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Environmental Drivers of Variation in Bleaching Severity of Acropora Species during an Extreme Thermal Anomaly

Environmental Drivers of Variation in Bleaching Severity of Acropora Species during an Extreme... ORIGINAL RESEARCH published: 27 November 2017 doi: 10.3389/fmars.2017.00376 Environmental Drivers of Variation in Bleaching Severity of Acropora Species during an Extreme Thermal Anomaly 1, 2 1, 2 1, 2 1, 2 Mia O. Hoogenboom *, Grace E. Frank , Tory J. Chase , Saskia Jurriaans , 1, 2 2 1 1, 2, 3 Mariana Álvarez-Noriega , Katie Peterson , Kay Critchell , Kathryn L. E. Berry , 1, 2 1, 3 1, 2 Katia J. Nicolet , Blake Ramsby and Allison S. Paley Marine Biology and Aquaculture, College of Science and Engineering, James Cook University, Townsville, QLD, Australia, 2 3 ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, QLD, Australia, AIMS@JCU, Australian Institute of Marine Science, Townsville, QLD, Australia Edited by: David Suggett, High sea surface temperatures caused global coral bleaching during 2015–2016. During University of Technology Sydney, Australia this thermal stress event, we quantified within- and among-species variability in bleaching Reviewed by: severity for critical habitat-forming Acropora corals. The objective of this study was David Obura, to understand the drivers of spatial and species-specific variation in the bleaching Coastal Oceans Research and Development in the Indian Ocean, susceptibility of these corals, and to evaluate whether bleaching susceptibility under Kenya extreme thermal stress was consistent with that observed during less severe bleaching Anthony William Larkum, events. We surveyed and mapped Acropora corals at 10 sites (N = 596) around the University of Technology Sydney, Australia Lizard Island group on the northern Great Barrier Reef. For each colony, bleaching *Correspondence: severity was quantified using a new image analysis technique, and we assessed Mia O. Hoogenboom whether small-scale environmental variables (depth, microhabitat, competition intensity) mia.hoogenboom1@jcu.edu.au and species traits (colony morphology, colony size, known symbiont clade association) Specialty section: explained variation in bleaching. Results showed that during severe thermal stress, This article was submitted to bleaching of branching corals was linked to microhabitat features, and was more severe Coral Reef Research, a section of the journal at reef edge compared with lagoonal sites. Bleaching severity worsened over a very short Frontiers in Marine Science time-frame (∼1 week), but did not differ systematically with water depth, competition Received: 27 June 2017 intensity, or colony size. At our study location, within- and among-species variation in Accepted: 09 November 2017 bleaching severity was relatively low compared to the level of variation reported in the Published: 27 November 2017 literature. More broadly, our results indicate that variability in bleaching susceptibility Citation: Hoogenboom MO, Frank GE, during extreme thermal stress is not consistent with that observed during previous Chase TJ, Jurriaans S, bleaching events that have ranged in severity among globally dispersed sites, with Álvarez-Noriega M, Peterson K, fewer species escaping bleaching during severe thermal stress. In addition, shaded Critchell K, Berry KLE, Nicolet KJ, Ramsby B and Paley AS (2017) microhabitats can provide a refuge from bleaching which provides further evidence of Environmental Drivers of Variation in the importance of topographic complexity for maintaining the biodiversity and ecosystem Bleaching Severity of Acropora Species during an Extreme Thermal functioning of coral reefs. Anomaly. Front. Mar. Sci. 4:376. doi: 10.3389/fmars.2017.00376 Keywords: spatial refugia, environmental gradients, Symbiodinium, niche construction, thermal performance Frontiers in Marine Science | www.frontiersin.org 1 November 2017 | Volume 4 | Article 376 Hoogenboom et al. Determinants of Coral Bleaching Severity INTRODUCTION during the 1998 bleaching event, massive Porites were more susceptible to bleaching in the Palm Islands on the central Mass coral bleaching in response to increased sea surface GBR than they were at nearby Magnetic Island (Marshall temperature is a major threat to the persistence of coral reefs. and Baird, 2000). Similarly, during a bleaching event in the Analyses of sea surface temperature data indicate that ocean central Pacific, bleaching was observed at some sites but not warming has accelerated in recent decades, and that coral others for each of several monitored species (Fagerstrom and reefs are increasingly being exposed to thermal stress (Heron Rougerie, 1994). Indeed, numerous studies report within-species et al., 2016). Since the 1980s, global mass bleaching events variation in bleaching severity across different habitats (e.g., have caused large-scale and significant coral loss. For example, Bruno et al., 2001; Aronson et al., 2002; Hardman et al., 2004). in 1998, increased seawater temperatures caused widespread There are numerous potential biotic drivers of this within-species bleaching and coral mortality in most of the world’s coral reef variability. First, different types of Symbiodium are more resistant regions, with mortality in excess of 90% on some reefs in the to increased ocean temperature than others (e.g., Thornhill et al., central and western Indian Ocean (Spalding and Brown, 2015). 2006; Jones et al., 2008; Lesser et al., 2010; Howells et al., 2013), Moreover, between June 2014 and April 2016, bleaching was and many coral species can associate with more than one type of observed throughout the global oceans during what is now Symbiodinium (Baker, 2003; Sampayo et al., 2008). Therefore, we considered to be the longest bleaching event on record (Eakin assessed whether species that have the capacity to associate with et al., 2016). In the context of bleaching, temperature stress is more than one symbiont type show lower bleaching severity, often measured in “degree heating weeks” (DHW, C-weeks), on average, than other species. Second, bleaching severity is a metric which summarizes the duration of time over which influenced by coral colony size. For example, larger colonies temperatures have been above the average temperature of the experienced more extensive bleaching than smaller colonies of warmest summer month at each location (e.g., Eakin et al., several species during a major Caribbean bleaching event in 2010). The recent thermal stress event caused severe bleaching 2005 (Brandt, 2009). However, other studies have found contrary on the northern section of the Great Barrier Reef in 2016, where results with higher bleaching for smaller colonies for some approximately one third of reefs experienced levels of heat stress species (Pratchett et al., 2013), or that colony size only influences that were up to two-fold higher than those experienced in the bleaching prevalence for certain colony morphologies in certain 1998 bleaching event in the same region (Hughes et al., 2017). locations (Wagner et al., 2010). Finally, other benthic organisms We here investigate whether species susceptibility to bleaching that compete for space with corals, such as soft corals and under extreme heat stress is consistent with species susceptibility macroalgae, contain secondary metabolites that can lead to the reported during previous bleaching events. expulsion of Symbiodinium (i.e., bleaching, Aceret et al., 1995). Different coral species respond differently to environmental Moreover, competition can influence coral fitness more generally stressors, leading to substantial among-species variability in (e.g., by growth suppression, see Horwitz et al., 2017), and such bleaching susceptibility. In general, the literature documents effects might act as an additional stressor that increases bleaching relatively high bleaching severity for branching corals from severity. To the best of our knowledge, effects of competition on the genera Stylophora, Acropora, and Pocillopora, and lower bleaching severity have not previously been investigated in situ. bleaching severity for mound-shaped Porites and Diploastrea The topographic complexity of reefs results in high variability (e.g., Marshall and Baird, 2000; Loya et al., 2001; van Woesik in environmental conditions over small spatial scales. For et al., 2011; Swain et al., 2016). However, bleaching severity instance, stable and biologically significant temperature variation is spatially patchy (e.g., Wooldridge and Done, 2004; Penin occurs at small scales (1–2 m, e.g., Gorospe and Karl, 2011), et al., 2007). For instance, bleaching severity varies between and also at larger between-habitat scales (hundreds of meters, habitats with some studies reporting bleaching to be less severe e.g., Lundgren and Hillis-Starr, 2008). Water flow also varies in shallow compared with deep lagoons (Grimsdich et al., 2010), within- and among-habitats (e.g., Fulton and Bellwood, 2005; while others report the opposite trend (Fisk and Done, 1985; Hoogenboom and Connolly, 2009). Therefore, spatial variation Muhando, 1999). Bleaching severity can also vary with depth in abiotic drivers, such as light intensity, water flow, temperature, (e.g., Penin et al., 2007), although some studies have reported no and turbidity, influences which corals bleach and where (e.g., significant variation in bleaching with depth when values were West and Salm, 2003). Previous studies report different effects pooled across genera (Bruno et al., 2001). While temperature of water flow on bleaching severity, with evidence of increased stress is recognized to be the primary driver of mass-bleaching bleaching severity at exposed sites with high wave activity (Berkelmans et al., 2004; Hughes et al., 2017), there is no strong (McClanahan et al., 2007), as well as evidence of reduced consensus about additional environmental drivers of spatial bleaching, along with higher survival of bleached corals, under variation in bleaching severity. It is likely that a combination of high water flow conditions (Nakamura and van Woesik, 2001; environmental factors (e.g., local light intensity and water flow) Nakamura and Yamasaki, 2005). Variability in bleaching among and biological factors (including species-specific responses, and different reef habitats is also associated with site-specific turbidity local abundances of susceptible vs. tolerant species) influence levels (e.g., Williams et al., 2010). However, observed responses spatial patterns of bleaching severity. range from a negative effect of turbidity whereby suspended In addition to among-species variation in bleaching particulates are thought to act as an additional stressor that susceptibility, there is often high variation in the bleaching lowers temperature tolerance (Williams et al., 2010; Hongo and responses of individuals of the same species. For instance, Yamano, 2013), to predictions that turbidity may lessen the Frontiers in Marine Science | www.frontiersin.org 2 November 2017 | Volume 4 | Article 376 Hoogenboom et al. Determinants of Coral Bleaching Severity severity of bleaching in some shallow habitats by reducing light loggers (Onset Hobo) measured an average temperature of ◦ ◦ penetration (West and Salm, 2003; Cacciapaglia and van Woesik, 30.3 C (range 27.7–33.2 C) at two reef crest sites during 2016). February and March 2016. At the time of the surveys, significant Methodological issues associated with quantifying bleaching bleaching of susceptible coral species had been observed, severity in the field might also lead to variation between studies. but mortality was still negligible (widespread bleaching-related While observer differences are unlikely to explain variation in mortality was observed on reefs in the region 1 month later, bleaching severity between habitats reported in a single study, Hoogenboom unpubl. data). Over a period of 8 days, divers observers can differ in color sensitivity or in training (e.g., Siebeck conducted in-water surveys at 10 sites where the bleaching status et al., 2006). Many observer methods measure bleaching in simple of ∼60 Acropora colonies was monitored per site. Colonies were categories (e.g., “pale,” “partially bleached,” and “bleached”), and selected haphazardly as divers swam along a depth contour from this categorization can obscure color gradation. To overcome a randomly selected starting place, making a conscious effort issues associated with categorization of bleaching, some studies to observe colonies from different reef microhabitats as far as estimate the proportion of each coral colony that is healthy practicable given the topography of each site. The spatial position vs. bleached (e.g., Obura, 2001), providing a finer resolution of of each colony was taken using a towed GPS (Garmin eTRex) bleaching severity. Despite these advances, however, a recent that was time-synchronized with a dive watch, and the depth review highlighted the relatively high measurement uncertainty of each colony was recorded using a dive computer (Suunto, for bleaching severity, and noted that standardizing measuring D4 and Zoop). Each colony was photographed from directly protocols would help to increase the precision of bleaching above (as described below), and additional photographs of colony estimates (Swain et al., 2016). To help standardize bleaching morphology, local reef topography and colony microhabitat, measurements, we developed a new quantification of bleaching neighboring competitors, and corallite shape were taken to enable severity by measuring coral “whiteness” in individually white- measurement of colony size and competition intensity, and to balanced images of healthy, pale and bleached corals. assist species-level identification. We also kept track of the time The objective of this study was to understand the drivers of and date of observations because ongoing heat stress suggested small-scale variation in the bleaching susceptibility of branching that bleaching severity would continue to increase during corals, and to evaluate whether bleaching susceptibility under and after the observation period. The full dataset, including extreme thermal stress is consistent with that observed during coral images and spatial positions, is available in Critchell and previous (less severe) bleaching events. We focused on corals Hoogenboom (2017). from the genus Acropora due to their high abundance on Indo- Pacific reefs, their importance for the structural complexity of Measurement of Bleaching Severity reefs, and their variable bleaching severity within- and among- species (e.g., Marshall and Baird, 2000; Loya et al., 2001; Swain (Response Variable) et al., 2016). Specifically, we aimed to understand whether Individual coral colonies were photographed from directly and how variation in bleaching severity was associated with overhead, without flash, and from as close as practicable, with depth, spatial location of colonies relative to the reef edge (a a Canon G16 digital camera in an underwater housing. Each measure of exposure to wave energy and general reef habitat), photograph contained a color reference chart and scale bar. microhabitat, colony size, colony morphology, and the level of As differing light conditions of each colony did not allow competition and the identity of competitors. We also evaluated for identical camera settings to be used in each photograph, whether association with multiple symbiont types could explain individual settings based on the highest image quality (pixel among-species variation in bleaching severity using data from count) and lowest sensitivity (ISO) settings were used. Post- the Geosymbio database (Franklin et al., 2012). Finally, we processing was conducted using Adobe Photoshop Creative compiled literature data on the response of Acropora species Cloud (2015) software with images transformed into the device- ∗ ∗ ∗ during previous thermal stress events, and assessed whether independent CIEL a b color space which measures color based those species that have been consistently reported to be severely on lightness (L), along a green-red gradient (a), and along a blue- bleached in previous studies were also the most severely bleached yellow gradient (b). All images were individually white balanced during the extreme thermal anomaly which occurred on the by identifying true black, true white, and 50% gray thresholds in Great Barrier Reef during the austral summer of 2016. each photograph. Subsequently, four regions of the colony were selected haphazardly from across the surface area of each coral colony, using the color sample tool. Each sampled region was a MATERIALS AND METHODS constant distance from the branch tip (1–2 cm), and avoided the Field Data Collection outer margins of the colonies where branches are often oriented Surveys of coral bleaching were conducted at predominantly in slightly different directions, and can be shaded by upper shallow, lagoonal sites, and at one additional mid-shelf location, branches. The color sample tool in the software was set to capture within and around the Lizard Island group (northern Great an 11 × 11 pixel sample for each region of the coral surface, and ◦ ◦ Barrier Reef, 14 40.140S, 145 27.649E) during early March 2016 calculated the average color across each 121 pixels region. The ∗ ∗ ∗ ∼2 weeks after bleaching was first reported at the location. four L a b color samples were averaged for each colony, in order Thermal stress at this location reached ∼10 DHW during this to gain a single numerical measurement of color, the divergence ∗ ∗ ∗ bleaching event (Hughes et al., 2017) and in situ temperature of each L a b average value from black was calculated as 1E Frontiers in Marine Science | www.frontiersin.org 3 November 2017 | Volume 4 | Article 376 Hoogenboom et al. Determinants of Coral Bleaching Severity (after Riggs, 1997). This method generated a value for each colony Spatial Data within a range of 0–100, with increasing values representing For each colony, depth data measured in the field were converted increasingly bleached (nearest to white) colonies. To determine to depth below lowest astronomical tide based on the known a reference point for the color of healthy (unbleached) corals, tidal height at the time of sampling. The spatial position data the same technique was used to calculate “whiteness” values for for each colony was used to calculate the position of each colony Acropora colonies (n = 12) that showed normal colouration, relative to the open ocean. To do this, the position of the reef and that were surveyed and photographed during March 2016 at edge was defined from reef polygons extracted from Google Earth sites around Orpheus Island. These additional colonies included images (Lizard Island, −14.666777S 145.462971E, image date the same species and colony morphologies as observed at Lizard 10/10/2011 accessed 06/02/2017 with eye altitude of 6.9 km; No Island. Name Reef, −14.641968S 145.653061E, image date 15/09/2016 accessed 07/02/2017 with eye altitude of 4.36 km), and were Drivers of Bleaching Severity (Explanatory imported into ArcGIS (ESRI, version 10.2). The spatial position Variables) of each coral colony and the reef polygons were transformed to Image Analysis GDA 1994 MGA Zone 55 projection to enable measurement of Images of each coral colony (N = 596) were analyzed to distances in meters with conversion from decimal degrees. The determine coral colony morphology after Wallace (1999) as “near” function was used in ArcGIS to calculate the distance (m) either digitate, corymbose, arborescent, tabular, arborescent of each point (i.e., each coral colony) from the nearest reef edge. table, or hispidose/caespitose. Each coral colony was identified to species level based on Wallace et al. (2012) and Wallace (1999) Coral-Symbiodinium Associations except for 7 colonies for which species identification could not Given the influence of different Symbiodinium on the thermal be reliably determined from the photographs (referred to in tolerance of Acropora corals (e.g., Howells et al., 2013), we our dataset as Acropora spp.). We note that many coral species determined the total number of Symbiodinium clades reported display morphological plasticity and certain pairs of species have in the GeoSymbio database for the surveyed Acropora species overlapping variation in morphology which poses a challenge (Franklin et al., 2012). Only records that identified Symbiodinium using denaturing gradient gel electrophoresis profiles of the for species identification. In our study, some colonies within the following species pairs were difficult to distinguish from each internal transcribed spacer 2 region of rDNA were included to avoid confounding effects due to the use of different methods of other from photos alone and, therefore, species-level differences between these pairs should be interpreted with caution: A. loripes identifying Symbiodinium. Furthermore, only Acropora species for which there were more than three records in the database and A. longicyathus, A. nasuta and A. valida, A. humilis and A. gemmifera. were included in this analysis. Colony planar surface area was measured for each colony Reported Bleaching Severity of Acropora during using image analysis in Image J (version 1.51 h, US National Institute for Health). For each colony we measured the longest Previous Bleaching Events diameter and the diameter perpendicular to that and calculated To compare the results from our in-water surveys with planar area based on the geometric formula for the area of an observations of Acropora bleaching in previous events, we ellipse. The microhabitat of each colony was also assessed from conducted a comprehensive literature search using Web of images of the localized reef topography, and was categorized as; Science to conduct cited reference searches for Marshall and “elevated” (where the topography of the reef meant the coral Baird (2000) and Loya et al. (2001), and an additional keywords was >∼40 cm above the surrounding corals) “open” (where the search for “Acropora” and “bleaching.” To capture the gray colony was on flat reef substratum without any obvious shading literature we also scanned all papers listed in the online bleaching by competitors), “crevice” (where the colony grew within a crack database ReefBase (1631 records, as of March 2016, ReefBase, in the reef matrix), “overhang” (where the colony was shaded by 2017) and extracted data from publications that were publically the reef matrix or other colonies), or “sand” (where the colony available. Among this set of publications, data were only used if grew above a sand patch). Competition intensity was measured the study reported field observations during a thermal bleaching by dividing each coral into 8 equal segments centered over the event (not laboratory experiments), if corals were identified to mid-point of the colony, and counting the number of these species level, and if bleaching was quantified in a way that “octants” in which a benthic competitor was within ∼5 cm of captured gradation in bleaching severity. We excluded papers the focal colony, after Hoogenboom et al. (2011). These data where bleaching effects were measured as a change in coral were subsequently categorized as either: “no competitors,” “low” cover between different observation periods due to difficultly (competitors present in 1–2 of octants), “medium” (competitors ascribing changes in abundances solely to bleaching. In total, present in 3–4 octants), and “high” (competitors present in >4 57 publications matched our criteria, yielding 527 records of octants). In addition, we noted whether competitors included bleaching for 86 Acropora species. We retained species names soft corals (categorical variable with soft corals present or as reported in the original publications despite some subsequent absent) and macroalgae (categorical variable with macroalgae synonymization of names (e.g., A. wallaceae was synonymized present or absent). Only 8 of 596 colonies were in competition with A. samoensis by Wallace, 1999), and we recorded colony with macroalgae so this variable was excluded from subsequent morphologies of species based on Wallace (1999) and Veron analysis. (2000). Frontiers in Marine Science | www.frontiersin.org 4 November 2017 | Volume 4 | Article 376 Hoogenboom et al. Determinants of Coral Bleaching Severity To standardize bleaching metrics between studies, data and “species within site.” All statistical analyses were performed extracted from each publication were re-categorized as follows: using the R statistical software (R Development Core Team, “none” means no bleaching of that species was reported in that 2017). study; “low” means that the study recorded the species to be Our assessment of the Acropora community naturally present partially bleached or with <25% of colonies affected; “moderate” at each site meant that we were likely to have different numbers means that 26–50% of colonies were bleached or there was of observations of bleaching severity for different species, partial bleaching with low levels of recorded mortality; “high” and a different composition of species at different sites. To means 50–80% of colonies were bleached and/or mortality was determine whether differences in species composition between observed; “severe” means that more than 80% of colonies of sites contributed to among-site variation in bleaching severity we that species were bleached and/or high levels of bleaching-related categorized sites as either “exposed” (<420 m from reef edge, 4 mortality were recorded. Data are presented as the percentages of sites) or “lagoon” (>510 m from reef edge, 6 sites), and calculated records for each species that fell within each of these categories. community similarity between pairs of sites using the Bray– In both the data from Lizard Island, and the literature data, Curtis index of dissimilarity. The categorization of “exposed” the measurement of bleaching severity reflects the short- and vs. “lagoon” was based on a natural distance division in our long-term thermal history of each colony because measurements data which yielded approximately equal numbers of sites in each were made under natural field conditions. The database we have category. This community similarity approach was chosen in compiled is accessible in the Supplementary Material. place of a multivariate species-by-site ordination because the latter technique is not recommended when there are many more Data Analysis variables (species) than samples (sites). A similar approach was To identify the strongest predictors of bleaching severity during used to assess whether the relative frequency of microhabitats the extreme thermal anomaly, we used a linear mixed-effects differed between exposed and lagoon sites using a χ goodness model that included all main effects (day of observation, of fit test. colony morphology, depth, microhabitat, competition intensity, Data describing Symbiodinium association of Acropora were presence of soft corals, colony size, and distance to open only available for a subset of the species we observed. These ocean, where the latter captures variation in environmental sparse data did not permit quantitative analysis and, therefore, conditions between reef-edge and lagoon habitats), and a set we used graphical analysis to assess whether the capacity to host of specific interaction terms that were established a-priori different symbiont types was related to bleaching severity. Finally, based on evidence in the literature. Water flow potentially hierarchical cluster analysis was used to group coral species based on their bleaching severity during previous bleaching events as modulates bleaching severity through effects on gas exchange which are, in turn, affected by both colony morphology and reported in the literature. Subsequently, we applied the same colony size (Hoogenboom and Connolly, 2009). Consequently, species groupings to the species observed at Lizard Island, and we included interaction terms between distance from ocean (a assessed whether mean bleaching severity observed at our study proxy for wave exposure and general reef habitat) and colony site differed systematically among these predetermined species morphology, and between distance from ocean and colony size. groups. Colony morphology determines how much light impinges on the coral tissue surface, and light intensity also changes with RESULTS depth (Hoogenboom et al., 2008). Therefore, we considered that different morphologies might bleach differently at different Bleaching severity values measured using our new method depths and included a depth by morphology interaction. ranged from 42 (least “white”) to 99 (very close to pure white) Different coral morphologies use different competition strategies across the 10 Lizard Island study sites. In contrast, “whiteness” and the outcome of competition can depend on colony size values for unbleached corals at Orpheus Island (photographed at (Jackson, 1979). Therefore, we included competition by colony the same time of year, and including the same coral species and size and competition by morphology interaction terms. Finally, morphologies as at Lizard Island) averaged 43 (±s.e. 3.2, range we considered that different coral morphologies might bleach 21–61). Overall, 97% of coral colonies observed at Lizard Island at different rates and included the interaction between day (N = 596) showed whiteness values outside of the range observed of observation and morphology. We had no a priori reason for unbleached corals at Orpheus Island, and 71% of colonies had to expect that effects on bleaching severity from the day of whiteness values >80 (Figure 1). observation (duration of exposure to thermal stress), or that Among the set of hypothesized correlates of bleaching effects of the presence of soft corals, should depend on any other severity, only day of observation, microhabitat, distance of environmental factor and therefore omitted those interactions. colonies from the open ocean, and colony morphology explained The dataset includes two random effects; “site” (because corals a significant amount of the variation in bleaching severity. We were observed at a random selection of sites at the location) observed a clear signal of increased bleaching severity over and “species” (because we observed a random subset of the time, despite the relatively short observation period (8 days, pool of species based on which species were present at each site Table 1). This temporal variation was equivalent in magnitude rather than observing species selected a priori). We used model to the variation in bleaching severity among microhabitats selection based on a likelihood ratio test to assess whether the (average bleaching values were ∼79 on day 1 and ∼88 on mixed-effects model should include random effects for both “site” day 8, Figures 2A,C). In addition, hispidose, digitate, and Frontiers in Marine Science | www.frontiersin.org 5 November 2017 | Volume 4 | Article 376 Hoogenboom et al. Determinants of Coral Bleaching Severity FIGURE 1 | Frequency distribution of bleaching severity measurements for Acropora corals (N = 596) at Lizard Island in March 2016, as measured from white-balanced images of corals in situ. Photos show representatives of coral colonies with different bleaching severity, and numbers in the upper right hand corner of each image show the bleaching severity for each coral. TABLE 1 | Results of general linear mixed effects model of bleaching severity, with microhabitats at reef edge sites compared with a higher frequency site and species included as random effects in the model. of elevated and crevice microhabitats at lagoonal sites (Goodness of fit test, χ = 19.3, df = 4, p < 0.001). Despite these Factor Df F p differences in microhabitat availability, Bray–Curtis similarity of species composition between pairs of sites was approximately Day of observation 1, 8 13.3 <0.01 equal when reef edge sites were compared with each other (mean Colony morphology 5, 381 3.5 <0.01 dissimilarity 0.54 between 6 pairs of sites), to when lagoonal sites Microhabitat 4, 381 20.6 <0.001 were compared with each other (mean dissimilarity 0.53 between Distance from open ocean 1, 381 5.5 <0.02 15 pairs of sites), and to when lagoonal sites were compared with All other main effects and interaction terms were not significant (p > 0.08) and were reef edge sites (mean dissimilarity 0.51 between 24 pairs of sites). excluded from the final model based on a backwards-deletion approach. Corymbose coral species, including A. secale, A. selago, and A. nasuta were among the least severely bleached whereas arborescent morphologies were the most severely bleached, arborescent species, including A. listeri, A. grandis and A. whereas tabular morphologies were the least severely bleached aspera, were among the most severely bleached (Figures 2B, (Table 1, Figure 2B). Finally, bleaching severity decreased with 4A). Species’ mean bleaching severity values ranged from 74 (for distance away from the open ocean, with corals at sites in the A. aculeus) to 95 (for A. carduus) and we observed relatively small lagoon generally showing lower bleaching severity than those at within-species variation in bleaching severity with the coefficient sites close to the reef edge (Table 1, Figure 2D). of variation of bleaching severity for each species ranging from 1 Corals growing in crevice and overhang environments showed to 21% (average 10%). However, clear interpretation of among- significantly less severe bleaching than corals in open, elevated, species variation is hindered by differences in sample sizes; our assessment of the in situ Acropora community meant that we and sand microhabitats (Figure 2, Table 1), supporting the general consensus that bleaching is more severe under conditions observed only single colonies of some species but >40 colonies of other species (Figure 4A). In addition, formal model selection of high irradiance. In contrast, depth (range −0.5 to 5 m below LAT) was not significantly associated with bleaching [GLMM, did not support the inclusion of “species within site” as a random “depth” effect, F = 0.08, p = 0.78]. The relative frequency effect in the GLME (likelihood ratio test, model with “species (1, 570) of different microhabitats occupied by the coral colonies we within site” was not superior to a model with only “site” as observed differed between sites that were close to the reef edge a random effect, likelihood ratio 0.49, p = 0.48). This result and sites that were close to the center of the lagoon (Figure 3). indicates that differences in bleaching intensity among species Overall, Acropora colonies were more frequently found in open were generally consistent among sites. Finally, although data Frontiers in Marine Science | www.frontiersin.org 6 November 2017 | Volume 4 | Article 376 Hoogenboom et al. Determinants of Coral Bleaching Severity FIGURE 2 | Environmental and morphological correlates of bleaching severity for corals at sites around Lizard Island in March 2016. Data show effects of (A) microhabitat, (B) colony morphology, (C) day of observation and (D) distance to open ocean from linear mixed effects model with N = 596 coral colonies, site included as a random effect, and main effects of the minimal model obtained from backwards deletion of non-significant terms. documenting symbiont clade diversity for the coral species we colony size [GLME, “colony area by distance,” F = 1.9, (1, 535) observed were too sparse to permit formal analysis, we found no p = 0.16]. Finally, our analysis did not support the hypothesis clear indication that species which associated with more than one that different morphologies bleached at different rates [GLME, symbiont clade bleached less severely (Figure 4B). “day by morphology,” F = 0.63, p = 0.68]. (5, 535) Competition intensity had no effect on bleaching severity Published records of bleaching severity of Acropora species [GLME, “competition” effect, F = 2.2, p = 0.09], nor from previous bleaching events indicate high variability between (3, 570) did the presence of soft corals [GLME, “soft corals” effect, morphologies (Figure 5), as well as high variability within and F = 0.31, p = 0.58], or the size of the coral colony among species (Figure 6). Consistent with our observations (1, 570) [GLME, “colony area” effect, F = 0.02, p = 0.90]. We of Acropora at Lizard Island, the literature demonstrates (1, 570) found no evidence that distance from the open ocean, depth, that arborescent and hispidose Acropora are more frequently or competition intensity affected bleaching severity differently observed to be severely bleached, while arborescent tables for different colony morphologies [GLME, “morphology by are among the least severely bleached in both datasets distance,” F = 1.8, p = 0.12; “morphology by depth,” (Figures 2B, 5). However, digitate and tabular morphologies (5, 535) F = 1.0, p = 0.39; “morphology by competition,” F showed contrasting bleaching severity at Lizard Island compared (5, 535) (15, 535) = 0.9, p = 0.57]. Similarly, the effect of competition intensity with the literature. When the responses of different coral species on bleaching severity did not depend on colony size [GLME, are considered, the literature indicates a greater degree of within- “competition by colony area,” F = 0.57, p = 0.63], nor and among-species variability in bleaching severity than we (3, 535) did the effect of distance from the open ocean depend on observed at Lizard Island, despite having similar number of Frontiers in Marine Science | www.frontiersin.org 7 November 2017 | Volume 4 | Article 376 Hoogenboom et al. Determinants of Coral Bleaching Severity surrounding entire colony circumference), or colony size (range 5–90 cm diameter) systematically influenced bleaching severity. At our study location, different colony morphologies differed in their bleaching severity under temperature stress, but within- and among-species variation in bleaching severity was low compared with the variation reported in the literature. Environmental Drivers of Bleaching Severity Our results generally support the hypothesis that coral bleaching is caused by a combination of high water temperature and high solar radiation (Jokiel and Coles, 1990; Lesser et al., 1990; Brown et al., 1994). Colonies in shaded microhabitats (crevices and overhangs) were less severely bleached than those in microhabitats with higher light exposure (open, elevated, and sand). The structural complexity of reefs causes high variation in irradiance among microhabitats (Brakel, 1979), whereby overhangs and crevices receive ≤40% of the irradiance that reaches open habitats at a similar depth (3–5 m, Anthony and Hoegh-Guldberg, 2003). Consistent with previous studies (e.g., Williams et al., 2010), colonies in sandy patches were FIGURE 3 | Relative frequency of different microhabitats for Acropora colonies the most severely bleached, likely because carbonate sand is (N = 596) observed at lagoonal sites (>510 m from reef edge, 6 sites) and reef highly reflective and amplifies light intensity (Ortiz et al., 2009). edge sites (<410 m from reef crest, 4 sites). While colonies in microhabitats with low irradiance can have low survival (Baird and Hughes, 2000) and growth (Anthony and Hoegh-Guldberg, 2003) under normal conditions, our observations in both cases (N = 596 colonies measured at Lizard results support that crevice and overhang habitats may serve Island, N = 532 literature records), and data for a large number as refuges from thermal stress (see also West and Salm, 2003). of species in both cases (40 species at Lizard Island, 87 species Consequently, reefs’ structural complexity supports ecosystem in the literature). In the literature, for the 48 species with at functioning and biodiversity not only by providing habitat least 5 records of bleaching severity, 27% (13 species) showed and shelter for mobile reef organisms (Syms and Jones, 2000; high fidelity to a single bleaching category despite inevitable Pratchett et al., 2008), but also by providing microhabitats that variation in the intensity of thermal stress among locations can increase coral survival during periods of thermal stress. and bleaching events. In addition, 63% of species had records In contrast to the strong effect of microhabitat, competition of bleaching within at least 3 categories, and 23% of species intensity had no effect on bleaching severity. One explanation showed the full range of bleaching severity scores (from none for this is that some corals retract their polyps when exposed to to severe, Figure 6). Only one species (A. desalwii) was never high water temperatures (Jones et al., 2000) which might lower recorded to show above “moderate” bleaching, likely due to its the incidence of contact between competitors and/or prevent the restricted geographic distribution and occurrence below 15 m release of secondary metabolites. However, other species increase depth (Wallace, 1999). Cluster analysis of the literature data their feeding rates in response to bleaching (Grottoli et al., 2006), for the subset of Acropora species we observed at Lizard Island which is likely to increase the incidence of tissue contact between revealed 7 clusters based on the bleaching severity categories adjacent colonies. Further research into species-specific tissue most often recorded for those species during previous bleaching retraction behaviors during thermal stress is required to explain events (Figure 7). However, we found no evidence of systematic this result. variation in average bleaching scores measured at Lizard Island In our study, water depth did not influence bleaching severity for these clusters of species (Figure 8). for corals that occur within the upper ∼6 m depths of the reef. A likely explanation for this finding is that water temperatures are often similar across this depth range, as the thermocline occurs DISCUSSION at depths that are usually well below 20 m on coral reefs (e.g., The results of this study show that during severe thermal stress, Grigg, 2006). Moreover, the generally high water clarity at the small-scale spatial variation in the bleaching susceptibility of study sites means there would have been limited attenuation branching corals is linked to microhabitat availability, and the of light over this depth range. Both still water conditions and proximity of sites to the open ocean, and that bleaching severity water clarity increase the penetration depth of solar radiation into worsens over a very short time-frame (∼1 week). We found seawater, consequently increasing radiant heating throughout the no evidence that water depth (range −0.5 to 5 m below LAT), water column and reducing variability in temperature with depth competition intensity (range no competition to competitors (Glynn, 1993; Brown, 1997). In our dataset, 90% of the surveyed Frontiers in Marine Science | www.frontiersin.org 8 November 2017 | Volume 4 | Article 376 Hoogenboom et al. Determinants of Coral Bleaching Severity FIGURE 4 | Variation in bleaching severity within- and between-species in the genus Acropora observed at sites around Lizard Island in March 2016. Bars show the mean bleaching severity (colony “whiteness”) measured from white-balanced images of colonies of each species. Error bars show standard error and numbers adjacent to error bars indicate sample sizes. In (A) bars are colored by colony morphology as: black (corymbose), gray (arborescent table), white (arborescent), yellow (table), blue (hispidose), and green (digitate) and numbers indicate colonies observed in the field. In (B) bars are colored by symbiont association as: black (species has been recorded to associate with multiple symbiont types) and white (species has been recorded to only associate with a single symbiont type) and numbers indicate records of Symbiodinium type in the Geosymbio database. colonies were located at a depth of <2.5 m below LAT (∼3–4 m associated with a local coral mortality event in Indonesia (Ampou water depth given the tidal range at the location). Based on et al., 2017), a strong depth-dependent pattern of bleaching estimates of light attenuation from other offshore reefs with high severity, with higher severity in the shallowest depths (i.e., <1 m water clarity (Cooper et al., 2007), light intensity at this depth depth), would be expected in areas where coral bleaching was would be ∼70% of subsurface light intensity. Collectively these caused by tidal emersion. results indicate that crevice and overhang microhabitats provide We used distance from the open ocean as a metric to a greater shading effect than light attenuation with depth in clear capture potential spatial variation in wave energy and other waters across the surveyed depth range. The absence of a depth environmental conditions between reef-edge and lagoonal effect also demonstrates that abnormally low sea levels were not sites. Previous studies reveal contrasting effects of water the cause of coral bleaching at our study location. Although flow on bleaching severity. Thermal bleaching is linked to low sea levels due to El Niño Southern Oscillation have been photoinhibition of photosynthesis (e.g., Jones et al., 2000) and Frontiers in Marine Science | www.frontiersin.org 9 November 2017 | Volume 4 | Article 376 Hoogenboom et al. Determinants of Coral Bleaching Severity studies have reported disparate results regarding the effect of colony morphology on bleaching, including: no clear effect of morphology (Williams et al., 2010); higher bleaching susceptibility for branching and tabular corals compared with massive and encrusting colonies (Marshall and Baird, 2000; Loya et al., 2001); and higher bleaching severity of massive corals compared with branching corals (Ortiz et al., 2009). These disparate results might be partially explained by variation in growth rates, both among-species and among-locations due to changes in environmental conditions. Fast-growing branching morphologies are more susceptible to bleaching than morphologies with slower growth rates (e.g., massive corals, Hoegh-Guldberg and Salvat, 1995; Marshall and Baird, 2000; Brandt, 2009). This pattern is thought to be related to metabolic rates: fast-growing colonies have higher metabolic FIGURE 5 | Records of bleaching severity for different Acropora colony rates and, thus, accumulate more harmful oxygen free radicals morphologies compiled from the literature. Bars show the percentage of which results in oxidative stress that is linked to bleaching records in the literature for each colony morphology in each bleaching severity susceptibility (e.g., Jokiel and Coles, 1974; Hoegh-Guldberg and category (N = 429). Data for elkhorn and encrusting colony morphologies have been excluded to facilitate comparison with data from Lizard Island Salvat, 1995; Baird and Marshall, 2002). Among Acropora corals plotted in Figure 2B. Numbers of records for each morphology are 19 (Arb. specifically, a recent study by Dornelas et al. (2017) showed that Table), 70 (digitate), 95 (corymbose), 64 (table), 149 (Arborescent) and 32 digitate and corymbose growth forms have slower growth rates (hispidose/caespitose). than arborescent and tabular growth forms. These results are broadly consistent with the bleaching severity of these species reported in the literature. However, in our surveys, tabular this inhibition can be mitigated by higher water flow (Nakamura corals were the least severely bleached despite having rapid et al., 2005). However, contrary to such effects, we found lower growth rates (Dornelas et al., 2017). At present, we do not bleaching severity in lagoon sites which generally have low have a clear explanation for these contrasting results and further wave energy and low flow compared with reef edge locations studies are required to disentangle the influence of growth rate (Fulton and Bellwood, 2005). This result is consistent with a compared with other environmental variables on coral bleaching field study in the Indian Ocean which also found a positive susceptibility. correlation between bleaching intensity and water flow speed The type of Symbiodinium present within coral tissues can (McClanahan et al., 2007). Coral reef lagoons are characterized have a significant influence on the bleaching susceptibility of by shallow water with limited mixing, which facilitates heating corals (e.g., Glynn, 1993; Baker, 2003; Berkelmans and Van until surface waves force cooler waters over the reef crest Oppen, 2006; Abrego et al., 2008). In particular, some corals can (Monismith, 2007). Consequently, corals in lagoon environments increase their thermal tolerance if they can change the dominant experience greater variability in their local temperature. Heat symbiont clade in their tissues to a more thermally tolerant one stress experiments indicate that corals from habitats with high (Berkelmans and Van Oppen, 2006). This implies that corals variability in temperature have lower mortality rates than corals harboring multiple symbiont types potentially have an ecological from habitats with moderate thermal variability (Oliver and advantage if they can shuffle their symbionts to “match” Palumbi, 2011). While we do not have site-specific temperature their ambient environmental conditions. However, under times data at our survey sites, temperature loggers deployed at the of stress, this advantage can only manifest if the symbiont study location indicate that the lagoon had slightly higher and community includes symbionts that are tolerant to a given more variable temperatures than the reef edge during December stressor. Our data showed no clear relation between bleaching through to March 2016 (reef edge site: average 29.7 C range severity and the capacity of Acropora species to harbor multiple ◦ ◦ ◦ 27.9–31.7 C; lagoon site: average 30.0 C range 25.6–33.2 C). Symbiodinium types. This result suggests that it is the presence Overall, our results support the hypothesis that prior exposure to of a specific heat-tolerant symbiont, rather than the ability to variable temperature regimes can promote thermal tolerance of host multiple symbiont types, that confers thermal tolerance. We coral colonies. Nevertheless, the declining bleaching severity with note, however, that while there is an increasing research emphasis distance from the open ocean might also be related to differences on the functional differences between Symbiodinium clades (e.g., in microhabitat availability across this gradient as we observed a Suggett et al., 2015, 2017), the coral species coverage of these higher frequency of crevice microhabitats, and a lower frequency data remains relatively sparse and this constrained our analyses. of open microhabitats, at lagoonal sites. We limited our analysis to the level of Symbiodinium clades, but differences in thermal tolerance exist among Symbiodinium Among-Species Variation in Bleaching belonging to the same clade (Tchernov et al., 2004; Sampayo Severity et al., 2008; Correa and Baker, 2009; LaJeunesse et al., 2014). Bleaching severity differed among the various branching Thus, while our results suggest that Acropora species known morphologies of Acropora observed at Lizard Island. Previous to associate with one or multiple Symbiodinium clades did not Frontiers in Marine Science | www.frontiersin.org 10 November 2017 | Volume 4 | Article 376 Hoogenboom et al. Determinants of Coral Bleaching Severity FIGURE 6 | Records of bleaching severity for different Acropora species compiled from the literature. Bars show the percentage of records in the literature for each species in each bleaching severity category (N = 527) and numbers adjacent to bars indicate number of records per species. Frontiers in Marine Science | www.frontiersin.org 11 November 2017 | Volume 4 | Article 376 Hoogenboom et al. Determinants of Coral Bleaching Severity FIGURE 8 | Mean bleaching severity for different groups of Acropora species observed at Lizard Island. Groups were identified using hierarchical cluster analysis and error bars show standard error. Second, the data are continuous which allows a more precise measure of bleaching severity by avoiding the loss of information that occurs with categorical data. Third, photographs provide a permanent photographic record of the state of each individual colony which may be useful for future comparisons. Finally, this technique can be developed further, and extended to other coral groups, by quantifying the “whiteness” of healthy corals to provide a species-specific baseline for coral colony health in the absence of environmental stressors. Despite these advantages, this new technique is more time consuming than in situ observer based techniques. White-balancing and color analysis took ∼3–5 min per image, with approximately half of this time spent on white-balancing. In addition, many corals contain fluorescent proteins in their tissues which give colonies a blue or pink colouration that overlays the golden brown color of the Symbiodinium within the coral cells (e.g., Alieva et al., 2008). Our technique likely underestimates bleaching severity of heavily pigmented colonies because these host-pigments make them appear to be less white than a non-pigmented colony FIGURE 7 | Cluster analysis of Acropora species observed at Lizard Island based on records of occurrence of different bleaching severity in the literature. with the same level of bleaching (i.e., symbiont loss). However, Color bars adjacent to each cluster show the bleaching severity observed in at this issue makes our results conservative as to the differences least 20% of records for the species (dark blue, no bleaching; pale blue, low between morphologies, microhabitats and sampling days because bleaching; yellow, moderate bleaching; orange, high bleaching; red, severe it introduces additional variability in the dataset. We also note bleaching). Percentage values adjacent to color bars show percentage of records in each bleaching category and values in parentheses show number of that, when colonies are only partially bleached (e.g., where the records. upper surface of the colony is whiter than the lower surfaces, Harriott, 1985), more than four measurement points may be needed to accurately represent the color distribution of each exhibit differences in bleaching resistance, finer-scale resolution colony. of symbiont identities may have explained additional variation in bleaching intensity (Sampayo et al., 2008). CONCLUSIONS A Standardized Method for Measuring Bleaching Severity During the extreme heat stress that affected the northern GBR The image analysis technique developed here provides a sensitive in 2016, 97% of Acropora colonies observed at our study measure of bleaching severity that captures gradation within and location were pale or bleached, and ∼70% of colonies had between species, and that overcomes some of the limitations of whiteness values consistent with a categorization of “severe” survey observation methods (e.g., Siebeck et al., 2006). First, our bleaching. In contrast, in previous bleaching events nearly a technique eliminates in situ observer bias and corrects for color quarter of Acropora species were reported to show high within- variation due to differences in the in situ light environment. species variability in bleaching severity, with scores ranging from Frontiers in Marine Science | www.frontiersin.org 12 November 2017 | Volume 4 | Article 376 Hoogenboom et al. Determinants of Coral Bleaching Severity “none” to “severe.” Overall, we consistently observed severe AUTHOR CONTRIBUTIONS bleaching during the extreme thermal anomaly experienced at All authors contributed to the initial conceptualization of this our study location, in comparison to more variable bleaching project. Field data were collected by GF, TC, and SJ (at Lizard severity reported during a broad range of bleaching events Island) and by KP, BR, KB, and MH (at Orpheus Island). described in the literature. These comparisons highlight the Color analyses were conducted by GF and AP, and colony importance of measuring and reporting the magnitude of size measurements were conducted by MÁ-N and SJ. Coral thermal stress experienced at different sites during bleaching identification, microhabitat and competition data were compiled so that species- and/or location-specific temperature thresholds by MH, KN, AP, TC, and GF. Spatial analyses were conducted by for different levels of bleaching can be quantified. Our results KC. MH analyzed the data and wrote the first draft of the paper also highlight the importance of monitoring and reporting with all authors making a substantial contribution to subsequent the timing of bleaching surveys relative to the onset of drafts (particularly SJ, KP, and MÁ-N). thermal stress, as our new image analysis technique detected a 10% increase in bleaching severity over a period of 1 week. Microhabitat structure, but not competition intensity, ACKNOWLEDGMENTS water depth or colony size, also contributed to variation in We thank staff from Lizard Island Research Station for assistance bleaching severity of Acropora corals. Crevices and overhang with field operations. We also thank J Madin for temperature microhabitats, which can mitigate bleaching severity, are data. This research was funded by the Australian Research more prevalent in structurally complex reefs. Such complexity Council to the ARCCOE for Coral Reef Studies CE140100020, is a product of the successful recruitment and growth of and James Cook University. morphologically complex species, such as Acropora species that are important contributors to spatial complexity in Indo- Pacific reefs (Pratchett et al., 2008). Collectively, these results SUPPLEMENTARY MATERIAL suggest a negative feedback loop whereby bleaching reduces the The Supplementary Material for this article can be found abundance of branching species, which lowers the occurrence online at: https://www.frontiersin.org/articles/10.3389/fmars. of shaded microhabitats, which then leads to more severe 2017.00376/full#supplementary-material bleaching. REFERENCES Baker, A. C. (2003). Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu. Rev. Ecol. Evol. Syst. 34, Abrego, D., Ulstrup, K. E., Willis, B. L., and van Oppen, M. J. (2008). 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Environmental Drivers of Variation in Bleaching Severity of Acropora Species during an Extreme Thermal Anomaly

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ORIGINAL RESEARCH published: 27 November 2017 doi: 10.3389/fmars.2017.00376 Environmental Drivers of Variation in Bleaching Severity of Acropora Species during an Extreme Thermal Anomaly 1, 2 1, 2 1, 2 1, 2 Mia O. Hoogenboom *, Grace E. Frank , Tory J. Chase , Saskia Jurriaans , 1, 2 2 1 1, 2, 3 Mariana Álvarez-Noriega , Katie Peterson , Kay Critchell , Kathryn L. E. Berry , 1, 2 1, 3 1, 2 Katia J. Nicolet , Blake Ramsby and Allison S. Paley Marine Biology and Aquaculture, College of Science and Engineering, James Cook University, Townsville, QLD, Australia, 2 3 ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, QLD, Australia, AIMS@JCU, Australian Institute of Marine Science, Townsville, QLD, Australia Edited by: David Suggett, High sea surface temperatures caused global coral bleaching during 2015–2016. During University of Technology Sydney, Australia this thermal stress event, we quantified within- and among-species variability in bleaching Reviewed by: severity for critical habitat-forming Acropora corals. The objective of this study was David Obura, to understand the drivers of spatial and species-specific variation in the bleaching Coastal Oceans Research and Development in the Indian Ocean, susceptibility of these corals, and to evaluate whether bleaching susceptibility under Kenya extreme thermal stress was consistent with that observed during less severe bleaching Anthony William Larkum, events. We surveyed and mapped Acropora corals at 10 sites (N = 596) around the University of Technology Sydney, Australia Lizard Island group on the northern Great Barrier Reef. For each colony, bleaching *Correspondence: severity was quantified using a new image analysis technique, and we assessed Mia O. Hoogenboom whether small-scale environmental variables (depth, microhabitat, competition intensity) mia.hoogenboom1@jcu.edu.au and species traits (colony morphology, colony size, known symbiont clade association) Specialty section: explained variation in bleaching. Results showed that during severe thermal stress, This article was submitted to bleaching of branching corals was linked to microhabitat features, and was more severe Coral Reef Research, a section of the journal at reef edge compared with lagoonal sites. Bleaching severity worsened over a very short Frontiers in Marine Science time-frame (∼1 week), but did not differ systematically with water depth, competition Received: 27 June 2017 intensity, or colony size. At our study location, within- and among-species variation in Accepted: 09 November 2017 bleaching severity was relatively low compared to the level of variation reported in the Published: 27 November 2017 literature. More broadly, our results indicate that variability in bleaching susceptibility Citation: Hoogenboom MO, Frank GE, during extreme thermal stress is not consistent with that observed during previous Chase TJ, Jurriaans S, bleaching events that have ranged in severity among globally dispersed sites, with Álvarez-Noriega M, Peterson K, fewer species escaping bleaching during severe thermal stress. In addition, shaded Critchell K, Berry KLE, Nicolet KJ, Ramsby B and Paley AS (2017) microhabitats can provide a refuge from bleaching which provides further evidence of Environmental Drivers of Variation in the importance of topographic complexity for maintaining the biodiversity and ecosystem Bleaching Severity of Acropora Species during an Extreme Thermal functioning of coral reefs. Anomaly. Front. Mar. Sci. 4:376. doi: 10.3389/fmars.2017.00376 Keywords: spatial refugia, environmental gradients, Symbiodinium, niche construction, thermal performance Frontiers in Marine Science | www.frontiersin.org 1 November 2017 | Volume 4 | Article 376 Hoogenboom et al. Determinants of Coral Bleaching Severity INTRODUCTION during the 1998 bleaching event, massive Porites were more susceptible to bleaching in the Palm Islands on the central Mass coral bleaching in response to increased sea surface GBR than they were at nearby Magnetic Island (Marshall temperature is a major threat to the persistence of coral reefs. and Baird, 2000). Similarly, during a bleaching event in the Analyses of sea surface temperature data indicate that ocean central Pacific, bleaching was observed at some sites but not warming has accelerated in recent decades, and that coral others for each of several monitored species (Fagerstrom and reefs are increasingly being exposed to thermal stress (Heron Rougerie, 1994). Indeed, numerous studies report within-species et al., 2016). Since the 1980s, global mass bleaching events variation in bleaching severity across different habitats (e.g., have caused large-scale and significant coral loss. For example, Bruno et al., 2001; Aronson et al., 2002; Hardman et al., 2004). in 1998, increased seawater temperatures caused widespread There are numerous potential biotic drivers of this within-species bleaching and coral mortality in most of the world’s coral reef variability. First, different types of Symbiodium are more resistant regions, with mortality in excess of 90% on some reefs in the to increased ocean temperature than others (e.g., Thornhill et al., central and western Indian Ocean (Spalding and Brown, 2015). 2006; Jones et al., 2008; Lesser et al., 2010; Howells et al., 2013), Moreover, between June 2014 and April 2016, bleaching was and many coral species can associate with more than one type of observed throughout the global oceans during what is now Symbiodinium (Baker, 2003; Sampayo et al., 2008). Therefore, we considered to be the longest bleaching event on record (Eakin assessed whether species that have the capacity to associate with et al., 2016). In the context of bleaching, temperature stress is more than one symbiont type show lower bleaching severity, often measured in “degree heating weeks” (DHW, C-weeks), on average, than other species. Second, bleaching severity is a metric which summarizes the duration of time over which influenced by coral colony size. For example, larger colonies temperatures have been above the average temperature of the experienced more extensive bleaching than smaller colonies of warmest summer month at each location (e.g., Eakin et al., several species during a major Caribbean bleaching event in 2010). The recent thermal stress event caused severe bleaching 2005 (Brandt, 2009). However, other studies have found contrary on the northern section of the Great Barrier Reef in 2016, where results with higher bleaching for smaller colonies for some approximately one third of reefs experienced levels of heat stress species (Pratchett et al., 2013), or that colony size only influences that were up to two-fold higher than those experienced in the bleaching prevalence for certain colony morphologies in certain 1998 bleaching event in the same region (Hughes et al., 2017). locations (Wagner et al., 2010). Finally, other benthic organisms We here investigate whether species susceptibility to bleaching that compete for space with corals, such as soft corals and under extreme heat stress is consistent with species susceptibility macroalgae, contain secondary metabolites that can lead to the reported during previous bleaching events. expulsion of Symbiodinium (i.e., bleaching, Aceret et al., 1995). Different coral species respond differently to environmental Moreover, competition can influence coral fitness more generally stressors, leading to substantial among-species variability in (e.g., by growth suppression, see Horwitz et al., 2017), and such bleaching susceptibility. In general, the literature documents effects might act as an additional stressor that increases bleaching relatively high bleaching severity for branching corals from severity. To the best of our knowledge, effects of competition on the genera Stylophora, Acropora, and Pocillopora, and lower bleaching severity have not previously been investigated in situ. bleaching severity for mound-shaped Porites and Diploastrea The topographic complexity of reefs results in high variability (e.g., Marshall and Baird, 2000; Loya et al., 2001; van Woesik in environmental conditions over small spatial scales. For et al., 2011; Swain et al., 2016). However, bleaching severity instance, stable and biologically significant temperature variation is spatially patchy (e.g., Wooldridge and Done, 2004; Penin occurs at small scales (1–2 m, e.g., Gorospe and Karl, 2011), et al., 2007). For instance, bleaching severity varies between and also at larger between-habitat scales (hundreds of meters, habitats with some studies reporting bleaching to be less severe e.g., Lundgren and Hillis-Starr, 2008). Water flow also varies in shallow compared with deep lagoons (Grimsdich et al., 2010), within- and among-habitats (e.g., Fulton and Bellwood, 2005; while others report the opposite trend (Fisk and Done, 1985; Hoogenboom and Connolly, 2009). Therefore, spatial variation Muhando, 1999). Bleaching severity can also vary with depth in abiotic drivers, such as light intensity, water flow, temperature, (e.g., Penin et al., 2007), although some studies have reported no and turbidity, influences which corals bleach and where (e.g., significant variation in bleaching with depth when values were West and Salm, 2003). Previous studies report different effects pooled across genera (Bruno et al., 2001). While temperature of water flow on bleaching severity, with evidence of increased stress is recognized to be the primary driver of mass-bleaching bleaching severity at exposed sites with high wave activity (Berkelmans et al., 2004; Hughes et al., 2017), there is no strong (McClanahan et al., 2007), as well as evidence of reduced consensus about additional environmental drivers of spatial bleaching, along with higher survival of bleached corals, under variation in bleaching severity. It is likely that a combination of high water flow conditions (Nakamura and van Woesik, 2001; environmental factors (e.g., local light intensity and water flow) Nakamura and Yamasaki, 2005). Variability in bleaching among and biological factors (including species-specific responses, and different reef habitats is also associated with site-specific turbidity local abundances of susceptible vs. tolerant species) influence levels (e.g., Williams et al., 2010). However, observed responses spatial patterns of bleaching severity. range from a negative effect of turbidity whereby suspended In addition to among-species variation in bleaching particulates are thought to act as an additional stressor that susceptibility, there is often high variation in the bleaching lowers temperature tolerance (Williams et al., 2010; Hongo and responses of individuals of the same species. For instance, Yamano, 2013), to predictions that turbidity may lessen the Frontiers in Marine Science | www.frontiersin.org 2 November 2017 | Volume 4 | Article 376 Hoogenboom et al. Determinants of Coral Bleaching Severity severity of bleaching in some shallow habitats by reducing light loggers (Onset Hobo) measured an average temperature of ◦ ◦ penetration (West and Salm, 2003; Cacciapaglia and van Woesik, 30.3 C (range 27.7–33.2 C) at two reef crest sites during 2016). February and March 2016. At the time of the surveys, significant Methodological issues associated with quantifying bleaching bleaching of susceptible coral species had been observed, severity in the field might also lead to variation between studies. but mortality was still negligible (widespread bleaching-related While observer differences are unlikely to explain variation in mortality was observed on reefs in the region 1 month later, bleaching severity between habitats reported in a single study, Hoogenboom unpubl. data). Over a period of 8 days, divers observers can differ in color sensitivity or in training (e.g., Siebeck conducted in-water surveys at 10 sites where the bleaching status et al., 2006). Many observer methods measure bleaching in simple of ∼60 Acropora colonies was monitored per site. Colonies were categories (e.g., “pale,” “partially bleached,” and “bleached”), and selected haphazardly as divers swam along a depth contour from this categorization can obscure color gradation. To overcome a randomly selected starting place, making a conscious effort issues associated with categorization of bleaching, some studies to observe colonies from different reef microhabitats as far as estimate the proportion of each coral colony that is healthy practicable given the topography of each site. The spatial position vs. bleached (e.g., Obura, 2001), providing a finer resolution of of each colony was taken using a towed GPS (Garmin eTRex) bleaching severity. Despite these advances, however, a recent that was time-synchronized with a dive watch, and the depth review highlighted the relatively high measurement uncertainty of each colony was recorded using a dive computer (Suunto, for bleaching severity, and noted that standardizing measuring D4 and Zoop). Each colony was photographed from directly protocols would help to increase the precision of bleaching above (as described below), and additional photographs of colony estimates (Swain et al., 2016). To help standardize bleaching morphology, local reef topography and colony microhabitat, measurements, we developed a new quantification of bleaching neighboring competitors, and corallite shape were taken to enable severity by measuring coral “whiteness” in individually white- measurement of colony size and competition intensity, and to balanced images of healthy, pale and bleached corals. assist species-level identification. We also kept track of the time The objective of this study was to understand the drivers of and date of observations because ongoing heat stress suggested small-scale variation in the bleaching susceptibility of branching that bleaching severity would continue to increase during corals, and to evaluate whether bleaching susceptibility under and after the observation period. The full dataset, including extreme thermal stress is consistent with that observed during coral images and spatial positions, is available in Critchell and previous (less severe) bleaching events. We focused on corals Hoogenboom (2017). from the genus Acropora due to their high abundance on Indo- Pacific reefs, their importance for the structural complexity of Measurement of Bleaching Severity reefs, and their variable bleaching severity within- and among- species (e.g., Marshall and Baird, 2000; Loya et al., 2001; Swain (Response Variable) et al., 2016). Specifically, we aimed to understand whether Individual coral colonies were photographed from directly and how variation in bleaching severity was associated with overhead, without flash, and from as close as practicable, with depth, spatial location of colonies relative to the reef edge (a a Canon G16 digital camera in an underwater housing. Each measure of exposure to wave energy and general reef habitat), photograph contained a color reference chart and scale bar. microhabitat, colony size, colony morphology, and the level of As differing light conditions of each colony did not allow competition and the identity of competitors. We also evaluated for identical camera settings to be used in each photograph, whether association with multiple symbiont types could explain individual settings based on the highest image quality (pixel among-species variation in bleaching severity using data from count) and lowest sensitivity (ISO) settings were used. Post- the Geosymbio database (Franklin et al., 2012). Finally, we processing was conducted using Adobe Photoshop Creative compiled literature data on the response of Acropora species Cloud (2015) software with images transformed into the device- ∗ ∗ ∗ during previous thermal stress events, and assessed whether independent CIEL a b color space which measures color based those species that have been consistently reported to be severely on lightness (L), along a green-red gradient (a), and along a blue- bleached in previous studies were also the most severely bleached yellow gradient (b). All images were individually white balanced during the extreme thermal anomaly which occurred on the by identifying true black, true white, and 50% gray thresholds in Great Barrier Reef during the austral summer of 2016. each photograph. Subsequently, four regions of the colony were selected haphazardly from across the surface area of each coral colony, using the color sample tool. Each sampled region was a MATERIALS AND METHODS constant distance from the branch tip (1–2 cm), and avoided the Field Data Collection outer margins of the colonies where branches are often oriented Surveys of coral bleaching were conducted at predominantly in slightly different directions, and can be shaded by upper shallow, lagoonal sites, and at one additional mid-shelf location, branches. The color sample tool in the software was set to capture within and around the Lizard Island group (northern Great an 11 × 11 pixel sample for each region of the coral surface, and ◦ ◦ Barrier Reef, 14 40.140S, 145 27.649E) during early March 2016 calculated the average color across each 121 pixels region. The ∗ ∗ ∗ ∼2 weeks after bleaching was first reported at the location. four L a b color samples were averaged for each colony, in order Thermal stress at this location reached ∼10 DHW during this to gain a single numerical measurement of color, the divergence ∗ ∗ ∗ bleaching event (Hughes et al., 2017) and in situ temperature of each L a b average value from black was calculated as 1E Frontiers in Marine Science | www.frontiersin.org 3 November 2017 | Volume 4 | Article 376 Hoogenboom et al. Determinants of Coral Bleaching Severity (after Riggs, 1997). This method generated a value for each colony Spatial Data within a range of 0–100, with increasing values representing For each colony, depth data measured in the field were converted increasingly bleached (nearest to white) colonies. To determine to depth below lowest astronomical tide based on the known a reference point for the color of healthy (unbleached) corals, tidal height at the time of sampling. The spatial position data the same technique was used to calculate “whiteness” values for for each colony was used to calculate the position of each colony Acropora colonies (n = 12) that showed normal colouration, relative to the open ocean. To do this, the position of the reef and that were surveyed and photographed during March 2016 at edge was defined from reef polygons extracted from Google Earth sites around Orpheus Island. These additional colonies included images (Lizard Island, −14.666777S 145.462971E, image date the same species and colony morphologies as observed at Lizard 10/10/2011 accessed 06/02/2017 with eye altitude of 6.9 km; No Island. Name Reef, −14.641968S 145.653061E, image date 15/09/2016 accessed 07/02/2017 with eye altitude of 4.36 km), and were Drivers of Bleaching Severity (Explanatory imported into ArcGIS (ESRI, version 10.2). The spatial position Variables) of each coral colony and the reef polygons were transformed to Image Analysis GDA 1994 MGA Zone 55 projection to enable measurement of Images of each coral colony (N = 596) were analyzed to distances in meters with conversion from decimal degrees. The determine coral colony morphology after Wallace (1999) as “near” function was used in ArcGIS to calculate the distance (m) either digitate, corymbose, arborescent, tabular, arborescent of each point (i.e., each coral colony) from the nearest reef edge. table, or hispidose/caespitose. Each coral colony was identified to species level based on Wallace et al. (2012) and Wallace (1999) Coral-Symbiodinium Associations except for 7 colonies for which species identification could not Given the influence of different Symbiodinium on the thermal be reliably determined from the photographs (referred to in tolerance of Acropora corals (e.g., Howells et al., 2013), we our dataset as Acropora spp.). We note that many coral species determined the total number of Symbiodinium clades reported display morphological plasticity and certain pairs of species have in the GeoSymbio database for the surveyed Acropora species overlapping variation in morphology which poses a challenge (Franklin et al., 2012). Only records that identified Symbiodinium using denaturing gradient gel electrophoresis profiles of the for species identification. In our study, some colonies within the following species pairs were difficult to distinguish from each internal transcribed spacer 2 region of rDNA were included to avoid confounding effects due to the use of different methods of other from photos alone and, therefore, species-level differences between these pairs should be interpreted with caution: A. loripes identifying Symbiodinium. Furthermore, only Acropora species for which there were more than three records in the database and A. longicyathus, A. nasuta and A. valida, A. humilis and A. gemmifera. were included in this analysis. Colony planar surface area was measured for each colony Reported Bleaching Severity of Acropora during using image analysis in Image J (version 1.51 h, US National Institute for Health). For each colony we measured the longest Previous Bleaching Events diameter and the diameter perpendicular to that and calculated To compare the results from our in-water surveys with planar area based on the geometric formula for the area of an observations of Acropora bleaching in previous events, we ellipse. The microhabitat of each colony was also assessed from conducted a comprehensive literature search using Web of images of the localized reef topography, and was categorized as; Science to conduct cited reference searches for Marshall and “elevated” (where the topography of the reef meant the coral Baird (2000) and Loya et al. (2001), and an additional keywords was >∼40 cm above the surrounding corals) “open” (where the search for “Acropora” and “bleaching.” To capture the gray colony was on flat reef substratum without any obvious shading literature we also scanned all papers listed in the online bleaching by competitors), “crevice” (where the colony grew within a crack database ReefBase (1631 records, as of March 2016, ReefBase, in the reef matrix), “overhang” (where the colony was shaded by 2017) and extracted data from publications that were publically the reef matrix or other colonies), or “sand” (where the colony available. Among this set of publications, data were only used if grew above a sand patch). Competition intensity was measured the study reported field observations during a thermal bleaching by dividing each coral into 8 equal segments centered over the event (not laboratory experiments), if corals were identified to mid-point of the colony, and counting the number of these species level, and if bleaching was quantified in a way that “octants” in which a benthic competitor was within ∼5 cm of captured gradation in bleaching severity. We excluded papers the focal colony, after Hoogenboom et al. (2011). These data where bleaching effects were measured as a change in coral were subsequently categorized as either: “no competitors,” “low” cover between different observation periods due to difficultly (competitors present in 1–2 of octants), “medium” (competitors ascribing changes in abundances solely to bleaching. In total, present in 3–4 octants), and “high” (competitors present in >4 57 publications matched our criteria, yielding 527 records of octants). In addition, we noted whether competitors included bleaching for 86 Acropora species. We retained species names soft corals (categorical variable with soft corals present or as reported in the original publications despite some subsequent absent) and macroalgae (categorical variable with macroalgae synonymization of names (e.g., A. wallaceae was synonymized present or absent). Only 8 of 596 colonies were in competition with A. samoensis by Wallace, 1999), and we recorded colony with macroalgae so this variable was excluded from subsequent morphologies of species based on Wallace (1999) and Veron analysis. (2000). Frontiers in Marine Science | www.frontiersin.org 4 November 2017 | Volume 4 | Article 376 Hoogenboom et al. Determinants of Coral Bleaching Severity To standardize bleaching metrics between studies, data and “species within site.” All statistical analyses were performed extracted from each publication were re-categorized as follows: using the R statistical software (R Development Core Team, “none” means no bleaching of that species was reported in that 2017). study; “low” means that the study recorded the species to be Our assessment of the Acropora community naturally present partially bleached or with <25% of colonies affected; “moderate” at each site meant that we were likely to have different numbers means that 26–50% of colonies were bleached or there was of observations of bleaching severity for different species, partial bleaching with low levels of recorded mortality; “high” and a different composition of species at different sites. To means 50–80% of colonies were bleached and/or mortality was determine whether differences in species composition between observed; “severe” means that more than 80% of colonies of sites contributed to among-site variation in bleaching severity we that species were bleached and/or high levels of bleaching-related categorized sites as either “exposed” (<420 m from reef edge, 4 mortality were recorded. Data are presented as the percentages of sites) or “lagoon” (>510 m from reef edge, 6 sites), and calculated records for each species that fell within each of these categories. community similarity between pairs of sites using the Bray– In both the data from Lizard Island, and the literature data, Curtis index of dissimilarity. The categorization of “exposed” the measurement of bleaching severity reflects the short- and vs. “lagoon” was based on a natural distance division in our long-term thermal history of each colony because measurements data which yielded approximately equal numbers of sites in each were made under natural field conditions. The database we have category. This community similarity approach was chosen in compiled is accessible in the Supplementary Material. place of a multivariate species-by-site ordination because the latter technique is not recommended when there are many more Data Analysis variables (species) than samples (sites). A similar approach was To identify the strongest predictors of bleaching severity during used to assess whether the relative frequency of microhabitats the extreme thermal anomaly, we used a linear mixed-effects differed between exposed and lagoon sites using a χ goodness model that included all main effects (day of observation, of fit test. colony morphology, depth, microhabitat, competition intensity, Data describing Symbiodinium association of Acropora were presence of soft corals, colony size, and distance to open only available for a subset of the species we observed. These ocean, where the latter captures variation in environmental sparse data did not permit quantitative analysis and, therefore, conditions between reef-edge and lagoon habitats), and a set we used graphical analysis to assess whether the capacity to host of specific interaction terms that were established a-priori different symbiont types was related to bleaching severity. Finally, based on evidence in the literature. Water flow potentially hierarchical cluster analysis was used to group coral species based on their bleaching severity during previous bleaching events as modulates bleaching severity through effects on gas exchange which are, in turn, affected by both colony morphology and reported in the literature. Subsequently, we applied the same colony size (Hoogenboom and Connolly, 2009). Consequently, species groupings to the species observed at Lizard Island, and we included interaction terms between distance from ocean (a assessed whether mean bleaching severity observed at our study proxy for wave exposure and general reef habitat) and colony site differed systematically among these predetermined species morphology, and between distance from ocean and colony size. groups. Colony morphology determines how much light impinges on the coral tissue surface, and light intensity also changes with RESULTS depth (Hoogenboom et al., 2008). Therefore, we considered that different morphologies might bleach differently at different Bleaching severity values measured using our new method depths and included a depth by morphology interaction. ranged from 42 (least “white”) to 99 (very close to pure white) Different coral morphologies use different competition strategies across the 10 Lizard Island study sites. In contrast, “whiteness” and the outcome of competition can depend on colony size values for unbleached corals at Orpheus Island (photographed at (Jackson, 1979). Therefore, we included competition by colony the same time of year, and including the same coral species and size and competition by morphology interaction terms. Finally, morphologies as at Lizard Island) averaged 43 (±s.e. 3.2, range we considered that different coral morphologies might bleach 21–61). Overall, 97% of coral colonies observed at Lizard Island at different rates and included the interaction between day (N = 596) showed whiteness values outside of the range observed of observation and morphology. We had no a priori reason for unbleached corals at Orpheus Island, and 71% of colonies had to expect that effects on bleaching severity from the day of whiteness values >80 (Figure 1). observation (duration of exposure to thermal stress), or that Among the set of hypothesized correlates of bleaching effects of the presence of soft corals, should depend on any other severity, only day of observation, microhabitat, distance of environmental factor and therefore omitted those interactions. colonies from the open ocean, and colony morphology explained The dataset includes two random effects; “site” (because corals a significant amount of the variation in bleaching severity. We were observed at a random selection of sites at the location) observed a clear signal of increased bleaching severity over and “species” (because we observed a random subset of the time, despite the relatively short observation period (8 days, pool of species based on which species were present at each site Table 1). This temporal variation was equivalent in magnitude rather than observing species selected a priori). We used model to the variation in bleaching severity among microhabitats selection based on a likelihood ratio test to assess whether the (average bleaching values were ∼79 on day 1 and ∼88 on mixed-effects model should include random effects for both “site” day 8, Figures 2A,C). In addition, hispidose, digitate, and Frontiers in Marine Science | www.frontiersin.org 5 November 2017 | Volume 4 | Article 376 Hoogenboom et al. Determinants of Coral Bleaching Severity FIGURE 1 | Frequency distribution of bleaching severity measurements for Acropora corals (N = 596) at Lizard Island in March 2016, as measured from white-balanced images of corals in situ. Photos show representatives of coral colonies with different bleaching severity, and numbers in the upper right hand corner of each image show the bleaching severity for each coral. TABLE 1 | Results of general linear mixed effects model of bleaching severity, with microhabitats at reef edge sites compared with a higher frequency site and species included as random effects in the model. of elevated and crevice microhabitats at lagoonal sites (Goodness of fit test, χ = 19.3, df = 4, p < 0.001). Despite these Factor Df F p differences in microhabitat availability, Bray–Curtis similarity of species composition between pairs of sites was approximately Day of observation 1, 8 13.3 <0.01 equal when reef edge sites were compared with each other (mean Colony morphology 5, 381 3.5 <0.01 dissimilarity 0.54 between 6 pairs of sites), to when lagoonal sites Microhabitat 4, 381 20.6 <0.001 were compared with each other (mean dissimilarity 0.53 between Distance from open ocean 1, 381 5.5 <0.02 15 pairs of sites), and to when lagoonal sites were compared with All other main effects and interaction terms were not significant (p > 0.08) and were reef edge sites (mean dissimilarity 0.51 between 24 pairs of sites). excluded from the final model based on a backwards-deletion approach. Corymbose coral species, including A. secale, A. selago, and A. nasuta were among the least severely bleached whereas arborescent morphologies were the most severely bleached, arborescent species, including A. listeri, A. grandis and A. whereas tabular morphologies were the least severely bleached aspera, were among the most severely bleached (Figures 2B, (Table 1, Figure 2B). Finally, bleaching severity decreased with 4A). Species’ mean bleaching severity values ranged from 74 (for distance away from the open ocean, with corals at sites in the A. aculeus) to 95 (for A. carduus) and we observed relatively small lagoon generally showing lower bleaching severity than those at within-species variation in bleaching severity with the coefficient sites close to the reef edge (Table 1, Figure 2D). of variation of bleaching severity for each species ranging from 1 Corals growing in crevice and overhang environments showed to 21% (average 10%). However, clear interpretation of among- significantly less severe bleaching than corals in open, elevated, species variation is hindered by differences in sample sizes; our assessment of the in situ Acropora community meant that we and sand microhabitats (Figure 2, Table 1), supporting the general consensus that bleaching is more severe under conditions observed only single colonies of some species but >40 colonies of other species (Figure 4A). In addition, formal model selection of high irradiance. In contrast, depth (range −0.5 to 5 m below LAT) was not significantly associated with bleaching [GLMM, did not support the inclusion of “species within site” as a random “depth” effect, F = 0.08, p = 0.78]. The relative frequency effect in the GLME (likelihood ratio test, model with “species (1, 570) of different microhabitats occupied by the coral colonies we within site” was not superior to a model with only “site” as observed differed between sites that were close to the reef edge a random effect, likelihood ratio 0.49, p = 0.48). This result and sites that were close to the center of the lagoon (Figure 3). indicates that differences in bleaching intensity among species Overall, Acropora colonies were more frequently found in open were generally consistent among sites. Finally, although data Frontiers in Marine Science | www.frontiersin.org 6 November 2017 | Volume 4 | Article 376 Hoogenboom et al. Determinants of Coral Bleaching Severity FIGURE 2 | Environmental and morphological correlates of bleaching severity for corals at sites around Lizard Island in March 2016. Data show effects of (A) microhabitat, (B) colony morphology, (C) day of observation and (D) distance to open ocean from linear mixed effects model with N = 596 coral colonies, site included as a random effect, and main effects of the minimal model obtained from backwards deletion of non-significant terms. documenting symbiont clade diversity for the coral species we colony size [GLME, “colony area by distance,” F = 1.9, (1, 535) observed were too sparse to permit formal analysis, we found no p = 0.16]. Finally, our analysis did not support the hypothesis clear indication that species which associated with more than one that different morphologies bleached at different rates [GLME, symbiont clade bleached less severely (Figure 4B). “day by morphology,” F = 0.63, p = 0.68]. (5, 535) Competition intensity had no effect on bleaching severity Published records of bleaching severity of Acropora species [GLME, “competition” effect, F = 2.2, p = 0.09], nor from previous bleaching events indicate high variability between (3, 570) did the presence of soft corals [GLME, “soft corals” effect, morphologies (Figure 5), as well as high variability within and F = 0.31, p = 0.58], or the size of the coral colony among species (Figure 6). Consistent with our observations (1, 570) [GLME, “colony area” effect, F = 0.02, p = 0.90]. We of Acropora at Lizard Island, the literature demonstrates (1, 570) found no evidence that distance from the open ocean, depth, that arborescent and hispidose Acropora are more frequently or competition intensity affected bleaching severity differently observed to be severely bleached, while arborescent tables for different colony morphologies [GLME, “morphology by are among the least severely bleached in both datasets distance,” F = 1.8, p = 0.12; “morphology by depth,” (Figures 2B, 5). However, digitate and tabular morphologies (5, 535) F = 1.0, p = 0.39; “morphology by competition,” F showed contrasting bleaching severity at Lizard Island compared (5, 535) (15, 535) = 0.9, p = 0.57]. Similarly, the effect of competition intensity with the literature. When the responses of different coral species on bleaching severity did not depend on colony size [GLME, are considered, the literature indicates a greater degree of within- “competition by colony area,” F = 0.57, p = 0.63], nor and among-species variability in bleaching severity than we (3, 535) did the effect of distance from the open ocean depend on observed at Lizard Island, despite having similar number of Frontiers in Marine Science | www.frontiersin.org 7 November 2017 | Volume 4 | Article 376 Hoogenboom et al. Determinants of Coral Bleaching Severity surrounding entire colony circumference), or colony size (range 5–90 cm diameter) systematically influenced bleaching severity. At our study location, different colony morphologies differed in their bleaching severity under temperature stress, but within- and among-species variation in bleaching severity was low compared with the variation reported in the literature. Environmental Drivers of Bleaching Severity Our results generally support the hypothesis that coral bleaching is caused by a combination of high water temperature and high solar radiation (Jokiel and Coles, 1990; Lesser et al., 1990; Brown et al., 1994). Colonies in shaded microhabitats (crevices and overhangs) were less severely bleached than those in microhabitats with higher light exposure (open, elevated, and sand). The structural complexity of reefs causes high variation in irradiance among microhabitats (Brakel, 1979), whereby overhangs and crevices receive ≤40% of the irradiance that reaches open habitats at a similar depth (3–5 m, Anthony and Hoegh-Guldberg, 2003). Consistent with previous studies (e.g., Williams et al., 2010), colonies in sandy patches were FIGURE 3 | Relative frequency of different microhabitats for Acropora colonies the most severely bleached, likely because carbonate sand is (N = 596) observed at lagoonal sites (>510 m from reef edge, 6 sites) and reef highly reflective and amplifies light intensity (Ortiz et al., 2009). edge sites (<410 m from reef crest, 4 sites). While colonies in microhabitats with low irradiance can have low survival (Baird and Hughes, 2000) and growth (Anthony and Hoegh-Guldberg, 2003) under normal conditions, our observations in both cases (N = 596 colonies measured at Lizard results support that crevice and overhang habitats may serve Island, N = 532 literature records), and data for a large number as refuges from thermal stress (see also West and Salm, 2003). of species in both cases (40 species at Lizard Island, 87 species Consequently, reefs’ structural complexity supports ecosystem in the literature). In the literature, for the 48 species with at functioning and biodiversity not only by providing habitat least 5 records of bleaching severity, 27% (13 species) showed and shelter for mobile reef organisms (Syms and Jones, 2000; high fidelity to a single bleaching category despite inevitable Pratchett et al., 2008), but also by providing microhabitats that variation in the intensity of thermal stress among locations can increase coral survival during periods of thermal stress. and bleaching events. In addition, 63% of species had records In contrast to the strong effect of microhabitat, competition of bleaching within at least 3 categories, and 23% of species intensity had no effect on bleaching severity. One explanation showed the full range of bleaching severity scores (from none for this is that some corals retract their polyps when exposed to to severe, Figure 6). Only one species (A. desalwii) was never high water temperatures (Jones et al., 2000) which might lower recorded to show above “moderate” bleaching, likely due to its the incidence of contact between competitors and/or prevent the restricted geographic distribution and occurrence below 15 m release of secondary metabolites. However, other species increase depth (Wallace, 1999). Cluster analysis of the literature data their feeding rates in response to bleaching (Grottoli et al., 2006), for the subset of Acropora species we observed at Lizard Island which is likely to increase the incidence of tissue contact between revealed 7 clusters based on the bleaching severity categories adjacent colonies. Further research into species-specific tissue most often recorded for those species during previous bleaching retraction behaviors during thermal stress is required to explain events (Figure 7). However, we found no evidence of systematic this result. variation in average bleaching scores measured at Lizard Island In our study, water depth did not influence bleaching severity for these clusters of species (Figure 8). for corals that occur within the upper ∼6 m depths of the reef. A likely explanation for this finding is that water temperatures are often similar across this depth range, as the thermocline occurs DISCUSSION at depths that are usually well below 20 m on coral reefs (e.g., The results of this study show that during severe thermal stress, Grigg, 2006). Moreover, the generally high water clarity at the small-scale spatial variation in the bleaching susceptibility of study sites means there would have been limited attenuation branching corals is linked to microhabitat availability, and the of light over this depth range. Both still water conditions and proximity of sites to the open ocean, and that bleaching severity water clarity increase the penetration depth of solar radiation into worsens over a very short time-frame (∼1 week). We found seawater, consequently increasing radiant heating throughout the no evidence that water depth (range −0.5 to 5 m below LAT), water column and reducing variability in temperature with depth competition intensity (range no competition to competitors (Glynn, 1993; Brown, 1997). In our dataset, 90% of the surveyed Frontiers in Marine Science | www.frontiersin.org 8 November 2017 | Volume 4 | Article 376 Hoogenboom et al. Determinants of Coral Bleaching Severity FIGURE 4 | Variation in bleaching severity within- and between-species in the genus Acropora observed at sites around Lizard Island in March 2016. Bars show the mean bleaching severity (colony “whiteness”) measured from white-balanced images of colonies of each species. Error bars show standard error and numbers adjacent to error bars indicate sample sizes. In (A) bars are colored by colony morphology as: black (corymbose), gray (arborescent table), white (arborescent), yellow (table), blue (hispidose), and green (digitate) and numbers indicate colonies observed in the field. In (B) bars are colored by symbiont association as: black (species has been recorded to associate with multiple symbiont types) and white (species has been recorded to only associate with a single symbiont type) and numbers indicate records of Symbiodinium type in the Geosymbio database. colonies were located at a depth of <2.5 m below LAT (∼3–4 m associated with a local coral mortality event in Indonesia (Ampou water depth given the tidal range at the location). Based on et al., 2017), a strong depth-dependent pattern of bleaching estimates of light attenuation from other offshore reefs with high severity, with higher severity in the shallowest depths (i.e., <1 m water clarity (Cooper et al., 2007), light intensity at this depth depth), would be expected in areas where coral bleaching was would be ∼70% of subsurface light intensity. Collectively these caused by tidal emersion. results indicate that crevice and overhang microhabitats provide We used distance from the open ocean as a metric to a greater shading effect than light attenuation with depth in clear capture potential spatial variation in wave energy and other waters across the surveyed depth range. The absence of a depth environmental conditions between reef-edge and lagoonal effect also demonstrates that abnormally low sea levels were not sites. Previous studies reveal contrasting effects of water the cause of coral bleaching at our study location. Although flow on bleaching severity. Thermal bleaching is linked to low sea levels due to El Niño Southern Oscillation have been photoinhibition of photosynthesis (e.g., Jones et al., 2000) and Frontiers in Marine Science | www.frontiersin.org 9 November 2017 | Volume 4 | Article 376 Hoogenboom et al. Determinants of Coral Bleaching Severity studies have reported disparate results regarding the effect of colony morphology on bleaching, including: no clear effect of morphology (Williams et al., 2010); higher bleaching susceptibility for branching and tabular corals compared with massive and encrusting colonies (Marshall and Baird, 2000; Loya et al., 2001); and higher bleaching severity of massive corals compared with branching corals (Ortiz et al., 2009). These disparate results might be partially explained by variation in growth rates, both among-species and among-locations due to changes in environmental conditions. Fast-growing branching morphologies are more susceptible to bleaching than morphologies with slower growth rates (e.g., massive corals, Hoegh-Guldberg and Salvat, 1995; Marshall and Baird, 2000; Brandt, 2009). This pattern is thought to be related to metabolic rates: fast-growing colonies have higher metabolic FIGURE 5 | Records of bleaching severity for different Acropora colony rates and, thus, accumulate more harmful oxygen free radicals morphologies compiled from the literature. Bars show the percentage of which results in oxidative stress that is linked to bleaching records in the literature for each colony morphology in each bleaching severity susceptibility (e.g., Jokiel and Coles, 1974; Hoegh-Guldberg and category (N = 429). Data for elkhorn and encrusting colony morphologies have been excluded to facilitate comparison with data from Lizard Island Salvat, 1995; Baird and Marshall, 2002). Among Acropora corals plotted in Figure 2B. Numbers of records for each morphology are 19 (Arb. specifically, a recent study by Dornelas et al. (2017) showed that Table), 70 (digitate), 95 (corymbose), 64 (table), 149 (Arborescent) and 32 digitate and corymbose growth forms have slower growth rates (hispidose/caespitose). than arborescent and tabular growth forms. These results are broadly consistent with the bleaching severity of these species reported in the literature. However, in our surveys, tabular this inhibition can be mitigated by higher water flow (Nakamura corals were the least severely bleached despite having rapid et al., 2005). However, contrary to such effects, we found lower growth rates (Dornelas et al., 2017). At present, we do not bleaching severity in lagoon sites which generally have low have a clear explanation for these contrasting results and further wave energy and low flow compared with reef edge locations studies are required to disentangle the influence of growth rate (Fulton and Bellwood, 2005). This result is consistent with a compared with other environmental variables on coral bleaching field study in the Indian Ocean which also found a positive susceptibility. correlation between bleaching intensity and water flow speed The type of Symbiodinium present within coral tissues can (McClanahan et al., 2007). Coral reef lagoons are characterized have a significant influence on the bleaching susceptibility of by shallow water with limited mixing, which facilitates heating corals (e.g., Glynn, 1993; Baker, 2003; Berkelmans and Van until surface waves force cooler waters over the reef crest Oppen, 2006; Abrego et al., 2008). In particular, some corals can (Monismith, 2007). Consequently, corals in lagoon environments increase their thermal tolerance if they can change the dominant experience greater variability in their local temperature. Heat symbiont clade in their tissues to a more thermally tolerant one stress experiments indicate that corals from habitats with high (Berkelmans and Van Oppen, 2006). This implies that corals variability in temperature have lower mortality rates than corals harboring multiple symbiont types potentially have an ecological from habitats with moderate thermal variability (Oliver and advantage if they can shuffle their symbionts to “match” Palumbi, 2011). While we do not have site-specific temperature their ambient environmental conditions. However, under times data at our survey sites, temperature loggers deployed at the of stress, this advantage can only manifest if the symbiont study location indicate that the lagoon had slightly higher and community includes symbionts that are tolerant to a given more variable temperatures than the reef edge during December stressor. Our data showed no clear relation between bleaching through to March 2016 (reef edge site: average 29.7 C range severity and the capacity of Acropora species to harbor multiple ◦ ◦ ◦ 27.9–31.7 C; lagoon site: average 30.0 C range 25.6–33.2 C). Symbiodinium types. This result suggests that it is the presence Overall, our results support the hypothesis that prior exposure to of a specific heat-tolerant symbiont, rather than the ability to variable temperature regimes can promote thermal tolerance of host multiple symbiont types, that confers thermal tolerance. We coral colonies. Nevertheless, the declining bleaching severity with note, however, that while there is an increasing research emphasis distance from the open ocean might also be related to differences on the functional differences between Symbiodinium clades (e.g., in microhabitat availability across this gradient as we observed a Suggett et al., 2015, 2017), the coral species coverage of these higher frequency of crevice microhabitats, and a lower frequency data remains relatively sparse and this constrained our analyses. of open microhabitats, at lagoonal sites. We limited our analysis to the level of Symbiodinium clades, but differences in thermal tolerance exist among Symbiodinium Among-Species Variation in Bleaching belonging to the same clade (Tchernov et al., 2004; Sampayo Severity et al., 2008; Correa and Baker, 2009; LaJeunesse et al., 2014). Bleaching severity differed among the various branching Thus, while our results suggest that Acropora species known morphologies of Acropora observed at Lizard Island. Previous to associate with one or multiple Symbiodinium clades did not Frontiers in Marine Science | www.frontiersin.org 10 November 2017 | Volume 4 | Article 376 Hoogenboom et al. Determinants of Coral Bleaching Severity FIGURE 6 | Records of bleaching severity for different Acropora species compiled from the literature. Bars show the percentage of records in the literature for each species in each bleaching severity category (N = 527) and numbers adjacent to bars indicate number of records per species. Frontiers in Marine Science | www.frontiersin.org 11 November 2017 | Volume 4 | Article 376 Hoogenboom et al. Determinants of Coral Bleaching Severity FIGURE 8 | Mean bleaching severity for different groups of Acropora species observed at Lizard Island. Groups were identified using hierarchical cluster analysis and error bars show standard error. Second, the data are continuous which allows a more precise measure of bleaching severity by avoiding the loss of information that occurs with categorical data. Third, photographs provide a permanent photographic record of the state of each individual colony which may be useful for future comparisons. Finally, this technique can be developed further, and extended to other coral groups, by quantifying the “whiteness” of healthy corals to provide a species-specific baseline for coral colony health in the absence of environmental stressors. Despite these advantages, this new technique is more time consuming than in situ observer based techniques. White-balancing and color analysis took ∼3–5 min per image, with approximately half of this time spent on white-balancing. In addition, many corals contain fluorescent proteins in their tissues which give colonies a blue or pink colouration that overlays the golden brown color of the Symbiodinium within the coral cells (e.g., Alieva et al., 2008). Our technique likely underestimates bleaching severity of heavily pigmented colonies because these host-pigments make them appear to be less white than a non-pigmented colony FIGURE 7 | Cluster analysis of Acropora species observed at Lizard Island based on records of occurrence of different bleaching severity in the literature. with the same level of bleaching (i.e., symbiont loss). However, Color bars adjacent to each cluster show the bleaching severity observed in at this issue makes our results conservative as to the differences least 20% of records for the species (dark blue, no bleaching; pale blue, low between morphologies, microhabitats and sampling days because bleaching; yellow, moderate bleaching; orange, high bleaching; red, severe it introduces additional variability in the dataset. We also note bleaching). Percentage values adjacent to color bars show percentage of records in each bleaching category and values in parentheses show number of that, when colonies are only partially bleached (e.g., where the records. upper surface of the colony is whiter than the lower surfaces, Harriott, 1985), more than four measurement points may be needed to accurately represent the color distribution of each exhibit differences in bleaching resistance, finer-scale resolution colony. of symbiont identities may have explained additional variation in bleaching intensity (Sampayo et al., 2008). CONCLUSIONS A Standardized Method for Measuring Bleaching Severity During the extreme heat stress that affected the northern GBR The image analysis technique developed here provides a sensitive in 2016, 97% of Acropora colonies observed at our study measure of bleaching severity that captures gradation within and location were pale or bleached, and ∼70% of colonies had between species, and that overcomes some of the limitations of whiteness values consistent with a categorization of “severe” survey observation methods (e.g., Siebeck et al., 2006). First, our bleaching. In contrast, in previous bleaching events nearly a technique eliminates in situ observer bias and corrects for color quarter of Acropora species were reported to show high within- variation due to differences in the in situ light environment. species variability in bleaching severity, with scores ranging from Frontiers in Marine Science | www.frontiersin.org 12 November 2017 | Volume 4 | Article 376 Hoogenboom et al. Determinants of Coral Bleaching Severity “none” to “severe.” Overall, we consistently observed severe AUTHOR CONTRIBUTIONS bleaching during the extreme thermal anomaly experienced at All authors contributed to the initial conceptualization of this our study location, in comparison to more variable bleaching project. Field data were collected by GF, TC, and SJ (at Lizard severity reported during a broad range of bleaching events Island) and by KP, BR, KB, and MH (at Orpheus Island). described in the literature. These comparisons highlight the Color analyses were conducted by GF and AP, and colony importance of measuring and reporting the magnitude of size measurements were conducted by MÁ-N and SJ. Coral thermal stress experienced at different sites during bleaching identification, microhabitat and competition data were compiled so that species- and/or location-specific temperature thresholds by MH, KN, AP, TC, and GF. Spatial analyses were conducted by for different levels of bleaching can be quantified. Our results KC. MH analyzed the data and wrote the first draft of the paper also highlight the importance of monitoring and reporting with all authors making a substantial contribution to subsequent the timing of bleaching surveys relative to the onset of drafts (particularly SJ, KP, and MÁ-N). thermal stress, as our new image analysis technique detected a 10% increase in bleaching severity over a period of 1 week. Microhabitat structure, but not competition intensity, ACKNOWLEDGMENTS water depth or colony size, also contributed to variation in We thank staff from Lizard Island Research Station for assistance bleaching severity of Acropora corals. Crevices and overhang with field operations. We also thank J Madin for temperature microhabitats, which can mitigate bleaching severity, are data. This research was funded by the Australian Research more prevalent in structurally complex reefs. Such complexity Council to the ARCCOE for Coral Reef Studies CE140100020, is a product of the successful recruitment and growth of and James Cook University. morphologically complex species, such as Acropora species that are important contributors to spatial complexity in Indo- Pacific reefs (Pratchett et al., 2008). Collectively, these results SUPPLEMENTARY MATERIAL suggest a negative feedback loop whereby bleaching reduces the The Supplementary Material for this article can be found abundance of branching species, which lowers the occurrence online at: https://www.frontiersin.org/articles/10.3389/fmars. of shaded microhabitats, which then leads to more severe 2017.00376/full#supplementary-material bleaching. REFERENCES Baker, A. C. (2003). Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu. Rev. Ecol. Evol. Syst. 34, Abrego, D., Ulstrup, K. E., Willis, B. L., and van Oppen, M. J. (2008). 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