Spring bleaching among Pocillopora in the Sea of Cortez, Eastern PaciWc

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1 DOI /s NOTE Spring bleaching among Pocillopora in the Sea of Cortez, Eastern PaciWc T. C. LaJeunesse H. Reyes-Bonilla M. E. Warner Received: 5 September 2006 / Accepted: 29 November 2006 Springer-Verlag 2007 Abstract A mild bleaching event was observed among Pocillopora spp. in the southern Gulf of California in the spring of Uniform bleaching occurred in numerous colonies on the upper portions of their branches. Most (»90%) colonies that exhibited bleaching contained a species of endosymbiotic dino- Xagellate, Symbiodinium C1b-c, which divered from the Symbiodinium D1 found inhabiting most unbleached colonies. Analysis of chlorophyll Xuorescence, indicated a decline in photosystem II photochemical activity, especially among colonies populated with C1b-c. By early August, most avected colonies had recovered their normal pigmentation and Xuorescence values were once again high for all colonies. No mortality was observed among tagged bleached colonies nor did symbiont species composition change during recovery. This unusual episode of bleaching did not appear to be a response to thermal stress, but may have been triggered by high levels of solar radiation during a period of unseasonally high water clarity in the early spring. Communicated by Biology Editor M. van Oppen. T. C. LaJeunesse (&) Department of Biology, OE 167, Florida International University, Miami, FL 33199, USA lajeunes@wu.edu H. Reyes-Bonilla Departamento de Biologia Marina, Universidad Autonoma de Baja California Sur., Apartado postal 19-B, CP La Paz, B. C. S., Mexico M. E. Warner University of Delaware, College of Marine and Earth Studies, 700 Pilottown Rd, Lewes, DE 19958, USA Keywords Coral bleaching Eastern PaciWc Pocillopora Ecophysiology Symbiodinium Introduction Arborescent stony corals in the genus Pocillopora are key components of the shallow water communities that exist along the eastern PaciWc coast from México to Ecuador (Glynn and Ault 2000). Their presence supplies habitat, shelter, and sources of nutrition for economically important invertebrate (e.g., crustaceans, mollusks) and Wsh faunas. The natural services that corals provide are vital for sustainable commercial Wsheries production and tourism. Local economies therefore benewt from the continued existence of these coral-dominated ecosystems. Coral bleaching, the precipitous reduction in population density and/or loss of pigmentation in photosynthetic endosymbiotic dinoxagellates (Symbiodinium spp.), typically occurs in the Eastern PaciWc during periods of El Niño Southern Oscillations (ENSOs), when high sea temperatures and calm, clear water are a feature. Sea surface temperatures are expected to rise more than 2 C in the coming century and there is both concern and debate regarding how corals will respond to these increases (Hoegh-Guldberg 1999). ENSOs have severely impacted many Eastern PaciWc marine communities (Glynn 1990, 2004). Bleaching induced mortality has been highest among colonies of Pocillopora spp., and during the last major ENSO in 1998, losses in live coral cover exceeded 60% in some areas along the coast of southwestern México, including Banderas Bay and Oaxaca (Reyes-Bonilla et al. 2002).

2 Isolated from the rest of the Eastern PaciWc, zooxanthellate corals living in the Sea of Cortez, Gulf of California, have avoided the severest conditions of these events (Reyes-Bonilla 2001). Hydrological barriers near to the entrance of the Gulf diminish the northern advance of warm water masses brought from the west by ENSO events (Fiedler 2002). While some bleaching has occurred among corals in this region, the muted intensity and duration of thermal stress has not resulted in the widespread mortality experienced by many coral communities distributed from southern México to Colombia. The study of coral communities living at sub-tropical latitudes may help us assess how they are changing with the present climate warming. A visit to the Gulf of California was made in the Wrst week of May in 2006 to establish Wxed transects for the long-term monitoring and experimentation with individually tagged coral colonies near La Paz, México. Unexpectedly, certain Pocillopora spp. colonies were visibly white relative to others. This phenomenon also occurred synchronously in other areas of the Gulf of California. This was unusual because widespread coral bleaching tends to occur in late summer or fall when nutrient reserves are lowest for the coral (Fitt et al. 2001), and because past bleaching in the Sea of Cortez has correlated with temperatures elevated above 31 C. Herein is a Wrst report of an anomalous spring bleaching event in this region. Materials and methods Following initial observations and reports, Weld surveys were conducted at Loreto Bay ( N, W), Espíritu Santo Island ( N, W), Punta Arenas ( N, W) and Cabo Pulmo ( N, W) in April and May 2006, to determine the extent of bleaching. Line transects (25 m, N = 5 at all sites) were laid parallel to the coast, and the percentage of discolored coral colonies (>5 cm diameter) was recorded. The genetic identity and physiological condition of Symbiodinium spp. populations in bleached and unbleached colonies on a near-shore transect at Punta Galeras, Baja California ( N, W) was investigated in May At this location, approximately 2 m below the surface, a small (0.5 ha) community of Pocillopora spp. covered 60 75% of the substrate. Here, a total of ten beached colonies consisting mostly of Pocillopora damicornis and P. verrucosa were tagged along with ten unbleached colonies, one of which was a P. meandrina. A central branch was removed from all 20 specimens and placed in a zip-lock bag. One unusual, variegated, colony of P. damicornis had entire branches that were either bleached or normally pigmented. In this specimen, a branch fragment was collected from each portion. Additional collections were made along this transect from colonies of P. damicornis, P. verrucosa, P. capitata, and P. meandrina. In all the collections described above, diverent morphotypes within these species were selected to avoid sampling from clone-mates (ramets). Collected fragments were returned to the laboratory for physiological measurements and for the extraction of symbiont populations for subsequent genetic analysis. Following dark acclimation (»30 min), the maximum quantum yield of photosystem II charge separation (F v /F m ) was recorded using a diving PAM Xuorometer (Walz, Germany) at replicate (n =3) positions along the tip and side of each branch. Samples were returned to the USA where the genetic identity of the Symbiodinium populations in each sample was later analyzed via PCR-denaturing gradient gel electrophoreses (DGGE) of the ITS 2 rdna (LaJeunesse 2002). These specimens were further analyzed by quantitative real time PCR (qpcr) in order to conwrm the dominant algal populations established by PCR- DGGE analysis. DNA concentrations from each sample were diluted to 1.0 ng μl 1. Each was then independently analyzed with clade D and clade C speciwc primers (Ulstrup and van Oppen 2003) producing two cycle threshold (C T ) values per sample. The C T values for reactions designed to detect clade C Symbiodinium were then compared against a standard curve of the C T values generated from dilution series ( ng; n =6; R 2 > 0.95) of DNA extracts from a cultured isolate of C1, Symbiodinium goreaui. The DNA concentration of D1 in each sample was calculated similarly based on a second standard curve generated from DNA extracts from a cultured isolate of D1a ( ng = 6; R 2 > 0.95). With the assumption that the average DNA content per cell is similar between symbionts (LaJeunesse et al. 2005), relative abundance was estimated based on diverences in DNA content. In early August 2006 the site was revisited for re-sampling and a repeat of the genetic and physiological analyses described above. Results and discussion Zooxanthellate scleractinians in the Sea of Cortez are adapted to wide Xuctuations in annual sea temperature (Fig. 1). In 2006, satellite sea surface skin temperatures (SST) were only slightly colder than usual in the southern

Average C 2000-2005 32 30 28 26 24 22 20 18 J F M A M J J A S O N D month Fig.

3 Average C J F M A M J J A S O N D month Fig. 1 Average monthly sea surface temperatures (SST) in the Sea of Cortez near La Paz, México for the years of (error bars mean SD based on the average of monthly means). The open circles represent monthly averages of SST for 2006 (readings taken every 48 h; error bars mean SD). All values calculated from 14 km North America satellite data at approximate coordinates N and W Gulf of California from January to March and then were normal during April and May (SST14NA, 14 km gridded data, acquired from the NOAA Satellite and Information Service: but never dropped below 19 C. By late June the southern gulf was C warmer than average, (monthly mean in La Paz in June is C; Lluch-Cota et al. 2000). During Weld visits to Punta Galeras in late May and mid June, temperature readings from dive computers were never above 26 C (instrument accuracy 0.5 C) at 1 2 m depth. Sea surface temperatures, therefore, were relatively normal during the bleaching event, and well below the estimated bleaching threshold of 29.6 C (Reyes-Bonilla et al. 2002). In the absence of a thermal cue for the observed bleaching, the possible contribution of solar radiation was considered. From early February until late April at these latitudes (24 25 N) the sun s diurnal noon altitude is increasing at its maximum rate, such that by the beginning of April, the direct noon time solar irradiance has already reached 94% of its annual peak value above the sea surface, and 97% underwater. Normally, corals in the waters around La Paz would be expected to be shielded from these high levels of solar radiation at this time of year because of a reduction in water clarity due to high springtime primary productivity. These spring phytoplankton blooms in the Gulf of California are driven by annual cycles of strong tidal mixing and nutrient inputs from cold waters up-welled from its deep southern basin (Kahru et al. 2004). In 2006, however, anecdotal reports from several biologists in the area suggested that there was an extended period of unusually clear water during the months of March and April, and in late April, sporadic bleaching was reported and noted in Weld locations around the southern Gulf region. It is feasible that this period of unusual water clarity may have negatively impacted the capacity for gradual photoacclimation in some symbionts for this time of year (Fitt et al. 2001), notwithstanding normal sea temperatures. Indeed, further observations are necessary to fully characterize the pattern of underwater light attenuation during and after spring phytoplankton blooms in this region. In response to this information, surveys at several locations in the region were conducted to determine the magnitude of this bleaching episode (Fig. 2). Bleaching was mainly restricted to Pocillopora spp., although some Pavona spp. colonies were also paled. The prevalence of whitened colonies was highest in Loreto ( %, mean SE) and lowest in Cabo Pulmo ( %). DiVerence in the percentage of bleached colonies among areas was signiwcant (F 3,764 = 4.58, P < 0.01, arcsine transformed values). Paled colonies were haphazardly distributed among normally pigmented ones while within individual colonies, bleaching appeared uniform. Glynn (1990) previously noted a similar unusual patchwork of pale, or white, colonies situated among apparently unavected pigmented colonies during the ENSO in Panama. An abundance of bleached colonies present at one of the long-term study sites, Punta Galeras, located opposite Isla Espíritu Santo, presented an opportunity to compare whether diverences in symbiont populations and/or their physiological condition explained why certain colonies were excessively paled while others were not (Fig. 3a, b). As was found in Panama (Glynn et al. 2001), the Pocillopora spp. at this location associated with two distantly related Symbiodinium Fig. 2 Percent bleached colonies based on Wve transects (25 m) at each of four locations along the coast of southern Baja California. Loreto Bay, farthest north, possessed the highest incidence (error bars = mean SE). The total number of colonies counted at each location is given in parentheses

Fig. 3 a Survey of 36 Pocillopora spp. colonies along a 25 m transect. The relative distance from each other, colony size, bleached or pigmented, and resident Symbiodinium taxon are given.

verrucosa exhibits healthy pigmentation, c PCR-DGGE analysis of the ITS 2 rdna on DNA extracts from the resident symbiont populations in colonies no. 9 through 18.

4 Fig. 3 a Survey of 36 Pocillopora spp. colonies along a 25 m transect. The relative distance from each other, colony size, bleached or pigmented, and resident Symbiodinium taxon are given. Only those colonies surveyed are depicted. P. damicornis (Pd), P. verrucosa (Pv), P. meandrina (Pm); b a colony of P. damicornis is bleached while adjacent P. verrucosa exhibits healthy pigmentation, c PCR-DGGE analysis of the ITS 2 rdna on DNA extracts from the resident symbiont populations in colonies no. 9 through 18. Banding patterns are Wxed and provide a diagnostic Wngerprint for each symbiont species, D1 and C1b-c, associating with Pocillopora spp., d the ratio of variable chlorophyll Xuorescence to maximium chlorophyll Xuorescence (F v /F m ) for tops and sides of bleached and unbleached colonies containing symbiont C1b-c and D1, respectively b c D1 C1b-c d 0.7 colony number a 18b MKR P< P= Pv (C1b-c) a Rock 1 Pv (D1) 2 Pd (C1b-c) 7 Pv (D1) 6 Pv (D1) Pocillopora sp. colony 3 Pd (D1) 5 Pv (C1b-c) Symbiont type D1 D1 (bleached) C1b-c C1b-c (bleached) 4 Pd (C1b-c) 11 Pv (D1) C1 12 Pv (C1b-c) D1 colony Pd 9 Pm (D1) 18a(C1b-c) B1 10 Pd (C1b-c) 14 unk (C1b-c) 18b(D1) variegated N 0.6 Fv/Fm unk (D1) 17 Pd (D1) Pd (D1) 16 Pd (C1b-c) 0.1 tops sides 20 Pd (C1b-c) 15 m 5m Punta Galeras Transect 3 19 Pd (D1) spp. The majority of the bleached colonies surveyed (9 of 10) possessed populations of C1b-c, as dewned by a characteristic ITS 2 rdna Wngerprints generated by PCR-DGGE (LaJeunesse 2002; Fig. 3c), while nine of ten adjacent colonies with normal pigmentation contained D1. Additional Pocillopora spp. colonies possessing normal pigmentation and unique morphologies were sampled along a transect line that bisected the area (Fig. 3a). While many of these colonies harbored D1, about 13% contained C1b-c. A numerical dominance of one symbiont type over the other occurred in all colonies examined. Homogenous symbiont populations, based on the limits of PCR-DGGE resolution (c.f. Thornhill et al. 2006), existed in three specimens that were sampled at ten points in the interior and exterior of each colony (one possessed C1c-b while two contained D1; data not shown). Based on normalizing to known DNA quantities from cultured isolates, qpcr detected traces of the other symbiont species at extremely low abundances. On average, C1b-c comprised 0.12% of the total symbiont population in colonies dominated by D1 (n = 10; mean SD 0.12%), whereas D1 comprised 1.28% of the population in colonies dominated by C1b-c (n = 11; mean SD 0.66%). In one unusual case, populations of each symbiont were found spatially segregated into diverent zones of the variegated bleached/unbleached colony (#18, Fig. 3a, c). Unlike coral species in the Montastraea annularis complex of the Caribbean (Rowan et al. 1997), symbiont mixtures sometimes found in Pocillopora spp. do not appear to be regulated by irradiance. Homogeneity in symbiont populations

5 therefore explains the homogeneous bleaching pattern observed for most colonies (Fig. 3b). The palest regions in each bleached colony began at the branch tips and extended down 1 2 cm along the sides before rapidly transitioning into a normal-looking brown pigmentation. Cell counts of the Symbiodinium spp. populations were not made and it was not possible to resolve whether the bleached appearance was due to a reduction in symbiont cell numbers or, reduced concentrations of photosynthetic pigment or, both. Mean ratios of variable to maximum chlorophyll Xuorescence (F v /F m ) were statistically diverent between bleached and normally pigmented colonies at both top and side branch locations, with the lowest PSII quantum yields noted in the algae within the top of the bleached colonies (Fig. 3d, ANOVA; F =44.9, P < 0.001; F =8.45, P = 0.01 for top and side bleached vs. non-bleached comparisons, respectively), providing some evidence for photosynthetic disruption in zooxanthellae within the bleached corals. Similar or greater losses in PSII photochemical potential have been previously noted in corals subjected to experimental or natural thermal bleaching (Warner et al. 1999; Jones et al. 2000). Over the next few months, periodic return visits were made to Punta Galeras to monitor the condition of the previously tagged bleached colonies. In late May, a few previously bleached colonies were still slightly discolored and, by June, many had regained their natural color. No mortality was observed among the colonies of our permanent transect and among those in the surrounding community. In August, symbiont populations were re-examined for each colony and no change in genetic type had occurred. Chlorophyll Xuorescence was also re-examined and revealed no signiwcant diverences in F v /F m between the previously bleached and non-bleached colonies (0.653, SD and 0.664, SD 0.027, respectively). In both groups, average F v /F m values were signiwcantly higher than measured in May. Higher F v /F m values for colonies with D1 Symbiodinium in August compared to May (0.664 vs. 0.57), provides some evidence that these algae were negatively impacted in the spring, albeit to a lesser degree. The extent to which genetic disparity and/or diversity among Symbiodinium corresponds with physiological variation is under intensive investigation (Iglesias- Prieto et al. 2004; Rowan 2004; Tchernov et al. 2004; Berkelmans and van Oppen 2006; Robison and Warner 2006; Warner et al. 2006). Still, much less is known about how physiological and biochemical diverences among Symbiodinium spp. inxuence, or modulate, the biology of the intact association. Assuming that the spring bleaching event in the Sea of Cortez was induced by high irradiance, the type D1 Symbiodinium sp. in Pocillopora ssp. appear able to acclimatize to episodes of high irradiance better than Clb-c. Acknowledgments We especially thank Robin Smith (FIU) for conducting qpcr analyses. Several people assisted us with Weldwork, including David A. Paz García (UABC), Miriam Mora Pérez (CICIMAR), Israel Sánchez Alcántara and Saúl González Romero (UABCS). Support for this work was provided by the National Science Foundation grants IOB and IOB , and Fondo Mexicano para la Conservación de la Naturaleza (grant E ). References Berkelmans R, van Oppen MJH (2006) The role of zooxanthellae in the thermal tolerance of corals: a nugget of hope for coral reefs in an era of climate change. Proc R Soc Lond B 273: Fitt WK, Brown BE, Warner ME, Dunne RP (2001) Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. 20:51 65 Fiedler PC (2002) Environmental change in the eastern tropical PaciWc Ocean: review of ENSO and decadal variability. Mar Ecol Prog Ser 244: Glynn PW (1990) Coral mortality and disturbances to coral reefs in the tropical eastern PaciWc. In: Glynn PW (ed) Global ecological consequences of the El Niño-Southern Oscillation. Elsevier Oceanography Ser 52, Amsterdam, pp Glynn PW (2004) EVects of the El Niño-Southern Oscillation on eastern PaciWc corals and coral reefs: an overview. Proc 9th Int Coral Reef Symp 1: Glynn PW, Ault JS (2000) A biogeographic analysis of the far eastern PaciWc coral reef region. 19:1 23 Glynn PW, Maté JL, Baker AC, Calderon MO (2001) Coral bleaching and mortality in Panama and Ecuador during the El Niño-southern oscillation event: spatial/temporal patterns and comparisons with the event. Bull Mar Sci 69: Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world s coral reefs. Mar Freshw Res 50: Iglesias-Prieto R, Beletran VH, LaJeunesse TC, Reyes-Bonilla H, Thome PE (2004) DiVerent algal symbionts explain the vertical distribution of dominant reef corals in the eastern PaciWc. Proc R Soc Lond B 271: Jones RJ, Ward S, Amri AY, Hoegh-Guldberg O (2000) Changes in quantum eyciency of Photosystem II of symbiotic dinoxagellates of corals after heat stress, and bleached corals after the 1998 Great Barrier Reef mass bleaching event. 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6 Lluch-Cota SE, Pacheco-Ayub CA, Bautista-Romero JJ, Hernández-Vázquez S, Lluch Cota BB (2000) Colección de información ambiental para el PacíWco. CD-ROM, Centro de Investigaciones Biológicas del Noroeste/Comisión Nacional de Cienciay Tecnología, Mexico City Reyes-Bonilla H (2001) EVects of the El Niño-Southern Oscillation on coral communities of the Gulf of California, México. Bull Mar Sci 69: Reyes-Bonilla H, Carriquiry JD, Leyte-Morales GE, Cupul-Magaña AL (2002) EVects of the El Niño-Southern Oscillation and the anti-el Niño event ( ) on coral reefs of the western coast of México. 21: Robison JD, Warner ME (2006) DiVerential impacts of photoacclimation and thermal stress on the photobiology of four diverent phylotypes of Symbiodinium (Pyrrhophyta). J Phycol 42: Rowan (2004) Thermal adaptation in reef coral symbionts. Nature 430:742 Rowan R, Knowlton N, Baker A, Jara J (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388: Tchernov D, Gorbunov MY, de Vargas C, Yadav SN, Milligan AJ, Haggblom M, Falkowski PG (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci USA 101: Thornhill D LaJeunesse TC, Kemp DW, Fitt WK, Schmidt GW (2006) Long-term surveys of coral-algal symbioses reveal patterns of stability and post-bleaching reversion. Mar Biol 148: Ulstrup KE, Van Oppen MJH (2003) Geographic and habitat partitioning of genetically distinct zooxanthellae (Symbiodinium) in Acropora corals on the Great Barrier Reef. Mol Ecol 12: Warner ME, Fitt WK, Schmidt GW (1999) Damage to photosystem II in symbiotic dinoxagellates: a determinant of coral bleaching. Proc Natl Acad Sci USA 96: Warner ME, LaJeunesse TC, Robison JD, Thur RM (2006) The ecological distribution and comparative photobiology of symbiotic dinoxagellates from reef corals in Belize: potential implications for coral bleaching. Limnol Oceanogr 51:

Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific

Received 20 November 2003 Accepted 25 March 2004 Published online 20 July 2004 Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific R. Iglesias-Prieto