Increasing complexity - decreasing flexibility. A ...

Profil 16: 135-147;3 Figs.; Stuttgart 1999

Increasingcomplexity- decreasing flexibility. A differentperspective of reefevolutionthroughtime Rrrruuolo R. LerrurelDER, MürucuEN* & Mnnll.lNose,SrurrcART**

Abstract The evolution of reef systems is dependent on a great variety of factors. Evolution, a d a p t i v e r a d i a t i o n ,a n d e x t i n c t i o n o f r e e f o r g a n i s m sp r o v i d e t h e r e e f b u i l d i n g p o t e n t i a l whereas plate tectonics,sea-level changes and oceanographicconditions define where and w h e n r e e f s a c t u a l l y d e v e l o p . H o w e v e r , t w o a d d i t i o n a li m p o r t a n t t r e n d s s u p e r i m p o s e t h i s p a t t e r n . T h e s e a r e ( 1 ) t h e e v o l u t i o n o f r e e f b u i l d i n g b l o c k s a n d ( 2 ) t h e v a r i a b l ew i d t h o f the global reef window. In terms of ecological structure and carbonate productivity, reefs are composed of diff e r e n t r e e f b u i l d i n gb l o c k s w h i c h d e f i n e t h e m o d u l a r c o m p l e x i t y o f a r e e f . S u c h b a s i c b u i l ding blocks include microbial,parazoan,metazoan, photosymbiontic and red algal modules. T h e s e b u i l d i n g b l o c k s s u c c e s s i v e l yd e v e l o p e d t h r o u g h o u t t h e e v o l u t i o n o f t h e S y s t e m Earth, and are still all availablein modern reef systems (Reirruen1997). The unidirectionalincrease in modular complexityis partly modified, partly paralleledby the variable environmental sets of physicochemicalconditions which reef organisms demanded and were adapted to. Until the base of the Cenozoic,such global 'reef windows' mostly widened, due to new adaptational strategies of reef organisms (e.g., photoautot r o p h y , b a f f l i n g ,a p h o t o s y m b i o t i ca n d p h o t o s y m b i o t i c r e e f b u i l d i n g ) .T h e r e e f w i n d o w s o f the Late Jurassic to Cretaceous were possibly the widest ever. Subsequently, the modular complexity of reefs and the interdependence of reef biota increased with the improvement of the photosymbioticrelation, the appearence of fast growing corals, new synecologic strategies,and the radiationof encrustingcoralline algae. This resulted in a distinct narrowing of the tropical reef window and, consequently, the separation of a new, distinct, deep-water coral mound window. Reef systems existed nearly throughout the entire Earth history. However, reef evolution was punctuated by global reef crises. Extinctionevents were rapid, but recovery times were very slow. ln the light of possible extinction of modern coral reefs by human impact, Earth history provides two major lessons:The high modular complexity of modern reefs which includes Archaean, Proterozoic,Phanerozoic,Mesozoic,and Cenozoic building blocks makes it likely that some robust reef types such as microbial reefs, Hatimeda-moundsor low-diversity coral meadows might survive. However, lag time for the reestablishment of complex systems, thus for modern coral reefs, are extremely large, often spanning millions of years and hence extendingfar beyond human time scales.

* Prof. Dr. Reinhold Leinfelder, Universitätsinstitut und Bayerische für Paläontologie Staatssammlung und Historische Ge o logieRic har d-Wa g n e r-S 1 0tr. , D -8 0 3 3 3M ü n c h en, Fax 089-2180 6601, r.l ei nfel der@ l rz.uni -muenchen. de emai l : ** Dr. Martin Nose, Institutfür Geologieund Paläontotogie, Universität Stuttgart,Herdweg51, D70174Stuttgart,Fax 0 7 11- 1211341,em a i l :ma rti n .n o s e @ g e o l o g i e . uni -stuttgart.de

136 in the course of reef evolufrom light, developed t i o n , o p t i m i z i n gr e c y c l i n ga n d d e p o s i t o r ys t r a t e gies.This was possibleonly by adaptiveevolution and modifiedthe Reefsystemshave accornpanied and adaptivebreakthroughsin the autecologyand System Earthsince its earliest stages.The oldest synecologyof reef organisms.As a consequence, reef-type bodiesare nearly as old as the oldest general reef variability f irst increasedwith the A r c h a e a nc r u s t ( e . g . N o r t h P o l e , A u s t r a l i a ,3 . 5 of new buildingblocks, but later dedevelopment b i l l i o ny e a r s , L o w E1 9 8 0 ) . D e s p i t et h i s l o n g e v i t y , c r e a s e dd u et o i n c r e a s i n gs p e c i a l i z a t i oann d i n t e r reef systemsare not at all a conservativeelement dependence of reef organisms,which evokednarbut have changedand evolved drastically through r o w i n go f e n v i r o n m e n t at ol l e r a n c e sf o r t h e e n t i r e time" Many different reef organismshave played system. ln each time slice, the physiologicaland important geobiological roles throughout the synecologicaldemandsand abilities of available evolutionof the Earth, producingoxygenduringthe reet organismsdefinethe boundaryconditionsf or Proterozoic,removingtoxic calciumat the end of reef growth. The ecospacebetweenthese multit h e P r e c a m b r i a ns, h a p i n gs h e l v e sa n d i n f l u e n c i n g factorial boundaryconditionscan be termed the t h e c a r b o nc y c l e d u r i n gt h e P h a n e r o z o i ce,s t a b l i global'reef window'of a given time-slice(cf. JarulEs shing strongcompartmentalization of shelf systems & NG 1997, Letrureloen 1992, GITpELDER & Bounoue e v e n i n h i g he n e r g y s e t t i n g sd u r i n gt h e T e r t i a r y , in prep.). As a consein prep., NG & l-eruremen and today assuringexistencefor billionsof people quenceof reef evolutionand availablehabitats,the b y p r o v i d i n gc o a s t l i n ep r o t e c t i o n ,f o o d , p h a r m a w i d t h o f t h e r e e f w i n d o ww a s m a t t e r o f f l u c t u a zeuticsubstances, and touristiceconomicvalue (cf . decreasef rom by a pronounced tions, accompanied l-rruremen & Bnüuuen1998, RErruen 1998, SrerrurruceR the Cenozoiconward(see below). & M n n o r u o1e9 9 7 ) . A widely held view of reef evolution through Like any other ecosystem, reef systems are time is that the many reef crises during Earth h ip a r t i c u l a r l yd r i v e n b y t h e a v a i l a b l ee n e r g y i n p u t storyhave had dramaticalimpactson the evolution and the removal of noxiousby-products.In reef o f t h e r e e f s y s t e m ,A c t u a l l y , s o m e g l o b a le x t i n c s y s t e m s , a d a p t a t i o nt o t h e s e b a s i c r e q u i r e m e n t s t i o n s ( e n d - P e r m i a n ,C r e t a c e o u s / T e r t i a r yb o u n w a s r e f i n e dt o g r e a t p e r f e c t i o n I. n m o d e r nr e e f s , dary)had a strong influenceon the biotic composie f f i c i e n c y i n t h e e n e r g y c o n s u m p t i o ni s n e a r l y r e e f s y s t e m s .O t h e rc r i s e s p a r t p e r f e cd t u e t o d i f f e r e n tn u t r i t i o ns t r a t e g i e s ,i n c l u - i o n o f s u b s e q u e n t ticularly affectedreef biota muchmore than other ding photosymbiosis. Removalof noxiousmatter is biota (such as the intra-Late Devonianand endmaintainedboth by recyclingof phosphates and niTriassic reef crises). Reefextinctionevents were trates via endosymbionts, and by enzymaticneua p p a r e n t l yr a p i d , b u t l a g t i m e s f o r c o m p l e t er e t r a l i z a t i o n ,l e a d i n gt o m i n e r a l i cd e p o s i t i o n s u c ha s establishmentof reef systems were enormous. removalof surpluscalciumby calcareousskeletons the intra-Late Devonianreef crisis it took After ( c f. K e u n Ee t a l . 1 9 8 9 ) . T h e s es t r a t e g i e se v e n t u a l l y m o r e t h a n 1 0 0 m i l l i o ny e a r s f o r m a j o r s h a l l o w resultedin the establishment of a largely indepenwater coral reefs to fully recover, althoughother d e n t , s e l f - s u s t a i n i nsgy s t e m ,w h i c h i s a s t a b l es y reef types were partiallyfilling this gap.After the stem within its environmentalboundaries,but is e n d - P e r m i a en x t i n c t i o ni t t o o k a b o u t f i v e m i l l i o n very vulnerable,if the amplitudeor frequencyof yearsfor the first reefsto reappear(FuÜcel1997), physicochemical disturbanceextendsbeyondthese after the reef crisis at the base of the Jurassic limits. thoughdebated,lag there is anotherconsiderable, ComparingAncientreefs with modernreefs has (Letrureoen1994). However, once re time to take processesof reef evolutioninto account. reefsgained,and increased,their preestablished, Maximumcomplexityof reefs has increasedcontivious modular complexity almost instantly. This n u o u s l yt h r o u g ht i m e , w h i c h i m p l i e st h a t t h e e n v i shows that extinction events and reef crises r o n m e n t afll e x i b i l i t yo f r e e f s y s t e m sw a s d i f f e r e n t mostly had an impacton the type and frequencyof duringearlierstagesin the evolutionof the System reefs by reducingthe diversity of important reef Earth. Trophic, structural and productiveaspects organisms(such as corals) or even eliminating of the reef systemcan be differentiatedin a modus o m e m a j o r t a x a ( e . g . a r c h a e o c y a t h i d sr,i c h t lar set of reef buildingblocks.Thesedifferent mohofeniidbrachiopods,rudistid bivalves), but not dulesappearedone after the other in the courseof generallyon the modularcomplexityof reefs when Earth history and remainedavailablein all subseo f b u i l d i n gb l o c k s .A s a w h o l e , r e e f q u e n tr e e f s ( R r m e n1 9 9 8 ; F i g . 1 ) . E n e r g ym a n a g e - s e e ni n t e r m s crises had therefore little impact on the general menthas not alwaysbeen as perfect as it is today. evolutionof the reef ecosystemthroughtime, ex' T h e m o d e r n ,n e a r l yc l o s e d - c i r c usi yt s t e m ,w h i c h i s cept for causinglargelag times. mainly dependenton the easily available energy

INTRODUCTION

137 relatedto bacterialfilms, probablysharingenergy flow in a symbiotic relation (cf. Rernen1993, et al. 1996). This results in preScHurvrRr.rr'r-Krruoel f e r r e d n o n - e n z y m a t i cm, i c r o b i a l l yi n d u c e dc a l c i f i microbolites (autocation of sponge-containing micrite formation sensu Rernvrnet al. 1995). Availabilityof soft and siliceousspongesprobably also increasedthe capacityto baffle allochthonous THE FIRSTMEGATREND: calcareousmuds and enlargedthe upward-facing I N C R E A S EO F R E E F B U I L D I N G area of reefs due to formation of irregular surfaces. Contributionof sponges ('parazoans')in B L O CK S reefsmay havearisenin Middleto Late Proterozoic times (RBB 3: Soft/Siliceous SpongeReef Building Microbialcalcification reefs composedof RBB1 (1998)has introducedthe con- Block).Sponge-microbial Recently,RetrrueR parts major of Earth history (see cept of modularityin reef systems.This conceptis 3 accompanied r e v i e w e d ,d i s c u s s e da, n de n l a r g e dh e r e ( F i g .1 ) . I n F i g .1 ) . Onset of enzymaticcalcification a b r o a dm a n n e r ,r e e f s r e p r e s e n tp r e s e r v a b l ec a r The next reef buildingblockto developwas the bonatebodiesproduced,or induced,by epibenthic organisms. This definition does not includeany spe- i n v e n t i o no f e n z y m a t i cc a l c i f i c a t i o ni n e p i b e n t h i c 'parazoans'(RBB 4: CalcareousSpongeReef Builc i f i c w a t e r d e p t ho r r e l i e f . I n t h i s b r o a d s e n s e , r e e f s e x i s t e d s i n c e t h e e a r l i e s t A r c h a e a nS . t r o - ding Block). This was invented by the enigmatic in the Neoproterozoic,about m a t o l i t e - l i k eb o d i e sa r e a s o l d a s 3 . 5 b i l l i o ny e a r s Claudina-organisms 1998), then refined by ( L o w e1 9 8 0 , W r u - r e1n9 8 3 ) . S i m p l e s t r o m a t o l i t i c 600 Mio years ago (Rrrruen ' c a l c a r e o ussp' o n g e si n t h e E a r l y C a m b r i a n( a r m i c r o b o l i t er e e f s p r o l i f e r a t e df r o m a b o u tt w o b i l - t h e reefs),andfurther developedboth by l i o n y e a r s o n w a r d ,a n d g r e a t l y c o n t r i b u t e dt o t h e chaeocyathid (now mostly consideredas the stromatoporoids originof hydrospheric and atmospheric oxygen.The si ncel e r o s p o n g e s w ' ) ,h i c hf l o u d e m o s p o n g i d ' c o r a l l rnicrobolites probably of the Archaeanwere mostly p a r t i c u l a r l y i n M i d P a l e o z o r i c e e f systems, r i s h e d built of chemolithotropha i cn d h e t e r o t r o p h i ca n group. sponges Coralline sponge and the Calcarea aerobic bacteria (RBB 1: Anaerobic Microbolite reef bodies formation of to the directly contributed Reef Building Block), whereas energy input has baffle to were also able with and their skeletons, changedto solar energy at least since the early w e r e o f imf o u r R B B s m e n t i o n e d A l l s e d i m e n t s . Proterozoic by the development of autotrophiccyaEarth portance reef during in types many different nobacteria,later accompanied by unicellularalgae these where they are still today, History and so (RBB 2: PhotoautotrophicMicrobolite Reef Building BIock)S . t r o m a t o l i t i cr e e f s , c o m p o s eodf R B B 1 - 2 , b a c t e r i a - s p o n gree l a t e d m o d u l e sp a r t i c u l a r l y d e were, from the base of the Phanerozoic onward, velopin cavesand cavitiesof moderntropical coral 1993). accompanied by many other reef types dominated, reefs(cf. Retrruen by highermetazoans Carbonateproduction or characterized, by 'parazoans' (sponges)or 'true' The nextstep to increasingthe modularcomplemetazoans.Probably due to this competition, s t r o m a t o l i t e sh a d t o w i t h d r a w t o e x t r e m e e n v i - xity of the reef ecosystemswas the occurrenceof 'true' metazoans,chiefly Paleoronmentsnot suitablefor other reef organisms. calcareoussessile Such settings include hypersalineponds, deep- zoic heterotrophiccorals, which fed on sources water settings, intratidal and supratidalflats, o r differentfrom thosefor the sponges.Spongesare f r e s h w a t e re n v i r o n m e n t sw, h e r e p u r e m i c r o b o l i t e s l a r g e l y b a c t e r i a - f i l t e r e rasn db a c t e r i a - c u l t i v a t o r s , 1997), can still be found today. Thoughoften overlooked, as well as osmotrophicfeeders (Knnurren m i c r o b i acl a r b o n a t e w s e r e , n e v e r t h e l e s so,f v a r i a - whereascorals, amongmany other ways of nutrible importancein most other Phanerozoic reef t y - tion feed on zooplanktonand small nekton, hence pes, includingpresent tropical coral reefs (Lerr'r-usingan alternativeenergy source (RBB 5: Meta' rs-DER et al. 1993b, Mourneerorur & Cnuorrl1ggg, zoan Reef BuildingBlock). ScHt',lto 1996). The scopeof this paper is to outlinea modern view of reef evolutionthroughtime by combining the conceptof increasingmodularcomplexitywith the conceptof waxing andwaningof reef windows throughtime, both of which are discussedin more detailin the followingchapters.

Microbial- soft sponge consortium

E n h a n c e m e not f m o d u l a r c o m p l e x i t y by autophototrophicsymbiosis

The next event in the evolutionof the reef ecosymbiotic of autophototrophic The development system was the rise of epibenthic'parazoans'and relationsin reef metazoanswas a major event in t h e i r i n d i r e c tc o n t r i b u t i o nt o r e e f f o r m a t i o n .S o f t r e e f e v o l u t i o n ,a l l o w i n gt h e i r h o s t s t o d i r e c t l y spongesand siliceousspongesare often intimately control primary organic and skeletal production

138

Quaternary

7b: Corallinealgaein highlyabrasiveseüings 7a. Corallinealgaeas majorbindersand constructors

6: Photosymbiontic metazoanrelation

5: Enzymatically calcifying,true'reef metazoans 4: Enzymatically calcifyingreef parazoans 3: Soft or SiO2-spiculedreef parazoans 2: Photoautotrophic microboliteformation 1: Anaerobicmicroboliteformation JuraSsic Reefs:

RBB 1-2: Pure microbolites RBB 1-3 (+/-4,5):Siliceoussponge - microbolitemounds RBB 1-6: Coral reefs

F i g ' 1 . T h e d e v e l o p m e n to f r e e f b u i l d i n gb l o c k s ( R R B s ) t h r o u g h o u tE a r t h h i s t o r y ( a f t e r F E n n r n1 9 9 8 , m o d i f i e d ) . M o d u l a r complexity in ecological structure and carbonate productivity increasestowards modern reefs. Time not to scale. Note t h a t a l l r e e f b u i l d i n g m o d u l e s h a v e s u n , i v e d a n d a r e f u n c t i o n a l u n t i l t o d a y . M o s t o f t h e P r e c a m b r i a nt o P a l e o z o i c modules today are present in the cavity system of modern reefs. At a given time slice, individual reefs need not have maximum potential modular complexity. This is exemplified by the Jurassic time slice (black frame). Jurassic reefs comprise at least three basic reef groups which differ by their modular complexity.

(RBB 6: Metazoan Photosymbiosis Reef Buitding a n d G t u e t a l . ( 1 9 9 5 ) , a m o n go t h e r s , g i v e a r g u B l o c k ) .l t i s u n c l e a ra s t o w h i c h t i m e i n t e r v a l p h o - mentsagainstphotosymbiosis in rudistids. t o s y m b i o s ifsi r s t d e v e l o p e dM . a n ym o d e r nc a l c a r e ous spongeshave photosymbionts,and based on The impact of coralline algae fairly rapid growth rates of paleozoicstromatopoThe last major event in reef evolutionwas the roids(Cowrru1988,KensHnwlgg8), it may be gues- participationof encrustingcoralline red algae in sed that quite some of them already possessed reef formation (RBB 7: Coralline Algae Reef Builphotosymbionts. As to corals it is widely debated ding Block).Redalgaeof various groupswere prewhetheror not Paleozoicforms had photosymbionts sent but, apart from several exceptions, not (Coweru 1988,Nuoos& Dnv 1gg7, RGEllet al. 1 g g 1 , s t r u c t u r a l l yi m p o r t a n tf o r r e e f f o r m a t i o np r i o r t o Scnurrroru 1998). Certainly, photosymbioticrela- Late Cretaceous and Tertiarytimes.Some,but protions were inventedvarious times independently bably not all phylloid algae of Palaeozoicreefs from each other.lt is also unclear,from which time might actually also representred algae (Rtotrue & onward the modern group of corals, the GtJo1992), but they were sedimentbaffler rather scleractinians, have developed photosymbiotic than encrusters.The first alga of coralline algal forms. There is good evidencethat at least since affinity, Marinella lugeoni, arose during the Late the Jurassic,and probablystartingin Late Triassic Jurassic(Letruremen 1993).Althoughocca& Wenruen time (Srnrulrv & Swnnrlgg5), scleractinianspos- s i o n a l l y o c c u r r i n g i n r o c k - f o r m i n g q u a n t i t i e si n sessedsymbiotic algae,althoughthe efficiencyof other environments, the taxon was only a marginal the symbioticsystem was certainly lower than to- elementin reef settings"lt was only from the later d a y , m a k i n gm a n y J u r a s s i c c o r a l s s t i l l s t r o n g l y part of the Cretaceousonward that encrusting dependenton heterotrophic uptake of food (Lerr.r-corallinealgaewere of major importancein reefs. reroenet al" 1996, NG & Lrrruretoen 1gg7). Also, Only since that time were the microbial binders for several other extinct reef organisms,such as ( R B B1 , 2 )g e n e r a l lay c c o m p a n i ebdy v e r y e f f e c t i v e somegroupsof the rudistid bivalves,photosymbio- bindingand cementing organisms.lt shouldbe noted sis is plausiblebut difficult to prove (Cower.r 1ggB, that the importanceof coralline algae in modern Keurunruru & Joilr.rsor.r 1g8B). Srn,een(1997, lggB) reefs in discussed controversially (Mnctrrnvne

139 1 9 9 7 ) , b u t t h e r e i s n o d o u b tt h a t i n m o d e r nr e e fs t h r o u g h o ut th e e n t i r e E a r t hh i s t o r y i n s e t t i n g su n of higherreef building pathogen-related lack of corallineschangesthe reef suitablefor the development system considerably(Lrnen & Lrrnrn 1997). Quite blocks. somemoderncoral reef examplesare even domi(3) Our present-day 1997, Tesre tropicalreefs havethe hignated by corallines (LeAo& Gtt{saunc 1 9 9 7 ) .D o u b t l e s sh, i g h - e n e r grye e f c r e s t f o r m a t i o n hest complexityregardingreef buildingblocks(RBB is only possibleby meansof corallines (Mnoru-rvne1 - 7 b ) .l t i s n o t i c e a b lteh a t n o b u i l d i n gb l o c ko f e a r 1 9 9 7 ) , l e a d i n gt o s t r o n g c o m p a r t m e n t a l i z a t i o fn l i e r r e e f s y s t e m sw a s a b a n d o n e dh,i g h l i g h t i ntgh e long, grosso modo, unidirectionalevolutionaryhireef zonesand adjacentenvironments. story of reef ecosystemstructure. Only reefs G e n e r a l a s p e c t s i n t h e d e v e l o p m e n t containingRBBs 1-7 shouldbe consideredhaving structuresimilarto modern reefs. of reef building blocks S e v e r a ls t r a t e g i e si n t h e e v o l u t i o no f r e e f b u i l dingblocksshouldbe emphasized:

THE SECOND MEGATREND W I D E N I N GA N D N A R R O W I N GO F THE REEF WINDOW

( 1 ) D e s p i t et h e f a c t t h a t m a n y e x t i n c t i o n sh a d strong impactson reef organisms(see above),the g e n e r a li n c r e a s ei n m o d u l a rc o m p l e x i t yi s l a r g e l y I n g e n e r a l , i n c r e a s i n gm o d u l a rc o m p l e x i t yo f u n i d i r e c t i o n aFl .o r m o s t o f t h e P h a n e r o z o itci m e , was paralleledby increasingadaptationand reefs of up to six RBBs reef ecosystemswere composed ce f reef organisms. s y n e c o l o g i c ai nl t e r d e p e n d e n o ( F i g . 1 ) . H o w e v e r t, h e i n t r a - L a t eD e v o n i a cno l l a p s e m o d u l a r H o w e v e r , s i m i l a r c o m p l e x i t yd o e sn o t n e o f t h e s t r o m a t o p o r o i d - c o r ar el e f s y s t e m p u s h e d i n d i c a t e s i m i l a r e n v i r o n m e n t adl e m a n d s . c e s s a r i l y m p o r t a n coef R B B 5 ( c a l c i f i e d b a c kt h e q u a n t i t a t i vi e photosymbiotic, r u d i s t i d b i v a l v e s w e r e P r o v i d e d m e t a z o a n sa) n d , i f a l r e a d ye x i s t i n ga t t h a t t i m e , R B B s t r u c t u i r d e e n t i c a l t o m o d e r nr e e f s p o s s i b l y e l i m i n a t e dm o s t o f R B B 6 ( m e t a z o a n t h e y h a d a p r o b a b l y m o s t l yl i v e d i n d i f f e r e n t p h o t o s y m b i o s iw s )h i c h p r o b a b l yw a s r e i n v e n t e di n b u t n e v e r t h e l e s s ( s e eb e l o w ) .M o r e o v e r ,t h e e n v i r o n m e n t a s l e t t i n g s r e e f s y s t e m so n l y i n t h e T r i a s s i c .T h e g a pw a s f i l led by widespreadand better developedRBB 4 fact that earlierreef buildingblockswere not aban(spongecalcification RBB),which gave rise to Late d o n e da l l o w e da m o r e o r l e s s w i d e v a r i a b i l i t y o f P a l e o z o iac n d , a g a i n ,M i d - T r i a s s i cr e e f t y p e s r i c h r e e f s w i t h d i f f e r e n t m o d u l a rc o m p l e x i t yw i t h i n a in calcareousspongesand microbialcarbonate.Ne- g i v e nt i m e s l i c e .l t i s m a i n l yt h e e n v i r o n m e n t adle of the availableparazoanand v e r t h e l e s s ,r e e f s i n c l u d i n gR B B5 ( c a l c i f i e dm e t a - mandsand adaptations reef metazoan taxa that definethe physicochemical zoans)were widespread, althoughthey did not f orm given reef is to. Besidesthis, gea adapted setting l a r g e s t r u c t u r e s .A s a n e x a m p l e ,U p p e r P e r m i a n o f s u i t a b le reef habitats is n e r a l a v a i l a b i l i t y calcisponge-dominated reefs such as the Capitanf a c t o r i n d e t e r m i n i n gw h e t h e r o r c r u c i a l a n o t h e r Massivemay be huge,but roughlycoevalreefs rich not reef types can develop. Generalreef hacertain in rugosan corals or richthofeniid brachiopods i s l a r g e l y a v a i l a b i l i t y c o n t r o l l e db y p l a t et e c b i t a t r e m a i n e ds m a l l ( W e r o u c1H9 9 7 , F w s e t a l . 1 9 9 7 ) . sea-level development and oceanographic tonics, The end-Permianextinction brought an enormous patterns (LerrureloEn 1 994). reductionin reef occurrencesand a subsequent lag time of reef development, but did not alter modular reef complexity trends. The end-CretaceousA r c h a e a n t o T r i a s s i c g l o b a l r e e f windows e x t i n c t i o ne l i m i n a t e da m a j o r r e e f b u i l d i n gg r o u p , the rudistid bivalves, but again, modular The environmental demands for the f i rs t c o m p l e x i t tyr e n d sd i d n o t s u f f e r( F i g . 1 ) . bacterialreefs in the Archaeanare unknownbut w e r e p o s s i b l y w e l l d e f i n e d ; c o n t r o l l i n gf a c t o r s (2) Not all reefsof a giventime had the potential might have beenavailabilityof organic matter o r m a x i m u m m o d u l a r c o m p l e x i t y i n r e e f b u i l d i n g inorganicmethaneas well as calcium and carbob l o c k s .F o r i n s t a n c e ,t h e m i d - P a l e o z o isct r o m a t o - nate/bicarbonateions, suitable water temperaporoid-coralreefs composed of RBBs1-5 or even t u r e s , a l k a l i n i t ya n d p H - v a l u e s ,a n d s t r o n g l y r e rates. A suitableset of these 1-6 were accompanied by spongereef moundscom- ducedsedimentation p o s e do f R B B s1 - 3 o n l y .T h e s a m ei s t r u e o f J u r a s - factorswas probablyonly rarely achieved,making of s i c r e e f sw h i c hi n c l u d ep u r e m i c r o b o l i t e( sR R B 1 " 2 ) Archaeanreef bodiesrare.With the development Precambrian ( R R B cooling of 1 - 3 ) , a s w e l l a s l i g h t - cyanobacteriaand the a n d s p o n g em o u n d s d e p e n d e ncto r a l r e e f s ( R R B1 - 6 ) ( F i g . 1 , 2 ) " P u r e oceans,stromatolitesexpandedvastly into many microbolite reefs (RBBs 1-2) even persisted p h o t i c e n v i r o n m e n t s ,a l t h o u g h l o w i l l u m i n a t i o n

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141 i s s u f f i c i e n tf o r s u c h s i m p l e o r g a n i s m sW . i t h t h e d u e t o i t s t r a n s i t i o n a ls i t u a t i o n .M a n y m a r g i n a l , onset of 'parazoan'and 'true' metazoandevelop- ' s t r e s s e dr' e e f s ( s i l i c i c l a s t irce e f s , b r a c k i s hw a t e r ment, reef ecosystemswere more widely defined. reefs, various deepshelf reefs, dysaerobicreefs) New energy sourceswere openedby new feeding existed,owingto the widespreadoccurrenceof the s t r a t e g i eo s f r e e f o r g a n i s m sM . o r e o v e r ,t h e a b i l i t y ' c o n s e r v a t i v er' e e f o r g a n i s m s( s p o n g e s m , icroboto tolerate certain sedimentationrates, owing to l i t e s ) t o g e t h e rw i t h t h e n e w l y e s t a b l i s h eadd a p t i v e t h e b a f f l i n ga n d b i n d i n ga c t i v i t i e so f t h e r e e f o r g a - s t r a t e g i e s ,p a r t i c u l a r l yw i t h i n c o r a l s . l t w a s t h e n i s m s , l i f t e d t h e m m o r e r a p i d l y t o h i g h e rf e e d i n g time of changetowards photic algal symbiosis in levels. Dependence uponlight diminisheddueto he- scleractiniancorals, with corals thriving both in t e r o t r o p h i cf e e d i n gs t r a t e g i e s .W i t h t h e d e v e l o p - m e s o t r o p h i a c n d i n i n c r e a s i n g l yo l i g o t r o p h i ce n v i s ,d d i t i o n ael n e r g ys o u r c e s ronments (Lerruremen m e n to f p h o t o s y m b i o s ia et al. 1996, NG & |.erruretoeR w e r e i n t r o d u c e dw , i t h o u t a b a n d o n i nrge e f s e t t i n g s 1 9 9 7 ,N o s e& L e r r u r e l o ri n p r e p . () F i g s 2 . ,3). on the deeper shelf. Increasedgrowth rates of 'parazoans' photosymbiotic and metazoans also hel- Cretaceousreef window p e dt o l e r a t i n gh i g h e rb a c k g r o u nsde d i m e n t a t i oann d The reef windowof the mid to late Cretaceous m o r e f r e q u e n t f r a g m e n t a t i o n b y h i g h - e n e r g y s t i l l r e m a i n st o b e d e f i n e d s, i n c et h e r e i s a l o t o f y .u r i n gt h e P a l e o z o i ct ,h e r e e f controversy e v e n t s ,r e s p e c t i v e l D as to the exact environmental demands w i n d o ww a s f a i r l y w i d e i n t h e M i d a n d e a r l y L a t e of rudistidreefsversusCretaceouscoral reefs (cf. Devonian(Fig. 2) (Nose& Lerrurrmrn in prep.), to Knurrvnru & JoHr.rsor.r 1988, Grr_r et al. 1gg5). In b e c o m ec u t o f f i n i t s s h a l l o w / h i g h - e n e r gpya r t g e n e r a lt,h e r e e fw i n d o wr e m a i n e da t l e a s t a s l a r g e o w i n g t o t h e e x t i n c t i o n ,o r d e c i m a t i o no, f h i g h - a s d u r i n gt h e L a t e J u r a s s i c , a l t h o u g hd e e p e rs h e l f e n e r g yr e e f o r g a n i s m sp a r t a t t h e i n t r a - L a t eD e v o - moundreefs becameless important, probablydue n i a nr e e f c r i s i s . F a m e n n i at no L o w e rC a r b o n i f e r o u sto stratified water bodies.Coral reefs started to c o r a l f a c i e s i s l a r g e l y r e s t r i c t e dt o d e e ps e t t i n g s c h a n g et o t h e c o r a l - c o r a l l i n ae l g a lt y p e w h i c h m i g h t ( e . 9 .G r s c s u R 1 9 9 6 ) . N e v e r t h e l e s st h , e m a r g i n so f h a v er e s u l t e di n n a r r o w i n go f t h e i r e n v i r o n m e n t a l t h e s u b s e q u e nrt e e f w i n d o w s , t h o u g h s t r o n g l y t o l e r a n c e sR. u d i s t sm i g h t h a v et a k e no v e r i n m o r e d y r e e f g a p s , r e m a i n e d u n s t a b l er e e f s e t t i n g s s u c h a s t h o s e i n v o l v i n g f l u c t u a t i n ga n d p u n c t u a t e b m o d e r a b l yw i d e , w i t h v e r y d i f f e r e n t y p e s o f r e e f s e l e v a t e d o r f l u c t u a t i n gn u t r i e n t c o n c e n t r a t i o n s , developingduring the Late Paleozoicand into the h i g h e r s e d i m e n t a t i o nr a t e s , o r h o t w a t er Triassic. t e m p e r a t u r e sa s a c o n s e q u e n coef a s u p e r - g r e e n house effect (cf. Glr-ret al. 1995, KAUFFMAN & Jurassic reef window JoHr.rsor.t 1988, 1997, SreueER 1996, 1997, Scorr The Jurassic reef examplesdemonstratethat 19 9 5 , V o r c r 19 9 5 ) . the reef window was very wide, which mostly is

Fig.2. Examplesfor general reef windows (modified from Ler.rreoen1997and Lert'reoen & Nose in prep.. Modern reef window based on Jnves& Bounoue1992, modified, Devonian reef window based on Mnv& Nose,in trlose & Lerrupepen in prep.). Note that the modern tropical/subtropical reef window is smaller than the Devonian and Late Jurassic reef window. Modern reefs occur within two distinct reef windows (tropical/subtropical reefs and deep-water mounds) separated by a bathymetric/nutrient gap. Contrasting, Jurassicreefs occupied a vast potential area across the shelf. Besides the variable size of the reef windows, major differences are the strong oligotrophy and the stronger compartmentalization of modern reefs, as caused by the highly developed photosymbiotic relation and t h e development of algal reef crests in highly abrasive settings. The position for optimum reefs (as defined by maximum modular complexity and maximum taxon diversity) is also variable through time, depending on the adaptional evolutionary stage of reef organisms.Modern optimum reefs occur in shallow, agitated, strongly oligotrophic waters. Jurassicoptimum reefs thrived in slightly deeper, mesotrophic waters. Reefs along the margins of the reef window ('stressed reefs') also differ considerablythrough time. Modern deep-water coral mounds are offset from the tropical reef window by a nutrient and bathymetricgap, and thus do not belong to the same reef window (see Fig. 3). Jurassic deep-water sponge mounds may grade into coral reefs and consequently occupy the same reef window. See text for further explanation.

a) LateJurassic

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143

Cenozoicto modern reef windows

become narrow again after the CretaceAfter the disappearance of the rudistidbivalves o u s / T e r t i a r yb o u n d a r y( F i g s .2 , 3 ) . T h e w i d e m i d d u r i n gt h e e n d - C r e t a c e o ucso, r a l r e e f s h a d d i f f i - Paleozoicand mid/late Mesozoic reef windows cultiesto take over all free marginalsettingsof the share some similarities (sponge reefs and r e e f w i n d o w ,p r e v i o u s l iyn h a b i t e db y r u d i s t s .A f t e r m u d m o u n disn t h e d e e p e r w a t e r s , d i f f e r e n t i a t e d a lag episodeof deep-watercoral reefs during the c o r a l a n do t h e r r e e f t y p e s i n t h e s h a l l o ww a t e r ) , Paleocene, coral-corallinealgal reefs reconquered but it appearsthat marginalsettings were more s h a l l o w e r e n v i r o n m e n t sa n d , i n t h e M i o c e n e , widely exploitedby reefs in the Mesozoicexample became adapted to abrasive highest energy ( F i g .2 ) . T h e n a r r o wL a t e P a l e o z o itco M i d - T r i a s s i c settings.This gave rise to the development of algal r e e f w i n d o w i s q u i t e d i f f e r e n t f r o m t h e n a r r o w to modern reef window, becauseLate ridges (Srnrumr 1989), which causedstrong com- Mid-Tertiary to Mid-Triassicreef types were largely p a r t m e n t a l i z a t i o fn r e e f i n t o e n v i r o n m e n t a lvl ye r y Paleozoic d i f f e r e nzt o n e s ,s u c ha s r e e f f r o n t , r e e f c r e s t / fl a t confinedto somewhatdeepersettings,whereasthe and back reef-lagoonal zones. This has also Cenozoictropical window is still narrower, and f u n d a m e n t a lcl yh a n g e dt h e s e d i m e n t o l o gwyi t h i n t h e r e e f s t h r i v e a l m o s te x c l u s i v e l yi n s h a l l o ww a t e r . (Fnrrwnmet reefs and the reef surroundings. Reef zonationhas Presentdeep-watercoral associations t a l . 1 9 9 7 ) a p p e a rn o t a t a m a r e x i s t e de a r l i e rb u t c o m p l e t es h e l t e r i nogf l a g o o n si n a l . 1 9 9 7 ,H e r u R r ceH h i g h e s te n e r g y e n v i r o n m e n t sn o r m a l l y w a s n o t g i n a l p o s i t i o nw i t h i n , b u t a r e d i s t i n c t l y s e p a r a t e d r el e f w i n d o w , possiblepriorto the development of algal ridges.lt f r o mt h e m o d e r nt r o p i c a l / s u b t r o p i c a their own ecologicalwindow. Kelp s e e m s t h a t m i c r o b i a l l y b o u n d h i g h - e n e r g yr e e f thus possessing r cosyc r e s t s d e v e l o p e do n l y v e r y e x c e p t i o n a l l yd u r i n g f o r e s t sa r e t h e i n t e r m e d i a t seh a l l o w - w a t e e stem modern between deep-water coral associa(Lrrrureloen earliertimesof Earthhistory 1992, l.lcs tions and moderntropical reefs (Fnerwnlo1993, & LerrurrloeR in prep.). H r r u n r ceHt a l . 1 9 9 7 )s, e p a r a t i nbgo t ha l o n ga t e m p e Waxing,waning and splitting of reef r a t u r e a n dn u t r i e n tg r a d i e n t( F i g s .2 , 3 ) . T h e o n l y reefs in slightlydeeperwater,which are not offset w i nd o w s from the moderntropical coral reef window, are l n c o n c l u s i o n ,t h e d e v e l o p m e n to f t h e r e e f w i n Halimeda-green algal mounds,mostly occurringin d o w d i m e n s i o n si s n o t p a r a l l e lw i t h t h e l a r g e l y u n i l e s w a t e r d e p t h s s t h a n 2 0 m ( F i g . 2 ) . H e n c e ,t h e y dir ec t ionaldev e l o p me n t o f re e f b u i l d i n g b l ocks, but overlapin water depthwith coral reefs, but reprere f lec t s bot h m a j o r g l o b a l e n v i ro n m e n ta lc ri ses and sent areaswith slightly highernutrition (RoBERrs et dif f er ent adap ti v e s tra te g i e s o f re e f o rg ani sms. al. 1987a,b) (Fig. 3). Actually, Halimedamay act T h e r e e f w i n d o w w i d e n e dc o n t i n u o u s l yu n t i l t h e i n as a 'pest organism'o , v e r g r o w i n gr e e f s c l e r a c t i tr a- Lat e Dev on i a n re e f c ri s i s , a n d re ma i n ed more n i a n si n p o l l u t e dr e e f s ( e . 9 . , C a r r i b e a n ,p e r s o n a l narrow until the Mid-Triassic. From the Late investigation.

T r i a s s i ct o t h e f i n a l C r e t a c e o u s ,i t w i d e n e d , o n l y t o

Fig. 3. Reef windows are multifactorialsystems which can only be graphicallypresented in a simplified manner. This figure comparesthe triple factor model of Jurassicreefs (a, after LeTTTELDER 1993 and LErrureloeR et al. 1996) with tentative models for modern reefs (b) and Precambrianreefs (c). In relation to the controlling factors 'sediment influx', 'water d e p t h ' , a n d ' n u t r i e n t a n d o x y g e n f l u c t u a t i o n s ' .J u r a s s i cr e e f s w e r e q u i t e t o l e r a n t , w i t h d i f f e r e n t r e e f t y p e s b e i n g t h e product of different positions within the reef window. Modern reefs are much more environmentally restricted than Jurassic reefs in terms of the three factors displayed, resulting in a much smaller reef window (cf. Fig. 2). Halimeda mounds overlap the depth distributionof tropical coral reefs, and are probably related to elevated nutrient influx. Note that modern deep-water coral mounds are offset by a bathymetricand nutrient gap and thus represent an own ecological window (cf. Fig. 2). The position of this window within the triple factor model is tentative. Archaean reefs also grew w i t h i n a v e r y l i m i t e d ,t h o u g h d i f f e r e n t r e e f w i n d o w , b u t p r o b a b l y e x t e n d e d d o w n t o a p h o t i c z o n e s . D u e t o m o d e r a t e light dependence, Proterozoicstromatolitereefs had a narrower window, but, unlike Archaean reefs, could probably cope up with subtle sedimentationowing to the development of trichomal cyanobacteriawith a small sediment baffling capacity.

144

CONCLUSIONS

or even hostilefor reef growth, on costs of their e n v i r o n m e n t af l e x i b i l i t y . lnfluence of geological f actors; Another im lncrease in ecologicaland productive complexity portantfactor influencing the width of a globalreef (modular complexity): Reef systems have existed windowis the generalplate-tectonic,geomorpholofrom Archaeantimes until today. Despitethe fact gic, and oceanographic framework of a given time. that reefs sufferedvarious times from globalexModern reefs grow within a tairly narrow global t i n c t i o n o r s e v e r e r e d u c t i o n ,t h e y h a v e c o n t i n u o u s l yi n c r e a s e d l a x i m u mm o d u l a r reef window not only due to the ouilinedincreased t h e i r p o t e n t i am complexitythroughtime. This is expressedas an modularcomplexity,but also due to partial lack of increasein numberof reef buildingblockswhich are other suitablereef settings.Presently, there obviously is an overall lack of habitatsfor potential the basic modulesfor reef growth, and which successivelyallowedeven complexreefs to deve- mid-rampreefs, which is related to Cenozoicrel o p i n t o a l a r g e l y s e l f - s u s t a i n i n gs y s t e m w i t h s t r u c t u r i n go f t h e s h e l v e sb y f r e q u e n t s e a - l e v e l e n e r g y i n p u t m a i n l y b e i n g d e r i v e d f r o m s o l a r changes,as well as the low sea-level of today (Lerrurelorn 1993, 1994). This does not permit energy. growthof reef spongemoundssimilar to the MesoThe reef window concept.Optimumand stressed zoic or Paleozoic,exceptfor extremely rare, nonreefs: Superimposed on the unidirectionalincrease & Bnnnre 1gg7). paro f a v a i l a b l eb u i l d i n gb l o c k sa r e t h e e n v i r o n m e n t a l reefal occurrences(Coruwnv t i a l l y m i r r o r i n g P h a n e r o z o i c c a r b o n a t ed e e p - w a t e r demandsand abilities of parazoan,metazoanand mounds are modern deep-water coral mounds floral reef organismswhich define the generalphyphanerozoice x (Fnerwnlo et al. 1997). Unlike sicochemical settingfor reef growth.Thesegeneral settingsare describedhere as 'reef windows'.The amples,theseare, however, offset from the moc e n t e ro f a r e e f w i n d o wr e p r e s e n t s' o p t i m u mc' o n - dern tropical reef window by a temperatureand d i t i o n sw h e r e r e e f s o f m a x i m u mm o d u l a rc o m p l e - b a t h y m e t r i cg a p . F o r e x a m p l e ,J u r a s s i c s i l i c e o u s s p o n g em o u n d ss o m e t i m e ss h a l l o w e dc o n t i n u o u s l y , x i t y a n d m a x i m u md i v e r s i t y d e v e l o pT . he window to transform gradually into coral reefs (Lerrurroen width definesthe toleranceof the globalreef s y e t a l . 1 9 9 3 aL, r r r u r E l o rent a l . 1 g g 4 ) . s t e m a t a g i v e n t i m e . T h e m a r g i n so f t h e w i n d o w The fate of modernreefs: ln general,the global a r e c h a r a c t e r i z ebdy l o w - d i v e r s i t y ,b u t n o t n e c e s s a r i l y l o w - m o d u l a rc o m p l e x i t y ,' s t r e s s e d ' r e e fs . reef window widenedin the course of the Late Paleozoicand most parts of the MesoM o d e r ns t r e s s e dr e e f s m a y e x h i b i t b o t h a l o w - d i - Proterozoic, z o i c b u t t h i s t r e n d w a s m a t t e r o f f r e q u e n tf l u c t u a v e r s i t y / l o w - c o m p l e x i tayn d l o w - d i v e r s i t y / h i g h p a r t i c u l a r l yf r o m t h e D e v o n i a nt o t h e M i d t i o n s , complexity pattern. Examples are nutrientstressed Halimeda mounds (cf. RoeEmset al. Triassic.Duringthis time span the width of the reef 1 9 8 7 b ) , a n d s e d i m e n t - s t r e s s ecdo r a l - a l g a lr e e fs windowwas a sum of evolution,adaptationand ext i n c t i o no f r e e f o r g a n i s m sa,n d v a r i a b l ea v a i l a b i l i t y (Gnea et al. 1996, LrAo& Grrusgunc, 1gg7), respecof reef habitats.Contrasting,the Cenozoictrend t i v el y . t o w a r d sf u r t h e r i n c r e a s e d c o m p l e x i t yo f r e e f b u i l Variablewindowdimensions:Global reef window ding blocks was negatively correlated with rapid dimensionswere constderably variableduringEarth n a r r o w i n g o f t h e r e e f w i n d o w ,m o s t l y o w i n gt o i n history. The width of a reef window defines how creasing synecological interdependence of reef oroptimumreefs are bufferedwithin the globalreef ganisms. This trend reflects general the adaptatios y s t e m .A w i d e r e e f w i n d o w i n d i c a t e sw i d e f l e x i n a l s t r a t e g y t o w a r d s a s e l f s u s t a i n i n gl,o w - o l i bility of the global reef system. For example,the gotrophy, buffered ecological system. lf situated in Jurassicglobalreef systemwas more flexible than the center of the reef window, modern reefs would the modernone, with special reef types growing u n d e re l e v a t e ds e d i m e n st t r e s s , f r e s h w a t e ri n f l u - be well bufferedand robust againstperturbances. ence, elevatednutrient flux, even partial oxygen H o w e v e r ,e n v i r o n m e n t as lt r e s s , i n c l u d i n go v e r f i s , h i n g , s e w a g ea n d s e d i m e n ti n f l u x , m a s s t o u r i s m , depletion(Lerruremen 1993, l_enrrmeR et al. 1g96). thinning of the ozonelayer,possibleglobalincrease M o r e o v e r ,t h e c e n t e ro f t h e J u r a s s i cr e e f w i n d o w ' o p t i m u m ' o f t e m p e r a t u r e sa, s w e l l a s i n c r e a s i n gf r e q u e n c y (the c o n d i t i o n sw ) a s n o t i d e n t i c a lw i t h amplitude and of El Nifro-relatedbleachingevents the centerof the modernone. This fact is relatedto pushedthe present coral reefs very has already lower efficiencyof the newly developed photosymbiotic relation in Jurassic corals and the lack of closeto the marginof the reef window, with many r e e f b u i l d i n gc o r a l l i n er e d a l g a ei n J u r a s s i ct i m e s individualcoral reefs having already passed the ( h e n c er e s u l t i n gi n l o w e r m a x i m u mm o d u l a rc o m - window margin. The fact that all reef building blocksare still availablein modernreefs makesit plexitythan today).Consequently, coral reefs have possibleglobalextinctionof moi n c r e a s i n g l cy o n q u e r ehda b i t a t sf o r m e r l y s t r e s s f u l likely that even a dern coral reefs by the outlinedfactors will not

145 completelyerase the globalreef system.Possibly, m i c r o b i a lr e e f s o r o t h e r r o b u s t l o w - c o m p l e x i t y reef types, such as oyster reefs,Halimedamounds, or oligospecificcoral meadowscould survive at places.However,Earth history clearly shows that lag timesfor reestablishment of even less complex reef types than moderncoral reefs are enormous, goingfar beyondhumantime scales.

A C K N O W L E D G E M E N TA SN D R EM A RK S This contribution is dedicated to the 7 S,h birthdayof R.L.'spredecessorand our colleaguein office at Stuttgart University, Prof. Dr. O. Geyer. O. Geyer was not only amongthe first in Germany to establisha successfulworking group for the study of modern coral reefs (see article by his f o r m e r s t u d e n t ,P r o f . D r . J ö r n G e i s t e r ,t h i s v o l u m e )h , e a l s oh a d a s t r o n gf o c u so n J u r a s s i cc o r a l fauna and spongereefs, and therefore has consid e r a b l yi n f l u e n c etdh e w o r k o f t h e p r e s e n ta u t h o r s . O. Geyeralreadywarnedof negativehumanimpact o n m o d e r nc o r a l r e e f s , a t t i m e s w h e r e r e e f p r o tectionwas no generaltopic. t r t i c l ei s a s h o r t e s s a yo n t h e e v o The presena l u t i o n o f r e e f s i n a f t e r m a t ho f t h e D F G - p r i o r i t y program 'Biogenic sedimentation- Evolutionof Reefs'.The article is basedon own researchprojects on Jurassic, Paleozoicand modernreefs, as w e l l a s o n o w n e x p e r i e n c e isn r e e f p r o t e c t i o ni s s u e s , b u t i t a l s o a t t e m p t st o i n t e g r a t ed i f f e r e n t views on reef evolutionprocesses.lt is hopedthat this article may serve as an ouilinefor future comparativeresearchon modernand ancientreef systems, particularlyon analysisof horizontal ( e c o s p a c e - r e l a t e dq) n O v e r t i c a l ( t i m e - r e l a t e d ) stress in reef ecosystems.The 'reef vrindowconcept'presentedhere is an attempttowardsa better understanding of conditionsfor reef growth. This knowledgeis also necessaryto successfullyminimizehumanimpacton existingcoral reefs, to give them a chancefor survival. Parts of this article are basedon fruitful disc u s s i o n sw i t h m a n y c o l l e a g e s ,p a r t i c u l a r l y w i t h D i e t e rS c h m i d ,M u n i c h J, o a c h i mR e i t n e r G , öttingen, A n d r d F r e i w a l d , B r e m e n ,E r i c F l ü g e l , E r l a n g e n , Paul Copper,Sudbury, and GeorgeStanley, J r. , Missoula.WinfriedWernerand AlexanderAltenbach ( b o t hM u n i c h )i s t h a n k e df o r c o n s t r u c t i v ec r i t i c i s m on the manuscript. Financialsupport from the German Research Foundation (DFG-projects Le 5 8 0 / 4 , L e 5 8 0 / 1 0 )i s g r a t e f u l l ya c k n o w l e d g e d .

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