Reef-building corals are obligate, mutualistic symbioses of heterotrophic animals and phototrophic dinoflagellates (Symbiodinium spp.)1. Contrary to the earlier, widely accepted belief that corals harbour only one symbiont, we found that the ecologically dominant Caribbean corals Montastraea annularis and M. faveolata can act as hosts to dynamic, multi-species communities of Symbiodinium. Composition of these communities follows gradients of environmental irradiance, implying that physiological acclimatization2,3,4 is not the only mechanism by which corals cope with environmental heterogeneity. The importance of this diversity was underlined by analysis of a natural episode of coral bleaching. Patterns of bleaching could be explained by the preferential elimination of a symbiont associated with low irradiance from the brightest parts of its distribution. Comparative analyses of symbionts before and after bleaching from the same corals supported this interpretation, and suggested that some corals were protected from bleaching by hosting an additional symbiont that is more tolerant of high irradiance and temperature. This ‘natural experiment’ suggests that temporal and spatial variability can favour the coexistence of diverse symbionts within a host, despite the potential for destabilizing competition among them5,6.
The corals Montastraea annularis and M. faveolata each host three distantly related taxa7 of the dinoflagellate genus Symbiodinium, denoted A, B and C, that are identified by restriction-fragment length polymorphisms (RFLPs) in genes encoding small ribosomal RNA (srRNA)7. A and B are common in shallow-water corals (high-irradiance habitats), whereas C predominates in deeper corals (low-irradiance habitats). Mixed samples A + C and B + C, common at intermediate locations7, suggest that symbionts may actually exist as complex communities that track differences in irradiance within a colony2.
To test this hypothesis we sampled four locations in each of 46 colonies (Fig. 1). All M. faveolata, and all but one colony of M. annularis, yielded two or three types of symbionts. As predicted, Symbiodinium A and B dominated locations with higher, downwelling irradiance (communities 1 and 2, unshaded colony tops), and C dominated locations of lower irradiance (communities 3 and 4, colony sides and shaded colony tops) (P < 0.001; χ2 test). These patterns of intra-colony zonation largely disappear at slightly greater depths (8–11m in M. annularis, and 6–12m in M. faveolata), where Symbiodinium C is predominant overall7. As before7, Symbiodinium A was more common in M. faveolata than in M. annularis.
Analyses at a finer scale (∼1cm) confirmed that symbionts occupy distinct but overlapping habitats (Fig. 2). Unshaded columns of M. annularis create a localized gradient of low (on the side, no downwelling) to high (on the top, full downwelling) irradiance, which we sampled along transects. At intermediate depths (3–7m) this gradient coincides with the transition from Symbiodinium C to B, B + C, or A (Fig. 2a–d). Analyses of shallower (1–2m) and deeper (9–12m) corals (Fig. 2d) show that depth7 and intracolony zonation of the symbionts occur in parallel. These consistent patterns strongly argue that zonation is controlled by ambient irradiance. Furthermore, experimentally toppled columns, which experienced immediate and severe changes in irradiance gradients, largely re-established expected patterns of symbiont zonation during a six-month period (Fig. 2e, f). This response shows that the patterns are maintained dynamically.
Symbioses between corals and dinoflagellates are stable mutualisms, with the notable exception of coral bleaching, which involves the loss of symbionts and/or photosynthetic pigments3,8. Bleaching is an ecologically important but poorly understood response to environmental stress3,8,9. Many bleaching events exhibit intra-specific variation distributed within and among habitats in ways that are difficult to explain9,10,11,12. Because irradiance and temperature act synergistically to induce bleaching12,13,14, and the symbionts of M.annularis and M. faveolata exhibit different associations with irradiance (Figs 1 and 2), we hypothesized that symbiont polymorphism underlies this variation.
We observed ‘paling’ in several colonies of M. annularis and M. faveolata on 18 September 1995, and bleaching was extensive by the second week in October, both in Panama and elsewhere15. At our study site, this event was ‘typical’: like a similar event there in 1983 (ref. 16), it followed a prolonged excursion above the mean summer maximum of temperature (Fig. 3e); it also coincided with atypically high water clarity (data in ref. 17), which implies increased irradiance at depth2. We also observed complex9,10,18 bleaching patterns in both M. annularis and M. faveolata. Bleaching was rare or slight at both shallow (<2m) and deep (>15m) sites; in between, however, both species displayed a curious pattern, with shallower colonies bleached preferentially in shaded places (Fig.3a, b) and deeper colonies bleached preferentially in unshaded places (Fig. 3c, d). Among M. annularis partitioned as in Fig. 1a (communities 1 and 2 versus 3 and 4) and by depth (above 8m versus below 8m), this difference was significant (n = 76 colonies, 64 bleached; P < 0.05, χ2 test). Some colonies exhibited a ‘ring’ of bleaching at the boundary between column top and side (Fig. 3a). M. faveolata colonies are not easily partitioned into two distinct irradiance microhabitats, but they clearly showed the same reciprocal pattern (Fig. 3b, d), with a shallower (∼6m) centre. Such observations have previously been hard to explain12 because the environment is isothermal, and the associations with irradiance and colony morphology are inconsistent.
Symbiont zonation provides a simple hypothesis to explain these bleaching patterns. Bleaching was disproportionately common in what seems to be the upper limit of Symbiodinium C's ‘adaptive zone’: low-irradiance parts of corals in shallower water, and high-irradiance parts of corals in deeper water. Slight increases in temperature and irradiance might push these symbioses, but not others, beyond some physiological limit, resulting in bleaching. This hypothesis accounts for our bleaching observations, including areas of slight bleaching9,15,19 (see Fig. 3a, b), if Symbiodinium C were expelled selectively from mixed symbiont communities.
An analysis of symbionts collected in late October supported this interpretation of events. Post-bleaching samples were obtained <1cm from many sites sampled the previous January (Fig. 1). All available samples from communities that had previously contained mixtures of Symbiodinium C plus either A or B (or both) were identified (Fig. 1) and analysed. We reasoned apriori (Fig. 2) that these sites accurately defined the limit of Symbiodinium C in corals under non-bleaching conditions. Such mixtures also allow the fates of different symbionts to be compared directly. We also tested archived samples taken at the same time as, and <1cm away from, the original (pre-bleaching event) samples. In every case, Symbiodinium srRNA RFLPs in these replicate, pre-bleaching pairs were equivalent (data not shown), indicating that the small distance between pre- and post-bleaching samples was unlikely to be significant.
As predicted, Symbiodinium C had decreased in relative abundance in all 18 communities tested (see Fig. 4a–c). Absolute responses of different symbionts within a mixed community were compared by using estimates of relative abundances (from RFLP data; see Fig. 4a–c) to partition direct counts of symbionts into each genotype (Fig. 4d). Losses of Symbiodinium C were typically close to 100%, whereas B underwent a median decrease of 14%, and A more than doubled in 3 of 5 instances. The single sample that contained all three symbionts exhibited these same trends (Fig. 4c, d). Changes in colony chlorophyll contents and subjective assessments of bleaching paralleled changes in symbiont numbers (Fig. 4e). From these data we can tentatively rank the ‘fitness’ of the different Symbiodinium taxa as symbionts under ‘bleaching conditions’. The ranking obtained in this manner is: A > B ≫ C.
Our study provides a fuller understanding of M. annularis and M. faveolata, which are dominant members of western Atlantic reefs20 and are widely used as model systems in reef biology and geology11,13,18,19,21,22. Each coral ‘species’ encompasses one animal and dynamic, multi-species communities of symbiotic dinoflagellates. This strongly contradicts the ‘one host, one symbiont’ view of reef corals1, in which host taxa alone are adequate units of biodiversity, environmental variability is accommodated largely by physiological acclimatization2,3,4, and bleaching variability is often not understood12. We conclude that polymorphic symbiont communities underlie the broad distributions20 and bleaching ecology of these corals. Directed shifts in symbiont populations following extreme environmental change (Figs 2e, f and 4) suggest that similar shifts may also occur over annual cycles of environmental variation19. For these corals, and for mutualisms in general, the ability to cope with environmental change through changes in symbiont community composition reflects the selective advantage of hosting several distinct symbionts, despite the potential for destabilizing competition among them5,6.
How typical and important are the patterns documented here? M. annularis and M. faveolata in the Bahamas also host Symbiodinium A, B and C (data not presented), and published photographs18 and descriptions9,10 of bleaching elsewhere strongly resemble our own (Fig. 3a–d). With respect to Caribbean corals in general, bleaching is often predominant at intermediate depths9. We can attribute this pattern (and its within-colony correlate) in M. annularis and M.faveolata to symbiont polymorphism and zonation. Moreover, at least three other species of Caribbean corals host (at least) both Symbiodinium A and C (ref. 23; our unpublished data). For other species, which might host multiple but not so distantly related symbionts, refinements of Symbiondinium taxonomy would be essential. However, symbiont polymorphism does not exclude the significance of other attributes that are important features of coral biology, such as physiological acclimatization of hosts and symbionts2,3,4 and genetic differences among hosts11,14.
It has been hypothesized that a global warming trend, with increased frequencies of world wide coral bleaching induced by increasing temperature or ultraviolet irradiation, could have catastrophic consequences for many living coral reefs3,8,21. Alternatively, coral communities may adjust to climate change by recombining their existing host and symbiont genetic diversities24,25,26. Our findings supply a precedent for this idea: that one species of coral can flexibly host more than one taxon of Symbiodinium to produce symbioses with distinct ecological properties. For example, M. annularis and M. faveolata might adjust to a warmer Atlantic ocean by hosting more Symbiodinium A and less Symbiodinium B and C. However, long-term consequences of such replacements would depend on how they affect rates of coral growth and reproduction.
Field collections and manipulations. Coral samples were collected at Aguadargana reef in San Blas, Panama27 by coring (1.1cm2 surface area) and freezing immediately in liquid nitrogen (data in Figs 1 and 4). Other colonies (data in Fig. 2) were sampled by removing a defined circular area (∼0.12cm2) of living tissue from freshly collected colonies with an airbrush. In transplant experiments (Fig. 2e, f), columns of M. annularis were broken off ∼15cm below the living tissue, turned on their sides, and cemented (at the non-living base) back to the colony at a comparable location; this increased (new top), decreased (new side), or did not change (side) local irradiance. All 28 transplants at a depth of 6m seemed to be normal after 6 months. Analyses of non-transplanted (control) columns showed that natural zonation patterns were stable over this period (data not shown).
Laboratory analyses. Symbionts and symbiont DNA were isolated from frozen7 and from fresh28 samples. Nuclear srRNA genes were amplified using the ‘universal’ PCR primers ss5 and ss3 (all data in Fig. 1) or a combination of ss5 and the ‘Symbiodinium-biased’ primer ss3Z (all data in Figs 2 and 4), and analysed with TaqI and DpnII (data were consistent in every case)7. The biased primer (ss3Z) does not discriminate (within this study) against unknown, specific Symbiodinium genotypes (discussed in ref. 28), as confirmed by sequencing7 and by comparing results from ‘universal’ and ‘biased’ amplifications of 30 samples that contained two genotypes (A + C or B + C) in various proportions.
Cloned srRNA genes from Symbiodinium A, B and C were used as standards7. They were amplified singly and from defined mixtures of two (Fig. 2b) or three (Fig. 4c) types7 to assign field samples to classes of symbiont relative abundance by visual comparison (Fig. 2a, b). To validate this procedure, approximately equal numbers of A, B and C cells, from three natural isolates of each type, were mixed in pairwise combinations and analysed. The results implied that Symbiodinium B and C yield (on a per-cell basis) equal signals, whereas A yields about twice that amount. Standard mixtures of cloned genes were adjusted accordingly.
Symbiont densities and chlorophyll contents (Fig. 4d, e) were determined from haemacytometer counts (8 replicate grids per sample) and spectrophotometrically from methanol extracts29, respectively. These symbionts were isolated quickly (with minimal washing) from frozen samples at 4°C under dim light. Symbiont genotypes, numbers and chlorophyll contents were obtained from subsamples of each isolate.
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We thank R. Robertson for alerting us to the bleaching event; J. Maté and E. Gomez for assistance; K. Kaufmann for help with temperature records; R. W. Buddemeier, J. B. C. Jackson and W.Toller for comments on the manuscript; and the Government of Panama and the Kuna nation for allowing access to the site and collecting. This research was supported by the Smithsonian Institution, the Andrew W. Mellon Foundation, the Office of Naval Research, the NIH and NOAA.
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Rowan, R., Knowlton, N., Baker, A. et al. Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388, 265–269 (1997). https://doi.org/10.1038/40843
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