Coral Reefs (2017) 36:395–400 DOI 10.1007/s00338-017-1550-4

NOTE

Bleaching response of species in the context of assemblage response

1,2 1 1 3 Timothy D. Swain • Emily DuBois • Scott J. Goldberg • Vadim Backman • Luisa A. Marcelino1,2

Received: 16 July 2016 / Accepted: 18 January 2017 / Published online: 27 January 2017 Ó Springer-Verlag Berlin Heidelberg 2017

Abstract Caribbean coral reefs are declining due to a Keywords Á Á Á mosaic of local and global stresses, including climate Thermal stress change-induced thermal stress. Species and assemblage responses differ due to factors that are not easily identifi- able or quantifiable. We calculated a novel species-specific Introduction metric of coral bleaching response, taxon-a and -b, which relates the response of a species to that of its assemblages Anomalously warm water disrupts mutualistic endosym- for 16 species over 18 assemblages. By contextualizing bioses between photosynthetic dinoflagellates ( species responses within the response of their assemblages, ) and coral hosts through the bleaching the effects of environmental factors are removed and response, eliminating the primary mode of energy acqui- intrinsic differences among taxa are revealed. Most sition for corals (Muscatine 1990) and leading to the experience either a saturation response, overly sensitive to degradation of globally (Wilkinson 2008). weak stress (a [ 0) but under-responsive compared to Bleaching responses differ across individuals, taxa, and assemblage bleaching (b \ 1), or a threshold response, events (e.g., Wooldridge 2014) through an unknown insensitive to weak stress (a \ 0) but over-responsive combination of factors intrinsic to the coral–Symbiodinium compared to assemblage bleaching (b [ 1). This metric holobiont (e.g., hosting Symbiodinium phylotypes with may help reveal key factors of bleaching susceptibility and differential thermotolerance; e.g., Barshis et al. 2013)or identify species as targets for conservation. extrinsic to the holobiont (e.g., differential thermal anomalies across reefs; e.g., Ban et al. 2014) with the added complexity of coral acclimation or adaptation to thermal stress (e.g., Guest et al. 2012; Howells et al. 2013). Communicated by Biology Editor Dr. Mark R. Patterson To isolate the effect of factors intrinsic to the holobiont, Electronic supplementary material The online version of this we propose a novel metric of bleaching response (taxon-a article (doi:10.1007/s00338-017-1550-4) contains supplementary and -b) that relates species-specific susceptibility to that of material, which is available to authorized users. the assemblages where they were surveyed. This metric is & Luisa A. Marcelino contextualized by the responses of the assemblage of cor- [email protected] als; if all coral species are equally susceptible the response

1 of each species would mirror its assemblage and react to Department of Civil and Environmental Engineering, bleaching stimulus and history of environmental conditions Northwestern University, 2145 Sheridan Road, Evanston, IL 60208, USA at that site identically. We argue that deviation from the bleaching response of the assemblage should mostly reflect 2 Integrative Research Center, Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, IL 60605, the effects of intrinsic factors on differential bleaching. USA Parameters a and b were originally derived to model the 3 Department of Biomedical Engineering, Northwestern effect of external and internal factors on differential University, 2145 Sheridan Road, Evanston, IL 60208, USA bleaching susceptibility among corals (Swain et al. 2016a). 123 396 Coral Reefs (2017) 36:395–400

Here we present taxon-a and -b as a species-specific metric 1 XJk of bleaching response calculated using 125 standardized SBRIk ¼ Bjk ð1Þ J records for 16 taxa at 18 Caribbean sites (Swain et al. k j¼1 2016a) which experienced thermally induced bleaching where Jk is the total number of taxa in site k. SBRIk was events separated by space and time, and were therefore calculated for coral assemblages with C3 taxa (363 Bjk exposed to dissimilar stress events and environmental records of 39 coral taxa at 49 sites from 1987 to 2006). histories. Using these data, we ask: (1) is the bleaching The effect of thermal stress on bleaching response was response of a coral species or assemblage a reflection of the assessed as the relationship between taxon-specific thermal-stress anomalies they are exposed to; and (2) does bleaching responses (Bjk) and thermal anomaly (6 month the bleaching response of species differ from that of the maximum DHW) at sites with C3 taxa (279 Bjk records of assemblages where they are found (i.e., do species over- 39 coral taxa at 36 sites from 1998 to 2006). react or under-react to similar thermal stress and environ- To compare bleaching response of taxon j with that of mental history)? its coral assemblage without the influence of target taxon j, the response of j was removed from the mean bleaching

response of the assemblage (site-Bjk or sBjk) (Swain et al. Methods 2016a) as: 1 XJk Data collection sB ¼ B ð2Þ jk J À 1 ik k i¼1;i6¼j Standardized records of bleaching and mortality for Car- ibbean corals were culled from Swain et al. (2016a). These where Jk is the total number of taxa in site k. Calculation of sBjk was restricted to sites containing C3 taxa with variable included 371 bleaching response records (Bjk, or bleaching response of taxon j at site k), that are a composite response bleaching responses (363 Bjk records of 39 taxa at 49 sites metric of bleaching and associated mortality that occurred from 1987 to 2006). following a thermal event (but not distal effects such as Sensitivity of individual taxon-specific bleaching disease or repeated bleaching) standardized across survey responses, Bjk; to that of the entire assemblage can be methods and bleaching criteria (Swain et al. 2016a), for 39 modeled (Swain et al. 2016a) as: taxa across 55 Caribbean sites from 1987 to 2006 (Electronic Bjk ¼ ujk þ bjsBjk þ aj; ð3Þ supplementary material, ESM, Table S1). Since bleached corals may either die or recover, and observation timing may where bj is the taxon-specific bleaching sensitivity (taxon- bias the data, both bleaching (greater in early surveys) and b), ujk is variability in estimation of Bjk due to error of associated mortality (greater in later surveys) were used to measurements with Var [ujk] = Var [dBjk], sBjk is descri- bed in Eq. 2, and coefficient aj is a taxon-specific param- calculate Bjk and provide a more accurate assessment. Thermal anomaly records, reported as degree heating weeks eter describing species-specific sensitivity to weak stress (DHW), for matching dates and locations were culled from (e.g., seasonal Symbiodinium density variation; Fitt et al. the U.S. National Oceanic and Atmospheric Administration 2000) in the absence of assemblage response (taxon-a). watch satellite monitoring database (http://cor Taxon-b can be directly measured as the linear regression coefficient in the regression of Bjk on sBjk as: alreefwatch.noaa.gov). DHW is the product of degrees (°C) ÀÁ ÀÁ above the highest monthly mean and ÀÁ Covk BÀÁjk; sBjk rkÀÁBjk its duration in weeks, and bleaching is considered likely at bj ¼ ¼ qk Bjk; sBjk ð4Þ Vark sBjk rk sBjk DHW [ 4 and mass bleaching and mortality at DHW [ 8 (http://coralreefwatch.noaa.gov). We used maximum DHW where Cov and Var are covariance and variance operators, within 6 months prior to survey to capture peak thermal q is the correlation coefficient, and r is standard deviation, stress for 42 sites from 1998 to 2006, which included 39 taxa all estimated for a given taxon (j = constant). Taxon- in 287 records. b * 1 indicates a rate of change in bleaching response of taxon j that is similar to the assemblages where it is found, Data analysis taxon-b \ 1 indicates an under-response relative to the rate of change of its assemblages, and taxon-b [ 1 indicates an Coral assemblage-level bleaching response (site-BRI or over-response relative to the rate of change of assemblages. SBRIk) was calculated as the mean of individual bleaching Taxon-b was calculated for taxa surveyed at C3 sites in and mortality responses (Bjk) for all taxa j at a given site k assemblages with C3 taxa (125 Bjk records of 16 taxa at 18 (Swain et al. 2016a) as: sites from 1987 to 2006).

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Results and discussion 39 taxa; ESM Fig. S1). These results suggest that differ- ential bleaching among assemblages is only partially Is bleaching response of a coral species explainable by exposure to different thermal anomalies, as or assemblage a reflection of the thermal-stress indicated by other studies (e.g., McClanahan et al. 2015). anomalies they are exposed to? We argue that, as a measure of assemblage bleaching response at a site, SBRIk should reflect the intensity and Thirty-six Caribbean coral assemblages [sites with C3 duration of thermal anomalies, thermal history of the site, taxa; 7.75 ± 4.55 (mean ± SD) taxa per site, 39 total chronic and acute environmental stresses that were not unique taxa] experienced thermal anomalies ranging directly observed, and capacity of the holobiont to resist 0–15.7 DHW from 1998 to 2006 (Fig. 1; ESM Table S1). thermal stress. Mean bleaching response of all taxa surveyed in a site (site-

BRI, or SBRIk;Eq.1) varied 19-fold among assemblages Does the bleaching response of species differ (SBRIk mean 23.0 ± 16.34%, range 2.75–52.9%; ESM from that of the assemblages where they are found? Table S1; Fig. 1). Bleaching response variability across sites has been used to identify factors affecting that Taxon-b, which is the regression coefficient relating response (e.g., water flow, thermal history, solar irradiance, bleaching response of a species (Bjk) to the response of its and acute thermal stress; McClanahan et al. 2005; Howells assemblages (sBjk) (Eq. 4), was determined for 16 species et al. 2013; Marcelino et al. 2013; Swain et al. 2016a, b). (limited to taxa surveyed in C3 sites, and sites with C3 Although there was a significant positive correlation taxa; Fig. 2; Table 1). Relative to the bleaching response of between DHW and SBRIk, DHW was a poor predictor of its assemblages, species: (1) over-responded, i.e., increased 2 SBRIk (linear regression: r = 0.21, p = 0.005, n = 36 bleaching response at a greater rate than their assemblages sites; Fig. 1a), which is consistent with other studies of (e.g., palmata, taxon-b [ 1); (2) under-re- Caribbean corals (e.g., Yee et al. 2008). Similarly, thermal sponded, i.e., increased bleaching response at a lesser rate anomalies significantly increased bleaching response of than their assemblages (e.g., labyrinthiformis, individual taxa, but DHW was a poor predictor of indi- taxon-b \ 1); or (3) responded similarly (e.g., Siderastrea vidual bleaching response (r2 = 0.10, p \ 0.001, n = 287, siderea, taxon-b * 1) (Fig. 2; Table 1). Because taxon-b

Fig. 1 Response of coral assemblages (SBRIk)at36 Caribbean sites (numerals correspond to site numbers in ESM Table S1) to thermal anomalies (6 months max degree heating weeks: DHW). Site bleaching response increases with thermal anomalies (r2 = 0.22, p \ 0.01; a), across the Caribbean at DHW of[8(b), 4–8 (c) and\4 (d). Shading of site markers corresponds to the gradient of SBRIk values, with lightest markers representing highest bleaching response values. Maps constructed using Mapbox and OpenStreetMap

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Fig. 2 Taxon-b for Caribbean corals. Responses of corals (Bjk) relative to their assemblages (sBjk) for 16 coral species (a) and exemplars of species with taxon-b [ 1 indicating over-response (b), taxon-b \ 1 indicating under-response (c), and taxon-b * 1 indicating similar response (d)

Table 1 Taxon-b and taxon-a values and associated errors, sample sizes, and significance for 16 coral species Taxon Taxon b Taxon a SE Correlation No of sites Mean taxa/site p value coefficient (r2)

Montastraea cavernosa 0.15 10.25 0.38 0.02 9 12.7 0.708 porites 0.15 23.85 0.39 0.02 9 13.2 0.709 Madracis myriaster 0.22 -1.25 0.33 0.13 5 15.4 0.56 0.29 14.76 0.43 0.04 13 10.8 0.509 Madracis decactis 0.37 -5.75 0.12 0.72 6 15.5 0.033 0.48 9.94 0.50 0.15 7 14.7 0.386 agaricites 0.70 33.54 1.41 0.04 8 12.4 0.635 Diploria labyrinthiformis 0.79 -6.37 0.24 0.58 10 11.9 0.011 1.06 7.56 1.31 0.12 7 13.3 0.455 natans 1.12 -10.24 0.34 0.61 9 12.6 0.013 Orbicella annularis 1.16 -6.42 0.60 0.25 13 10.0 0.08 Siderastrea siderea 1.18 -10.00 0.21 0.82 9 12.9 0.0007 Diploria strigosa 1.28 -13.62 0.47 0.51 9 12.6 0.031 Favia fragum 1.46 10.15 0.58 0.76 4 9.0 0.127 Diploria clivosa 2.38 -37.04 0.55 0.95 3 17.3 0.145 Acropora palmata 2.53 -30.29 0.98 0.77 4 6.0 0.124

accounts for the bleaching response of a taxon in relation to Although taxon-b quantifies relative differences in the its assemblages, it removes the effects of environment and rate of bleaching response increase, taxon-a further con- history on the response of species and reveals the intrinsic textualizes the response of the target taxon by indicating its (physiological) differences between taxa. species-specific sensitivity to weak stress in the absence of

123 Coral Reefs (2017) 36:395–400 399 assemblage response (Table 1). Considered together, the Limitations and general considerations 16 Caribbean species fall under two main categories of response with a trade-off between taxon-a and taxon-b: (1) Accuracy of taxon-a and -b (standard error, p value of corals that are overly sensitive to weak stress in the absence regression, and y-intercept; Table 1) depends on the num- of assemblage bleaching (taxon-a [ 0) but under-respon- ber of sites where a taxon is surveyed and on accuracy with sive to increasing thermal stress compared to assemblage which assemblage bleaching response is determined. The bleaching response (taxon-b \ 1, Fig. 3a quadrant II; latter, in turn, depends on (1) the number of taxa surveyed Fig. 3b); or (2) corals that are insensitive to weak stress in at each site (which was the primary factor determining the absence of assemblage bleaching (taxon-a \ 0) but accuracy in our dataset), (2) how representative those taxon over-responsive to increasing thermal stress compared to responses are of assemblage response, and (3) other factors assemblage bleaching response (taxon-b [ 1; Fig. 3a, including differences in survey methods and bleaching quadrant IV). Additionally, a few species were either criteria which have been accounted for by the standard- overly sensitive and over-responsive relative to their ization of individual Bjk records (Swain et al. 2016a). A assemblages (taxon-a [ 0 and taxon-b [ 1; Fig. 3a quad- low p value of the linear regression corresponds to a rant I) or insensitive and under-responsive relative to their smaller standard error of the estimation of taxon-b assemblages (taxon-a \ 0 and taxon-b \ 1; Fig. 3a quad- (Table 1). Although some of the regressions are significant rant III). (p \ 0.05), many are non-significant due, in part, to small Bleaching responses of corals with a trade-off between site sample sizes. The accuracy of taxon-a and -b should taxon-a and taxon-b proceed on opposing trajectories increase as more surveys of bleaching response become (Fig. 3a quadrants II and IV). Corals within the high taxon- available, particularly with inclusion of sites with a large a and low taxon-b category (Fig. 3a quadrant II, Fig. 3b) number of taxa presenting a wide range of bleaching demonstrate a saturation bleaching response where corals responses. over-respond compared to the baseline assemblage By relating the response of a coral to its assemblage, response, but under-respond as the assemblage response extrinsic factors in the bleaching response are removed and increases. Corals within the low taxon-a and high taxon-b the effect of individual intrinsic factors can be assessed category (Fig. 3a quadrant IV) demonstrate a threshold through analysis of variance of taxon-a and -b. Individual bleaching response where corals under-respond compared intrinsic factors could be identified experimentally by their to the baseline assemblage response, but over-respond as effect on the bleaching response, and by ranking their the assemblage response increases. Survival of a mild or importance as bleaching determinants by the portion of short thermal-stress event would be of greater concern for taxon-a and -b variance that they could explain. If the corals with a saturation bleaching response, while survival number and total effect of intrinsic factors are known, the of a severe or long thermal-stress event would be of greater approximate upper bound on the effect of the remaining concern for corals with a threshold bleaching response. intrinsic factor could be inferred. However, individual Corals within the high taxon-a and high taxon-b category intrinsic factors may not act independently (e.g., the effect (Fig. 3a quadrant I) would be considered as taxa of highest of Symbiodinium thermotolerance may be influenced by concern (due to consistent over-response), while those skeletal light scattering; Swain et al. 2016b) and extrinsic within the low taxon-a and taxon-b category (Fig. 3a factors such as thermal history may lead to acclimation or quadrant III) would be considered as taxa of least concern adaptation of corals (Guest et al. 2012; Pratchett et al. (due to consistent under-response). 2013).

Fig. 3 Relationship between taxon-a and taxon-b for Caribbean corals (r2 = 0.56, p \ 0.001; a), with an exemplar species (b) demonstrating a relatively high a (9.94) but low b (0.48) values typical of quadrant II (a)

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