A study on the recovery of Tobago's coral reefs ...

MPB-07439; No of Pages 9 Marine Pollution Bulletin xxx (2016) xxx–xxx

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Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul

A study on the recovery of Tobago's coral reefs following the 2010 mass bleaching event Salome Buglass a,⁎, Simon D. Donner a, Jahson B. Alemu I b a b

Department of Geography, University of British Columbia, 1984 West Mall, Vancouver, BC, Canada Biodiversity and Ecology Research Programme, Institute of Marine Affairs, Hilltop Lane, Chaguaramas, Trinidad and Tobago

a r t i c l e

i n f o

Article history: Received 27 August 2015 Received in revised form 19 January 2016 Accepted 25 January 2016 Available online xxxx Keywords: Coral bleaching Coral size frequency analysis Coral recruitment Sediment stress Eastern Caribbean Tobago

a b s t r a c t In 2010, severe coral bleaching was observed across the southeastern Caribbean, including the island of Tobago, where coral reefs are subject to sedimentation and high nutrient levels from terrestrial runoff. Here we examine changes in corals' colony size distributions over time (2010–2013), juvenile abundances and sedimentation rates for sites across Tobago following the 2010 bleaching event. The results indicated that since pre-bleaching coral cover was already low due to local factors and past disturbance, the 2010 event affected only particular susceptible species' population size structure and increased the proportion of small sized colonies. The low density of juveniles (mean of 5.4 ± 6.3 juveniles/m−2) suggests that Tobago's reefs already experienced limited recruitment, especially of large broadcasting species. The juvenile distribution and the response of individual species to the bleaching event support the notion that Caribbean reefs are becoming dominated by weedy non-framework building taxa which are more resilient to disturbances. © 2016 Elsevier Ltd. All rights reserved.

1. Introduction Caribbean coral reefs are among the most heavily impacted marine ecosystems on the planet (Bellwood et al., 2004; Edmunds and Elahi, 2007). Since the 1970s many Caribbean reefs have experienced unprecedented levels of decline in coral cover, from about 50% to 10%, and are transitioning into algal dominated environments (Gardner et al., 2003; Roff et al., 2011; Jackson et al., 2014). This ecological change has been attributed to the reduction of herbivory, due to overfishing and the regional die-off of grazing urchins in the 1980s, increased terrestrial runoff, marine pollution and possibly related disease outbreaks (Hughes, 1994; Jackson et al., 2014). Furthermore, ocean warming has led to episodes of mass coral bleaching and related coral mortality, which have contributed to the overall decline in coral cover (Eakin et al., 2010). Considering that the frequency and intensity of thermal stress is projected to increase in the near future in the Caribbean (Donner et al., 2007), the future of Caribbean coral reefs depends in part on their resistance and resilience to bleaching. Bleaching, the paling of corals due to the loss of the symbiotic microalgae Symbiodinium, makes coral colonies vulnerable to complete or partial mortality and susceptible to infectious diseases (Ward et al., 2000). Severe mass bleaching events can often lead to a significant decline in coral cover and a change in community composition (Hoegh-Guldberg et al., 2007). Bleaching-induced mortality can alter the abundance and size of colonies within a population (McClanahan et al., 2009), which in turn may affect the reproductive ⁎ Corresponding author. E-mail address: [email protected] (S. Buglass).

output and by extension the post-beaching recovery of the reef. The recovery of a given population from bleaching depends on the diversity, abundance, size and health of surviving coral colonies, as well as their fecundity, larval settlement success, recruitment success, and the suitability of the environmental conditions (Tamelander, 2002; Baker et al., 2008; Crabbe, 2009). Other environmental disturbances such as terrestrial runoff or fishing pressure may further undermine the recovery process (Burt et al., 2008). To improve our understanding of post-bleaching recovery it is important to assess the impact of bleaching on coral assemblages and the ability of coral taxa to sexually reproduce within their given environment (Birrell et al., 2005; Smith et al., 2005; Irizarry-soto and Weil, 2009). Coral reefs in Tobago have experienced many of the same stressors as many other Caribbean coral reefs like sedimentation, nutrient runoff, and the thermal stress events of 1998, 2005 and 2010 (Eakin et al., 2010; Lapointe et al., 2010; Mallela et al., 2010). Bleaching was observed in 29–60% of colonies across Tobago in 2010 (Alemu I and Clement, 2014); only 2–8% of bleached corals suffered from mortality but the post-bleaching spread of coral disease likely led to further mortality (Alemu I, 2011). While there have been assessments of benthic cover, recruitment on artificial substrates and some growth modeling in Tobago (Mallela and Crabbe, 2009), little is known about the ability of different coral populations to recover from the bleaching events and whether it is influenced by local problems of terrestrial runoff and sedimentation (Lapointe et al., 2010; Mallela et al., 2010). In this study, we investigate the recovery of coral communities from the 2010 mass bleaching event across three distinct reef systems exposed to different levels of sedimentation. First, we evaluate the effect of the bleaching event on demographics of the dominant coral species

http://dx.doi.org/10.1016/j.marpolbul.2016.01.038 0025-326X/© 2016 Elsevier Ltd. All rights reserved.

Please cite this article as: Buglass, S., et al., A study on the recovery of Tobago's coral reefs following the 2010 mass bleaching event, Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.01.038

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S. Buglass et al. / Marine Pollution Bulletin xxx (2016) xxx–xxx

by examining the changes in the population size structure from 2010 to 2013. Second, we quantify the juvenile coral community across different reef systems, as juvenile abundance indicates the ability of coral populations to reproduce sexually and recruit (Ritson-williams et al., 2009; Arnold and Steneck, 2011). Third, we assess the rate and composition of sedimentation at each site, as high levels of sedimentation are known to affect the growth stages of coral lifecycle (Wittenberg and Hunte, 1992; Miller et al., 2000; Fabricius, 2005). While there are a few studies of changes in coral population structures following mass bleaching in the region (Manfrino et al., 2013; Crabbe, 2009), this is the first to integrate population size structure, juvenile abundance and sediment data to assess the factors that influence recovery from disturbance. The results support the growing body of research on how heat stress and disease are shaping the trajectory of Caribbean coral communities.

recreational divers, artisanal fishing and boat anchorage. Speyside, on the north-eastern side of the island, features a large network of fringing reefs along small islands and rocky outcrops. Like Culloden, Speyside's coastline remains relatively undeveloped apart from Speyside village (a fishing community) and a few medium-sized hotels. Two study sites were established at each reef system. The Buccoo sites (Western Reef and Outer Reef) represented systems exposed to land pollution from runoff and sewage. The Culloden sites (Culloden East and Culloden West) experience similar marine conditions but less land-based pollution. The Speyside sites (Black Jack Hole and Angel Reef) are more exposed to the Atlantic Ocean and less affected by mainland terrestrial runoff. All surveys were conducted between 8 and 12 m depth at all sites using SCUBA from mid-May to late June of 2013.

2.2. Coral size surveys 2. Materials and methods 2.1. Study area This study was conducted on three of Tobago's major reef systems: Buccoo Reef, Culloden Reef and Speyside (Fig. 1). Tobago is a hilly 300 km2 island of volcanic origin covered mostly by forest and shrublands, though the south-western part of the island has undergone significant urbanization and agricultural development. The island's fringing coral reefs developed under the influence of nutrient and sediment outflow from the Orinoco and Amazon Rivers of nearby South America. Consequently, Tobago's coral communities have lower species diversity than other Caribbean reefs (Laydoo, 1991). Buccoo Reef is composed of five large, sloping reef flats covering about 4 km2 and is Tobago's only official marine protected park (since 1973). In the last three decades, the adjacent land has experienced rapid urbanization; untreated sewage and uncontrolled storm waters drain into Buccoo Bay (Potts et al., 2004; Lapointe et al., 2010; Parkinson, 2010). The horseshoe shaped reef of Culloden covers ~0.05 km2 and is located in a remote bay surrounded mostly by forested hills (Laydoo, 1991). Human activities in the area are limited to occasional

At each reef site, 10 transects were conducted, and the length of all adult corals (colonies ≥ 5 cm) that lay within 50 cm on each side of a 10 m transect tape were measured following the protocol outlined by Done et al. (2010). All measured colonies were identified to the species level, except for the genus Agaricia. Only colonies with N50% of the living tissue within the belt transect area were recorded in the survey. Colonies that exhibited partial mortality or fission such that separate patches of living tissue were N3 cm apart from each other were considered independent colonies and were measured individually (Adjeroud et al., 2007; McClanahan et al., 2008; Done et al., 2010). To identify changes in the coral community and population structure over time, we used unpublished data collected in September 2010 (before bleaching induced coral mortality) and in March 2011 (after bleaching induced coral mortality) at all sites except Angel Reef by the Trinidad and Tobago Institute of Marine Affairs (IMA). As the IMA surveyed both length and width of each living colony along four 10 m × 2 m belt transects, the mean dimension was employed in this analysis. The IMA surveys covered a total of 80 m2 per reef. So that a balanced statistical comparison could be made between the IMA and 2013 assessments, eight transects were randomly subsampled from the 2013 assessment.

Fig. 1. Map of Tobago and location of study sites.

Please cite this article as: Buglass, S., et al., A study on the recovery of Tobago's coral reefs following the 2010 mass bleaching event, Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.01.038

S. Buglass et al. / Marine Pollution Bulletin xxx (2016) xxx–xxx

2.3. Juvenile community surveys Juvenile coral colonies, hereafter referred to as juveniles, were enumerated and identified by carefully scrutinizing the reef benthos in sixty randomly-placed 0.25 m2 quadrats per site (Carpenter and Edmunds, 2006). Juveniles were defined as any colony of large-sized coral taxa visible to the naked eye with a maximum diameter of 5 cm (e.g., Orbicella spp., Pseudodiploria spp., Siderastrea spp., etc.) or 2 cm for small sized coral taxa (Porites spp., Favia fragum, Agaricia spp., etc.). This distinction was made as small-sized corals tend to be sexually mature adults once larger than 2 cm (Chiappone and Sullivan, 1996; Miller et al., 2000; Irizarry-soto and Weil, 2009). Small living coral fragments that are not a product of sexual reproduction were omitted from the count (Trapon et al., 2013). Juveniles were identified by species when possible and otherwise by genus. If more than three quarters of the benthic cover within the quadrats were covered by non-settling substrate, e.g. sand or living coral, the quadrat was moved to the side or the aforementioned process was repeated (Edmunds et al., 1998). 2.4. Sedimentation assessment Three sediment traps were deployed for at least a month at each reef as guided by English et al. (1997), Hill and Wilkinson (2004) and Storlazzi et al. (2009). At each site, sediment traps consisted of three sets of three cylindrical 5 × 20 cm PVC tubes fixed onto a 1 m metal rod, such that the cylinders were 0.75 m above the substrate. Traps were spaced ~30 m from each other in order to maintain adequate coverage of the reef site. After 30–37 days (20–27th of June 2013) the sediment traps were recovered. Out of the 54 tubes (18 traps) set, a total of 45 were recovered as tubes broke or disappeared at Culloden East (3), Culloden West (4), Black Jack Hole (1) and Angel Reef (1). Sediment content from each tube was washed thoroughly with distilled water to remove salts and oven-dried at 105 °C for at least 12 h. Sedimentation rates (mg cm−2 d−1) were determined by dividing the dry weight by the area of the sediment trap aperture width and the measurement period (Abdullah et al., 2011). Sediment composition was analyzed using the loss on ignition (LOI) method (Heiri et al., 2001) to determine what fraction of the sediment was composed of organic and carbonate matter; the remaining non-carbonate material represented the terrigenous fraction of the sample. This method is predominantly used by paleolimnologists on lake core samples and is known to provide rough estimates of sediment composition (Santisteban et al., 2004). Samples from each trap set were pooled to form a composite sample because many individual tubes contained b 2 g of sediment. Particle size analysis of sediments per trap set was conducted using the wet sieving method (Syvitski, 2007), using ~0.5 g from each composite sediment sample separated into five fractions according to the Wentworth size class system. 2.5. Statistical analysis Statistical analysis was done in R version 2.15.1. All juvenile and sediment data were tested for normality using the Shapiro–Wilk test and homogeneity of variance using graphical methods. Sedimentation rate data were found to be normally distributed, although juvenile data did not follow a normal distribution. Differences in sedimentation rates between sites were tested employing a one-way ANOVA, followed by a Tukey HSD post-hoc test to detect pairwise differences. Differences in juvenile densities between sites were tested employing Kruskal– Wallis test by Dunn's post-hoc pairwise test (using packages multcomp 1.2.17 and coin 1.0-23) (Miller et al., 2000). Correspondence analysis (CA) was performed on eight genus groups found at each site, after removing all rare taxa, to explore the distribution of species composition across all sites (Irizarry-soto and Weil, 2009) using ordination analysis tools in the Vegan Package in R software.

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Demographic data on colony abundance and size was analyzed independently at each site for the coral species with ≥12 colonies at that site each year. Following this minimum constraint, a total of 26 different populations of coral species were analyzed, consisting of 6 species at Outer Reef, 6 species at Western Reef, 5 species at Culloden East, 5 species at Culloden West and 4 species at Black Jack Hole. Annual mean size, standard deviation, standard error, median, skewness and skewness standard error were calculated for these dominant populations at each site. Skewness values greater than two times the standard error were considered to be significantly skewed from normal (McClanahan et al., 2008). The percent cover for each coral species at each site was calculated following Done et al. (2010):   C ¼ 100  NπD2 =4 =½ðW þ DÞL; where C is the percentage cover, N is the number of colonies, D is the mean dimension of the N colonies, W is the width of the belt transect in centimeters (100 cm) and L is the total length of the belt transects. The equation assumes that all colonies are circular in shape with a diameter equal to the mean lateral dimension and that the width of the sampling area is the width of the actual belt (1 m) plus the mean diameter of all colonies, to account for colonies extending beyond the belt. Though this index tends to over-estimate the true percent of the coral cover, it provides comparable values for assessing differences in the percent coral cover between sites and over time. Size distribution data were log transformed; however the assumptions of normality of data (Shapiro–Wilk test) and homogeneity of variance (Levene's test) were not met. Kruskal–Wallis tests were employed to test for the significant differences in size between years and sites (McClanahan et al., 2008), followed by post-hoc pairwise Mann–Whitney U-tests comparisons, and Kolmogorov–Smirnov tests to test for differences in size frequency distribution (Adjeroud et al., 2007). To avoid Type I errors across multiple comparison tests, critical values for all tests were adjusted using the Bonferroni correction, resulting in an α-level of 0.0167. The impact of the bleaching event on the coral community of each site over the three years was also analyzed using a non-metric multidimensional scaling (NMDS) based on Bray–Curtis dissimilarities of each species abundance per site, using vegan package version 2.010 (Borcard et al., 2011). 3. Results 3.1. Changes in coral population size structure and composition The dominant species across the five sites assessed in 2010, 2011 and 2013 included Orbicella faveolata, Pseudodiploria strigosa, Siderastrea siderea, Montastraea cavernosa, Agaricia spp., Porites astreoides, Colpophyllia natas, and Diploria labyrinthiformis. O. faveolata was by far the most dominant species at all sites (Supplementary Table 1). From the 2010 pre-bleaching survey to the 2013 survey, there was a significant change in the size frequency distribution and mean colony size of 10 of the 26 coral populations identified as dominant across the different sites (Supplementary Table 2). The changes over the three years obscure the complex and partially opposing effects of the bleaching event and the post-bleaching recovery on the coral community. Between the 2010 pre-bleaching assessment and the 2011 post-bleaching assessment, percent coral cover declined among the majority of dominant species at the different sites (16 of 26). The colony abundance also declined among close to half (12 of 26) of the dominant species (Supplementary Table 1). In 2010, coral size distributions among most species were dominated by small colonies; this is reflected by the positive skewness in the size frequency distributions in the 2010 surveys (Supplementary Table 1). After the bleaching event, mean colony size declined for nine of the populations (Fig. 2) although the decline was significant (Mann–Whitney test,

Please cite this article as: Buglass, S., et al., A study on the recovery of Tobago's coral reefs following the 2010 mass bleaching event, Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.01.038

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S. Buglass et al. / Marine Pollution Bulletin xxx (2016) xxx–xxx

Fig. 2. Boxplot and mean colony size (white dots) for the dominant species at each site. Significant differences in mean colony size between years (Mann–Whitney U test, P b 0.016) are noted on the plots (*).

P b 0.016) in only five cases: Agaricia spp. at Outer Reef, S. siderea at Western Reef and Culloden East, and for O. faveolata at Outer Reef and Black Jack Hole (Fig. 2). By 2011, size frequency distributions significantly changed (KS-test, P b 0.016) only among Agaricia spp. at Outer Reef, S. siderea at Western Reef and O. faveolata at Black Jack Hole (Fig. 3; Supplementary Table 1). Between 2011 and 2013, percent cover increased for 10 of the 26 populations assessed, and declined for 5 populations (Supplementary Table 1). Colony abundance also increased among half of the populations, and the size frequency distribution of the majority of populations (16 of 26) became positively skewed (an increase from 8 in 2011), reflecting an increase in small colonies. O. faveolata showed the most consistent increase in cover and abundance across all sites, with the exception of Black Jack Hole where it remained unchanged. Abundance and percent cover of Agaricia spp. and P. astreoides also more than doubled by 2013 at most sites. Significant decline in mean size and size frequency distribution from 2011 to 2013 was noted only for O. faveolata, S. siderea and P. astreoides at Black Jack Hole, and P. strigosa at Culloden East (Figs. 2 and 3; Supplementary Table 2).

The nMDS analysis, based on colony abundances of all species present per site, illustrates how the community composition remained relatively similar across the three assessed years, especially among the Culloden sites (Fig. 4). The largest community composition change from 2010 to 2013 occurred at Black Jack Hole likely due to an increase in P. astreoides and decline in M. cavernosa. The community composition shift at the Buccoo sites appears to be due in part to an increase in the abundance of Agaricia spp.

3.2. Juvenile density and composition A total of 428 juvenile corals were counted over a total area of 90 m2 (15 m2 at each site). The Buccoo Reef sites had the lowest abundance, richness and diversity (Table 1). Overall, mean juvenile density was 5.4 ± 6.3 m− 2; the juvenile distribution was patchy with 20–49% of quadrats containing no juveniles. Mean juvenile abundances were similar between most sites with the exception of Angel Reef, where abundances were significantly higher (Dunn's test, P b 0.05) when compared to all other sites except Culloden West.

Please cite this article as: Buglass, S., et al., A study on the recovery of Tobago's coral reefs following the 2010 mass bleaching event, Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.01.038

S. Buglass et al. / Marine Pollution Bulletin xxx (2016) xxx–xxx

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Fig. 3. Size frequency distributions across the three years of populations that significantly differed between years. Significant Kolmogorov–Smirnov tests are noted on plots (*).

The majority of juvenile observed were brooding corals, such as Agaricia, Porites, Madracis, Scolymia, and Favia (Table 1). The few broadcast spawning taxa belonged to the genera Siderastrea, Pseudodiploria, Montastraea, Orbicella and Colpophyllia. Agaricia spp. was the most dominant species at most sites with the exception of Black Jack Hole, where Porites spp. dominated. The juvenile community composition differed

greatly from the adult coral community composition (Fig. 5). Dominant adult coral species, like Orbicella spp., were unrepresented in the juvenile sample counted. Conversely, adult Agaricia represented less than 5% of adult coral cover at each site, despite being the most dominant juvenile group. Siderastrea and Diploria were the only genera to have similar juvenile and adult relative abundance.

Please cite this article as: Buglass, S., et al., A study on the recovery of Tobago's coral reefs following the 2010 mass bleaching event, Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.01.038

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S. Buglass et al. / Marine Pollution Bulletin xxx (2016) xxx–xxx

there is a greater potential for coarse and medium sand particles reaching the four reef zones with enough current and wave energy. 4. Discussion

Fig. 4. Non-metric multidimensional scaling using Bray–Curtis dissimilarities plot of the coral communities at each of the sites per year. Site names and years are indicated on the plot. NMDS stress = 0.133.

3.3. Characterization of sedimentation The mean sediment accumulation rate across all sites was 5.6 ± 4.2 mg cm−2 d−1 (Table 2). Sediment rates were not significantly different between sites, with the exception of Culloden West (Tukey HSD, P N 0.05) where rates were four times higher than at all other sites (15.1 ± 2.9 mg cm− 2 d− 1). Terrigenous material dominated at all sites and represented the most dominant fraction of the collected material, ranging between 51.6 ± 0.2% and 73.0 ± 0.3%, with the highest rates at Culloden. Carbonate materials were less common, ranging from 22.0 ± 0.7% to 40.1 ± 0.2%, with the highest rates at the Buccoo sites. Organic matter, largely composed of turf algae that grew inside the tubes, represented b8% of the sediment composition of the samples at all the sites. The sediment grain size distributions differed between the three reef systems. The dominant grain size was silt/clay (b63 μm) at the Buccoo sites and very fine sand (63–125 μm) at the Culloden sites. Sediment at the Speyside sites, on the north-eastern side of the island, was dominated more by fine sand (125–250 μm) and had the highest proportions of medium and coarse sands (N125 μm) among all sites. Although these sites were farther from Tobago's shore, Black Jack Hole and Angel Reef are 50 m or less from the shore of small islands, so

Overall, the results suggest that the 2010 bleaching event and postbleaching recovery did not dramatically alter coral cover or colony size distribution among most dominant species at most sites. Although the bleaching event reduced the cover and abundance of the majority of dominant species, only 5 of the 26 assessed coral populations at the different sites experienced a significant change in population size structure after the event (Supplementary Table 2). The cover and abundance of half of the assessed populations increased from the post-bleaching survey in 2011 to the 2013 survey, although the change in size structure was again significant only in five cases. This limited overall response to the bleaching event is not surprising given that pre-bleaching coral cover was already low (b 25%), likely due to a combination of local human disturbances and the previous bleaching event in 2005 (Mallela et al., 2010; Alemu I and Clement, 2014). Despite the limited overall reef-level response to the bleaching event, the size distribution data reveals a scarcity of large colonies which may have long-term implications for composition and physical structure of reefs in Tobago. Population size distributions tended to be positively skewed, due to the dominance of small colonies, across all sites irrespective of the differences in levels of land-based pollution. The lack of large colonies, even among large growing species, across all sites may be a legacy of past disturbances fragmenting colonies and/or limiting the survival and growth of large colonies. For several key species (e.g., Agaricia spp. at Outer Reef, S. siderea at Western Reef and O. faveolata at Black Jack Hole) the bleaching event further increased skewness, likely as a consequence of bleaching-induced partial mortality and related fragmentation. By 2013, the size distribution of several species continued to become positively skewed towards smaller colonies, especially at Black Jack Hole where the most extensive bleaching and bleaching-induced mortality were recorded (Alemu I and Clement, 2014). The post-bleaching rise in smaller size classes may be due to the disease-related partial morality; incidence of disease was noted to have increased at the time of the 2011 survey (Alemu I, 2011). Other studies have also found disease outbreaks to be a greater cause of post-bleaching mortality, than the bleaching itself (Miller et al., 2006; Wilkinson and Souter, 2008; Brandt and McManus, 2009). Future projections also indicate that climate-related disease outbreaks will likely cause substantial coral mortality in the coming decades (Maynard et al., 2015). The reduction of colonies' mean size as result of partial mortality and fragmentation following the bleaching event, whether

Table 1 Summary of juvenile taxa found at each site. Taxa

Outer Reef

Western Reef

Culloden East

Culloden West

Black Jack Hole

Angel Reef

Agaricia spp. Colpophyllia spp. Pseudodiploria spp. Eusmilia fastigiata Favia fragum Madracis decatis Madracis mirabillis Montastraea cavernosa Orbicella spp. Mycetophyllia spp. Porites astreoides Porites porites Scolymia spp. Siderastrea spp. Total no. of juveniles Density (m−2)

51 – – – – – – – 2 1 1 – – 4 59 3.9 ± 4.8

24 2 7 1 – – – – – – – – 2 14 50 3.3 ± 4.2

34 – 8 – 6 4 – 1 – – – – 9 2 64 4.3 ± 4.2

26 – 16 – 1 3 – 5 – – 3 – 19 26 99 6.6 ± 7.7

1 – 15 – 8 4 – 2 5 – 27 – – 7 69 4.6 ± 5.9

85 – 1 – 3 5 27 – 5 – 8 1 2 9 146 9.7 ± 7.9

Please cite this article as: Buglass, S., et al., A study on the recovery of Tobago's coral reefs following the 2010 mass bleaching event, Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.01.038

S. Buglass et al. / Marine Pollution Bulletin xxx (2016) xxx–xxx

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Fig. 5. Relative abundance of major taxa (genus) groups at each site for (A) juvenile and (B) adult population based count data.

caused by bleaching or post-bleaching mortality due to disease, could possibly reduce the coral resilience to future disturbances. Smaller colonies are more likely to succumb to stressors (Hughes, 1984; McClanahan et al., 2008), and may also be less fecund than larger colonies (Szmant, 1986), although not all experimental studies support this notion (Graham and van Woesik, 2013). This change in population demographics could in turn delay post-disturbance recovery and further set back framework-building coral communities from dominating reefs. The low density of juveniles (5.4 ± 6.3 juveniles/m−2), particularly of broadcasting species, suggests that the rise in smaller size classes is due to partial mortality, rather than the addition of sexually produced juveniles to the population. A low juvenile population dominated by brooding taxa with weedy life history strategies is common across Caribbean reefs (Miller et al., 2000; Moulding, 2005; Irizarry-soto and Weil, 2009; Manfrino et al., 2013). Based on growth rates of 0.37 to 0.73 mm/month (Birkeland, 1977), most juveniles recorded in this study are estimated to be between 5 and 10 years old; thus it is likely that the assessed communities were likely shaped by the 2005 bleaching event. While coral juveniles tend not to suffer greatly from bleaching-induced mortality (Mumby, 1999; Shenkar et al., 2005), the bleaching of adult colonies is known to reduce the reproductive output of corals in the years following the thermal stress (Ritson-williams et al., 2009; Ward et al., 2000; Mallela and Crabbe, 2009). Broadcasting taxa in the Caribbean are especially vulnerable as most bleaching events tend to occur during their yearly spawning period between August and October (Szmant and Gassman, 1990). Consequently, it is possible that the juvenile densities reported in this study were even lower than usual, due to the impact of the earlier 2005 bleaching event (Szmant and Gassman, 1990). Both the juvenile distribution and the response of individual species to the bleaching event supports the notion that Caribbean reefs are

becoming more dominated by weedy non-framework building coral taxa with greater ability to persist through disturbance (Green et al., 2008; Côté and Darling, 2010; Perry et al., 2014). For example, S. siderea was among the most affected across all sites, except Culloden West, and showed little recovery by 2013 at all sites, except Outer Reef. Other studies have reported S. siderea to be among the species most susceptible to bleaching, bleaching-induced mortality and post-bleaching disease (Gochfeld et al., 2006; Oxenford et al., 2007; van Hooidonk et al., 2012). Conversely, the brooders Agaricia spp. and P. astreoides, which tend be fecund and more successful at recruiting (Arnold and Steneck, 2011), were among the least affected by the bleaching event. The rise in abundance, particularly of small size classes, of both species by 2013 may have resulted from fragmentation but also from an input of juveniles; Agaricia and Porites comprised 30–80% of the juvenile population at the sites where the genera were present. The disparity between juvenile and adult population of broadcasting species such Orbicella further supports the evidence of a shift towards non-framework building taxa. Juveniles of the Orbicella genus were exceptionally rare despite its having the greatest parental stock; Orbicella accounts for N 60% of the coral cover of most of Tobago's reefs (Alemu I and Clement, 2014). Low numbers of Orbicella recruits have been well documented across Caribbean reefs (Hughes and Tanner, 2000; Irizarry-soto and Weil, 2009; Vermeij et al., 2011). Although the exact reasons remain unclear, Ritson-Williams et al. (2009) suggested that many Caribbean framework building species evolved with low sexual recruitment levels, and instead rely on the production of recruits from fragmentation or budding. However, since fecundity studies have found Orbicella species to have successful spawning cycles, it has also been suggested that the problem lies in the post-spawning processes, i.e. fertilization, larval settlement and/or post recruitment survival (Szmant, 1991). The lack of grazing herbivores across Tobago's reefs

Table 2 Mean and standard deviations of sediment measurements.

Traps recovered (#) Mean weight (g) Rate (mg cm−2 d−1) Composition (%) Terrigenous CaCo3 Organic Grain size (%) Course sand Medium sand Fine sand Very fine sand Silt/clay

Outer Buccoo

Western Buccoo

Culloden East

Culloden West

Black Jack Hole

Angel Reef

9 2.5 ± 0.7 3.4 ± 0.9

9 3.2 ± 0.5 4.3 ± 0.7

5 3.1 ± 1.0 4.8 ± 1.6

6 9.2 ± 1.8 15.1 ± 2.9

8 3.62 ± 2.2 4.9 ± 3.1

8 2.7 ± 1.3 3.6 ± 1.8

56.5 ± 0.2 35.6 ± 0.5 7.9 ± 0.2

51.6 ± 0.3 40.5 ± 0.2 7.9 ± 0.2

71.0 ± 0.6 23.5 ± 0.3 5.5 ± 0.1

73.0 ± 0.3 22.0 ± 0.7 5.0 ± 0.4

65.3 ± 2.4 27.0 ± 3.9 7.7 ± 1.6

58.8 ± 4.6 35.9 ± 5.7 5.3 ± 1.1

1.4 ± 0.1 3.1 ± 1.3 22.6 ± 4.5 21.8 ± 8.9 51.0 ± 10.7

5.5 ± 1.7 10.5 ± 1.6 18.2 ± 1.6 29.0 ± 0.7 36.7 ± 4.3

3.3 ± 1.5 7.6 ± 1.1 26.0 ± 1.0 44.4 ± 6.8 18.8 ± 3.3

3.5 ± 3.1 4.1 ± 0.0 29.8 ± 1.3 45.5 ± 2.4 17.1 ± 0.7

15.9 ± 5.9 20.2 ± 2.2 35.0 ± 3.8 20.5 ± 5.2 8.4 ± 4.9

8.8 ± 1.8 21.7 ± 4.1 42.9 ± 11.2 15.3 ± 5.3 11.3 ± 7.6

Please cite this article as: Buglass, S., et al., A study on the recovery of Tobago's coral reefs following the 2010 mass bleaching event, Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.01.038

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(Mallela et al., 2010) and spread of turf microalgae over dead coral structures (based on anecdotal observation) may be undermining the recruitment and settlement processes. Sedimentation is also known to impede reproduction and recruitment processes. However, we found that sedimentation rates were low (b5 mg cm−2 d−1) among most of Tobago's reef sites. The exception was the higher rates (N 15 mg cm− 2 d− 1) at Culloden West, which may reflect small-scale variation in sedimentation rates but could also be an artifact of the sampling method. Reefs at the Buccoo Reef sites were exposed to the highest proportions of silt/clay sediment (at least 20% higher than at other sites), which could be a consequence of exposure to prevailing winds and currents, facilitating sediment deposition or bottom resuspension. Though both coarse and fine-grained sediments have the potential to harm corals, fine sediments can remain suspended in the water column for longer and thus more efficiently attenuate light, reducing photosynthetic rates (Abdullah et al., 2011). The sedimentation rates reported in this study are a limited snapshot from the end of the dry season; a sediment accumulation profile that covers both the dry and rainy seasons is necessary to capture the full range of sedimentation rates experienced at the different sites. 5. Conclusion This study found that the cover and size spectra of most dominant coral species across Tobago's reefs were not significantly altered by the 2010 bleaching event. Instead, with pre-bleaching coral cover already low due to local factors and past disturbances, the 2010 event affected particular susceptible populations and increased the proportion of small colonies. The low density of sexually produced juveniles is indicative that Tobago's reefs are already experiencing limited successful recruitment, especially of large growing broadcasting species. Overall, this suggests the rate of post-disturbance recovery will be much slower than the projected return period of bleaching-level thermal stress, given that these are predicted to be more frequent and intense as the oceans continue to warm (Donner et al., 2007; Hoegh-Guldberg et al., 2007). Consequently, it is likely that Tobago's coral community will continuously become dominated by small-sized colonies. This shift in the size frequency distribution would affect the reproductive output of coral communities and lead species that are naturally more fecund, such as brooders Agaricia spp. and P. astreoides, to become more dominant. Given the possible role of coral disease in fragmentation of coral colonies after the mass bleaching event, classifying and recording the spatial extent of coral diseases is critical to future monitoring of reefs in Tobago and the region. While a shift towards more resilient weedy species means that reefs in Tobago may still be dominated by stony corals in the future, it is possible that the calcification rate of these coral assemblages may not have the capacity to maintain the framework and functions of coral reefs (Alvarez-Filip et al., 2013). Thus the maintenance of reef-building taxa, such as Orbicella, should be a key conservation priority across Tobago's reefs. Tobago's population relies heavily on its fringing coral reefs for income from tourism and inshore fisheries, and also for protection from wave action and storms. In order to safeguard these ecosystem services, it is essential to increase the opportunities for successful recruitment among reef building coral species. It is paramount that local coastal ecosystem management efforts target increasing herbivory and reducing sedimentation and nutrient enrichment among the reefs still feature sufficient coral cover. Acknowledgments Funding for this project was provided by the NSERC TerreWEB and BRITE programs, a NSERC Discovery Grant (Donner), and donations from generous individuals to this project's crowdfunding campaign. We thank the dedicated volunteers and IMA staff for the support that

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Please cite this article as: Buglass, S., et al., A study on the recovery of Tobago's coral reefs following the 2010 mass bleaching event, Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.01.038