Coral Bleaching as an Adaptive Mechanism

Author(s): Robert W. Buddemeier and Daphne G. Fautin

Source: BioScience, Vol. 43, No. 5 (May, 1993), pp. 320-326
Published by: University of California Press on behalf of the American Institute of Biological Sciences
Stable URL: http://www.jstor.org/stable/1312064 .
Accessed: 15/09/2013 02:28

Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .
http://www.jstor.org/page/info/about/policies/terms.jsp

.
JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of
content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms
of scholarship. For more information about JSTOR, please contact support@jstor.org.

University of California Press and American Institute of Biological Sciences are collaborating with JSTOR to
digitize, preserve and extend access to BioScience.

http://www.jstor.org

This content downloaded from 66.194.72.152 on Sun, 15 Sep 2013 02:28:36 AM

All use subject to JSTOR Terms and Conditions
 Coral Bleachingas an
Adaptive Mechanism
A testable hypothesis

Robert W. Buddemeier and Daphne G. Fautin

leaching in organisms such as temperature stress associated with ei-

hard and soft corals, giant ther the 1982-1983 El Nifio event or
clams, and sea anemones is the
We posit that bleaching with the 1987 Caribbean warm event.
loss of pigment associated with their allows a host to be However, partial or low-level bleach-
symbiotic algae (zooxanthellae). ing also occurs in the absence of per-
Bleaching can be the result of loss of
the pigmented algae from the host or
repopulatedwith a ceptible stress (Fisk and Done 1985,
Gates 1990). Such background bleach-
of loss of pigment from the algae. This differentpartner ing may well have been regarded as an
article considers only the phenom- unexceptional feature of coral reef
enon of algal loss. Most attention has variability before the concern gener-
been directed to bleaching in 1991, Goreau 1990, Williams and ated by mass bleachings and associ-
scleractinian (hard) corals in the trop- Bunkley-Williams 1990). ated mortality in the middle to latter
ics (e.g., Brown 1990, Glynn 1990, In this article, we examine briefly 1980s (Oliver 1985). Thus, bleaching
Williams and Bunkley-Williams some of the salient attributes of bleach- appears to be a basic physiological
1990). It is a subject of concern be- ing and its biological participants, to attribute of many, if not all, organ-
cause of mortality and local extinc- which we refer by the names used in isms having zooxanthellae, both in
tions associated with large-scale the primary literature. We fully real- response to a variety of stresses and in
bleaching episodes (Glynn and de ize that these names may not be accu- the absence of obvious stress.
Weert 1991; but see Glynn and Fein- rate (see Knowlton et al. 1992 for an
gold 1992), the widespread belief that example) and that taxonomic preci- Characteristics of bleaching
bleaching episodes have increased dra- sion of both partners is essential for
matically in frequency and inten- understanding symbioses. We propose Based on published data, we identify
sity within the past decade (D'Elia et a conceptual hypothesis for the role of three key features of coral bleaching
al. 1991), and speculation about pos- bleaching in coral reef ecology and attributed to high temperature:
sible links to global warming (Glynn evolution that is consistent with most
of the available data. We indicate * The upper temperature limit (be-
RobertW. Buddemeieris a senior scien- how this hypothesis can be tested, and yond which bleaching results) is lo-
tist and chief of the GeohydrologySec-
tion at the Kansas Geological Survey,
we discuss its implications for research, cally defined: corals may experience
management, and conservation. local maxima from the mid-20s to the
Lawrence,KS 66047, and courtesypro- Acute bleaching is a generalized mid-30s degrees C, but at least some
fessor of geographyat the Universityof
stress response resulting from a vari- corals of most taxa bleach when the
Kansas,Lawrence,KS 66045. His inter-
ests include coral growth, reef and atoll ety of environmental conditions out- temperature rises a few degrees above
environments,hydrologic systems, and side the normal local range. It can be the local average maximum (Coles et
the effectsof climatechangeand variabil- induced by stimuli such as unusually al. 1976, Cook et al. 1990, Jokiel and
ity. Daphne G. Fautinis an adjunctpro- high or low temperatures, low light Coles 1990). Temperature sensitivity
fessor in the Departmentof Systematics levels or constant light, high levels of is therefore not specific to the coral
and Ecology, Snow Museum, University UVradiation, salinity shock, and other taxon, but it involves some other com-
of Kansas,Lawrence,KS 66045, and an chemical insults (summarized by, e.g., ponent of adaptation.
adjunct senior scientist at the Kansas Cook et al. 1990, D'Elia et al. 1991, * There are consistent habitat differ-
GeologicalSurvey,Lawrence,KS 66047. Gates 1990), some or all of which may ences in bleaching resistance at a given
She is a coelenterate biologist with a
operate synergistically (Coles and locale: corals in habitats that are more
long-standingresearchinterestin marine variable or more prone to stresses of
symbioses.? 1993 AmericanInstituteof Jokiel 1978). Much recent concern
Biological Sciences. has focused on the result of high- various sorts, including thermal (such

320 BioScience Vol. 43 No. 5

This content downloaded from 66.194.72.152 on Sun, 15 Sep 2013 02:28:36 AM

All use subject to JSTOR Terms and Conditions
as shallow water or fringing reefs),
tend to be less bleached than those in
more normally equable environments
(Cook et al. 1990, Hoeksema 1991).
* Despite apparent environmental ad-
aptations, there are consistent taxo-
nomic differences in vulnerabilities to
stress-related bleaching and in associ-
ated mortality at a particular site (e.g.,
Cook et al. 1990, Hoeksema 1991,
Jaap 1985). Prevalence of bleaching
appears to be higher in species that
have high rates of recruitment and
grow rapidly (weedy species) than in
other corals in the same general envi-
ronment (e.g., Gates 1990, Jokiel and
Coles 1990, Salvat 1991), and mortal-
ity after bleaching is higher in some
branching species-particularly mem-
bers of Acropora-than in many mas-
sive corals (e.g., Brown and Suharsono
1990, Fisk and Done 1985, Oliver
1985, Salvat 1991). However, intra- Corals in close proximity such as these Malaysian Turbinaria(left foreground)and
specific variability in environmental Acropora (background)may host differenttypes of algae. Photo: D. G. Fautin.
sensitivity has also been documented,
with some but not all sympatric colo- which partners range from generalists gradual reversion to stress-prone but
nies/individuals bleaching (e.g., Brown to specialists, we consider it likely otherwise advantageous symbiotic
and Suharsono 1990, Hoeksema 1991, that some taxa of hosts and algae can units in stable environments or in the
Oliver 1985). Jokiel and Coles (1990) form stable associations with more absence of extreme conditions.
identified temperature-sensitive and than one taxon of symbiont. On that
temperature-resistantclones of Porites basis, we propose that bleaching has
compressa in Hawaii. the following attributes: Host-alga symbioses
The underlying assumption in studies Symbiont specificity. Uniform, wide-
* Physiological responses (including
of algal symbiosis formerly was that spread bleaching is uncommon, even
those related to stress) of the symbi-
all zooxanthellae belong to Symbio- among members of a single host spe-
otic unit are primarily characteristics cies in a particular locale under wide-
dinium microadriaticum Freudenthal, of the combination, rather than of the
1962. The evidence for diversity is spread stress (e.g., Brown and
host or symbiotic algal partner alone. Suharsono 1990, Lang et al. 1988,
now overwhelming: biochemical
* Symbiotic units with one common Salvat 1991), and commonly bleach-
(Ciereszko 1962, 1991, Trench 1971,
Von Holt and Von Holt 1968), elec- partner vary in their stress responses ing occurs only in portions of some
and the degree to which they are colonies (Hayes and Bush 1990, Oliver
trophoretic (Schoenberg and Trench
1980a), morphological (e.g., Blank adapted to different environmental 1985) or even individuals (Hoeksema
conditions. 1991). We suggest that at least some
1987, Blank and Trench 1985a), and of this variation is due to different
genomic (Rowan and Powers 1991). * Multiple types of both zooxanthel-
Whether the algal populations for- lae and host species are commonly types of algae in conspecific hosts or
available on reefs. even in parts of a genetically uniform
mally are species, races, strains, or host unit.
ecotypes, their functional distinguish- * Bleaching provides an opportunity
Schoenberg and Trench (1976,
ability is adequate to support the hy- for the host to be repopulated with a
1980a) found that some species of
pothesis we advance. We refer to them different type of partner; frequent
hosts contain more than one type of
as types. We recognize that our hy- stress tends to favor a stress-resistant
zooxanthella; in some cases the host
pothesis would be invalidated by the combination.
units were sympatric, in others they
finding of only one possible combina- * Altered environmental conditions were geographically separated-but a
tion of host species and algal type as
(which include altered frequency of single individual or colony had algae
surely as it would be by the existence stressful events and altered types of of only one type. Rowan and Powers
of a single type of alga in all hosts.
stress) favor establishment of combi- (1991) found two restriction fragment
nations of symbionts that were less length polymorphisms of single-
The hypothesis adaptive under previous conditions. stranded small ribosomal subunit RNA
From the available data on the plant- * Stress-sensitive combinations may in algae from one of the ten species of
animal symbiosis, and by analogy with have competitive advantages in the reef-forming corals for which mul-
other symbioses (e.g., Fautin 1991) in absence of stress, which implies tiple samples were examined (as well

May 1993 321

This content downloaded from 66.194.72.152 on Sun, 15 Sep 2013 02:28:36 AM

All use subject to JSTOR Terms and Conditions
as in a congeneric species, details for ity among partners provides variabil- other reason than the pre-existing com-
which were not provided), although ity on which natural selection can bination experienced those conditions
Rowan1 doubts that that result is taxo- operate and the potential for recombi- as stressful. Laboratory studies dem-
nomically significant. Morphological nation in the event of mass stress, onstrating that homologous algae dis-
and physiological differences in algae although we recognize that for a zoox- place experimentally introduced het-
from well-lighted and shaded parts of anthella to have one primary pre- erologous ones (Fitt 1985) illustrate
a cnidarian colony (e.g., Berner et al. ferred host (or even a few) would be a precisely this characteristic, for the
1987 and studies cited therein) may stabilizing community force in the experimental setting is manipulated
imply multiple types of zooxanthel- short term. Repopulation following to approximate favorable natural con-
lae, contrary to the usual interpreta- bleaching may result in any of the ditions, which are those of the pre-
tion of photoadaptation, by analogy following: an unstable relationship existing symbiotic unit. Frequency of
with experiments on monocultures of that breaks down rapidly; a stable episodic stress will also affect which
free-living phytoplankters. Level of relationship in which the alga may be combination (or combinations) per-
illumination may be important in de- eliminated by competitively superior sists, because reversion is rarely in-
fining microhabitats suitable for dif- types over evolutionary/population stantaneous.
ferent types of algae, and thus account time scales of the host; an advanta-
for bleachingin corals moved into unfa- geous combination resistant to inva- Bleaching mechanism. How bleach-
miliar light regimes (Dustan 1982). sion by other symbionts under ing occurs is poorly understood. From
The potential for exchange of sym- nonstress conditions; or coexistence laboratory experiments on a coral and
bionts has been demonstrated experi- of more than one type, as in the sea a sea anemone exposed to low-tem-
mentally: Kinzie and Chee (1979) anemones Anthopleura elegantissima perature shock, Gates et al. (1992)
infected a sea anemone with zoo- and Anthopleura xanthogrammica, inferred a breakdown in host-cell ad-
xanthellae from a clam, a nudibranch, which may simultaneously harbor hesion. It is unknown how general
and a medusa; Schoenberg and Trench zoochlorellae and zooxanthellae this mechanism is across taxa of hosts
(1980a) infected an anemone with (Muscatine 1971). and types of algae, or how it relates to
algae from another anemone, a me- Because a symbiotic unit is likely to duration and intensity of stress. Com-
dusa, and three corals; and Fitt (1985) have attributes possessed by neither plete sloughing of the endodermal cells
induced production of medusae in partner in isolation (Karakashian and in which zooxanthellae lodge seems
scyphozoan polyps with zooxanthel- Siegel 1965), we expect a species of to us pathological, and therefore un-
lae from 19 other species, including coral to vary in stress response with likely to account for the reversible
anemones, corals, zoanthids, and symbiont type and a type of zooxan- bleaching that appears characteristic
clams, and he infected larval clams of thella to vary in physiology depending of many corals. We believe that in
two species with algae from anemo- on its host. For any physiological prop- some hosts or under some stresses, the
nes and zoanthids. In the field, erty, assessing the contribution of one mechanism of loss/regulation is prob-
Schoenberg and Trench (1980a) and symbiont is not a simple matter of ably less violent and the mechanism of
Rowan and Powers (1991) found al- subtracting from the value for the Gates and colleagues may operate
gae of a particular type in hosts be- intact symbiosis the contribution of primarily in taxa with high mortality
longing to different classes or phyla. the other symbiont measured in isola- rates attendant upon bleaching or in
Although many hosts and algae can tion. Experiments by Trench (1971), cases of severe stress. Alternatively,
live with more than one symbiotic for example, provided preliminary some host species may be more toler-
partner, there is a spectrum of their evidence that a particular type of zoo- ant of such damage. Our hypothesis
abilities to do so. Some types of algae xanthella differs biochemically in host does not depend on a particularmecha-
will not establish in heterologous hosts corals of various species, and those by nism nor on a determination of
(Schoenberg and Trench 1980b), oth- Schoenberg and Trench (1976,1980b) whether the host (as is commonly
ers establish but do not persist (Kinzie demonstrated that algae of various assumed) or algal partner initiates
and Chee 1979), and some are a poor types differ when grown in genetically bleaching.
physiological fit, as demonstrated by identical hosts.
their failure to induce medusa pro- In addition to physiological fea- Mechanisms of infection and algal
duction in scyphozoan polyps (Fitt tures of the partners and the combina- spread. Our hypothesis requires that
1985). Specialists may be more obli- tion, we hypothesize that environ- free-living zooxanthellae (swarmers)
gate than generalists, the degree of mental conditions affect specificity. be available as colonizers. They pre-
bleaching mortality possibly reflect- This idea is not new: Kinzie and Chee sumably must be conveyed through
ing the dependence of hosts on their (1979) pondered whether ecological water, although, given that densities
symbionts. For example, the virtually setting might be more important in in seawater are low, vectors such as
universal mortality of bleached corals explaining features of the symbiosis crustaceans or fish may be important
of the genus Acropora (Salvat 1991) than identity of the partners. A return (Fitt 1984, Muller Parker 1984). De-
suggests a tightly bound combination. to prestress conditions after bleaching tailed predictions based on our hy-
The range of specificity and stabil- may favor restoration of the original pothesis will differ depending on
symbiotic combination. However, whether the process of bleaching ren-
when the stress represents a shift in ders either partner temporarily or per-
1R. Rowan, 1992, personal communication.
Australian Institute of Marine Science, environmental conditions, the combi- manently unable to form a symbiosis,
Townsville, Queensland, Australia. nation is likely to change, if for no and whether swarmers are affected by

322 BioScience Vol. 43 No. 5

This content downloaded from 66.194.72.152 on Sun, 15 Sep 2013 02:28:36 AM

All use subject to JSTOR Terms and Conditions
stress similarly to the same type ofbut not to symbiotic hosts (Fitt 1984). if intervals between bleaching events
alga in a symbiotic unit. Factors determining which types of are long compared with the time re-
algae and how many of each survive
We infer that the repetitive nature quired for reversion, and if the envi-
of small-scale bleachings (Jokiel and
may include, in addition to external ronment returns to its prestress state.
Coles 1990) reflects a lack of reas-environment, physiological compat- The resulting advantageous but vul-
ibility, initial numbers, and growth
sortment in symbiotic partners. If the nerable relationship is episodically
types in the water are taxonomicallyand reproductive rates (probably vary- disrupted by relatively rare extreme
the same as those in the symbiotic ing with host species or microhabitat events.
population, odds are high that a local-
within host). Elimination through alga-
ized/mild bleaching will produce alga competition is known among Research needs
reinfection with the type of zooxan-chlorellae (Rahat 1985), and Fitt
thella the host had before. Alterna-(1985) showed such elimination for There is increasing interest in attempt-
tively, reinfection by the same typezooxanthellae: in clams, those of a ing to define coral and reef commu-
may be due to "sufficient cells gener-
faster-growing type (isolated from a nity responses to rising temperature
ally remain[ing] for the coral to re-
sea anemone) gradually overwhelmed and other environmental stresses. Ex-
cover pigmentation after the stress is
algae of a slower-growing type (iso- perimentally induced bleaching and
removed" (Jokiel and Coles 1990, p. lated from a zoanthid). However, predictions of stress response are in-
156). The more severe the bleaching,
subtle differences in the microhabi- conclusive in the absence of definitive
the less likely the latter mechanismtats of various parts of a host might taxonomy of both symbiotic partners
and the greater the variety of symbi-
favor different types of algae, result- and some knowledge about the distri-
otic taxa likely to be affected, so the
ing in a mosaic or chimera, an effect butions, abundances, and diversity of
more likely corals are to be repopulated
that would be absent in controlled taxa or types in nature. It is important
by algae from the external environ- laboratory experiments. (In a chimera, to resolve these taxonomic and eco-
ment (Hayes and Bush 1990), result- what stresses one type of alga might logical issues before committing ex-
ing in a higher probability of change.
not stress another, allowing the resis- tensive resources to field or labora-
Repopulation is unlikely to be en-
tant one to remain and dominate the tory studies of inadequately
tirely random. Some combinations of host after bleaching.) characterized systems.
host and symbiont are not viable (Fitt We consider partial, background The hypothesis we advance bears
1985, Schoenberg and Trench 1980b).bleaching to be not pathological, but directly on these issues and can be
Thus, the original combination- rather a normal regulatory process verified or refuted, in part or in the
which, ipso facto, is viable-has a that maintains remarkably stable whole, by technically feasible experi-
higher-than-random probability of populations of symbiotic algae de- ments. Regardless of outcome, the
being re-established, particularly if
spite reproductive potential greatly in research we suggest would provide a
conditions return to prestress levels.
excess of that of their hosts (e.g., conceptually unified approach to a
However, to the extent that the Muscatine et al. 1985). It may also multifaceted subject.
alga is rendered incapable of infection
provide an important route of entry Symbiont specificity within indi-
by bleaching or that the stress persists,
for zooxanthellae under nonstress vidual coral colonies and in different
repopulation by a different type is conditions. This mechanism permits colonies of the same host species should
more likely. The factors that governcontinuous sampling of ambient al- be investigated in a range of sensitive
the types of zooxanthellae in an area
gae, the fittest ones of which can and robust symbiotic units, as well as
may be analogous to the factors spread to areas already populated by in diverse geographic locations.
thought to govern the diversity of algae that are either identical or less Within-colony studies should focus
corals on a reef (Oliver 1985): weedy
competitive. on corals with characteristics possibly
species tend to dominate in the short We infer from empirical evidence indicative of internal algal diversity-
term but their vulnerability to stress
of repetitive bleaching that algae in a for example, recent or repeated par-
eliminates them disproportionately, stress-resistant symbiotic unit may be tial bleaching, variations in pigmen-
checking their number and areal ex- gradually displaced by a less stress- tation or light exposure, and multiple
tent and allowing survival of those resistant type of zooxanthella that is, growth forms (e.g., a massive colony
that grow more slowly but are more in at least some symbiotic associa- with a platy skirt). Between-colony
stress resistant. tions, better adapted in other ways. comparisons should pursue local host
Indeed, Fitt (1985) found that hosts
For example, combinations with the differences in habitat, timing of re-
of faster-growing algal types grow highest individual or combined growth production, seasonality of skeletal
faster themselves; if rapid growth is
rate may not necessarily be the fittest density band formation (Lough and
associated with vulnerability to stress,
in all respects: anemones "infected Barnes 1990), depth, colony morphol-
then fast-growing types would readily
with homologous algae achieve a ogy and growth rate (Barnes and
establish but be subject to repeatedsomewhat larger biomass but pro- Lough 1989), pigmentation, or em-
bleaching. Reinfection, whether by duce fewer offspring than polyps in- pirically observed stress resistance. If
the original or by another type (or fected with [heterologous] zooxan- algal symbiont type can influence skel-
types) of alga, may be facilitated by
thellae" (Kinzie and Chee 1979, p. etal architecture, taxonomic problems
the attraction of motile zooxanthellae
324). Reversion to the symbiotic unit in genera where species are difficult to
to an aposymbiotic host (a normally existing before bleaching is most likely separate conclusively on the basis of
symbiotic individual lacking algae) if large populations o:fthe host exist, skeletal morphology (e.g., Knowlton

May 1993 323

This content downloaded from 66.194.72.152 on Sun, 15 Sep 2013 02:28:36 AM

All use subject to JSTOR Terms and Conditions
 of biochemical products (e.g., num-
ALGA-CONTROLLED PROCESSES
Infectionof host ber, type, condition, or effluvia of
times
Algallife/reproduction
Competitiveexclusionof otheralgae expelled zooxanthellae) that may act
Recoveryfromstress-inducedbleaching above some threshold as a signal analo-
gous to the alarm pheromone antho-
HOSTCHARACTERISTICS
Reproductionfrequencies
pleurine (Howe and Sheikh 1975). A
Organismlifespans mechanism for propagating mass
Reef community'lifespans"
ages, host families
Evolutionary bleachings beyond the effect of a ma-
age, scleractinianlineage
Evolutionary jor primary stress (e.g., to greater
ENVIRONMENTAL FACTORS
depth or protected sites) would help
Bleaching-inducingstress events, duration to explain the puzzling local distribu-
Bleaching-inducingstress events, retumperiod
Minorclimateoscillations
tion of some bleaching events. If the
Majorclimateoscillations algae precipitate the bleaching, they
could benefit by increasing the diver-
-2 -1
-6 -5 -4 -3 0 1 2 3
Log time (years)
4 5 6 7 8 9
sity or number of available hosts into
which to settle. Alternatively, if the
hosts were responsible for eliminating
Figure 1. Time scales relevant to bleaching-inducedadaptation. Bleaching and their algae, they could benefit by in-
infection mechanismsoperate at time scales characteristicof the motile and short- creasing the diversity or density of
lived algal symbionts.These time scales are short comparedwith host organismtime potential symbionts in the water.
constants and most environmentalvariation.The symbiotic unit is therebyable to Chemosensory attraction has been
adapt to stress and changes over time scales both longer and shorter than host implicated in the infection process
lifetimes.The punctuatedadaptationproducedby reshufflingsymbiontsresultsin a
(Fitt 1984).
highlevelof apparentevolutionarystabilityfor a relativelyspecializedand apparently
fragile organism.Dashed lines indicate possible but not probableextensions of the
ranges. Evolutionary and
ecological implications
et al. 1992) may be easier to under- scleractinian corals may acquire zoo- Except for the Merulinidae, all cur-
stand. Because the biogeography and xanthellae from host organisms of rently extant families of reef-forming
ecology of zooxanthella types is es- other taxa. Some symbiotic combina- corals had evolved by the Miocene
sentially unknown, it would be desir- tions may be obligate, whereas the (and most are Mesozoic in age; Wells
able to replicate these studies over physiological bond of others may be 1956). Most corals have lifetimes on
large latitudinal and longitudinal looser. Determination of preferences/ the order of decades (centuries in the
ranges. hierarchies will complement informa- case of some species), but during the
Surveys to determine the density, tion on the extent to which displace- Quaternary, reef environments have
variety, and infectivity of swarmers ment of one algal type by another repeatedly undergone rapid climate-
should be done in various localities occurs. induced environmental changes on
that differ in dominant symbiotic or- Empirical studies of stability and time scales of centuries to millennia
ganisms, and surveys should also be physiological features of various coral- (Figure 1). Under these conditions,
done through time (e.g., seasonally) alga partnerships should be accompa- the fact that the coral lineages have
at those same sites. It would be espe- nied by laboratory experiments on experienced neither rapid taxonomic
cially instructive to compare free-liv- variability in stress responses. These diversification nor substantial extinc-
ing zooxanthellae populations during experiments should address both natu- tions (Wells 1956) is perhaps unex-
or immediately after a bleaching epi- rally occurring symbiotic combina- pected, and the reasons may prove re-
sode with those during normal cir- tions and deliberate cross-infections levant to present concerns about the
cumstances. and should investigate variability in effects of greenhouse effect-induced
Laboratory studies on stress re- competitive interactions among algal climate change (Smithand Buddemeier
sponses (especially to temperature) of types under various conditions, ex- 1992).
various types of free-living zooxan- panding on work such as that by The rapid potential generation time
thellae are necessary to test our hy- Kinzie and Chee (1979), Fitt and of zooxanthellae compared with that
pothesis. These studies should investi- Trench (1981), and Fitt (1985). of most hosts might appear to make
gate not only viability but also effects Our hypothesis has implications them (and hence their symbiotic units)
on reproduction, photosynthesis and for applied research. It suggests that evolutionarily more responsive to lo-
respiration, infectivity, and biochemi- ecosystem management and restora- cal conditions than the hosts. How-
cal products. tion could become simpler and more ever, a sexual phase is unknown for
We need to know the hierarchy of effective if resistance to stress can be zooxanthellae (Blank and Trench
host species preference by various enhanced by manipulating popula- 1985b), which calls into question their
zooxanthella types and vice versa, tions of algae instead of the larger and potential evolutionary responsiveness.
and how this hierarchy may vary with slower-growing hosts. The probable evolutionary stasis of
environmental parameters. Studies Finally, although not integral to both host and symbiont may be com-
must include the complete spectrum of our hypothesis, we suggest testing the pensated for by the creation of new
reef-dwelling symbiotic units, because possibility that stress induces release symbiotic units through recombining

324 BioScience Vol. 43 No. 5

This content downloaded from 66.194.72.152 on Sun, 15 Sep 2013 02:28:36 AM

All use subject to JSTOR Terms and Conditions
symbiotic partners. scleractinian corals: fine banding and sea- Bivalvia). Biol. Bull. 161: 213-235.
We view bleaching as providing an sonal patterns.J. Exp. Mar. Biol. Ecol. 126: Freudenthal, H. D. 1962. Symbiodinium gen.
119-134. nov. and S. microadriaticum sp. nov., a
opportunity for reshuffling, a potent Berner, T., Y. Achituv, Z. Dubinsky, and Y. zooxanthella: taxonomy, life cycle and
adaptive mechanism that instantly Benayahu. 1987. Pattern of distribution and morphology. J. Protozool. 9: 45-52.
creates a host-symbiont combination adaptation to different irradiance levels of Gates, R. 1990. Seawater temperature and
with features that may prove more zooxanthellae in the soft coral Litophyton sublethal coral bleaching in Jamaica. Coral
robust under altered conditions. Such arboreum (Octocorallia, Alcyonacea). Sym- Reefs 8: 193-197.
biosis 3: 23-40. Gates, R. D., G. Baghdasarian, and L.
a mechanism of adaptation, which Blank, R. J. 1987. Evolutionary differentiation Muscatine. 1992. Temperature stress causes
Saffo (1992) considered as indirectly in gymnodinoid zooxanthellae. Ann. N.Y. host cell detachment in symbiotic cnidarians:
affecting evolution, could account not Acad. Sci. 503: 530-533. implications for coral bleaching. Biol. Bull.
Blank, R. J., and R. K. Trench. 1985a. Specia- 182:324-332.
only for currently observed local and tion and symbiotic dinoflagellates. Science Glynn, P. W. 1990. Coral mortality and distur-
regional variations in sensitivity to 229:656-658. bances to coral reefs in the tropical Eastern
stress of nominally identical host spe- .1985b. Symbiodinium microadriati- Pacific. Pages 55-126 in P. W. Glynn, ed.
cies, but also for the remarkable ro- cum: a single species? Proc. Intl. Coral Reef Global Ecological Consequences of the
bustness of coral species and reef Congr. 6:113-117. 1982-1983 El Nino-Southern Oscillation.
Brown, B. E., ed. 1990. Coral bleaching: special Elsevier, New York.
community structure throughout the issue. Coral Reefs 8: 153-232. .1991. Coral reef bleaching in the 1980's
climatic oscillations of the Quaternary. Brown, B. E., and Suharsono. 1990. Damage and possible connections with global warm-
Time scales of some environmental and recovery of coral reefs affected by El ing. Trends Ecol. Evol. 6: 175-179.
variations are comparable to those of Nifio related seawater warming in the Thou- Glynn, P. W. and W. H. de Weert. 1991. Elimi-
sand Islands, Indonesia. Coral Reefs 8: nation of two reef-building hydrocorals fol-
background cross-infection and com- 163-170. lowing the 1982-83 El Nifio warm event.
petitive elimination of algae from a Ciereszko, L. S. 1962. Chemistry of coelenter- Science 253: 69-71.
host (Figure 1). Therefore, the hetero- ates. III. Occurrence of antimicrobial terpe- Glynn, P. W., and J. S. Feingold. 1992. Hydro-
geneity of algae in a host at any time noid compounds in the zooxanthellae of coral species not extinct. Science 257:1845.
reflects some combination of com- alcyonarians. Trans. N.Y. Acad. Sci. 24: Goreau, T. J. 1990. Coral bleaching in Jamaica.
502-503. Nature 343:417.
petitiveness of the algae, time since .1991. Sterol and diterpenoid produc- Hayes, R. L., and P. G. Bush. 1990. Micro-
the most recent stress, frequency of tion by zooxanthellae in coral reefs: a re- scopic observations of recovery in the reef-
stress, and local diversity of zooxan- view. Biol. Oceanogr. 6: 363-374. building scleractinian coral, Montastrea
thellae. Rapid environmental change Coles, S. L., and P. L. Jokiei. 1978. Synergistic annularis, after bleaching on a Cayman
effects of temperature, salinity and light on reef. Coral Reefs 8: 203-209.
may thereby produce punctuated ad- the hermatypic coral Montipora verrucosa. Hoeksema, B. W. 1991. Control of bleaching in
aptation of the symbiotic units, which Mar. Biol. 49: 187-195. mushroom coral populations (Scleractinia:
has been neglected as a subject of Coles, S. L., P. L. Jokiel, and C. R. Lewis. 1976. Fungiidae) in the Java Sea: stress tolerance
study because of the tendency to as- Thermal tolerance in tropical versus sub- and interference by life history strategy.
cribe stable attributes to the host spe- tropical Pacific reef corals. Pac. Sci. 30: Mar. Biol. Prog. Ser. 74: 225-237.
159-166. Howe, N. R., and Y. M. Sheikh. 1975.
cies as a unitary entity.
Cook, C. B., A. Logan, J. Ward, B. Luckhurst, Anthopleurine: a sea anemone alarm phero-
Rather than an absence of specific- and C. J. Berg Jr. 1990. Elevated tempera- mone. Science 189: 386-388.
ity between partners, our hypothesis tures and bleaching on a high-latitude coral Jaap, W. C. 1985. An epidemic zooxanthellae
posits that specificity changes as envi- reef: the 1988 Bermuda event. Coral Reefs expulsion during 1983 in the lower Florida
ronmental conditions do. Thus, al- 9:45-49. Keys coral reefs: hyperthermic etiology.
D'Elia, C. F., R. W. Buddemeier, and S. V. Proc. Intl. Coral Reef Congr. 6: 143-148.
though bleaching may represent in- Smith. 1991. Workshop on coral bleaching, Jokiel, P. L., and S. L. Coles. 1990. Response of
stability in the short term, it promotes coral reef ecosystems and global change: Hawaiian and other Indo-Pacific reef corals
long-term stability by enhancing sur- report of proceedings. Maryland Sea Grant to elevated temperature. Coral Reefs 8:
vival chances of both zooxanthellae College publication no. UM-SG-TS-91-03, 155-162.
and hosts under conditions that are University of Maryland, College Park. Karakashian, S. J., and R. W. Siegel. 1965. A
Dustan, P. 1982. Depth-dependent photo- genetic approach to endocellular symbiosis.
not those of the prestress environ- adaptation by zooxanthellae of the reef Exp. Parasitol. 17: 103-122.
ment. Potential hosts and habitats are coral Montastrea annularis. Mar. Biol. 68: Kinzie, R. A. III, and G. S. Chee. 1979. The
many, so the combination of environ- 253-264. effect of different zooxanthellae on the
mental variability and symbiotic ad- Fautin, D. G. 1991. The anemonefish symbio- growth of experimentally reinfected hosts.
sis: what is known and what is not. Symbio- Biol. Bull. 156: 315-327.
aptation acts to conserve both genetic sis 10: 23-46. Knowlton, N., E. Weil, L. A. Weigt, and H. M.
and symbiotic diversity. Fisk, D. A., and T. J. Done. 1985. Taxonomic Guzman. 1992. Sibling species in Mon-
and bathymetric patterns of bleaching in tastraea annularis, coral bleaching, and the
corals, Myrimidon Reef (Queensland). Proc. coral climate record. Science 255: 330-333.
Acknowledgments Intl. Coral Reef Congr. 6: 149-154. Lang,J. C., R. I. Wicklund, and R. F. Dill. 1988.
We are grateful to colleagues too nu- Fitt, W. K. 1984. The role of chemosensory Depth- and habitat-related bleaching of
behavior of Symbiodinium microadriaticum, zooxanthellate reef organisms near Lee
merous to mention for the time and intermediate hosts, and host behavior in the Stocking Island, Exuma Cays, Bahamas.
attention they gave to a previous ver- infection of coelenterates and molluscs with Proc. Intl. Coral Reef Symp. 3: 269-274.
sion of this manuscript. Their com- zooxanthellae. Mar. Biol. 81: 9-17. Lough, J. M., and D. J. Barnes. 1990. Intra-
ments helped us to focus our ideas and .1985. Effect of different strains of the annual timing of density band formation of
zooxanthella Symbiodinium micro- Porites coral from the central Great Barrier
sharpen our prose. adriaticum on growth and survival of their Reef. J. Exp. Mar. Biol. Ecol. 135: 35-37.
coelenterate and molluscan hosts. Proc. Intl. Muller Parker, G. 1984. Dispersal of zooxan-
References cited Coral Reef Congr. 6: 131-136. thellae on coral reefs by predators of
Fitt, W. K., and R. K. Trench. 1981. Spawning, cnidarians. Biol. Bull. 167: 159-167.
Barnes, D. J., and J. M. Lough. 1989. The development,and acquisition of zooxan- Muscatine, L. 1971. Experiments on green al-
nature of skeletal density banding in thellae by Tridacna squamosa (Mollusca, gae coexistent with zooxanthellae in sea

May 1993 325

This content downloaded from 66.194.72.152 on Sun, 15 Sep 2013 02:28:36 AM

All use subject to JSTOR Terms and Conditions
 anemones. Pac. Sci. 25: 13-21.
Muscatine, L., L. R. McCloskey, and Y. Loya.
1985. A comparison of the growth rates of
zooxanthellae and animal tissue in the Red
Sea coral Stylophora pistillata. Proc. Intl.
Coral Reef Congr. 6: 119-123.
LatinAmerican Oliver, J. 1985. Recurrent seasonal bleaching
and mortality of corals on the Great Barrier
Insects Reef. Proc. Intl. Coral Reef Congr. 4:
201-206.
and Entomology Rahat, M. 1985. Competition between
Chlorellae in chimeric infections of Hydra
CHARLESL. HOGUE viridis: the evolution of a stable symbiosis.
This is the firstcomprehensive J. Cell. Sci. 77: 87-92.
guideto insectlifein a partof the Rowan, R., and D. A. Powers. 1991. A molecu-
world known for its abundant, lar genetic classification of zooxanthellae
and the evolution of animal-algal symbio-
Fish and endangered, life forms. ses. Science 251: 1348-1351.

An Enthusiast's
Guide Hogue's scholarshipembraces Saffo, M. B. 1992. Invertebrates in endosymbi-
vast geographicalterritoryand otic associations. Am. Zool. 32: 557-565.
PETERB. MOYLE Salvat, B. 1991. Bleaching and mortality of
generousnumbersof represen- scleractinian corals, event and causes, Soci-
byChrisMar vanDyck
Illustrated
tativeinsects,to serveboth the ety Islands, 1991. Paper presented at the
Moyle introducesus to the great annual meeting of the International Society
advancesin knowledgeof fish professionalentomologistand for Reef Studies, Berkeley, CA, 14 Decem-
the seriousamateur. ber 1991.
biologyand behaviorthathave $85.00 cloth,illustrated Schoenberg, D. A., and R. K. Trench. 1976.
occurred over the last twenty Specificity of symbioses between marine
years.VanDyck'sdramatic paint- cnidarians and zooxanthellae. Pages
423-432 in G. O. Mackie, ed. Coelenterate
ingsandexquisitelinedrawings Ecology and Behavior. Plenum Press, New
illustrateMoyle'sdescriptions. York.
$25.00 cloth,illustrated 1980a. Genetic variation in Symbio-
dinium (=Gymnodinium) microadriaticum
Freudenthal, and specificity in its symbiosis
with marine invertebrates. I. Isozyme and
Thelepson I
i ~~~~~
4
I
v
t
soluble protein patterns of axenic cultures
of Symbiodinium microadriaticum. Proc.
Manual R. Soc. Lond. B 207: 405-427.
.1980b. Genetic variation in Symbiodi-
HigherPlants nium (=Gymnodinium) microadriaticum
of California Freudenthal, and specificity in its symbiosis
with marine invertebrates. III. Specificity
JAMESC. HICKMAN,Editor and infectivity of Symbiodinium microa-
"A single work . . . simultan- driaticum. Proc. R. Soc. Lond. B 207:
eously accessibleto dedicated AnnualCycles 445-460.
Smith, S. V., and R. W. Buddemeier. 1992.
beginnersand indispensableto
professional botanists.... For of Diving Global change and coral reef ecosystems.
Annu. Rev. Ecol. Syst. 23: 89-118.
the first time in one volume a
floraof theexceed-
Behaviorand Trench, R. K. 1971. The physiology and bio-
chemistry of zooxanthellae symbiotic with
user-friendly
ingly diverse higher plants of Ecologyof the marine coelenterates. II. Liberation of fixed
14Cby zooxanthellae in vitro. Proc. R. Soc.
California."
-Mildred E. Mathias,editorof
WeddellSeal Lond. B 177: 237-250.
Von Holt, C., and M. Von Holt. 1968. The
MICHAELA. CASTELLINI, secretion of organic compounds by zooxan-
Flowering Plantsin theLandscape RANDALLW. DAVIS,and thellae isolated from various types of
"Setsnew standardsfor excel- Zoanthus. Comp. Biochem. Physiol. 24:
GERALDL. KOOYMEN 83-92.
lence... andpicksup beautifully This work details more than Wells, J. W. 1956. Scleractinia. Pages
on the contemporaryidea that ten years of work in the Ant- F328-F444 in R. C. Moore, ed. Treatise on
botanicalwork should be fully arcticon the diving biology of Invertebrate Paleontology. Part F.
Coelenterata. Geological Society of America
accessibleto the generalpublic Weddell seals. and University of Kansas Press, Lawrence.
as well as to scientists." Bulletinof theScrippsInstitution
of Williams, E. H. Jr., and L. Bunkley-Williams.
-Peter H. Raven,Missouri Oceanography 1990. The world-wide coral reef bleaching
$8.00 paper
BotanicalGarden cycle and related sources of coral mortality.
Atoll-Res. Bull. 335: 1-71.
$55.00 clothuntil6/30/93,
$65.00 after,illustrated

At bookstoresor ordertoll-free1-800-822-6657.

Universityof CaliforniaPress *
BerkeleyLosAngeles New York London 1893 1 9 93
BioScience Vol. 43 No. 5

This content downloaded from 66.194.72.152 on Sun, 15 Sep 2013 02:28:36 AM

All use subject to JSTOR Terms and Conditions