N O T E
Zooxanthella densities within a Caribbean octocoral during bleaching and non-bleaching years
Received: 15 November 2001 / Accepted: 9 November 2002 / Published online: 6 February 2003 Springer-Verlag 2003
Keywords Coral bleaching Æ Symbiosis Æ Gorgonian Æ Coral reef
Introduction
The 1998 El Nin˜o Southern Oscillation (ENSO) was one of the strongest ENSO events to affect coral reefs in recorded history (Wilkinson 2000), and along with causing extensive coral bleaching and mortality, it fo- cused a great deal of attention on the causes and nature of coral bleaching. The 1998 event while at the extreme of recently observed bleaching events was not uniformly catastrophic across both sites and taxa. At some sites, earlier bleaching events had greater effects (c.f. Shulman and Robertson 1996), and among some zooxanthellate taxa bleaching appears to be far less common than among the scleractinians. The increasing incidence of bleaching and concern for the future of coral reef eco- systems have heightened interest in the complexity of the temporal, spatial, and taxonomic pattern of bleaching.
Here, I report on variation in zooxanthella density in a zooxanthellate Caribbean octocoral. Octocorals are of- ten significant if not dominant members of reef faunas, yet relatively little is known about their symbiosis with zooxanthellae. The data presented here, although not a continuous survey, characterize zooxanthella density over a 15-year period and document zooxanthellae densities during a year with extensive coral bleaching as well as years with no apparent bleaching.
Bleaching is the extreme at one end of a continuum of variation in zooxanthella density (Fitt et al. 2000).
Among zooxanthellate cnidarians, zooxanthella density varies across species (Drew 1972), habitat/depth (Drew 1972; Dustan 1979), temporally (Stimson 1997;
Fagoonee et al. 1999; Fitt et al. 2000), and with position within a colony (Lasker 1977; Berner et al. 1987; Fitt and Cook 2001). Bleaching events exhibit even greater variation in their effects across taxa, localities, depths, and positions on colonies (Lasker et al. 1985; Glynn 1990; Done 1992; Lang et al. 1992; Berkelmans and Oliver 1999). While these studies demonstrate a highly dynamic symbiosis among scleractinians, similar data for octocorals have been unavailable, and some studies on the diversity of zooxanthellae within octocorals suggest that the symbiosis of zooxanthellae with octo- corals may be more conservative than that with scler- actinians (Goulet and Coffroth 1997; Goulet 1999).
In an effort to characterize the dynamics of the symbiosis among octocorals, I report on zooxanthella densities in specimens of the Caribbean gorgonian Plexaura kuna collected intermittently over a 15-year period from sites in the San Blas Islands, Panama. P.
kuna spreads clonally via the production and re- attachment of fragments (Lasker 1984, 1990), and at some sites populations consist of dense aggregations made up of only a few individual clones (Coffroth and Lasker 1998). During the 1983 ENSO event when ex- tensive bleaching was observed in the San Blas Islands, P. kuna did not bleach. However, subsequent research has indicated that branches maintain a pigmented ap- pearance even when they have lost large proportions of their zooxanthellae (S.R. Santos, personal commu- nication). This study was undertaken to determine whether zooxanthella density had varied independent of the lack of observed changes in colony pigmentation during the 1983 bleaching event in Panama, and to characterize variation in zooxanthellae density between colonies and reefs over time.
Methods
Zooxanthella density was determined from a variety of P. kuna samples from the San Blas Islands that were collected between 1983 and 1998. In 1983 and 1984 monthly samples of a group of marked Coral Reefs (2003) 22: 23–26
DOI 10.1007/s00338-003-0276-7
H.R. Lasker
H.R. Lasker
Department of Biological Sciences, University at Buffalo, Box 60-1300, Buffalo, New York, 14260-1300, USA E-mail: hlasker@buffalo.edu
colonies were collected in order to determine the reproductive cycle ofP. kuna(reported in Brazeau and Lasker 1988). Those samples were collected during the 1983 bleaching event and the collections extended to recovery phase in the San Blas (Lasker et al. 1985).
Some of the samples from six of those colonies (131 samples) were still available and were analyzed. In subsequent years, samples were collected during summer months in order to determine re- productive status of colonies in conjunction with other studies (i.e., Lasker et al. 1996). Samples came from five different sites, all in the San Blas Point region, and in some cases include samples from tagged colonies collected over multiple months and/or years.
Samples were not collected from all sites in all years.
Additional samples were collected in 1998 when climatic data suggested the onset of a large ENSO event. Colonies were sys- tematically sampled in April and then again in June, when bleaching was initially anticipated (206 samples from six reefs).
Unfortunately, bleaching was not observed in Panama until Oc- tober, but subsequent sampling was precluded by the closure of the Smithsonian Tropical Research Institute San Blas Field Station.
Samples, which usually consisted of a single 10-cm branch, were initially preserved in 5% formalin and later transferred to 70% ethanol. Zooxanthella densities were determined from 1-cm subsamples of branch fragments taken 1 cm below the branch tip (i.e., the piece 1–2 cm from the tip). Length and diameter of the 1-cm piece was measured with Vernier calipers and the piece was ground in a glass tissue homogenizer with 1 ml of water. Density was determined from counts of 10 replicate aliquots, which were viewed using a hemacytometer with improved Neubauer ruling.
All zooxanthellae found within 0.16 mm2on the hemacytometer grid were counted (i.e., 16ll). Zooxanthella density was de- termined with respect to linear length of the branch, branch surface area, and branch volume. Inspection of the data for a group of six colonies that were sequentially monitored over 2 years indicates that variance among the colonies was lowest when density was considered on a unit length basis and all subsequent analyses are restricted to density per linear length.
Data were analyzed using repeated measures analysis of variance for cases in which the same colonies were sampled multiple times and multi-way analysis of variance when samples came from different colonies. In the repeated measures analysis, clone and site were separately used as classification variable for colonies, but the two could not be analyzed simultaneously due to the large number of clones for which only a single sample was analyzed. Variation between clones but within a site was assessed by a repeated measures analysis of the Korbiski Reef samples.
Samples from different colonies but the same clone were treated as independent replicate measurements since the history of one colony did not affect the zooxanthella density within a clone- mate.
Results and discussion
Zooxanthella density among the 928 samples averaged 2.11·10
6(standard error =0.05·10
6) cells/cm. P. kuna zooxanthella cell counts are reported in terms of linear centimeter of branch because that index of density had the lowest within-colony variation. When converted to density per unit area using the measured branch dia- meter to calculate area, zooxanthella density within branches ranged from 0.1·10
6to 6.2·10
6cells/cm
2with a mean value of 2.5·10
6cells/cm
2. Those values are si- milar to zooxanthella densities reported among scler- actinians (Drew 1972; Lasker 1977; Dustan 1979;
Stimson 1997; Fagoonee et al. 1999).
Approximately 2% of the samples had densities less than 10% of the mean, indicating that extensive loss of zooxanthellae can occur in nature. Those samples were
not obviously pale in coloration and were not restricted to any specific colony, reef, or sample period. Santos (personal communication) has induced bleaching among P. kuna that were maintained in the dark. While pale in coloration, none of those colonies was obviously
‘‘bleached.’’ In contrast, Plexaurella spp. will lose all coloration (personal observation) and take on the classic
‘‘bleached’’ appearance. Thus, coloration may be less of an indicator of zooxanthellae density in octocorals than it is among scleractinians.
Zooxanthella densities among the tagged colonies at Korbiski Reef were used to determine whether the 1983 bleaching event also affected zooxanthella densities within P. kuna colonies. Zooxanthella densities among the colonies at Korbiski were variable between months but did not decline in the summer of 1983 (Table 1, Fig. 1). The variance among the 1983 samples was large, and while zooxanthella densities were significantly higher in some months than others, post-hoc tests did not identify a distinct series of months with uniformly greater zooxanthella differences. Samples from summer months in other years were lower than those in 1983, a pattern that occurred on the other reefs as well (Fig. 1 and below).
In 1998 samples from a group of tagged colonies coming from multiple clones were collected from Kor- biski Reef in both April and June. Zooxanthella density among those samples differed significantly between clones and months (Fig. 2, Table 1). June values were lower than those in April for all eight clones that were surveyed and were lower in 25 of the 27 colonies that were sampled in both months.
Temporal variation in zooxanthella density is again evident in Fig. 3, which depicts zooxanthella density as a function of month and site among the 1998 samples.
Density varied between April and June as well as be- tween sites (Table 1). The clearest overall effect was a decrease in zooxanthella density between April and June. Some sites, such as Point 24, had greater zoox- anthella densities than most of the other sites, while samples from Korbiski had lower zooxanthella density than samples from most other reefs (post-hoc tests). The differences between April and June were not uniform between the sites and there was a significant reef x month interaction in the data (Table 1).
The most striking element of the data set was the absence of any suggestion of bleaching during 1983, a year in which there was extensive bleaching among scleractinian corals in the San Blas Islands (Lasker et al.
1985). In 1983 P. kuna zooxanthella densities were un- affected by temperatures that exceeded 30 C [tempera- ture data reported in Lasker et al. (1985)]. This suggests that while ‘‘bleaching’’ can and occasionally does occur among P. kuna, there have not been large systematic bleaching events in this species.
Fagoonee et al. (1999) and Fitt et al. (2000) have both reported extensive seasonal variation in zoox- anthella density among scleractinians. Although absent in 1983, there was a distinct drop in density between
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April and June in 1998. Changes in light level (Berner et al. 1987; Titlyanov et al. 1999; Fitt and Cook 2001) as well as nutrient levels (Muscatine et al. 1989; Stim- son and Kinzie 1991) can affect zooxanthella density.
April/May coincides with the transition from the dry to rainy season in Panama and both light levels and nu- trient supply to the reef may change at that time.
Samples from one of the sites, Sail Rock, were col- lected from slightly deeper depths (5–8 m vs. 3–5 m) than at the other sites, but the zooxanthella densities from Sail Rock were not different from those from the other sites (Fig. 3).
Analysis of colonies from Korbiski Reef also de- monstrated differences in zooxanthella density among clones. Since clones at Korbiski are usually spatially
distinct (Coffroth and Lasker 1998), it is impossible to exclude within-reef habitat effects, but most of the clones at Korbiski were in close proximity of each other. The possibility of intrinsic differences in the dynamics of the symbiosis within different clones is intriguing. Goulet (1999) found that each P. kuna clone at Korbiski was dominated by a different clade B zooxanthellae geno- type. Differences in zooxanthella density between clones may relate to host traits, zooxanthellar traits, or some interaction of the two.
As in the symbiosis in other cnidarians, zooxanthella densities within the gorgonian P. kuna varied dramati- cally over time as well as between sites and genetic in- dividuals. However, a striking difference between Caribbean octocorals and other zooxanthellate cnidar- ians is their seemingly greater resistance of bleaching.
While there have been numerous reports of scleractinian coral bleaching throughout the world’s tropical oceans,
Table 1Analysis of variance tablesfor zooxanthellae density inPlexaura kunacolonies from the San Blas Islands, Panama
Source df Mean Square F Significance
Between colonies on Korbiski Reef during 1983/1984
Time 7 6.299x1011 4.30 <0.001
Colony 9 4.315x1011 1.50 0.162
Time by Colony 24 3.567x1011 1.24 0.234
Error 90 2.885x1011
Between clones on Korbiski Reef in 1998
Clone 6 1.579x1012 3.11 0.030
Error 17 5.069x1011
Time 1 6.440x1012 39.67 <0.001
Time by Clone 6 5.347x1011 3.29 0.025
Error (Time) 17 1.624x1011
Between sites in 1998
Site 3 2.179x1012 2.91 0.042
Error 60 7.483x1011
Time 1 2.090x1013 38.14 <0.001
Time by Site 3 1.580x1012 2.88 0.043
Error (Time) 60 5.479x1011
Fig. 1 Zooxanthella densities amongPlexaura kunacolonies from Korbiski Reef collected in different months and years. Error bars are one standard error
Fig. 2 Zooxanthella densities among clones of identicalPlexaura kunacolonies from Korbiski Reef in May and June 1998. Error bars are one standard error. Clones without error bars were represented by a single colony
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there have been far fewer observations of bleaching among octocorals; the data presented here show that while many scleractinians and a few octocorals were affected by the 1983 bleaching event, P. kuna zoox- anthella densities were unaffected. If the increasing in- cidence of bleaching events continues, the relative insensitivity of most gorgonians to high temperatures may have important consequences for Caribbean reefs.
Acknowledgments I thank M.A. Coffroth and S.R. Santos for their comments. Many individuals assisted with the fieldwork over the many years that samples were collected. In particular I thank the staff of the Smithsonian Tropical Research Institute San Blas Field Station for facilitating the work in the San Blas. Marie Balfour carried out the endless task of quantifying zooxanthella densities.
The comments of two anonymous reviewers greatly improved the manuscript. The work was supported by NSF grants OCE 8214894, OCE8521684, OCE9012168, OCE9217014, and OCE9813776.
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