Temperature Regimes Impact Coral Assemblages along Environmental Gradients on Lagoonal Reefs in Belize

Coral reefs are increasingly threatened by global and local anthropogenic stressors such as rising seawater temperature, nutrient enrichment, sedimentation, and overfishing. Although many studies have investigated the impacts of local and global stressors on coral reefs, we still do not fully understand how these stressors influence coral community structure, particularly across environmental gradients on a reef system. Here, we investigate coral community composition across three different temperature and productivity regimes along a nearshore-offshore gradient on lagoonal reefs of the Belize Mesoamerican Barrier Reef System (MBRS). A novel metric was developed using ultra-high-resolution satellite-derived estimates of sea surface temperatures (SST) to classify reefs as exposed to low (lowTP), moderate (modTP), or high (highTP) temperature parameters over 10 years (2003 to 2012). Coral species richness, abundance, diversity, density, and percent cover were lower at highTP sites relative to lowTP and modTP sites, but these coral community traits did not differ significantly between lowTP and modTP sites. Analysis of coral life history strategies revealed that highTP sites were dominated by hardy stress-tolerant and fast-growing weedy coral species, while lowTP and modTP sites consisted of competitive, generalist, weedy, and stress-tolerant coral species. Satellite-derived estimates of Chlorophyll-a (chl-a) were obtained for 13-years (2003–2015) as a proxy for primary production. Chl-a concentrations were highest at highTP sites, medial at modTP sites, and lowest at lowTP sites. Notably, thermal parameters correlated better with coral community traits between site types than productivity, suggesting that temperature (specifically number of days above the thermal bleaching threshold) played a greater role in defining coral community structure than productivity on the MBRS. Dominance of weedy and stress-tolerant genera at highTP sites suggests that corals utilizing these two life history strategies may be better suited to cope with warmer oceans and thus may warrant protective status under climate change.


Introduction
Florida Keys, coral growth rates and coral cover were higher in nearshore environments exposed 85 to more variable seawater temperatures than on deeper reefs experiencing more stable 86 temperatures [21]. In contrast, while many studies suggest that high temperature variability leads 87 to higher coral resilience [14,15,16], there is also evidence that corals experiencing moderate long 88 term temperature variability (either annual or daily variation) are better able to cope with stress 89 [13]. Collectively, these studies emphasize the importance of thermal variability on the response 90 of corals to environmental stress, and highlight its capacity to shape coral community composition 91 across a reef system.  Competitive corals are by definition not very stress tolerant [22]. As such, region-wide 103 decline of these species would be expected as the impact of anthropogenic stressors increase 104 (including coral disease). This decline has already occurred in the Caribbean [6]. Generalist corals 105 became dominant on Caribbean reefs in the late 1970s following mass die off of competitive corals. 106 Generalists are more stress tolerant than competitive species but bleaching and other stressors have 107 led to high mortality of Orbicella spp. in the Caribbean [25] and continued decline is expected as 108 temperature stress increases [6,26,27], leading to a decline in reef complexity [28] 109 Weedy and stress tolerant corals have been shown to be more resilient than competitive 110 and generalist species [22,24], and are hypothesized to dominate warmer and more impacted reefs 111 (e.g., reefs closer to the shore). A shift from dominance of competitive and generalist species to 112 weedy and stress tolerant species occurred on Okinawan reefs following the 1998 El Niño 113 bleaching event [29,30] and an overall decline in coral cover and abundance currently occurring 114 in the Caribbean has been coupled with an increase in abundance of weedy species [27,31]. 115 Interestingly, fossil assemblages from excavated pits on reefs in Panama reveal that mortality and 116 changes in reef communities caused by anthropogenic impact (such as land clearing and 117 overfishing) predate mass bleaching events, indicating that other sub-lethal stressors can impact 118 coral community structure [32,33,34]. Collectively, evidence suggests that differential responses 119 between coral species to increasing anthropogenic stressors may lead to community scale shifts in 120 reef composition from dominance of competitive and generalist species to dominance of stress 121 tolerant and weedy species.

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The purpose of the current study was to investigate the impact of thermal regimes on 123 present day coral community composition (coral abundance, species richness, diversity, percent 124 cover, density, and life history strategies) of lagoonal reefs (i.e., region extending from the barrier 125 reef's crest to the mainland) across the Belize MBRS. A novel GIS-based metric was developed 126 to characterize lagoonal reefs across this reef system into three thermally distinct regimes. Within 127 these three regimes, thirteen reef sites were identified and benthic surveys were conducted to 128 quantify coral community composition. These thermal regimes exist along a nearshore-offshore 129 productivity gradient, which may also influence coral community structure. Quantifying coral 130 community differences among these thermally distinct reefs will help us better predict how coral 131 community structure may be impacted by climate change. Identifying which areas and species are 132 best able to cope with environmental stress (and which are least able) may allow for more targeted 133 management strategies, as it is important to protect both high-risk and low-risk reef sites to 134 improve our chances of conservation success [ Multiple thermal parameters were calculated at different temporal resolutions and examined 157 across thirteen lagoonal reef sites (S1 Table). Lagoonal reefs are located between the barrier reef's 158 crest and the mainland, and therefore do not include the seaward facing fore-reef. Instead, lagoonal . For all four parameters, areas that were classified in bins ≥1 SD above the 170 mean were designated high temperature parameter (highTP) sites (Fig 1). Moderate temperature 171 parameter (modTP) sites were classified as areas where all values were 0.5 to 1 SD above the 172 average annual temperature range and the average annual maximum temperature, and within 1 SD 173 of the average annual consecutive days and the average annual number of days above the regional 174 bleaching threshold (Fig 1). Low temperature parameter (lowTP) sites were classified as bins that 175 were 0.5 SD above the average to 2 SD below the average for annual temperature range and annual 176 maximum temperature, and below the average for consecutive and annual days above the regional 177 bleaching threshold (Fig 1). Using the metric presented in Fig 1,  were not surveyed as corals were not located within the marked geographic area) ( Table 1, Fig 1).    The four guilds are primarily separated by colony morphology, growth rate, and reproductive rate.

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The classification was based on a thorough sampling of global Scleractinian coral diversity. Each 214 coral that is included in a guild in Darling  for each parameter based on each linear model (S2 Table). For NMDS1, data were also divided by 256 site type in order to assess within site type variation (S3 Table). (p=0.005) and modTP (p=0.020) sites, but was not significantly different between lowTP and modTP 268 sites (Fig 2A). Coral cover, Shannon diversity, coral density, and species richness also followed 269 these same patterns (p≤0.020; Fig 2B- represent between site type differences (Fig 3). parameters, as well as chl-a, also had significant effects on NMDS2 variation (S2 Table; Fig 4), while modTP sites did not differ from lowTP 307 or highTP sites (Fig 4) Chlorophyll-a 315 Annual average chl-a concentrations varied over time and differed by site type (p<0.001), 316 but were consistently lowest at lowTP sites and highest at highTP sites regardless of year (Fig 5A).   Coral community composition 335 Coral species richness, abundance, diversity, density, and percent cover were all lower at 336 highTP sites compared to lowTP and modTP sites (Fig 2) (Fig 2).

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Our results also contrast those of Lirman and Fong (2007) [21], which showed that 361 nearshore reefs (equivalent to our highTP sites) exhibited higher coral cover and growth rates than stress event or are exposed to chronic stress (e.g., temperature, eutrophication) that prevents such 397 species from succeeding in these environments. It is also possible that highTP sites are more Cross-reef chl-a concentrations follow the same patterns as temperature (elevated 408 nearshore and decreasing with increasing distance from the Belize coast) (Fig 1, S2 Fig). This with proximity to shore in Belize (Fig 1) highTP sites (populations of major towns and cities in Belize can be seen in S4 Table). Analysis 484 of spatial autocorrelation revealed no significant differences between highTP sites or between 485 highTP sites and sites that were further offshore, suggesting that proximity to human population 486 centers did not have a major impact on coral community composition.

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HighTP reefs exhibit lower coral diversity, abundance, species richness, and cover than do 489 lowTP and modTP reefs in Belize. These highTP reefs are exposed to higher annual temperatures, 490 greater temperature variability, more time above the regional bleaching threshold, elevated chl-a   providing GIS expertise, and C. Berger and S. Hackerott for assistance with coding. We also 567 thank NASA JPL for access to MUR SST data used in this paper, NOAA ERDAAP for access to 568 chl-a and temperature data, Belize Fisheries Department for issuing permits that has allowed this 569 research to occur, and Garbutt's Marine for providing local expert guides and boats for field 570 research. The authors declare that no conflict of interests exists.