Borchet R. Water Status and Development of Tropical Trees During Seasonal Drought

8/12/2019 Borchet R. Water Status and Development of Tropical Trees During Seasonal Drought

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Trees (1994) 8:115-125

9 Springer-Verlag 1994

a te r s ta tu s and dev e lop m en t o f t rop ica l t r eesd u r i n g s ea so n a l d r o u g h t

R o l f B o r c h e r t

Department of Physiology and Cell Biology, University of Kansas, Haworth Hall, Lawrence KS 66 045-2106, USA

Received November 11, 1992/April 14, 1993

Su mm ar y. Bud break, shoot growth and flowering of treesinvolve cell expansion, known to be inhibited by moderatewater deficits. In apparent contradiction to physiologicaltheory, many trees flower or exchange leaves during the6 month-long, severe dry season in the tropical dry forestof Guanacaste, Costa Rica. To explore this paradox,changes in tree water status during the dry season weremonitored in numerous trees. Water potent ial of stem tis-sues (tlJstem) was obtained by a modifica tion of the pressurechamber technique, in which xyl em tension was releasedby cutting defoliated branch samples at both ends. Duringthe early dry season twigs bearing old, senescent leavesgenera lly had a low le af water potential (Wleaf), while t J s t emvaried with wate r availability. At dry sites, Wstem was very

low in hardwood trees (-0.2 MPa) in lightwood trees storing water with osmoticpotentials between -0.8 and -2.1 MPa. At moist sites treesbearing old leaves rehydrated during drought; their Wstemincreased from low values (


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Fi g . 1 . A n n u a l v a r i a t i o n i n w a t e r c o n t e n t o f b a rk a n d w o o d o fPopulusdeltoides and S alixfragilis( r e d r a w n f r o m G i b b s 1 9 5 8 )

M e a s u r e m e n t o f s e a so n a l c h a n g e s i n t h e w a t e r st a tu s o ft r o p i c a l t r e e s p r e se n t s a d d i t i o n a l p r o b le m s , wh ic h d o n o ta r is e i n t e m p e r a t e t r e e s a n d h e n c e h a v e n o t b e e n a d d r e s s e din t h e p a s t . Fo r e x a m p le , wa te r s t o r a g e i n t h e t r u n k s o fm a n y t r o p i c a l tr e e s w i t h l o w - d e n s i t y w o o d e n a b l e s f l o w e r -i n g o f b a r e t r e e s d u r i n g t h e e a r l y d r y s e a s o n o r b u d b r e a kd u r i n g t h e l a t e d r y s e a s o n , w h e n s t e m s h r i n k a g e i n d i c a te sw a t e r l o ss R e i c h a n d B o r c h e r t 1 9 8 4 ; B u l l o c k a n d S o l is -M a g a l l a n e s 1 9 9 0 ). A n a l y s i s o f s u c h p h e n o m e n a r e q u i re sm e t h o d s t o a s s es s q u a n t i t y a n d w a t e r p o t e n t i a l o f s t o re dw a t e r a n d w a t e r t r a n s p o r t t o d e v e l o p i n g o r g a n s . I n o t h e rsp e c i e s , l a rg e d i f f e r e n c e s in t h e wa te r s t a tu s o f o rg a n sw i t h i n t h e s a m e t r e e c r o w n m a y a r i s e b e c a u s e c o n s e c u t i v eg r o w th c y c l e s o f t r o p i c a l t re e s a r e n o t a s we l l s e p a r a t e d i nt i m e a s i n t e m p e r a t e b r o a d l e a v e d t re e s . F o r e x a m p l e , t h el a r g e , s c l e r o p h y l l o u s l e a v e s o fabebu ia ro sea a r e sh e dg r a d u a l ly d u r in g th e d r y se a so n . L e a f a b sc i s s io n s t a rt s in

t h e u p p e r p a r t o f t h e c r o w n , a n d l a r g e fl o w e r s o p e n o n t h eb a r e , u p p e r b r a n c h e s w h i l e t h e l o w e r b r a n c h e s s ti ll c a r r yo ld , s t r o n g ly d e s i c c a t e d l e a v e s l a c k in g s to m a ta l c o n t r o lR e i c h a n d B o r c h e r t 1 9 8 8 ) . S i m i l a r l y, i n m a n y l e a f - e x -

c h a n g i n g s p e c i e s te r m i n a l o r a x i l l a ry b u d s b e g i n t o e x p a n do n b r a n c h e s b e a r i n g o l d l e a v e s. C e l l e x p a n s i o n i n g r o w i n gb u d s o r f l o we r s , su p p o se d ly se n s i t i v e t o wa te r s t r e s s , t h u st a k e s p l a c e i n a c r o w n o r o n b r a n c h e s b e a r i n g s t r o n g l ywa te r - s t r e s se d , s e n e sc e n t l e a v e s .

I n t hi s s t u d y, t h e p re s s u r e c h a m b e r w a s u s e d i n a n o v e lwa y to m e a su r e t h e w a te r p o t e n t i a l o f s t e m t i s su e s Wste m )a f t e r e l i m i n a t i o n o f x y l e m t e n s i o n . E s t a b l i s h m e n t o f a h i g hq Js te m d u r in g d r o u g h t , w h ic h d e p e n d e d o n wa te r a v a i l a b i l i -

t y a n d t h e p r e s e n c e o f h i g h s o l u t e c o n c e n t ra t i o n s i n s t e mt i s su e s , wa s f o u n d to b e a p r e r e q u i s i t e f o r f l o we r in g a n db u d b r e a k d u r i n g t h e d r y s e a s o n .

a t e r ia l s a n d m e t h o d s

Field si te .F i e l d o b s e r v a t i o n s w e r e m a d e a t H a c i e n d a L a P a c i f i c a( G u a n a c a s t e , C o s t a R i c a ) lo c a t e d a t 4 5 m e l e v a t i o n in t h e Tr o p i c a l d r yf o r e s t , m o i s t p r o v i n c e t r a n s i t i o nsensuH o l d r i d g e ( H a r t s h o r n 1 9 8 3 ) .F i e l d s i t e a n d c l i m a t e h a v e b e e n d e s c r i b e d i n d e t a il e l s e w h e r e ( R e i c h a n dB o r c h e r t 1 9 8 2 , 1 9 8 4; B o r c h e r t 1 9 9 3 a ) . A n n u a l m e a n t e m p e r a t u r e i s2 7 . 8 ~ a n d m e a n p r e c i p i t a t i o n d u r i n g t h e l a s t d e c a d e w a s1 2 4 0 + 3 8 5 m m ( H a g n a u e r 1 9 9 3) . M o r e t h a n 9 5 % o f an n u a l r a in f a llo c c u r s d u r i n g t h e r a i n y s e a s o n b e t w e e n l a t e M a y a n d N o v e m b e r .

Table 1 . S i t e s a n d t r e e e c o t y p e s i n t h e t r o p i c a l d r y f o r e s t o f G u a n a c a s tC o s t a R i c a

D RY U P L A N D F O R E S T . T r ee r o o ts h a v e n o a cc e s s t o t h e g ro u n d w a tt a b l e . So i l w a t e r r e s e r v e s a r e d e p l e t e d e a r l y i n t h e d r y s e a s o n i n d e nt r ee s t ands .D h ar d - D e c i d u o u s h a r d w o o d t r e e s s h e d l e a v e s g r a d u a l ly d u r i n g t h e e ad r y s e a s o n a n d d e s i c c a t e s t r o n g l y ; r e h y d r a t i o n a n d b u d b r e a k o c c u r o na f t e r t h e f i rs t h e a v y r a i n s o f t h e r a i n y s e a s o n .

D lig ht - D e c i d u o u s l i g h t w o o d t r e e s w i t h h i g h s t e m w a t e r s t o r a g e s hm e s o m o r p h i c l e a v e s r a p i d ly a t t h e b e g i n n i n g o f t h e d r y s e a s o n a n d r e ta h i g h w a t e r c o n t e n t t h r o u g h o u t t h e d r y s e a s o n w h i l e s t e m s s h r i nm a r k e d l y . M o s t s p e c i e s f l o w e r o v e r p r o l o n g e d p e r i o d s d u r i n g t h e e a rd r y s e a s o n a n d b u d b r e a k o c c u r s l a t e i n t h e d r y s e a s o n b e f o r e t hb e g i n n i n g o f r a i n s .

U P L A N D S A VA N N A - R o o t s o f w i d e l y s p a c e d t r ee s h a v e n o a c c e s s tt h e g r o u n d w a t e r t a b le , b u t t a p s u b s o i l w a t e r r e s e r v e s n o t a c c e s s i b l e t o th e r b a c e o u s v e g e t a t io n .D s of t D e c i d u o u s s o f t w o o d t re e s r e h y d r a t e a n d fl o w e r a f te r l e a f s h ed i n g d u r i n g t h e d r y s e a s o n .

M O I S T L O W L A N D S I T E S - T r ee ro o t s h a v e a c c es s t o s u b so i l m o i st u r e t h r o u g h o u t t h e d r y s e a s o n .E V~ o~ - E Ve r g r e e n s o f t w o o d t r e e s e x c h a n g e c o r i a c e o u s l e a v e s a nf l o w e r d u r i n g t h e d r y s e a s o n .E V li gh t - E V e rg r e e n l i g h t w o o d t r e e s e x c h a n g e l e a v e s a n d m a i n t a i n a h iw a t e r c o n t e n t d u r i n g t h e d r y s e a s o n

P h e n o l o g y a n d c h a n g e s i n t r e e w a t e r st a tu s w e r e o b s e r v e d d u r i n g t wc o n s e c u t i v e d r y s e a s o n s , J a n u a r y - J u n e 1 9 91 a n d D e c e m b e r 1 9 9 1 - Fer u a r y 1 9 9 2 . T h e l a t t e r p e r io d , f o r w h i c h c h a n g e s i n t r e e w a t e r r e l a ti oa n d p h e n o l o g y a r e r e p o r t e d h e r e , w a s u n u s u a l l y d r y : t h e l a s t s u b s t a n tr a i n f e ll o n O c t o b e r 1 4 1 9 9 1 , a n d t h e r e w a s n o p r e c i p i t a t i o n e x c e e d i3 m m .

Experimental trees.Tr e e s p e c i e s u s e d a r e g i v e n i n Ta b l e 2 . T h e y a r er e p r e s e n t a t i v e o f m o r e t h a n 3 5 s p e c i e s s t u d i e d in s o m e d e t a i l (B o r c h e1 9 9 3 a ) . Sp e c i e s n a m e s f o l l o w H a r t s h o r n ( 1 9 8 3 ) , w h e r e a u t h o r n a m

m a y b e f o u n d . Sp e c i e s w i l l b e r e f e r r e d t o b y g e n u s n a m e o n l y. E x p e rm e n t a l t r e e s , r a n g i n g f r o m 5 t o 1 4 m i n h e i g h t , w e r e s t u d i e d a t s it e s f r ov e r y l o w ( d r y u p l a n d f o r e s t ) t o g o o d s o i l m o i s t u r e a v a i l a b il i ty ( Ta b l e Tr e e d e v e l o p m e n t ( p h e n o l o g y ) w a s m o n i t o r e d w e e k l y o r b i w e e k l y ad e s c r i b e d i n B o r c h e r t ( 1 9 9 3 a ) .

Measurement of t ree water status.Wa t e r p o t e n t i a l w a s m e a s u r e d w i t h ap r e s s u r e c h a m b e r i n s a m p l e s o b t a i n e d f r o m l o w e r t r e e b r a n c h e s w i t ht r e e p r u n e r o r f r o m t h e c r o w n o f 1 2 f o r e s t t r e e s a c c e s s i b l e f r o m 1 0 h i g h b a m b o o s c a f f o l d i n g . Tr i p l i c a t e s a m p l e s w e r e c o l l e c t e d w e e k l yu s u a l l y b e t w e e n 0 5 3 0 a n d 0 7 0 0 h o u r s , a n d i m m e d i a t e l y p l a c e d i np l a s t i c b a g s , s t o r e d i n a c o o l e r c o n t a i n i n g m o i s t p a p e r , a n d p r o c e s sw i t h i n 2 h a f t e r s a m p l i n g . I f v a r ia t i o n a m o n g s a m p l e s e x c e e d e d 0 .3 M Pm e a s u r e m e n t s w e r e re p e a t e d t h e n e x t d a y. W h e n m a x i m u m c o m p e n st i o n p r e s s u r e a t t a i n a b l e w i t h t h e p r e s s u r e c h a m b e r u s e d ( 4 M Pa ) w

i n s u f f i c i e n t t o c a u s e e m e rg e n c e o f x y l e m s a p a t t h e c u t s u r f a ce , a w a tp o t e n t ia l o f < 4 M P a w a s re c o r d e d .Lea f water po tential(Wleaf), am e a s u r e o f x y l e m t e n s io n , w a s o b t a i n e d f r o m l e a v e s o r l e a f - b e a ri nb r a n c h s e c t i o n s . D u r i n g t h e e a r ly d r y s e a s o n a l l l e a v e s w e r e 6 - 8 m o n to l d a n d s o m e w h a t s e n e s c e n t ; s t o m a ta l c o n d u c t a n c e o f d a r k e n e d l e a vr a r el y d e c l i n e d b e l o w 3 0 - 5 0 % o f l e a v e s in l i g h t (C . M a r t in , p e r s o nc o m m u n i c a t i o n ) . To m e a s u r e e q u i l i b r a ti o n o f s u c h l e a v e s w i t h s o i l m o it u r e , le a v e s w r a p p e d i n a l u m i n u m f o i l a n d e n c l o s e d i n p l a s ti c b a g s i n te v e n i n g w e r e c o l l e c t e d t h e n e x t m o r n i n g a t 0 6 00 h o u r s f o r m e a s u r e m eof p r eda wn Wlea f.

I n a m o d i f i c a t i o n o f t h e s t a n d a r d p r e s s u r e c h a m b e r t e c h n i q u e ,stemw a t e r p o t e n t ia l(~IJ st em) Was mea su re d in ba re o r de fo l i a t ed , 10 cm - lon gb r a n c h s e c t io n scut at both endst o r e l e a s e x y l e m t e n s i o n . R e s u l t s o b t a i n -e d w i t h t h i s m e t h o d w i l l b e e v a l u a t e d i n t h e d i s c u s s i o n .

E l e c t r i c r e s i s t a n c e t o A C o f < 1 k H z ( o r i m p e d a n c e ) b e t w e e n e l e ct r o d e s i n t r e e tr u n k s v a r i e s w i t h t h e a m o u n t a n d i o n c o n t e n t o f c e l l s


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Tab le 2 . Exper im en tal species and ecophysio log ical and pheno log ical character is tics o f t ree eco types in the t rop ical d ry fo res t o f G uanacaste dein Tab le 1

E C O T Y P E - Species P h en o lo g y S t em Wate r s t a tu s F ig u re

S h ed F lu sh F lo w er D en s i ty M ax w a te r W lea f W s tem S Mm o n t h g c m - 3 % D W M P a %C D E F G H I

Dhard Mea ns of 9 species: 0 .94Lys i loma seemani i 2 - 4 6 - 7 7 0 .9 2Tabebuia ochraceasubsp . 1 - 2 5 - 6 af ter 1 .1neochrysantha ra in

D l i g h t Mea ns of 6 spec ies : 0 .40Enterolobium cyclocarpum 1 - 2 2 - 4 2 - 4 0 . 4 9Spondias purpurea 12 5 - 6 1 - 2 0 .37

Dsoft Mea ns of 9 spec ies : O. 71Cordia a l l iodora 2 - 3 6 2 0 .70Gua z um a u l m i f o l i a 1 - 2 4 - 5 3 - 4 0 .6 7M yr os pe r m um f r u t e s c e n s 12 -1 4 - 5 1 - 2 0 .80Pterocarpus rohri i 1 2 - 1 4 - 5 2 0 . 52

EVsoft Mea ns of 9 species: 0 .64Andi ra inermis 11 - 1 2 0.70

Licania a rborea i r regu lar 1 0 .59Pi thece lobium saman 3 3 0.14

E V l i g h t Mean s of 5 spec ies : 0 .47Eugenia sa tamens i s 3 - 5 4 - 6 3 - 6 0 .60Gmel ina a rborea i r regu lar 12 - 2 0 .42

3 2 - 3 . 7 - 3 . 9 313 0 < -4 < -4 3 1 6 C2 0 -3 . 9 < -4 2 9 3 A

1 93 - 1 .5 - 0 .5 6 31 25 -2 . 3 -1 . 1 5 2 4 A191 -1 69 4B

6 5 - 2 .5 - 2 . 4 4 76 3 -3 . 7 < -4 3 7 3 B7 1 -2 . 5 -1 . 7 4 5 3 C4 8 -3 . 5 -3 . 6 4 4 6 D

11 4 -2 -2 . 2 4 2 3D

74 - :2 .5 -1 .6 466 4 -1 -0 . 3 4 4 6 B

1 0 0 - 4 - 0 . 5 5 0 2 A - C5 7 -2 . 7 -2 . 4 4 9 6 A

143 -2 .0 ~9.8 518 9 -3 . 5 -1 . 5 4 9 2 D - F

1 67 -1 . 6 -0 . 8 5 4 4 C

Co lum ns: A - Species ( fo r au thors and famil ies see Borch er t 1993 a) ;B -D - P h en o lo g y : m o n th o f lea f sh ed d in g (D ) , f lu sh in g (E ) , f l o w er in g(F) ; E , F - Woo d p roper t ies : E - wood densi ty ; F - percen tage max i-m u m w a te r co n ten t o f w o od . G - I - Tree w a te r s t a tu s du r in g th e d ry

season . Al l measurements rep resen t the lowest observed values dur inthe dry season. G - Wleaf; H ~ t I J s t e m ;I - s tem moistu re . J Refere nceto F igure in Resu l ts (data f rom B orche r t 1993 a)

r e l eased b y ce l ls w o u n d ed d u r in g e l ec tro d e i n se r t i o n an d h en ce w i thabund ance and w ater s ta tus o f l iv ing cel ls in s tem t issues (Blanch ard e ta l . 1983) . For avocado(Persea) an d sp ru ce(Picea), elect r ic res is tance,ex p res sed a s p e rcen t o f t h e sp ec i es - sp ec if i c m ax im u m , w as fo u n d to b eh igh ly co rrela ted w i th ~Jleaf (Dixon et a l . 1978) . Because twigs fo rm easu rem en t o f~ t s tem a r e d iff icu l t to ob tain fo r ta l l fo res t t rees , measur e-men ts o f e lect r ic res is tance were used to es t imate s i te- and species-spe-ci f ic d i fferences in water s ta tus o f numerous t rees . For each measure-men t , a pai r o f paral le l nai ls (40 mrn long) was d r iven 20 mm deep and10 mm apar t in to bark and sapwood o f t ree t runks. Resis tance betweenth ese e l ec t ro d es w as m easu red w i th a B o u y o u co s so i l m o i s tu re m e te r(M o d e l B N -2 B u s in g A C o f 4 8 0 H z , B eck m an , C ed a r G ro v e , N . J . ) .I n s t ead o f t h e i n s t ru m en t ' s i n co n v en ien t ex p o n en t i a l s ca l e fo r O h m , t h el inear, arb i t rary scale ind icat ing percen t avai lab le so i l mois tu r e wasused and data are g iven aspercent s t em mois ture(S M ) , w h ich th u sconst i tu tes arelative measure based on elect r ic res is tance o f the ou ter2 0 m m o f t r ee t ru nk s . M easu rem en t s w ere fo u n d to b e h ig h ly co r r e la t edw i th o th e r m easu res o f t r ee w a te r s t a tu s an d d ev e lo p m en ta l ch an g esdur ing the d ry season (Tab le 2 ; Borch er t 1993 a; Borcher t , in p repara-

tion).C h an g es i n s t em c i r cu m fe ren ce( s t em shr inkage)w ere m easu redu s in g a lu m in u m d en d ro m ete r b an d s i n s t al l ed a t b r eas t h e ig h t (L im in g1957) . For l igh t- and so f twoo d t rees ,woo d de n s i ty a n d m a x i m um wa t e rcontent (Tab le 2 ) were determined in wood cores excised wi th an incre-m en t b o re r (5 m m d iam e te r, 3 0 m m lo n g ) an d w e ig h ed f r e sh , a f t e r so ak -ing fo r 24 h , and af ter oven d ry ing (Schu lze e t a l. 1988) . For hardw oodspecies res is t ing the increm en t borer, wo od densi ty o f the same o r re la tedsp ec ie s w as o b t a in ed f ro m B ara j a s -M o ra l e s (1 9 87 ) , an d m ax im u m w a te rco n ten t (M W C ) w as ca l cu l a ted as % M W C = (1 -D/1.5) 1 0 0 /D , w h ereD = w ood densi ty and 1 .5 is the me an densi ty o f wood substance. Valueso b ta in ed w i th t h is fo rm u la w ere c lo se r t o m easu red v a lu es t h an th o seca l cu la t ed u s in g th e r e l a t io n % M W C = -0 . 9 3 + 1 . 0 2 /D , d e r iv ed f ro mmea surem ents wi th t rop ical deciduous t ree species (Schu lze e t a l. 1988) .

Osmo t ic concent ra t iono f b a rk an d w o o d t i s su es w as o b t a in ed f ro m co res(9 cm long , 5 mm d iameter) f resh ly excised wi th an increm en t boreSect ions o f bark and wood (5 and 10 mm long , respect ively ) wersqueezed wi th a pai r o f p l iers and the osmolal i ty o f the expel led sapab so rb ed o n to f il t e r p ap e r d i sk s (5 m m d iam e ter ) , w as m easu red in ao sm o m ete r (M o d e l 5 1 0 0 A Vap o r P res su re O sm o m ete r, Wesco r, P ro vU tah ) . Wate r co n ten t o f b a rk an d w o o d w as d e t e rm in ed b y w e ig h insect ions af ter excis ion and af ter oven d ry ing .

F ield data were analyzed and g raphed using the Quat t ro -Pro sp readsheet (Borland In ternat ional , Sco t ts Val ley, Cal i f . ) , Axum (Trimetr ixSeat t le , Wash . ) an d a Hewlet t -Pack ard Laser P r in ter.

R e s u l t s

D i f f e r e n c e s b e t w e e n ~ l e a f a n d ~ lstem

A t m o i s t s i t e s , L i c a n i a i s a n e v e r g r e e n t r e e b e a t i n g t h el e a t h e r y , s c l e r o p h y l l o u s l e a v e s o f 2 - 3 c o n s e c u t i v e f l u s h e so n l o ng , r e l a t iv e l y th i n b r a n c h e s , w h o s e e x t e n s i o n g r o w t he n d s w i t h t h e f o r m a t i o n o f a t e r m i n a l i n f l o r e s c e n c e . A b -s c i s s i o n o f o l d l e a v e s i s ir r e g u l a r , a n d i n o l d e r b r a n c h e sl e a f - b e a r i n g s e c t i o n s a l te r n a t e w i t h 1 0 - 2 0 c m l o n g b a r es e c t i on s . U s i n g t h e p r e s s u r e c h a m b e r , w a t e r p o t e n t i a l w a sm e a s u r e d i n M a r c h 1 9 9 1 i n s e ts o f s t e m s a m p l e s w i t h orw i t h o u t a t t a c h e d o r g a n s , c u t f r o m t h e s a m e b r a n c h ( F i g. 2 )C o n s i s t e n t l y , t h e w a t e r p o t e n t i a l o f b a r e s t e m s e c t i o n s( ~ s t e m ) w a s q u i t e h i g h ( o f t e n > - 0 . 2 M P a ) , q J le af o f a d j a -c e n t b r a n c h s e c t i o n s b e a r i n g o l d , b r it t l e l e a v e s w a s v e r yl o w ( < - 4 M P a ) , a n d b r a n c h e s b e a t i n g y o u n g l e a v e s o rd e v e l o p i n g f r u it s h a d w a t e r p o t e n t i a l s b e t w e e n - 0 . 6 a n d


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118

LIC NI EUGENI

D

o

-4.

Fi g . 2 . D i f f e r e n c e s i n w a t e r p o t e n t i a l b e t w e e n s t e m s e c t i o n s a n d o rg a n so n t h e s a m e b r a n c h e s o f t w o t r o p i c a l t r e e s g r o w i n g a t a m o i s t s i t e . Wa t e rp o t e n t i a l f o r e a c h d a t a s e t w a s m e a s u r e d d u r i n g t h e d r y s e a s o n i n t h es a m e b r a n c h i n a d j a c e n t 1 0 c m - l o n g s e c t i o n s c u t a t b o t h e n d s . B r a n c hsec t io ns we re ba re (~ tem ) o r ca r r i ed a l ea f (~t lea f) o r a t e rmin a l in f ru te s -c e n c e ~ / f r u i t ) .Licani a arborea: A - b a r e s t e m a n d o l d l e a f; B - b a r es t e m , o l d l e a f a n d i n f r u t e s c e n c e ; C - b a r e s t e m , i n f ru t e s c e n c e a n d n e wlea f .Eugenia salamensis: b a r e s t e m a n d o l d l e a f b e f o r eD, E) a n d 2 d a y sa f t e r i r r iga t ion o f the t r ee (F) . 9 Stem ; [ ] O ld l ea f; [ ] Ne w lea f ; [ ] Fru i t

- 1 .0 M Pa F ig . 2 A - C) . To e l im in a t e t h e p o ss ib i l i t y th a th i g h t I J s t e mv a l u e s r e s u l t e d f r o m e x p u l s i o n o f w a t e r f r o mv e s s e l s e x t e n d i n g t h r o u g h t h e e n t i r e l e n g t h o f t h e s t e msa m p le s , s t e m se g m e n t s c o m p r i s in g th e l a s t a n d f i rs t n o d e s

o f c o n se c u t iv e fl u sh e s , i. e . , b r a n c h se g m e n t s w i th d i sc o n -t i n u o u s v e sse l s , we r e t e s t e d a n d f o u n d to g iv e t h e sa m er e su l t s a s se g m e n t s f r o m a s in g l e f l u sh .

M e a s u r e m e n t s t h u s r e v e a l e d d r a m a t i c d i f f e r e n c e s b e -twe e n th e wa te r p o t e n t i a l s o f b a r e s t e m se c t io n s( t ISs tem) ,inw h i c h x y l e m t e n s io n w a s r e l e a s ed b y c u t t in g a t b o t h e n d sa n d s t e m se c t io n s w i th a t t a c h e d o rg a n s , i n wh ic h x y le m

te n s io n p e r s i s t e d(~lSleaf, tIJfruit).

T h e r e w e r e a l s o l a r g ed i f f e re n c e s b e t w e e nt lSleaf o f o l d a n d y o u n g l e a v e s o n t h esa m e b r a n c h . I n p a r a l l e l t o t h e p a r a d o x ic a l o b se r v a t io n s oTabebuia rosea se e I n t r o d u c t io n ) t h e se d a t a sh o w th a ty o u n g l e a v e s a n d f ru i ts w e r e g r o w i n g o n b r a n c h e s c a r r y i nd e s i c c a t e d o ld l e a v e s .

In Eugenia s t a n di n g n e a r t h e a b o v eLicania ~s te m a n d~I'tleafo f o ld l e a v e s we r e b o th l o w d u r in g in i t i a l m e a su r e -m e n t s o f d r o u g h t - s t r e s se d t r e e s F ig . 2 D , E ) . Wi th in2 d a y s a f t e r i rr i g a t i o nUrlstemi n c r e a se d t o - 0 . 1 M P a , w h i l et l J l ea f r e m a i n e d v e r y l o w F i g. 2 F ) .uX'tstemthUS var ied inde-p e n d e n t l y o ft lYlea f w i t h a c h a n g e in t r e e wa te r s t a tu s . I nEnte ro lob ium Guazuma Spond iasa n d a f e w o th e r sp e -c i e s , wh o se tw ig s c o n ta in l a rg e , t h in - wa l l e d , o f t e n s l im yp i th c e l l s d e sc r ib e d f o rP s e u d o b o m b a xi n Ro th 1 9 8 1 ) ,l i q u i d w a s r e p e a t e d l y o b s e r v e d t o e m e r g e f r o m t h e c u ts u r f a ce o f b r an c h s e g m e n t s a s s o o n a s t h e y w e r e e x p o s e dto t h e v e r y l o w p r e ssu r e g e n e r a t e d b y c lo s in g th e l i d o f t hp r e ssu r e c h a m b e r q Ss te m > - 0 .1 M P a ) . Fo r t h e se sp e c i esv e r y l o w p r e ssu r e wa s t h e r e f o r e su f f i c i e n t t o e x p e l l i q u idf r o m w a te r - f i ll e d v e sse l s a n d w a te r - s to r in g p i th .

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Fi g . 3 - 4 . Va r i a ti o n i n p h e n o l o g y ( b o t t o m ) a n d~ s t e m ,Wleaf, and s t em mo is tu reupper curves) i n t rop ica l d ry

7of o r e s t t re e s o f d i f f e r e n t e c o t y p e s d u r i n g t h e e a r l y d r ys e a s o n 1 9 9 1 / 1 9 9 2 . Fo r d e s c r i p t i o n o f e c o t y p e sDh~rd,e tc . ) and s i t e s s ee Tab le 1 .

so 2 . Fig . 3 . A - Tabebuia ochracea s u b s p ,neochrysanthaco i n a d ry up lan d fo re s t ; B -Cordia alliodora i n a d ryi s avann a . C - Guazuma ulrnifolia i n a d r y s a v a n n a ;

D - Pterocarpus rohrii a t a m o i s t l o w l a n d s i te .30 Fig . 4 . A, B -Enterolobium cyclocarpum and

Spondiaspurpurea a t a d ry up lan d fo re s t s i t e .I n B , s t e m s h r i n k a g e w a s m e a s u r e d a t b r e a s t h e i g h t .C - Gmelina arborea at a m ois t s i te . Wstem;9 . . . . 9 WL c~; 9 - - 9 s tem mo istu re ; IllUll eaff a l l ; 0 0 f low er ing


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ing at a m oist si te, both q stem and q~leaf of th e last le ave s tobe shed increased dur ing lea f fa l l and the bare t ree f low eredabundant ly af ter ful l rehydrat ion (Fig . 3D; Table 2 G-I ) .S tem mois tu re con ten t (SM) in so f twood spec ies washigher than in hardwood t rees but var ied only l i t t le wi thi n c r e a s i n g ~ t s te m ( e .g. Figs. 3 D, 6 D) .

In s t r ik ing contrast to hardwood t rees growing at thesame very dry upland si tes , water-stor ing l ightwood t rees,charac te r i zed by w ood dens i ti e s be low 0 .5 g c m 3 and asaturat ion water content above 125% dry weight (Table 2) ,m a i n t a i n e d ~stem near saturat ion level and wel l a bov e qJleafbefo re l ea f shedd ing (F ig . 4A, B vs F ig . 3A) . The h ighwate r con ten t o f the 15 -2 0 mm - th ick bark o f such l igh t-wood t rees (Fig . 5E,Enterolobium was ref lected in high

SM va lues . The w eigh t o f cu t, t h i ck b ranches o f l i gh twootrees indicated that water content throughout the s tem waas h igh as in the ana lyzed sam ples o f the ou te r wo od(Fig. 5) ; the amoun t of wa ter s tored in large t rees i s thusubstantial (Table 3).

Spondias and o ther sha l low- roo ted l igh twood spec iesshed leaves rapidly dur ing the ear ly dry season (data noshown) and then f lowered fo r p ro longed per iods . Use os to red wate r fo r f lower expans ion and evapora t ion f romf lower s i s i nd ica t ed by decreas ing s t em c i r cumference~{'tstemand SM (F ig . 4B; Re ich and Borcher t 1984) .

Solute concentrat ions of water s tored in the extensiveparenchymat i c t i s sues o f ba rk and woo d o f dec iduoul igh twood t r ees f rom dry s i t e s (Ro th 1981) r anged f rom0.34 to 0 .85 osmol , cor responding to osmot ic potent ia lb e t w e e n -0 . 8 a n d -2 . 1 M P a ( F ig . 5 A - C ) . T h e y w e r e m o r

than twice those measured in the everg reen l igh twood species Gmelina grow ing at m oist s i tes (Fig. 5 D) . In a l l spe-cies analyzed, osmot ic concentrat ions were dist inct lyh igher in the w ood than in the ba rk and dec l ined f rom thou te r t owards the inner l ayer s o f t he wo od .

Facu l t a t ive ly everg reen , l ea f - exchang ing so f twoo d species wi th cor iaceou s leaves, adapted to mo ist lowland si tesdesiccated only moderately and at ta ined saturat iont l J s t e mwee ks befo re l ea f f al l (Fig . 6A, B) . Fo l lowing the inc reasin W stem, preda wn Wleaf of several t rees inc reased in e xposed l eaves o r in l eaves wrapped in a luminum fo i(Figs. 3D , 6 A , D ) . F lower ing or f lushing of ten star tedbefo re o ld l eaves had been shed comple te ly (F ig . 6B ) .

Dec iduous ha rd - and so f twood t r ees g rowing a t moi slow land si tes re ta ined thei r leaves longer and ma intained higher SM than thei r conspeci f ics a t dry upland si tes(Fig. 6 C, Dvs Fig. 3 A) . As in evergreen t rees a t the samesi tes , Wstem of suc h t rees increased to saturat ion valuebefo re absc i ss ion o f the senescen t mes ic l eaves , r esu l t ingin large di fferences betw een q~stem and Wleaf (Fig . 6 C, Das f i r s t obse rved inLicania and Eugenia (Fig. 2) . Faculta-t ively evergreen l ightw ood t rees a t moist s i tes maintained saturat ion Wstem and a very high SM as wel l as a h igh~ J l e a fthroughout the dry season (Fig . 4C) .


6/11

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F i g . 6 A - D . Va r i a ti o n i n p h e n o l o g ybottom) an d ~/s tern , ~/ leaf, an d s te mm o i s t u r e upper curves)i n t r o p i c a l d r y f o r e s t t r e e s o f d i f f e r e n t e c o t y p e sd u r i n g t h e e a r l y d ry s e a s o n 1 9 9 1 / 1 9 9 2 . A , B -Pi thece lobium sam an andAndi ra inermisa t m o i s t l o w l a n d s i te s . In A , l e a v e s w e r e w r a p p e d i na l u m i n u m f o i l a n d p l a s t i c b a g s i n t h e e v e n i n g a n d p r e d a w n ~ l e a f w a sm e a s u r e d t h e n e x t m o r n i n g . I n B , ~ le ~f w a s m e a s u r e d i n o l d l e a v e s b e f o r es h e d d i n g a n d l a t' er i n n e w l y e x p a n d e d l e a v e s . C , D -Lysi loma seeman-ni i a n d M yr os pe r m um f r u t e sc e n sa t a m o i s t l o w l a n d s i t e. C o m p a r e t oh a r d - a n d s o f tw o o d s p e c ie s a t d r y s it e s i n F i g. 3 A , B . - - , h ~9 . . . . 9 h ~ 9 9 ste m m ois tur e ; I]lllll ea f fa l l

i s c us s i on

Water status and the development o f tropical treesduring drought

Most studies of the relations between tree water status andphysiological processes deal with the effect of water defi-

cits on leaf functions such as stomatal conductance andphotosynthesis or with drought resistance of leaves intemperate or tropical trees (Sobrado 1986; Hinckley et al.1991; Olivares and Medina 1992). The role of tree waterstatus in the growth of buds, flowers and shoots of trees hasreceived much less attention (Hinckley et al. 1991). Con-sequently, the current deba te on the merits of various mea-sures of water status is mainly concerned with the value oftl/leaf vs relative leaf water content (RWfleaf; Sinclair andLudlow 1985). Likewise, most studies of osmotic adjust-ment, turgor loss and the role of the elastic modulus insensing water deficits deal with leaves and rely on use ofthe pressure-volume technique (Pallardy et al. 1991). Incontrast, this study is concerned with the effect of water

stress on organ growth in trees. Specifically, it attempts toresolve the apparent paradox that in many tropical treesleaf fall, known to be accelerated by drought stress (Ad-dicott 1991), is followed by the expansion of flower orvegetative buds during severe climatic drought, and thatthese processes may occur simultaneously on the samebranch or tree crown (see Introduction). Bud break de-pends on the rehydration of the supporting branch and thusultimately on the availability of water stored in the subsoilor in tree stems (Borchert 1993 a). Measurement of thewater status of stem tissues thus appears to be central to theanalysis of tropical tree development during seasonaldrought.

easurement of t P s t e mwith the pressure chamber

In normal use of the pressure chamber, tension in thexylem of terminal organs ( t l J x y l e mof bare stem, leaf, in-florescence or fruit; Fig. 2) is measured by interrupting thexylem with a single cut and compensating the tensionpulling water into the organ s tissues by applying externalpressure. If bare branch sections are cut at both ends, asdone for measurements o f qJstem in this study (see Fig. 2;Material and methods), xylem tension is released and theretention of water should depend only on the pressurecomponent of the water potential o f parenchymatic tissuesadjacent to the xylem and of apoplastic water in the wood.If tissues near the xylem are fully saturated, xylem waterwill not be absorbed upon cutting a branch section and canbe be expelled by very low pressure in the pressure cham-ber (see Results). High Wstem-Values measured in st emsections including the apical and basal ends of consecutiveflushes of shoot growth are unlikely to be the result of

releasing water from long vessels extending through theentire experimental sample. Measurement of progressivelylower values of ~I / s t em should indicate increasing waterdeficits of parenchymatic tissues in sapwood and bark,possibly in conjunction with increasing cavitation of vesselelements. Wstem should increase upon irrigation of drought-stressed trees, as indeed observed (Fig. 2D-F; Borchert1993 b). Lightwood trees mainta ining a high water contentin bark and wood also maintain a Wstem near saturation atvery dry sites (Figs. 4A, 5), where hardwood trees desic-cate to values of qJstem below -4 MPa (Fig. 3 A). qJstem husconstitutes a measure of tree water status which is differentfrom and independent of t rl J le a f o r ~ I / x y l e m ( F i g s .3-6). The

roles of Wstem and Uxlleafin tree development will be dis-cussed below.The observed differences of 3-4 MPa between ~- t s t em

a n d ~ l e a f of the same twig (Figs. 2; 6C, D) illustrate theproblem of measuring tree water status and show thatparenchymatic tissues near the xylem of a rehydratedbranch may be water-saturated while xylem tension ishigh. Because of the high elastic module of wood, theseparenchymatic tissues - likely to have a high solute con-tent (see below) - apparently reach the turgor loss pointand equilibrium with ~IJxy lemwith minimal water loss andchange in cell volume (Pallardy et al. 1991), such that ahigh ~gstem is measured after elimination of ~ J x y l e m bydefoliation and double cutting the branch. These considera-


7/11

tions suggest that ~IJstem constitutes an indirect measure ofthe relative water content of parenchyma cells near thexyl em (RWCstem), which is uncou pled fro m daily var iationin ~IJxylemand depends on both predawn ~ and theRWC o f adjacent parenchymatic stem tissues. In analogyto RWCleaf (Sinclair and Ludlo w 1985), Wstem appears tobe relatively stable and tends to integrate the water balanceof stem tissues over days or weeks (see time scale inFigs. 3, 4, 6). In hardwood trees with little stem waterstorage ~IJstemshould vary mainly with changes in pre-dawn ~ txylemand thus provide an estimate of the waterstatus of soil layers accessible to the tree s root sys tem (seebelow).

Measurements of SM indicate electric resistance andreflect the amount of cell sap released by insertion of

electrode nails into the outer 20 mm of tree trunks. SM thusconstitutes a crude, relative measure of water storage in theouter tree trunk, as opposed to Wstem, which indicates thewater status of parenchymatic tissues near the xylem oftwigs. Accordingly, SM ranged from high values in water-storing lightwood trees (Fig. 4; Table 2) to lower values intrees with low water storage growing at moist (Fig. 6C, D)or dry sites (Fig. 3A, B). SM was found to be wellcorrelated with wood density, stem water storage andm i n i m u m ~ s t e min more than 30 species (Figs. 3-6;Table 2; Borchert 1993 a). During rehydration of stronglydesiccated hardwood trees after irrigation, a rise in tlJstemfrom -0.2 MPa within 48 h was accompanied byan increase in SM to maximum values within 6-8 days,indicating that rapid refilling of vessels and rehydration oftissues near the xylem of twigs was followed by a slowerrehydration of outer trunk tissues supplied by slow lateralwater transport (Borchert 1993 b). In contrast, slower in-creases in ~stem during climatic drought were only rarely

followed by a distinct rise in SM (Figs. 3- 6) , suggestingthat physiologically significant increases in ~stem oftwigs may occur in the absence of full saturation of trunktissues.

Water defic i ts an d leaf absciss ion dur ing drought

In confirmation of earlier observations (Addicott 1991),qJleaf genera lly reached its mini mum jus t before leaf shed-ding (Figs. 3 A- C; 6A -C ), but in some trees at moist sites~ le a fof the last leaves to be shed increased in parallel witha s imult aneous increase in Wstem (Figs. 3 D; 6 D). The ob-served minim a of Wleaf were strongly correlated with theminima o f Wstem and SM, which in turn varied wi th theavailability of stored water in tree stems or in the subsoil(Table 1: Sites; Table 2 F- I ; Borchert 1993a). Hard- andsoftwood trees growing at dry sites had the lowest Wleaf,~xJstemand SM (Fig. 3 A, B; Table 2G - H). With increasingsoil moisture availability these values became larger(Figs. 3 C, D; 6). The highest values were maintained inwater-storing lightwood species at dry and moist sites(Fig. 4A, C; Table 2E-I).

121

7tstem and bu d deve lopmen t

Bud break and subsequent growth of flowers or shootsinvolve cell expansion, known to be inhibited by evenmodera te water stress (Hinck ley et al. 1991). Water supplyto expanding buds is strongly affected by the vascularconnections between a bud and its supporting stem (Braun1960). Resting terminal buds usually remain connected tothe vascular system of the stem and exp and rapidly afterbud break. In resting lateral, axillary buds o f broadleavedtrees vascular connections are severed during growth ingirth after bud inception and initial growth after bud breakis slower, because water and nutrients have to be suppliedto the growing tissues via cell-to-cell transport from theadjacent parenchymatic pith or bark tissues. Formation ofnew vascular connections begins only during early leafexpansion in the young shoot (Braun 1960). Water satura-tion of stem tissues, as indicated by a high ~IJstem,shouldthus be a prerequisite for early bud growth. I n keeping withthese considerations, in almost all observed trees Wstemapproached saturation before flowering or flushing(Figs. 3 C, D; 4 B; 6 A, B; Borcher t 1993 a). In leaf -bearingbranches with a high qJstem bud development rarely pro-gressed beyond initial swelling, being apparently inhibitedby low Wleaf.

Differences in location and developmental status arelikely to determine the priority of bud break in flower andvegetative buds of rehydrating trees. For example, the ter-minal flower buds of Tabebuia ochraceabegin to expandwithin 2 days after irrigation o r rain, as soon as Wstem hasincreased to >-0.2 MPa, and are fully expanded after6 days; expansion of lateral vegetative buds begins laterand leaf expansion is completed only about 3 weeks afterirrigation (Borchert 1993b). Similarly, only well vascu-

larized flower buds in offea arabicaopen aft er rain (Cri-sosto et al. 1992).

Increase in tffstemduring climatic drought

Measurements of tIJstem given in Figs. 3 -6 started on8 December, 1991, i.e., 8 weeks after the last rainfall. Re-hydration of stem tissues shown in Figs. 3 and 6 thusoccurred after trees had been exposed to 3-4 months ofhigh evaporation stress in the absence of rain (Reich andBorchert 1984). This raises questions as to the source ofwater enabling rehydration.

Rehydration of stem tissues should be preceded by animprovement of the tree s water balance due to changes inthe soil-plant-atmosphere continuum, such as an increasedcapacity for water absorption or a reduction o f water loss(Borchert 1991). Rehydration of hard- and softwood treesstoring little water in their trunks will depend on the ab-sorption of water remaining in the subsoil after the dryingof upper soil layers during the ea rly dry season. The inabil-ity of hardwood trees in dry upland forests to rehydrateafter leaf fall indicates that accessible subsoil moisturereservoirs had been depleted (Fig. 3 A). A mong widelyspaced savanna trees subsoil moisture was adequate tobalance the water eco nomy after the elimination of tran-spirational water loss (Fig. 3 C). Predictably, in such trees


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122

7o 90 130 95 130 80 50

90 95 llO 95 tlO 60 20

B C

Fig. 7 A- C. Changes in water content due to starch degradation, osmoticwater uptake and water shifting in upper top halJ) and lower stemslower ham of Populus before bud break in spring. A, B - Stem sections

of intact young trees (6 cm s tem diameter) in February (A) and April (B);C - Stem sections of a rootless young tree, cut in February and ana-lyzed in April (redrawn from Braun 1961). Water content [ ] 120 ;[] Starch

ignore timing and rate o f stem rehydration varied widelywith site water availability and the time of leaf fall(Figs. 3B-D; Borchert 1993a). Similarly, in seven dryforest species stem shrinkage during lea f shedding, indica-tive of a declining RWCstem, was followed by moderatestem expansion, i.e., partial rehydration, in the absence ofrain. This rehy dration resulted in flushing accompanied by

renewed stem shrinkage indicating water loss by newfoliage (Daubenmire 1972).

In contrast to trees at dry sites, rehydration at moist siteswas sometimes remarkably fast, occurring well before leaffall and in the absence of apparent changes in the soil-plant-water con tinuum (Fig. 6). Extension of fine roots intomoist subsoil layers and increased absorbing capacity oftree tissues due to osmotic adjustment will be consideredbelow as possible causes for rehydration.

Water-storing lightwood trees growing at very dry siteshave sha llow root systems (Olivares and Medina 1992) andshed their mesic leaves during early drought, i.e., suchtrees neither transpire nor absorb water during most of the

dry season. Saturation water content of lightwood trees isroughly 3 and 6 times that of soft- and hardwood trees,respectively (Table 2). Both soft- and lightwood trees de-plete about 30 of their stored water during the dry season,but the remaining water content in the latter is more thantwice the saturation water content of the former (153 vs67 DW; Schulze et al. 1988). Reflecting their high watercontent, t lJstem and SM are generally high in lightwoodtrees (Fig. 4). Water consumption during flower expan-sion, possibly in conjunction with evaporative water lossthrough the bark, caused not only a decrease in q~stem, butalso a decline in SM and shrinkage of the trunk (Fig. 4B;Reich and Borchert 1984). This implies that stored waterused in the branches was replenished in part by water from

the trunk. Similarly, bud break in man y lightwood speciesoccurs during the late dry season while trunks continue toshrink. However, root and leaf expansion remain arrestedat an early stage until the first heavy rains enable resatura-tion (expansion) o f the trunk and full le af expansion (Reichand Borchert 1984; Bullock and Solis-Magallanes 1991).Shoots and roots also sprout readily from cut branches ofBursera and Spondias, which are widely planted as livingfences.

Water shifting in leafless temperate trees

Slow, upward water transport in the xylem resulting fromosmotic water uptake by stem tissues or expanding buds inbare trees wa ter shifting) has received little attention inrecent discussions of tree water relations (e. g. Hinckley etal. 1991), although it plays an important role in the waterrelations of both temperate and tropical trees before andduring bud break (Braun 1984). Some rarely cited studiesof water shifting in temperate trees will be therefore re-viewed as a basis for understanding dry-season develop-ment of tropical trees.

Parenchymatic tissues in stem and bark obtain water viaosmotic water movement along gradients in water poten-tial. In bare temperate trees, rising temperatures in earlyspring cause the transformation of starch into sugars andosmotic water uptake by bark tissues followed by slowupward water shifting from the root system through thewood (Fig. 7; Braun 1961; Sauter 1966). The amount ofwater absorbed and moved before bud break is muchsmaller than that transported in leaf-bearing, transpiringtrees (e.g. Betula: 0.05 dm3 day-I March 12-April 9 vs

4.3 dm3 day-1 May 7 -1 3; Braun 1984). In intact temperatetrees water sh ifting is usual ly accompanied by water trans-port driven by root pressure, but in rootless trees watershifting to the bark tissues of the upper b ranches results ina decreasing water content o f the lower trunk (Fig. 7 C);such trees dry out and die when leaves start expanding. Adeclining water potential of parenchymatic bark tissuesdue to increasing solute content, i.e. osmotic adjustment,thus causes an increase in symplastic water content of thesetissues and a decreasing water content in the wood apoplast(compare Fig. 1). The resulting high water and sugar con-tent of bark tissues is a prerequisite for subsequent budbreak (see above).

In contrast to most other temperate hardwood trees, inwalnut Juglans regia) >90 of fine roots die during thewinter and leaf development is unusually slow (Fig. 8;Bode 1959). In parallel with rootless temperate trees anddrought-stressed tropical lightwood trees (Figs. 4B, 7C),the water content of short-shoots declined after bud breakduring flowering and initial leaf expansion, indicating thatwater absorbed by expanding young shoots and flowerswas not fully replaced (Fig. 8, day 0- 7) . Subsequent, en-hanced starch-sugar conversion resulted in rehydration ofshoots and bleeding from leaf scars (Fig. 8, day 7-10).Osmotic water uptake by growing shoots was thus accom-panied by the development of xylem pressure. Such pres-sures, referred to variously as bleeding pressure, stem or


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100

ogo

40 ~

2

zrt l l I I I I I I I J I

o 0 5 10 15 20 25 30 35DA YS AFTER BUD BREAK APR.25)

Fig . 8 . The t ime course o f bud b reak , roo t g rowth and leaf expansion inw a ln u t Juglans regia)during sp r ing . The water con ten t o f shor t shoo tsb ea r in g ex p an d in g b u d s d ec reased d u r in g g ro w th o f m a le f l o w er s(catk ins) and in i t ia l leaf expansion . Subsequen t rehydrat ion was fo l -lowed by b leed ing , rap id g rowth o f f ine roo ts and leaf expansion ( red -r aw n f ro m B o d e 1 9 59 ) . ~ L eav es ; (3 F lo w ers ; 9 R o o t s ; . . . . S h o o tw a te r

root pressure, presumably result from secretion of sugarsinto the xylem sap (Sauter 1980; Braun 1984) and causerefilling of embolized vessels. A burst of fine root growthfollowed rehydration of shoots and enabled increasedwater absorption and accelerated shoot and leaf expansion(Fig. 8, day 10-35). In J u g l a n s as in tropical lightwoodtrees, a phase of slow initial shoot development relying onuse of stored water and water shifting thus precedes rapidshoot growth and leaf expansion, wh ich require mois t soil,a well-developed root system and rapid water transport

driven by water loss in the expanding foliage.Differences in the water content of bark and wood areenhanced after the unfolding of leaves. Wood water con-tent declines throughout the summer with increasing tran-spiration, while bark water content almost doubles duringearly summer, when soluble products of photosynthesisabound, and then declines during late summer, when starchaccumulates at the expense of the solute content of barkparenchyma (Fig. 1; Gibbs 1958; Sauter 1966). Woodwater content increases again in fall after the elimination oftranspirational water loss by le af abscission.

O s m o t i c w a t e r t r a n s p o r t a n d w a t e r s h if t in gin t rop ica l t rees

As in temperate trees, water content of the bark in baretropical lightwood trees was about twice that of the wood,a fact more likely to reflect the higher dry weight of woo dthan significant physiological differences (Fig. 5). In allspecies analyzed, solute content was d istinctly higher inthe wood than in the bark and had a maximum in theoutermost layer of the wood (Fig. 5), foun d to be free ofstarch deposits in B u r s e r a and other lightwood species(Fink 1982). Although such trees lack distinct annual ringsand a distinction between sap- and heartwood, there is a

123

Tab le 3 . Water and so lu te con ten t o f a fa l lenCochlospermum trunkb asedon data in F ig . 5

Heigh t o f main t runk 12 .15 mB ase d i am e te r 4 2 . 6 cmTop d iame ter 16 .6 cmVo l u m e 8 3 6 d m3W o o d d en s i ty 0 . 1 9 g . cm 3W a t e r c o n t e n t ( e s ti m a te d 7 0 % ) 5 8 5 d m 3

So lu te con ten t (es t imated 0 .4 osmol) 234 molS u cro se , 2 3 4 m o l 8 0 k g

clear physiological zonation with respect to solute contentand starch deposition. The parenchymatic sheath sur-rounding the vessels (paratracheal contact parenchyma)usually remains free of starch and contains acidphosphatases, enzymes inv olved in the secretion of sugarsinto the xylem, which are found only around functioning,water-conducting vessels and are most active during budbreak in temperate and tropical trees (Fink 1982; Braun1984).

Maxima o f solute concentrations in the outer wood con-taining the vessels active in water transport indicat e a Wosmbetween -1.7 and -2.1 MPa at the lowest end of a waterpotential gradient (A ~ approx. 1 MPa) drawing waterfrom the inner to the outer layers of the woo d (Fig. 5). Thisgradient is similar to, but much more extended than,gradients measured 70 years ago (>60 mm v s 10 cell lay-ers; Ursprung and Hayoz 1922). To enable upward watershifting, Wosm in branches should be even more negativethan in the trunk.

In the the evergreen lightwood-tree G m e l i n agrowing ata moist site, Udleaf and U~osm of the wood parenc hyma were

about twice as high (Figs. 4 C, 5 D) as in the drought-toler-ant lightwood species E n t e r o l o b i u m(Figs. 4A , 5 C). Ex-trapolation of the solute content of stem cores to thevolume of a whole tree yields substantial quantities ofsoluble carbohydrates (Table 3; Fig. 5), which were notreduced during growth of lightwood species (Bullock1992).

In leaf-exchanging tropical trees acid phosphatase ac-tivity around vessels is less seasonal than in temperatetrees, and guttation or bleeding, indicative of x ylem pres-sure, have been observed repeatedly (Fink 1982). Pi th e -c e lo b iu m which rehydrates before leaf shedding(Fig. 6 A), is referred to as rain tree because of the abun-

dant guttation of young shoots expanding after leaf fallduring the dry season (Fink 1982; Braun 1984). In view ofsuch observations and the seasonality of fine root prolifera-tion in tropical dry forests (Kummerow et al. 1990), itappears like ly that as in J u g l a n s (Fig. 8) extension of rootsinto moist soil layers as well as osmotic adjustment instems contribute to the increase in t l Js tem before leaf fall(Fig. 6). Increased availability of subsoil water or osmoticadjustment in leaves are indicated by the observed in-creases in predawn Udleaf during rehydration of stem tissues(Fig. 6A, D). As in leaves, osmotic adjustment of stemtissues of tropical trees is likely to be triggered by waterstress (Pallardy et al. 1991).


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Water s ta tus and deve lopme nt in t ropical andtemperate t rees

Flow er ing and f lushing af ter leaf fa l l dur ing the dry seasonwere p rop osed ea r l i e r t o r esul t f rom ba lancing t r ee wa te recono my by l ea f shedd ing Re ich and Borcher t 1984 ;Borc her t 1991, 1992) . The com parat ive analysis of bud

break and f lowe r ing under a var ie ty of condi tions indicatesthat the prerequisi tes for rehydrat ion and bud break aremore complex. In t ropical as in temperate t rees establ ish-men t of re la t ively high solute concentrat ions in s tem t is-sues by osmot i c a d jus tmen t i s needed bo th to p rov ide thedr iving force for rehydraf ion of desiccated branches and asa supply in organic nutr ients for growing bu ds Figs. 6, 7) .Once wate r supp ly i s adequa te and embol i zed vesse l s havebeen ref i l led , osmot ic water uptake by stem t issues wi l lesta blis h a hig h Udstem.Correspondingly, cont inued mainte-nanc e of a h igh Udstemdepend s on maintaining a high soluteconc entra tion e. g. bare Dlight trees, Fig. 5; shoots bearingyoung , matu re l eaves , F ig . 1 M ay- Jun e) . Vege ta t ive o rr ep roduc t ive buds wi l l expand and shoo t g rowth wi l l besustaine d only if and as lon g as bot h Udstem andU~txylem= q~leaf ) remain higher than the grow th- induced water p o-

tent ia l generated b y the expanding ce l ls of a grow ing organBoyer 1988) .

Character izat ion of t ree water s ta tus by two var iables,tI tstemand t lOleaf (= Uttxylem), as rec om me nde d ea rlier Brad-ford and Hsiao 1982) , proved crucial for understanding theobserved pa t t e rns o f t r ee deve lopm ent dur ing seasona ld rough t . For example , f lower ing o r bud g rowth r emaininhibi ted in rehydrated branches wi th a high ~stem by thepresence o f senescen t l eaves wi th a low~ l e a f Fig. 6) orma y be ar rested by a decre ase in Wstem resul t ing f rominsuff ic ient replenishment of water v ia water shi f t ing

F i g s . 4 B ; 8 ,0 - 7 days ; a rr es t o f ea r ly shoo t g rowth indrought-st ressed l ightwood t rees) . S imilar ly, growth ofnew organs on shoo t s bear ing young l eaves wi th h ighsolute product ion, such as prolonged sh oot extension e . g .Populus, Sal ix , recurrent f lushing e .g .Quercus orf lower ing a t the end o f a f lush o f shoo t g rowth hapaxan-thic f lower ing of ma ny t ropical t rees) should occur only aslong as soil moisture is plentiful and a high Udleaf s main-tained.

Acknowledgements.I am v e ry g ra t e fu l t o t h e m o re t h an 3 0 E A RT H -WA T C H v o lu n tee r s , w h o se f i n an c i a l su p p o r t an d re l i abl e an d en th u s i a s-t ic co l laborat ion made th is s tudy possib le . Thanks are a lso due to thefo l lowing persons, who con tr ibu ted in var ious ways to the p ro ject : the

man agers o f La Pacif ica , P. Net t and Ing . F. Estrada, p rov ided log is t icalsu p p o r t an d p e rm is s io n to d o f i e ld w o rk in t h e h ac i en d a ; W. H ag n au e rgave valuab le log is t ical support and adv ice; Dr. Ken Glander, DukeUniver s i ty, and the Cen tro Eco lbg ico La Pacif ica p rov ided keys to largesets o f tagged an d class i f ied t rees . I appreciate the valuab le suggest ionsof the rev iew ers o f th is paper.

R e f e r e n c e s

A d d ico t t F r r (1 9 9 1 ) A b sc i s s io n : sh ed d in g o f p a r t s. I n : R ag h av en d ra A S(ed ) P h y s io lo g y o f tr ees . Wi l ey, N ew Yo rk , p p 2 7 3 - 3 0 0

Barajas-Morales J (1987) Wood specif ic g rav i ty f rom two t rop ical fo r-e s t s i n M ex ico . IAW A B u l l n s 8: 1 4 3 -1 4 8

B lan ch a rd R O W, S h o r t le W C , D av i s W (1 9 8 3 ) M ech an i sm re l a t in gcamb ial e lect ric res is tance to per iod ic g rowth ra te o f balsam f i r. CanJ F o r R e s 1 3 : 4 7 2 - 4 8 0

B o d e H R (1 9 5 9 ) U b er d en Z u sam m en h an g zw i sch en B la t t en tf a l t u ng u nN eu b i ld u n g d e r S au g w u rze ln b e iJuglans. B er D t sch B o t G es 7 2 :9 3 - 9 8

B o rch e r t R (1 9 9 1 ) G ro w th p e r io d i c it y an d d o rm an cy. In : R ag h av en d rA S (ed ) P h y s io lo g y o f tr ees. Wi l ey, N ew Yo rk , 2 1 9 - 2 4 3

Borc her t R (1992) Compu ter s imulat ion o f t ree g rowth per iod ici ty ancl imat ic hydroper iod ici ty in t rop ical fo res ts . B io t rop ica 24 :3 85 - 395

Borc her t R (1993 a) S i te water avai lab i l ity and s tem water s to rage determine water s ta tus , pheno logy and d is t r ibu t ion o f t rees in a t rop icald ry fo res t in Costa Rica. Eco logy ( in p ress)

Borc her t R (1993 b ) Rain - induced rehydrat ion and bud b re ak in deciduous hardw ood t rees o f a t rop ical d ry fo res t in Costa Rica. T rees ( inp ress)

Boye r JS (1988) Cel l -en largem ent and g row th- induced water po ten t ia lsPhysio l P lan t 73 :31 1 - 316

Bradfo rd KJ, Hsiao TC (1982) Physio log ical responses to moderatwater s t ress . In : Lange OL, Nobel PS , Osmond CB, Z ieg ler H (edsPhysio log ical p lan t eco logy I I . W ater re la t ions and carbon ass imila-t ion . Spr inger, Ber l in Heidelberg New York , pp 263 -3 24

B rau n H J (1 9 6 0 ) D er A n sch lu ss y o n L au b k n o sp en an d as H o lz d eTrag ach sen . B e r D t sch B o t G es 7 3 :2 5 8 - 2 6 4

Brau n HJ (1961) D ie f r t ih jah rszei t l iche Wa sservers ch iebung in Bi iumenund Pfropfreisern . Z Bo t 49 :9 6 - 109Brau n HJ (1984) The s ign if icance o f the accesso ry t i ssues o f the hy

d ro sy s tem fo r o sm o t i c w a te r sh i f ti n g . IAW A B u l l n s 5 :2 7 5 - 2 9 4Bul lock SH (1992) Seasonal d i fferences in non-s t rnctu ral carbohydr ate

in tw o d i ec io u s m o n so o n -c l im a te tr ees. B io t ro p i ca 2 4: 1 4 0 -1 4 5B u l lo ck S H , S o l i s -M ag a l l an es JA (1 9 9 0 ) P h en o lo g y o f can o p y t r ees o f

t rop ical deciduous fo res t in Mexico . B io t rop ica 22 : 22 - 35C r i so s to C H , G ran tz D A , M ein ze r F C (1 9 9 2 ) E ffec t s o f w a te r d e f i c it o

f lower open ing in co ffee Coffea arabicaL.). Tree Physiol 10:1 2 7 - 1 3 9

Daubenmire R (1972) Pheno logy and o ther character is t ics o f t rop icasemi-deciduous fo res t in nor thwestern Costa Rica. J Eco l 60 :1 4 7 - 1 7 0

D ix o n M A , T h o m p so n R G , F en so m D S (1 9 7 8 ) E lec tr i c r e si s t an ce m easurem ent o f water po ten t ia l in avocado and w hi te sp ruce. Can J F o

R es 8 : 7 3 - 8 0F in k S (1 9 8 2 ) H i s to chem isch e U n te r su ch u n g en t i b e r S t~ k ev e r t e i l u n g

und Ph osphataseak t iv id i t im H olz e in iger t rop ischer Baum arten .H o lz fo r sch u ng 3 6 : 2 9 5 - 3 0 2

F ran k ie G W, B ak er H G , O p le r PA (1 9 7 4 ) C o m p ara t iv e p h en o lo g icastud ies o f t rees in t rop ical wet and d ry fo res ts in the lowlands o fC o s t a R ica. J E co l 6 2 :8 8 1 -9 1 9

Gibbs RD (1958) Pat terns o f the seasonal water con ten t o f t rees . InT h im an n K V (ed) T h e p h y s io lo g y o f fo re s t tr ees. R o n a ld , N ew Yo rkpp 43 - 69

Hagnauer W (1993) E1 s is tema agroeco log ico de Guanacaste : oportun idades y desaf ios para la ag r icu l tu ra y e l tu r ismo . Fund . Desarro l loSost. Cafias. Cafias, C osta Ric a

Hartshorn GS (1983) P lan ts . In t roduct ion . In : Janzen DH (ed)Costa Rican natu ral h is to ry. Un ivers i ty o f Ch icago Press , Ch icagop p 11 8 - 1 5 7

Hinck ley TM, Rich ter H, Schu l te PJ (1991) Water re la t ions . In :Ragha vendra AS (ed ) Physio logy o f t rees . Wiley, New York ,p p 1 3 7 - 1 6 2

L im in g F G (1 9 5 7 ) H o m e-m ad e d en d ro m ete r s . J F o r 5 5 : 5 7 5 - 5 7 7Kum mer ow J , Casf i l lanos J , Ma as M, Lar igauder ie A (1990) P roduct io

of f ine roo ts and the seasonal i ty o f thei r g rowth in a Mexican d eciduo u s d ry fo res t . Veg e ta ti o 9 0 : 7 3 - 8 0

Olivares E , Me dina E (1992) W ater and nu tr ien t re la t ions o f woodyperenn ials f rom t rop ical d ry fo res ts . J Veg Sci 3 :3 83 - 39 2

Pal lardy SG , Perei ra JS , Parker WC (1991 ) Measur ing the s ta te o f watein t ree systems. In : Lasso ie JP, Hinck ley TM (eds) Techn iques andapproaches in fo res t t ree ecophysio logy. CRC Press , Boca Raton ,p p 2 7 - 7 6


11/11

Reich PB, Borcher t R 1982) Phenolog y and ecoph ys io logy of the tropi -cal t ree Tabebu ia neochrysan tha Bignoniaceae) . Ecology 63:2 9 4 - 2 9 9

Reich PB, Borcher t R 1984) W ater s tress and t ree phenology in at r op ic a l d ry f o r e s t i n t h e lowl a n ds o f Co s t a R i c a . J Ec o1 7 2 : 61 - 74

Reich PB, Borche r t R 1988) Chang es wi th l eaf age in s tomata l func t ionand water s t a tus of severa l t ropica l t r ee spec ies . Biot ropica 20:6 0 - 6 9

Roth I 1981) St ruc tura l pa t te rns of t ropica l barks , Enc ycloped ia of p lantana tomy v ol IX/3 , Gebr. Bornt raeger, Ber l in

Sauter JJ 1966) Untersuchun gen zur Phys io lo gie der Pappel -holzs t rahlen . I . Jahresper iodi scher Ve r lauf der Starkespe ichernng imHol z s t ra h l pa re nc h y m . Z P f l a nz e np hy s i o155 : 246 - 2 58

125

Sauter JJ 1980) Seasonal var ia t ion of sucrose content in the xylem sapSalix.Z P f l a n z e n p h y s io 1 9 8 : 3 7 7 - 3 9 1

Sc hu l z e ED, M oon e y HA, Bu l l o c k SH, M e ndoz a A 1 988 ) Wa t e r c otent s of woo d of t ropica l dec iduous fores t s dur ing the dry season. BSoc Bo t M e x 48 : 11 3 - 118

S i nc l a ir TR, Lud l ow M M 1 9 85) W h o t a ugh t p l a n ts t h e r m o dy na m i cThe unful f i l l ed potent i a l of the water potent i a l . Aus t J Plant Phys i1 2 : 2 1 3 - 2 1 7

Sobrado MA 1986) A spec t s of t i s sue water re la t ions and seasonchanges in l eaf water potent i a l compon ents of evergreen and dec idous spec ies coexi s t ing in t ropica l fores t s . Oe cologia 68:413 -4 16

Ursprung A, Hay oz C 1922) Zur Kenntni s der Saugkraf t . VI . Ber DtsB o t G es 4 0 : 3 6 8 - 3 7 5

Borchet R. Water Status and Development of Tropical Trees During Seasonal Drought

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