e s e t u m o r s are typified b y a l o c a l i z e d area of i n c r e a s e d growth rate r e s u l t i n g in r o u g h l y circular p r o t u b e r a n c e s e x t e n d i n g u p to 4.5 cm a b o v e the colony's surface. In b o t h species, similar proportions of t h e i r p o p u l a t i o n s carried tumors (24.1% in 1:'. pini a n d 18.7 % in P. sinensis). Larger colonies ( > 80 cm in diameter) are at least 7 times more likely to possess tumors t h a n s m a l l e r colonies ( < 40 c m i n diameter). X - r a d i o g r a p h s of t h e s k e l e t a l malformations i n d i c a t e a p o i n t of origin, p r e s u m a b l y from a s i n g l e b u d d e d p o l y p w i t h s u b s e q u e n t , localized, a c c e l e r a t e d growth. T h e m e a n r a d i a l g r o w t h rate of t h e t u m o r o u s a r e a was 29 % g r e a t e r t h a n that of the s u r r o u n d i n g n o r m a l regions. In contrast to t h e n o r m a l tissue, the tumorous tissue e x h i b i t e d proliferation of cells, a t r o p h i e d g a s t r o d e r m a l cells a n d m e s e n t e r i a l f i l a m e n t s w h i c h w e r e larger a n d disordered in structure. T h e e n v i r o n m e n t a l c o n d i t i o n s at Cockle Bay are r e l a t i v e l y extreme with h i g h turbidity, periodic e x p o s u r e of the reef flat, a b r u p t c h a n g e s in salinity d u r i n g the wet s e a s o n a n d m e c h a n i c a l d a m a g e to corals c a u s e d b y u n p r e d i c t a b l e cyclonic storms. It is s u g g e s t e d t h a t a c o m b i n a t i o n of e n v i r o n m e n t a l stresses c o u p l e d w i t h a n i n j u r y inflicted on t h e corals are possible stimuli t h a t initiate t h e d e v e l o p m e n t of t h e s e a b n o r m a l g r o w t h t h r o u g h e i t h e r bacterial attack or the d e v e l o p m e n t of a n a b e r r a n t polyp d u r i n g tissue repair.
I N T R O D U C T I O N
I n t h e p r e s e n t s t u d y w e r e p o r t t h e o c c u r r e n c e of s k e l e t a l m a l f o r m a t i o n s i n t h e m a s s i v e m e a n d r o i d c o r a l Platygyra ( F a v i i d a e ) , o n a n i n s h o r e f r i n g i n g r e e f i n t h e G r e a t B a r r i e r R e e f p r o v i n c e . S k e l e t a l m a l f o r m a t i o n s h a v e b e e n p r e v i o u s l y d e s c r i b e d i n s o m e s c l e r a c t i n i a n c o r a l s a s n e o p l a s m s ( S q u i r e s , 1 9 6 5 a , b) o r t u m o r s ( C h e n e y , 1975). O t h e r s h a v e b e e n s h o w n t o b e g r o w t h r e a c t i o n s t o i n v a s i o n b y p a r a s i t e s ( C h e n g & W o n g , 1974), e n d o z o i c a n i m a l s ( P a t t o n , 1976) o r c o n t a c t w i t h a d j a c e n t c o r a l s ( H i l d e m a n n e t al., 1975). H o w e v e r , s o m e of t h e s t r u c t u r e s d e s c r i b e d i n t h e l i t e r a t u r e a s t u m o r s a r e a c t u a l l y h y p e r p l a s i a or u n u s u a l p r o l i f e r a t i o n s of t y p i c a l c e l l u l a r c o m p o n e n t s i n r e s p o n s e to i n j u r y or p a r a s i t i c i n v a s i o n ( S p a r k s , 1972). T u m o r - l i k e g r o w t h s h a d b e e n o b s e r v e d p r e v i o u s l y i n S c l e r a c t i n i a f r o m t h e P a c i f i c , a l t h o u g h t h e e t i o l o g y of t h e s e g r o w t h s h a s r e m a i n e d l a r g e l y o b s c u r e ( S q u i r e s , 1 9 6 5 a , b ; W h i t e , 1 9 6 5 ; S o u l e , 1 9 6 5 ; C h e n e y , 1975).
T h e a b n o r m a l g r o w t h f o r m a t i o n s d e s c r i b e d h e r e a p p e a r o n t h e s u r f a c e of t h e c o l o n y a s r o u g h l y c i r c u l a r p r o t u b e r a n c e s ( " b u m p s " ) e x t e n d i n g a b o v e t h e c o l o n y ' s s u r f a c e (Fig. 1). W e h a v e t e r m e d t h e s e b u m p s a s t u m o r s , s i n c e w e c o n s i d e r t h a t t h e y r e s u l t e d from a n i n d e p e n d e n t l o c a l i z e d a c c e l e r a t i o n of t i s s u e - g r o w t h .
100 Y. L~ya, G. Bull & M. Pich~n
Fig. 1. A colony of
Platygyra sinensis
(approximately 90 cm in diameter) emersed at spring low tide. A tumor of approximately 200 crn 2 (1% of the colony's surface area) can be seen in front of thecolony
i n f r e q u e n t a n d their a u t h e n t i c i t y h a s often b e e n q u e s t i o n e d . S q u i r e s (1965a) i n t e r p r e t e d the p r e s e n c e of 3 a b n o r m a l corallites from the o n l y k n o w n s p e c i m e n of
Madrepora
kauaiensis
as n e o p l a s i a . S i n c e tissue was not p r e s e r v e d , the a s s u m p t i o n was d e r i v e d solely from s k e l e t a l e x a m i n a t i o n . White (1965) a n d Soule (1965) p r o v i d e a l t e r n a t i v e i n t e r p r e t a t i o n s to S q u i r e s ' s u g g e s t i o n s , T h e y s u g g e s t e d that the a b n o r m a l corallites w e r e p r o d u c e d i n r e s p o n s e to some s e d e n t a r y virus, b a c t e r i u m or i n v e r t e b r a t e (White, 1965) or i n d i v i d u a l of a n o t h e r s p e c i e s g r o w i n g a t t a c h e d to the c o l o n y (Soule, 1965). S q u i r e s (1965b) d i s a g r e e d w i t h the latter i n t e r p r e t a t i o n b e c a u s e e x a m i n a t i o n of the exterior a n d i n t e r i o r of the s p e c i m e n s h o w e d no e v i d e n c e of o v e r g r o w t h b y a n o t h e r o r g a n i s m . A d d i t i o n a l l y , the s k e l e t a l e l e m e n t s of the a b n o r m a l corallites w e r e organi- cally c o n n e c t e d to the c o l o n y a n d his i n t e r p r e t a t i o n w a s that t h e y h a v e b e e n formed a s e x u a l l y b y p o l y p s l o w e r on the b r a n c h .T h e o n l y other report w e are a w a r e of c o n c e r n i n g t i s s u e t u m o r s i n s c l e r a c t i n i a n corals w a s g i v e n b y C h e n e y (1975) w h o d e s c r i b e d a t y p i c a l growths ("tumors") of the coral
Acropora formosa
i n s h a l l o w a n d p r o t e c t e d areas of the reefs of G u a m . He i n t e r p r e t e d t h e s e growths as true n e o p l a s m s , a n d n o t just h y p e r p l a s t i c r e s p o n s e s to m a c r o s c o p i c o r g a n i s m s . C h e n e y s u b j e c t e d l a r g e n u m b e r s of theAcropora
tumors to microscopic e x a m i n a t i o n , b u t d i d n o t find a n y f o r e i g n e t i o l o g i c a l a g e n t ,T u m o r f o r m a t i o n s i n s c l e r a c t i n i a n corals 101
is not yet k n o w n w h e t h e r the g r o w t h of the
Acropora
g a l l occurs solely i n r e s p o n s e to the d a m a g e c a u s e d b y g r a z i n g , or if a n o t h e r e t i o l o g i c a l a g e n t (e.g. a s e c o n d a r y i n v a d e r ) is involved.A different sort of g r o w t h a b e r r a t i o n i n s c l e r a c t i n i a n corals i n r e s p o n s e to l a r v a l t r e m a t o d e s w a s d e s c r i b e d b y C h e n g & W o n g (1974). T h e y r e p o r t e d t h e o c c u r r e n c e of p i n k i s h n o d u l e s 3 - 5 m m i n d i a m e t e r , e n c y s t e d i n p o l y p s of t h e coral
Porites
sp. i n Hawaii. T h e n o d u l e s e x t e n d e d 1-2 m m a b o v e t h e surface of t h e c o l o n y a n d c o n t a i n e d t r e m a t o d e m e t a c e r c a r i a e ofPlagioporous
sp. T h e o n l y h i s t o l o g i c a l a l t e r a t i o n s o b s e r v e d w e r e c o m p r e s s e d e p i t h e l i a l cells a n d p a v e m e n t e d cyst walls, i n the few cases w h e n the cyst h a d a p p a r e n t l y p e r f o r a t e d the g a s t r o v a s c u l a r cavity.N o n e of the a b n o r m a l g r o w t h proliferations, d e s c r i b e d so far i n the l i t e r a t u r e for s c l e r a c t i n i a n corals, r e s e m b l e d the s k e l e t a l m a l f o r m a t i o n s e n c o u n t e r e d i n
Platygyra
colonies at Cockle Bay. O u r i n i t i a l r e s e a r c h o b j e c t i v e s w e r e to q u a n t i f y t h e o c c u r r e n c e of these tumors o n corals i n the s t u d y area, s t u d y p o s s i b l e differences b e t w e e n the a b n o r m a l growths a n d a d j a c e n t n o r m a l c o l o n y parts, a n d a t t e m p t to d e t e c t p o s s i b l e causative a g e n t s to this p h e n o m e n o n .
STUDY AREA A N D M E T H O D S
T h e s t u d y w a s c a r r i e d out o n t h e reef flat of C o c k l e Bay, M a g n e t i c I s l a n d (19 ° 9' S, 146 ° 50' E), a h i g h c o n t i n e n t a l i s l a n d i n front of C l e v e l a n d Bay, a p p r o x i m a t e l y 8 k m north of T o w n s v i l l e . (For m a p of t h e T o w n s v i l l e a r e a s h o w i n g M a g n e t i c I s l a n d a n d s u r r o u n d i n g area, see Morrissey, 1980.)
E n v i r o n m e n t a l factors at C l e v e l a n d Bay a n d n e a r b y b a y s w e r e s u m m a r i z e d b y Collins (1978), Morrissey (1980) a n d Bull (1982). M o n t h l y m e a n s of surface s e a w a t e r t e m p e r a t u r e s vary from 21.8 °C i n J u l y (winter) to 31.2 °C i n J a n u a r y (summer) r e s u l t i n g i n a n a n n u a l r a n g e of 9.4 °C (Kenny, 1974). Reef flat areas show g r e a t e r v a r i a t i o n i n d i u r n a l s e a w a t e r t e m p e r a t u r e r e a c h i n g 14 °C i n m i d - w i n t e r (Morrissey, 1980). G r i g g (1972) recorded a n a n n u a l v a r i a t i o n i n s a l i n i t y from 27.1%0 to 37.1%0 for o n e station i n C l e v e l a n d Bay. D u r i n g p e r i o d s of m a x i m u m r a i n f a l l ( J a n u a r y - F e b r u a r y ) s a l i n i t i e s i n the r a n g e of 17.0 %0 to 36 %o w e r e m e a s u r e d b y C o l l i n s (1978) i n N e l l y Bay, s i t u a t e d close to Cockle Bay. W a t e r t u r b i d i t y (Secchi disc visibility) i n N e l l y Bay v a r i e s a n n u a l l y from 0.8 m to 6.5 m, with a n a v e r a g e of 1.8 m (Collins, 1978). T h e t i d a l r e g i m e for C l e v e l a n d Bay is s e m i - d i u r n a l w i t h d i u r n a l i n e q u a l i t y . S p r i n g tides a l t e r n a t e r e g u l a r l y w i t h n e a p tides. M e a n s p r i n g tide r a n g e is 2.5 m a n d the m e a n n e a p t i d e r a n g e is 0.8 m. T h e reef flat at Cockle Bay e m e r g e s p e r i o d i c a l l y for 3 to 4 h d a i l y d u r i n g s p r i n g l o w tides o n l y (Fig. 2). T h e r e is a s e a s o n a l c h a n g e i n the t i m e of o c c u r r e n c e of the d a i l y l o w - w a t e r , d u r i n g s p r i n g tides: i n s u m m e r t h e y occur at n i g h t a n d i n w i n t e r d u r i n g t h e afternoon.
102 Y. Loya, G. Bull & M. P i c h o n
Fig. 2. Emersion of reef-flat d u r i n g s p r i n g low tide at Cockle Bay, M a g n e t i c Island. Note the fiat, d e a d tops on some of the colonies. Right-colony with a tumor; s e c o n d colony from left shows
e x p e r i m e n t a l " e x t e n s i v e l e s i o n "
T h e g r o s s m o r p h o l o g y of t h e s k e l e t a l m a l f o r m a t i o n s is d e s c r i b e d o n t h e b a s i s of o b s e r v e d e x t e r n a l s k e l e t a l f e a t u r e s a n d X - r a d i o g r a p h s of s k e l e t a l s e c t i o n s . T h e X- r a d i o g r a p h s w e r e d o n e w i t h a S h i m a d z u l m f c a p a c i t o r d i s c h a r g e X - r a y u n i t , u s i n g K o d a k M i n R o r F u j i M I - N C f i l m s . S e c t i o n s of 1.0 t o 1.5 c m t h i c k n e s s c u t r a d i a l l y f r o m t h e c o l o n i e s g a v e g o o d d e f i n i t i o n of t h e a n n u a l b a n d s a n d t h e o r i e n t a t i o n of c a l i c e a x e s .
M a t e r i a l for m i c r o s c o p i c e x a m i n a t i o n w a s f i x e d i n 4 % s e a w a t e r f o r m a l i n for 24 h, r i n s e d for h a l f a n h o u r a n d t r a n s f e r r e d to 7 0 % a l c o h o l for f u r t h e r s t u d i e s . T h e s k e l e t o n w a s d e c a l c i f i e d u s i n g f o r m i c a c i d a n d s o d i u m c i t r a t e i n d i s t i l l e d w a t e r ( s e e R i n k e v i c h & L o y a , 1 9 7 7 f o r d e t a i l s ) . T h e r e m a i n i n g t i s s u e w a s p a r a f f i n e m b e d d e d , s e c t i o n e d a t 7 ~ m a n d s t a i n e d w i t h h e m a t o x y l i n a n d e o s i n o r G o m o r i t r i c h r o m e .
E x p e r i m e n t a l l e s i o n s w e r e m a d e o n s e v e r a l c o r a l s p e c i e s i n t h e e x p e r i m e n t a l p l o t , i n o r d e r to t e s t t h e p o s s i b i l i t y t h a t t h e a b n o r m a l g r o w t h s d e v e l o p e d a s a r e s u l t of m e c h a n i c a l d a m a g e . W e m a d e 2 s e r i e s of c i r c u l a r l e s i o n s o n d i f f e r e n t c o l o n i e s , I n b o t h s e r i e s , t h e t i s s u e a n d s k e l e t o n w e r e d a m a g e d u s i n g a h a m m e r a n d c h i s e l . T h e f i r s t s e r i e s c o n s i s t e d of 12 t o 140 c m ~ l e s i o n s w i t h a v e r a g e d e p t h of 0.4 c m ( " s u p e r f i c i a l l e s i o n s " ) . T h e s e c o n d s e r i e s c o n s i s t e d of l e s i o n s of s i m i l a r s i z e , b u t t h e a v e r a g e d e p t h of t h e w o u n d w a s 1.5 c m ( " e x t e n s i v e l e s i o n s " ) .
R E S U L T S
T u m o r f o r m a t i o n s i n s c l e r a c t i n i a n c o r a l s 103
of t u m o r s i n n e a r b y r e e f s o r e l s e w h e r e d u r i n g s u r v e y s of a l a r g e n u m b e r of r e e f f l a t s of t h e G r e a t B a r r i e r R e e f . T h e t u m o r s e x t e n d u p t o 4.5 c m f r o m t h e c o l o n y ' s s u r f a c e . T h e o r i e n t a t i o n a n d l e n g t h of t h e m e a n d e r s ( v a l l e y s ) c o m p a r e d w i t h a d j a c e n t h e a l t h y a r e a s is d i s t i n c t l y a l t e r e d ( F i g s 3, 4). T h e m e a n d e r s w i t h i n t h e t u m o r s a r e u s u a l l y s h o r t e r w i t h s m a l l e r n u m b e r s of m o u t h s p e r v a l l e y (Fig. 3). I n s o m e c a s e s , t h e t h e c a l w a l l s w i t h i n t h e
Fig. 3. Close-up of a t u m o r from t h e colony s h o w n in F i g u r e 1. Note t h e c h a n g e in l e n g t h a n d orientation of m e a n d e r s (valleys) w i t h i n the tumorous area c o m p a r e d w i t h its e d g e s a n d a d j a c e n t
n o r m a l areas
t u m o r o u s a r e a a r e m u c h t h i c k e r t h a n n o r m a l t h e c a e (Fig. 5). T h e v a l l e y s o n t h e b o u n d a r y b e t w e e n t h e t u m o r o u s a r e a a n d a d j a c e n t n o r m a l a r e a a r e c o n d e n s e d a n d d i f f e r i n t h e i r m o r p h o l o g y b o t h f r o m t h e a b n o r m a l a n d n o r m a l m e a n d e r s , A l t h o u g h v a l l e y s a r e n o t c o n t i n u o u s a c r o s s t h e b o u n d a r y b e t w e e n a b n o r m a l a n d n o r m a l a r e a s , s e p a r a t i o n is o n l y b y a n o r m a l t h e c a l w a l l . V e r o n e t el. (1977) i n d i c a t e d t h a t t h e n u m b e r s of m o u t h s or c e n t e r s p e r v a l l e y a r e v a r i a b l e i n b o t h P. p i n i a n d P, sinensis. A l t h o u g h d i f f e r e n t i n t h e i r m o r p h o l o g y , t h e v a l l e y g r o w t h f o r m s w i t h i n t h e t u m o r o u s a r e a s a n d i n t h e n o r m a l p a r t s of t h e c o l o n i e s , a r e b o t h w i t h i n a r a n g e a c c e p t a b l e for t h e s p e c i e s ,
1 0 4 Y. L o y a , G . B u l l & M . P i c h o n
Fig. 4. C l o s e - u p of a t u m o r o n a c o l o n y of
Platygyra pini.
N o t e t h e u n u s u a l l y t h i c k a n d l a r g e t h e c a l w a l l s of t h e t u m o r o u s a r e aT u m o r f o r m a t i o n s i n s c l e r a c t i n i a n c o r a l s 105 Table 1. F r e q u e n c y of skeletal malformations (tumors) in massive corals {with m e a n d i a m e t e r :>25
cm) in a 700 m 2 reef-flat area (standard deviations of coral sizes are g i v e n in p a r e n t h e s e s )
Species Total No. of No. of Coral size (Dc) in cm
colonies colonies w i t h o u t w i t h
with tumors tumors tumors
Platygyrapini 108 26 61.3 (29.4) 87.3 (26.4)
P. sinensis 64 12 48.4 (22.9) 67.6 (26.4)
Symphylliarecta 55 0 65.2 (24.8) -
Lobophyllia hemprichi 5 0 59.3 (24.7) -
Poritessp. 3 0 74.0 (35.0) -
Platygyra daedalea 2 0 2 9 . 5 (3.0) -
Favia favus 1 0 3 5 . 0 -
A n a n a l y s i s o f t u m o r i n c i d e n c e a s a f u n c t i o n o f c o r a l s i z e ( g e o m e t r i c m e a n d i a m e t e r } is g i v e n i n F i g u r e 6 f o r P. plni a n d i n F i g u r e 7 f o r P. sinensis. A s s i z e i n c r e a s e s , c o l o n i e s w i t h a b n o r m a l g r o w t h s r e p r e s e n t a n i n c r e a s i n g p r o p o r t i o n o f t h e t o t a l . I n b o t h s p e c i e s t h e h i g h e s t p r o p o r t i o n of t u m o r s w a s f o u n d i n c o l o n i e s o f 81 to 100 c m i n d i a m e t e r . A p p r o x i m a t e l y 50 % of a l l Platygyra c o l o n i e s > 80 c m i n d i a m e t e r h a v e a t l e a s t o n e t u m o r f o r m a t i o n . I n s m a l l Platygyra c o l o n i e s { 2 5 - 4 0 c m d i a m e t e r } , t h e i n c i d e n c e o f a b n o r m a l g r o w t h s is 0 % i n P. pini a n d 6.6 % i n P. sinensl$. T h u s , l a r g e r c o l o n i e s
30
==
c ,
S
O O z
25
20
15
10
P
b
J
b
I 2 5 - 4 0m
i
41 - 6 0 M E A N
6 1 - 8 0 8 1 - 1 0 0 1 0 1 - 1 2 0 1 2 1 - 1 4 0 > 1 4 0 D I A M E T E R O F C O L O N I E S
(cm)
Fig. 6. Frequency of tumor occurrence in different size classes (geometric m e a n diameter) of
106 Y. Loya, G. Bull & M. P i c h o n 30
25
2O
z
S
0
==
10
I
2 5 - 4 0
MEAN
41-60 61-80 81-100 >100
DIAMETER OF COLONIES ( c m }
Fig. 7. Frequency of tumor occurrence in different size classes of Platygyra sinensis. See Figure 6 for explanation
(> 80 c m in d i a m e t e r ) are at l e a s t 7 t i m e s m o r e l i k e l y to p o s s e s s t u m o r s t h a n s m a l l e r c o l o n i e s ( < 40 c m in diameter}. N o t u m o r s w e r e d e t e c t e d in v e r y s m a l l c o l o n i e s {e.g. < 25 c m in d i a m e t e r ) . M e a n s i z e s of t u m o r s on P. p i n i w e r e Dt = 11.6 _ 7.6 c m (n = 26) a n d o n P. s i n e n s l s Dt = 13.2 __ 10.6 c m (n = 19}. O n l y o n e t u m o r p e r c o l o n y w a s r e c o r d e d in P. s l n e n s i s w h e r e a s in P. p l n i t h e r e w e r e s o m e c o l o n i e s w i t h m o r e t h a n o n e t u m o r (one c o l o n y h a d 4 tumors, 4 c o l o n i e s h a d 2 t u m o r s a n d the rest h a d 1 t u m o r each}.
T h e r e is n o s i g n i f i c a n t d i f f e r e n c e in t h e a v e r a g e c o l o n y size c a r r y i n g a b n o r m a l g r o w t h s b e t w e e n P. p i n i a n d P. s i n e n s i s (t-test, p > 0.05). C a l c u l a t i o n of t h e ratio b e t w e e n t h e s u r f a c e a r e a of t h e t u m o r a n d t h e surface a r e a of its c o l o n y r e v e a l s that in P. s i n e n s i s t h e t u m o r o u s a r e a o c c u p i e s a n a v e r a g e of 1.2 % of t h e c o l o n y ' s surface area, w h i l e in P. p i n i it is o n l y 0.6 %. N o s i g n i f i c a n t c o r r e l a t i o n w a s f o u n d b e t w e e n t h e sizes of t u m o r s (Dt) a n d t h e s i z e s of c o l o n i e s (Dc) o n w h i c h t h e y o c c u r r e d .
T u m o r f o r m a t i o n s i n s c l e r a c t i n i a n c o r a l s 107
Fig. 8. X-radiograph of a section of
Platygyra pini
(actual size) with annual growth bands. Normal part of the colony (left); tumorous part (right)m e a n r a d i a l g r o w t h r a t e of a b n o r m a l s k e l e t o n s w a s 29 % g r e a t e r t h a n t h a t of n o r m a l areas ( r a n g e 2 0 - 4 1 % , T a b l e 2). O b s e r v a t i o n of r a d i a l l i n e s of c a l i c e a x e s i n d i c a t e t h a t the t u m o r s a l s o h a v e a g r e a t e r c i r c u m f e r e n t i a l g r o w t h r a t e t h a n t h e r e s t of t h e i r c o l o n i e s , causing a b u n c h i n g u p of n o r m a l c a l i c e s at t h e p e r i p h e r y . In n o n e of t h e X - r a y e d colonies w a s t h e r e a n y i n d i c a t i o n of i n f a u n a l i n v a s i o n , or r e g r o w t h a f t e r d e a t h or d a m a g e at t h e p o i n t s of o r i g i n of t h e t u m o r s .
108 Y. Loya, G. Bull & M. P i c h o n
Table 2. Skeletal growth rate in abnormal areas vs adjacent normal areas of different Platygyra colonies. Age (years) represents the number of annual growth bands over which the growth
increment was measured
Age (years) Radial growth (ram) Percent increase in
Normal area Tumor growth of tumor
18 122 167 36.9
20 127 159 25.2
10 81 97 19.8
5 28 34 21.4
5 36 51 41.7
f i l a m e n t s a p p e a r e d larger, m o r e d i s o r d e r e d in s t r u c t u r e a n d m o r e b r a n c h e d t h a n the n o r m a l ones. T h e g a s t r o d e r m a l c e l l s l i n i n g t h e c a l i c o b l a s t i c e p i t h e l i u m w e r e r e d u c e d in size (atrophied), w i t h v a c u o l a t e d a n d u n e v e n a p p e a r a n c e c o m p a r e d w i t h t h e n o r m a l tissues. A d e t a i l e d S E M s t u d y of t h e c e l l u l a r c o m p o n e n t s of t h e t u m o r o u s t i s s u e s is in p r o g r e s s (Loya et al., in prep.). T h e c a l i c o b l a s t i c l a y e r s a n d z o o x a n t h e l l a e d e n s i t i e s w e r e s i m i l a r a n d t h e r e w a s no e v i d e n c e of i n f a u n a or p a r a s i t e s in t h e a b n o r m a l areas. D e v e l o p i n g o o c y t e s w e r e p r e s e n t i n t h e s a m p l e s of b o t h t h e n o r m a l a n d t u m o r o u s areas, in 3 of t h e 4 c o l o n i e s of P. pini e x a m i n e d in J u l y 1981. E x a m i n a t i o n of tissue sections from b o u n d a r i e s b e t w e e n n o r m a l a n d a b n o r m a l a r e a s s h o w e d c o m p l e t e tissue fusion, w i t h n o i n d i c a t i o n s of a l l o g r a f t m o r p h o l o g y . F u r t h e r m o r e , d i s t u r b a n c e d e s i g n e d to e l i c i t t e n t a c u l a r c o n t r a c t i o n r e s u l t e d in a c o n t i n u o u s w a v e of r e a c t i o n t h r o u g h b o t h a b n o r m a l a n d n o r m a l r e g i o n s .
A l l c o l o n i e s in t h e a r e a a r e p e r i o d i c a l l y e x p o s e d to air at s p r i n g l o w t i d e s and, as a result, m a n y h a v e flat, d e a d tops (Fig. 2). T h e p r e v a i l i n g w i n d s e n t e r i n g C l e v e l a n d Bay are e a s t e r l y or s o u t h e a s t e r l y for m o s t of t h e y e a r a n d a n e a s t e r l y s w e l l is u s u a l l y present. N e v e r t h e l e s s , t h e c o m p a s s a n g l e s to w h i c h t h e t u m o r s f a c e d s h o w e d no s i g n i f i c a n t g r o u p i n g w i t h r e s p e c t to d i r e c t i o n ( R a y l e i g h - t e s t , p > 0.05).
T u m o r f o r m a t i o n s i n s c l e r a c t i n i a n corals 109 D I S C U S S I O N
A b n o r m a l s k e l e t a l growths (tumors) of
Platygyra pini
a n dP. sinensis
i n C o c k l e Bay are typified b y l o c a l i z e d a n d i n c r e a s e d s k e l e t a l growth. T h e t u m o r s e x t e n d out of the colony's surface a n d differ i n t h e i r m o r p h o l o g y from s u r r o u n d i n g n o r m a l r e g i o n s (Figs 3-5). T h e X - r a d i o g r a p h s i n d i c a t e t h a t t h e t u m o r s o r i g i n a t e i n o n e s m a l l a r e a of t h e colony (Fig. 8), p r e s u m a b l y from a s i n g l e polyp, w h i c h d i v i d e s to g i v e rise to the a b n o r m a l growth p r o t u b e r a n c e o n t h e colony. This p r o l i f e r a t i o n is i n d e p e n d e n t a n d faster t h a n the n o r m a l rate of s k e l e t a l g r o w t h of the s u r r o u n d i n g coral a r e a s (Fig. 8). W h e t h e r the faster g r o w t h of t u m o r s d e s c r i b e d h e r e results from n u t r i e n t s d r a w n from n e a r b y n o r m a l tissue, as s u g g e s t e d b y C h e n e y (1975) forAcropora formosa
r e m a i n s to b e shown. To date w e h a v e n o t o b s e r v e d a n y a d v e r s e effects of t h e t u m o r s o n t h ePlatygyra
colonies.A l t h o u g h s k e l e t a l m a l f o r m a t i o n s h a v e b e e n p r e v i o u s l y d e s c r i b e d i n a v a r i e t y of s c l e r a c t i n i a n corals, n o n e fall w i t h i n a n y of A n t o n i u s ' s (1981a) c a t e g o r i e s of coral diseases. A n t o n i u s (1981a, b) d i s t i n g u i s h e d 4 different coral diseases: ( a ) " B a c t e r i a l infections": Bacteria d e v e l o p o n m u c u s s e c r e t e d b y t h e corals i n r e s p o n s e to e n v i r o n - m e n t a l p e r t u r b a t i o n . T h e i n c r e a s e d b a c t e r i a l activity r e d u c e s the l e v e l of d i s s o l v e d o x y g e n at the surface of the coral to zero, r e s u l t i n g i n its death. (b) "Black b a n d d i s e a s e " : A l t h o u g h the m a c r o s c o p i c a p p e a r a n c e of the d i s e a s e is s i m i l a r (a d a r k b a n d s u r r o u n d i n g a n d c o n s t a n t l y e n l a r g i n g a n a r e a of d e n u d e d coral skeleton), its m i c r o b i o l o g i c a l n a t u r e a n d etiology h a v e r e m a i n e d l a r g e l y o b s c u r e (see A n t o n i u s 1973, 1977, 1981a; G a r r e t & Ducklow, 1975; D u c k l o w & Mitchell, 1979b). T h e coral tissue is d e s t r o y e d at a rate of several c e n t i m e t e r s p e r w e e k . W h i l e s m a l l c o l o n i e s are k i l l e d i n this w a y w i t h i n days or weeks, i n l a r g e c o l o n i e s the i n f e c t i o n s h a v e a t e n d e n c y to d i s a p p e a r . (c) " W h i t e b a n d disease": A p p e a r s as a n i n t e r f a c e across a coral colony, s e p a r a t i n g l i v i n g t i s s u e from white skeleton, a d v a n c i n g u p to s e v e r a l m i l l i m e t e r s p e r d a y (no p a t h o g e n h a s b e e n found yet). ( d ) " S h u t - d o w n r e a c t i o n " : A complete, s p o n t a n e o u s d i s i n t e g r a t i o n of the coral tissue, i n r e s p o n s e to c o n s i d e r a b l e e n v i r o n m e n t a l stress.
T h e X - r a d i o g r a p h s a n d h i s t o l o g i c a l s e c t i o n s of
Platygyra
from C o c k l e Bay h a v e n o t s h o w n a n y i n d i c a t i o n s of i n f a u n a or p a r a s i t e s a s s o c i a t e d w i t h t h e t u m o r formations. Therefore, the i n i t i a t i o n of t h e s e a b n o r m a l g r o w t h s c a n n o t b e a t t r i b u t e d to a v i s i b l e foreign agent. T h e p o s s i b i l i t y r e m a i n s that virus or b a c t e r i a l attack m i g h t h a v e c a u s e d a b n o r m a l d e v e l o p m e n t . G a r r e t & D u c k l o w (1975) a n d D u c k l o w & M i t c h e l l (1979b) h a v e c h a r a c t e r i z e d d e g e n e r a t i v e d i s e a s e s of b a c t e r i a l o r i g i n i n s c l e r a c t i n i a n corals from the A t l a n t i c a n d i m p l i c a t e d such d i s e a s e s as s i g n i f i c a n t c a u s e s of coral mortality, b u t t h e y did not report a b n o r m a l growth i n these corals.It is p o s s i b l e that the s t i m u l u s i n i t i a t i n g the l o c a l i z e d a c c e l e r a t e d g r o w t h of the t u m o r s o r i g i n a t e d from a g i v e n c o m b i n a t i o n of e n v i r o n m e n t a l stresses p o s s i b l y c o u p l e d with some sort of i n j u r y i n f l i c t e d o n t h e corals. T h e e n v i r o n m e n t a l c o n d i t i o n s i n C o c k l e Bay are r e l a t i v e l y e x t r e m e w i t h h i g h t u r b i d i t y , p e r i o d i c a l e x p o s u r e of t h e reef flat d u r i n g spring low tides, a b r u p t c h a n g e s i n s e a - w a t e r s a l i n i t y d u r i n g the w e t s e a s o n a n d m e c h a n i c a l d a m a g e to corals c a u s e d p e r i o d i c a l l y b u t u n p r e d i c t a b l y b y e x t e n s i v e cyc- lonic storm surge a n d w a v e action.
110 Y. Loya, G. Bull & M. P i c h o n
i n c i d e n c e of a l g a l t u m o r s i n t h e g o r g o n i a n p o p u l a t i o n s o b s e r v e d b y t h e a u t h o r s at B o n a i r e a n d T r i n i d a d w a s h i g h l y l o c a l i z e d a n d c l e a r l y n o n - u n i f o r m . A l l t h e i r o b s e r v a - tions of t u m o r s in
G. ventalina
o c c u r r e d at reefs m a n i f e s t l y e x p o s e d to e n v i r o n m e n t a l stress (e.g. h i g h l y l o c a l i z e d storm d a m a g e or c h r o n i c e x p o s u r e to c o n d i t i o n s of low s a l i n i t y a n d h i g h t u r b i d i t y ) , T h e h i g h l y l o c a l i z e d o c c u r r e n c e of a b n o r m a l g r o w t h s inPlatygyra
c o l o n i e s at C o c k l e Bay a n d t h e e n v i r o n m e n t a l s t r e s s e s e n c o u n t e r e d in this l o c a l i t y , c l o s e l y r e s e m b l e t h e p a t t e r n a n d d i s t r i b u t i o n of e n v i r o n m e n t a l c o n d i t i o n s r e p o r t e d b y M o r s e et al. (1977) forG. ventalina.
M o r s e et al. (1981) s u g g e s t e d t h a t this n o n - u n i f o r m d i s t r i b u t i o n m a y r e f l e c t e i t h e r a d e p e n d e n c e u p o n some, as yet, u n i d e n - t i f i e d e n v i r o n m e n t a l or e c o l o g i c a l factor(s) c o n t r o l l i n g i n f e s t a t i o n a n d t u m o r i g e n e s i s , or g e n e t i c a l l y d e t e r m i n e d d i f f e r e n c e s in c l o n a l s e n s i t i v i t y or r e s i s t a n c e a m o n g p o p u l a t i o n s of t h e g o r g o n i a n .T h e s e r i e s of e x p e r i m e n t a l l e s i o n s i n f l i c t e d o n
Platygyra
c o l o n i e s w e r e d e s i g n e d to test t h e i n f l u e n c e of p h y s i c a l i n j u r y on t h e r a t e a n d form of r e g e n e r a t i o n . N o n e of t h e c o r a l s in t h e " s u p e r f i c i a l l e s i o n " s e r i e s p r o d u c e d a b n o r m a l g r o w t h formations, d u r i n g 3 m o n t h s in w h i c h t h e y fully r e c o v e r e d . As n o t e d b e f o r e , f i l a m e n t o u s a l g a e c o l o n i z e d t h e e x p e r i m e n t a l s c a r s 3 to 4 w e e k s a f t e r i n f l i c t i o n of t h e lesions. P h a g o c y t i c a m o e b o c y t e s a r e k n o w n to r e s p o n d to i n v a s i o n of f o r e i g n m a t e r i a l in c o e l e n t e r a t e s (Sparks, 1972) a n d a r e i n v o l v e d in w o u n d r e p a i r a n d r e g e n e r a t i o n ( P a t t e r s o n & Landolt, 1979). F u r t h e r m o r e , t h e y h a v e b e e n i m p l i c a t e d i n m o r p h o g e n e t i c c o n t r o l of t i s s u e d i f f e r e n t i a t i o n (Prey, 1968; in M o r s e et al., 1977). It is, therefore, p o s s i b l e t h a t d e v e l o p m e n t of a n a b e r r a n t p o l y p , g i v i n g r i s e to a b n o r m a l growth, m a y b e m o r e l i k e l y to o c c u r d u r i n g t h e p r o c e s s of tissue r e p a i r , t h a n d u r i n g n o r m a l g r o w t h of u n i n j u r e d t i s s u e . S i n c e t h e " e x t e n s i v e l e s i o n s " h a d not c o m p l e t e l y h e a l e d d u r i n g t h e 12 m o n t h s of t h e s t u d y , it is p r e m a t u r e to d r a w a n y c o n c l u s i o n s on t h e i r e v e n t u a l o u t c o m e .A n o t h e r p o s s i b i l i t y , a l t h o u g h of l e s s e r l i k e l i h o o d , is t h a t t h e
Platygyra
p o p u l a t i o n at C o c k l e B a y is g e n e t i c a l l y i s o l a t e d a n d h a s t h e p o t e n t i a l to p r o d u c e t u m o r s e i t h e r s p o n t a n e o u s l y , b y s i n g l e p o l y p m u t a t i o n , or t h r o u g h t h e a c t i o n of m u t a g e n i c a g e n t such a s U.V., d u r i n g l o w tide. T r o p i c a l r e g i o n s a r e k n o w n to h a v e a h i g h i n c i d e n c e of n e o p l a s t i c s k i n g r o w t h in m a m m a l s , d u e to t h e h i g h l e v e l of U.V. i r r a d i a t i o n ( U r b a c h et al., 1974; L a d d s & E n t w i s t l e , 1977).G o l d b e r g & M a k e m s o n (1981) r e p o r t e d a t u m o r o u s c o n d i t i o n a f f e c t i n g t h e s k e l e t o n of t h e g o r g o n i a n coral
Pseudoplexaura
sp. T h e i n c i d e n c e of i n f e c t e d c o l o n i e s , w h i l e not strictly d e n s i t y d e p e n d e n t w a s a s s o c i a t e d w i t h p a t c h r e e f a r e a s w h e r e t h e coral d e n s i t i e s w e r e g r e a t e r t h a n 0.7 p e r m 2. T h e t u m o r c o n s i s t e d of m a s s e s of f i l a m e n t o u s g r e e n a l g a e t h a t s e p a r a t e d t h e n o r m a l l y t i g h t l y o p p o s e d l a m i n a e of t h e g o r g o n i a n s k e l e t o n . T h e axis e p i t h e l i u m w a s f o u n d to b e a n a p l a s t i c a n d a p p a r e n t l y d i s f u n c t i o n a l . A n a b n o r m a l p r o l i f e r a t i o n of m e s o g l e a l a m o e b o c y t e s a n d a x i a l s t e m c a n a l s w a s also noted. The a u t h o r s i n d i c a t e d t h a t l a r g e rPseudoplexaura
c o l o n i e s ( > 80 c m high) a r e 2.5 t i m e s as l i k e l y to p o s s e s s t u m o r s as s m a l l e r i n d i v i d u a l s .R e c e n t l y , B a k (1983) r e p o r t e d a n a b n o r m a l p r o c e s s of calcification, s u c h as r e g e n e r a t i n g l e s i o n s a n d n e o p l a s i a s i t u a t e d n e a r t h e t i p s of c o l o n i e s of
Acropora
palmata,
w h i c h s u p p r e s s e d n o r m a l l i n e a r growth. B r a n c h e s h a v i n g n e o p l a s i a at a l a r g e r d i s t a n c e t h a n 25 c m from t h e tip d i d not g r o w s i g n i f i c a n t l y d i f f e r e n t l y from controls. H e i n t e r p r e t e d this a s i n d i c a t i o n of a f u n c t i o n a l m i n i m a l a r e a t e r m s of e n e r g y s u p p l y .T u m o r f o r m a t i o n s i n s c l e r a c t i n i a n c o r a l s 111 t u m o r s is of i n t e r e s t , s i n c e s i z e is m o s t p r o b a b l y c o r r e l a t e d w i t h a g e , a s s h o w n for o t h e r s c l e r a c t i n i a n c o r a l s (Loya, 1 9 7 6 b ) . T h e P l a t y g y r a c o l o n i e s a t C o c k l e B a y w e r e t h e l a r g e s t w e h a v e e n c o u n t e r e d a m o n g s t p o p u l a t i o n s of h i g h a b u n d a n c e , o n t h e r e e f f l a t s of t h e G r e a t B a r r i e r R e e f {Fig. 2). S o m e c o l o n i e s w e r e u p t o 120 c m i n d i a m e t e r . T h e i n c i d e n c e of a b n o r m a l g r o w t h s w i t h i n p o p u l a t i o n s of b o t h P. p i n i a n d P. s i n e n s i s i s a t l e a s t 7 t i m e s h i g h e r i n o l d e r c o l o n i e s ( > 8 0 c m i n d i a m e t e r ) t h a n i n y o u n g e r c o l o n i e s ( < 4 0 c m i n d i a m e t e r ) , T h i s m a y e x p l a i n t h e l o w o c c u r r e n c e , o r a l m o s t c o m p l e t e a b s e n c e of s u c h a b n o r m a l g r o w t h s i n o t h e r l o c a l i t i e s i n t h e v i c i n i t y of M a g n e t i c I s l a n d o r o t h e r r e e f f l a t s o n t h e G r e a t B a r r i e r R e e f , w h e r e t h e v a s t m a j o r i t y of P l a t y g y r a c o l o n i e s a r e v e r y s m a l l . It is l o g i c a l to a s s u m e t h a t o l d e r c o l o n i e s h a v e h a d a h i g h e r c h a n c e of e n c o u n t e r i n g t h e e x a c t c o m b i n a t i o n of e n v i r o n m e n t a l c o n d i t i o n s i n d u c t i v e t o t h e d e v e l o p m e n t of s u c h t u m o r s . F u r t h e r m o r e , l a r g e r c o l o n i e s a r e e x p o s e d for l o n g e r p e r i o d s of t i m e d u r i n g s p r i n g l o w t i d e s , h e n c e t h e y p r o d u c e l a r g e a m o u n t s of m u c u s a s a p r o t e c t i v e l a y e r . A n i n c r e a s e d r a t e of m u c u s p r o d u c t i o n a l s o o c c u r s i n r e s p o n s e t o s e d i m e n t a t i o n o r h i g h t u r b i d i t y { H u b b a r d & P o c o c k , 1972; L o y a , 1 9 7 6 a ; D o d g e & V a i s n y s , 1977), w h i c h a r e e n v i r o n m e n t a l s t r e s s e s t h a t t y p i f y C o c k l e B a y . D u c k l o w & M i t c h e l l ( 1 9 7 9 a ) i n d i c a t e d t h a t b a c t e r i a l p o p u l a t i o n s i n c o r a l m u c u s r e s p o n d t o s t r e s s e s a p p l i e d to t h e h o s t c o r a l b y h i g h e r p o p u l a t i o n l e v e l s i n t h e m u c u s . It s t i l l r e m a i n s t o b e s h o w n w h e t h e r s p e c i f i c b a c t e r i a d e v e l o p o n t h e m u c u s s e c r e t e d b y P l a t y g y r a , w h i c h m i g h t c a u s e l o c a l d a m a g e { d e a t h ) of p a r t of t h e c o l o n y a n d i n d u c e d e v e l o p m e n t of a b n o r m a l g r o w t h , d u r i n g t h e r e g e n e r a t i o n p r o c e s s of t h e t i s s u e .
A c k n o w l e d g e m e n t s . We are grateful to C. Wilkinson, C, Wallace, a n d I. P a p e r n a for t h e i r h e l p f u l comments on the m a n u s c r i p t a n d e s p e c i a l l y to P. Yevich a n d E. Peters for t h e i r h e l p w i t h the histopathological i n t e r p r e t a t i o n of the samples. Y. L. is i n d e b t e d to the Q u e e n E l i z a b e t h F e l l o w s h i p C o m m i t t e e for financial support d u r i n g his stay in A u s t r a l i a as a S e n i o r Q u e e n ' s Fellow a n d to the A u s t r a l i a n Institute of M a r i n e Science a n d J a m e s Cook U n i v e r s i t y of N o r t h Q u e e n s l a n d for hospitality a n d p r o v i d i n g facilities.
L I T E R A T U R E C I T E D
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