‡Rhode Island Hospital and Brown Medical School,Rhode Island 02903, USA§Department of Neurology, Children’s Hospital,Boston, Massachusetts 02115, USA1. Patrick, G. N. et al. Nature 402, 615–622 (1999).2. Lee, K. Y. et al. Neurosci. Res. 34, 21–29 (1999).3. Nguyen, M. D., Lariviere, R. C. & Julien, J.-P. Neuron 30,135–147 (2001).4. Grynspan, R., Griffin, W. R., Cataldo, A., Katayama, S. &Nixon, R. Brain Res. 763, 145–158 (1997).EcosystemsReef corals bleach tosurvive changeThe bleaching of coral reefs, in whichsymbiotic algae are lost from reef-building invertebrates, is usually con-sidered to be a drastic and damagingresponse to adverse environmental condi-tions1,2. Here I report results from trans-plant experiments involving differentcombinations of coral host and algal symbiont that support an alternative view,in which bleaching offers a high-risk ecological opportunity for reef corals to ridthemselves rapidly of suboptimal algae and to acquire new partners. This strategycould be an advantage to coral reefs that face increasingly frequent and severeepisodes of mass bleaching as a result ofprojected climate change2,3.Coral reefs are built by symbiosesbetween scleractinian (stony) corals andphotosynthetic dinoflagellate algae. Thesediverse algae4are important species becausetheir loss during bleaching can lead towidespread coral mortality and degradationof reef ecosystems5. Different types of algalsymbiont often show strong zonal patternswithin their coral hosts that correspond tolight intensity (shallow, ‘high-light’ algae ordeep, ‘low-light’ algae)6–8.To investigate the effect of bleaching onthe stability of these depth distributions, Ireciprocally transplanted eight species ofCaribbean scleractinian coral between ‘shallow’ (2–4 m) and ‘deep’ (20–23 m) sitesin the San Blas archipelago, Panamá. Iassessed transplanted and control coloniesfor bleaching after 8 weeks, and for mortali-ty and changes in symbiont taxa after 12 months (Fig. 1).‘Upward’ (deep-to-shallow) transplantsshowed significant bleaching after 8 weeks(11 of 24 colonies partially or severelybleached; 2 others pale), whereas ‘down-ward’ (shallow-to-deep) transplants showedless bleaching (0 of 37 colonies bleached;x2420.7, Fisher’s exact P*0.0001). Surpris-ingly, despite more extensive bleaching,upward transplants showed no mortalityafter 12 months (0 of 24 colonies dead),unlike downward transplants (7 of 37colonies dead; x245.13, Fisher’s exactP40.0358). Control transplants showed nosignificant bleaching or mortality.Changes in the structure of symbiontcommunities explained these surprisingpatterns of bleaching and mortality. Sur-veys of restriction-fragment-length poly-morphisms in genes encoding large-subunitribosomal RNA4,8identified four groups ofSymbiodinium algae (termed A, B, C, and apreviously unassigned clade, D4,8,9) fromthese coral hosts. Five of the eight coral hostspecies showed strong intraspecific patternsof depth zonation in their symbionts; theother three showed no such patterns8(Fig.1). Transplanted coral species that hosteddifferent algae at deep and shallow sitesadjusted their algae distributions to theirnew depths only when transplantedupwards (12 of 16 colonies), and not whentransplanted downwards (1 of 25 colonies;x2422.7, Fisher’s exact P*0.0001).These results reveal an unexpected rela-tionship between acute stress-inducedbleaching (sudden exposure to increasedirradiance after upward transplantation),adaptive change in symbiont communities,and reduced coral host mortality. This contrasts with a lack of bleaching inresponse to chronic stress (lower sustainedirradiance after downward transplanta-tion), no change in symbiont communities,and increased coral mortality. Together,these findings support the view (first pro-posed by theorists10) that coral bleachingcan promote rapid response to environ-mental change by facilitating compensatorychange in algal symbiont communities.brief communicationsNATURE|VOL 411|14 JUNE 2001 |www.nature.com 765Without bleaching, suboptimal host–symbiont combinations persist, leadingeventually to significant host mortality.Reef corals are flexible associations thatcan switch or shuffle symbiont com-munities in response to environmentalchange4,8,10,11. However, there may be costsinvolved, as shown by higher mortality inthe five coral species that vary their algaewith depth (9 of 79 colonies) than in thethree species that do not (0 of 39 colonies;x244.81, Fisher’s exact P*0.0289).Changes in symbiont communities maybe slow unless existing symbionts are firstremoved, suggesting that established symbionts have a significant competitivehome advantage over invasive (or low-abundance) symbionts. Coral bleaching canrapidly remove these symbionts, facilitatingtheir replacement by alternative algae thatare better suited to the new environmentalconditions. Furthermore, the process ofcommunity change, which is facilitated by bleaching, may provide a window for unusual opportunistic symbionts to colonize hosts (and/or proliferate insidethem)9,11,12, as shown by the behaviour ofSymbiodinium A and D in upward-trans-plant experiments.Symbiosis recombination may help toresolve the paradox of reef corals as environ-mentally fragile yet geologically long-livedassociations13. Despite the extreme risksinvolved1,2, and the likely high incidence ofmortality in some regions (such as thatresulting from the 1997–98 El Niño14),Figure 1 Symbiont diversity and mortality responses to bleaching in transplanted corals. Bars show symbiont community structure (Symbiodinium clades A–D) before transplantation and 12 months after transplantation: white, A; orange, B; red, C; green, D; black,dead. Pie charts indicate bleaching status of host colonies before transplantation and 8 weeks after transplantation: dark green, healthy;light green, pale; orange, partial bleaching; white, severe bleaching; black, dead. Vertical axes, number of colonies; horizontal axes, coralspecies. Si, Pg, Pb, Dl, Ds and Ac (white background) have strong light-related patterns of symbiont diversity; Ss, Cn and Mc (blue back-ground) exhibit no light-related patterns of symbiont diversity. Control colonies accompanied the transplanted corals to their new locationbefore being returned immediately to their original depths. ND, no data: Ds and Ac were very rare at the deeper location and underwentshallow-to-deep transplantation only (at similar depths nearby they were not