Corals of the genus [i]Porites[i] are a locally abundant ...95 In November and December of 2013 and...

Corals of the genus Porites are a locally abundant componentof the epibiont community on mangrove prop roots atCalabash Caye, Turneffe Atoll, BelizeZachary A Bengtsson, Kirsten M Kuhn, Anya T Battaglino, Allen S Li, Matthew N Talbot, Marzie Wafapoor, Calder J Atta, Michael BKowalski, Sarah P Margolis, Ekaterina A Rar, Elizabeth M Burmester, Kathryn C Lesneski, Karina Scavo, Les Kaufman, Nathan LStewart, John R Finnerty

Mangrove prop roots support diverse epibiont communities, but they are generallyregarded as inhospitable for corals. However, recent reports have documented coralsthriving on mangrove roots in the U.S. Virgin Islands and Cuba, and it has been proposedthat mangroves may provide a refuge from environmental conditions that trigger coralmortality on nearby reefs. It also raises interesting questions about the potentialevolutionary significance of coral populations in mangrove forest. We investigated diversemangrove habitats for the presence of corals at Calabash Caye, Belize, part of a recentlydesignated marine reserve on Turneffe Atoll. Here we present data on the distribution, sizeand morphology of 127 colonies of branching Porites found in a survey of 1858 meters ofmangrove prop roots fringing three qualitatively distinct bodies of water: a high-flowchannel, a moderate-flow creek, and a low-flow mangrove pond. The distribution of Poriteswas highly clumped, with 108 colonies occurring in a 178-meter stretch of shoreline alongthe high flow channel. Colony morphology varied widely, from bushy colonies with morethan 40 branch tips per 1000 cm3 of ecological volume, to spindly colonies with fewer than10 branch tips per 1000 cm3, to new recruits that have not yet developed distinctbranches. Comparisons of the same coral-bearing roots in 2013 and 2014 revealed thatcolonies can experience substantial growth in a year’s time. We also document a muchmore diverse coral fauna living in the mangroves at Crooked Creek, a high flowenvironment on the western edge of Turneffe Atoll. The data described here contribute toan emerging picture of mangroves as potentially important habitat for corals, whilesuggesting that different types of mangrove habitat vary in their suitability for differentspecies of coral. Future studies are needed to identify the critical environmental featuresof mangrove habitats that support coral, to further characterize those corals that canutilize mangrove habitat, and to investigate potential connectivity between coralpopulations in mangroves and nearby reef habitats.

PeerJ PrePrints | https://dx.doi.org/10.7287/peerj.preprints.1453v1 | CC-BY 4.0 Open Access | rec: 27 Oct 2015, publ: 27 Oct 2015

1

2

3 Corals of the genus Porites are a locally abundant component of the epibiont

4 community on mangrove prop roots at Calabash Caye, Turneffe Atoll, Belize

5

6 Zachary A. Bengtsson1,^, Kirsten M. Kuhn1,2,^, Anya T. Battaglino2, Allen S. Li2, Matthew N.

7 Talbot1,2, Marzie Wafapoor1,2, Calder J. Atta2, Michael B. Kowalski1,2, Sarah P. Margolis2,

8 Ekaterina Rar2, Elizabeth M. Burmester1, Kathryn C. Lesneski1, Karina Scavo1, Les Kaufman1,2,

9 Nathan L. Stewart1,2 and John R. Finnerty1,2*

10

11 Boston University Biology Department1 and Marine Program2

12 5 Cummington Mall, Boston, MA 02215

13

14 ^These authors contributed equally to this manuscript.

15

16 *Corresponding Author:

17 Telephone: 617-353-6984

18 Fax: 617-353-6340

19 e-mail: [email protected]

20

21 Keywords: coral; mangrove; epibiont; Porites,

22

23 Running Head: Coral epibionts of mangrove roots in Belize


24 Abstract

25 Mangrove prop roots support diverse epibiont communities, but they are generally regarded as

26 inhospitable for corals. However, recent reports have documented corals thriving on mangrove

27 roots in the U.S. Virgin Islands and Cuba, and it has been proposed that mangroves may provide

28 a refuge from environmental conditions that trigger coral mortality on nearby reefs. It also raises

29 interesting questions about the potential evolutionary significance of coral populations in

30 mangrove forest. We investigated diverse mangrove habitats for the presence of corals at

31 Calabash Caye, Belize, part of a recently designated marine reserve on Turneffe Atoll. Here we

32 present data on the distribution, size and morphology of 127 colonies of branching Porites found

33 in a survey of 1858 meters of mangrove prop roots fringing three qualitatively distinct bodies of

34 water: a high-flow channel, a moderate-flow creek, and a low-flow mangrove pond. The

35 distribution of Porites was highly clumped, with 108 colonies occurring in a 178-meter stretch of

36 shoreline along the high flow channel. Colony morphology varied widely, from bushy colonies

37 with more than 40 branch tips per 1000 cm3 of ecological volume, to spindly colonies with fewer

38 than 10 branch tips per 1000 cm3, to new recruits that have not yet developed distinct branches.

39 Comparisons of the same coral-bearing roots in 2013 and 2014 revealed that colonies can

40 experience substantial growth in a year’s time. We also document a much more diverse coral

41 fauna living in the mangroves at Crooked Creek, a high flow environment on the western edge of

42 Turneffe Atoll. The data described here contribute to an emerging picture of mangroves as

43 potentially important habitat for corals, while suggesting that different types of mangrove habitat

44 vary in their suitability for different species of coral. Future studies are needed to identify the

45 critical environmental features of mangrove habitats that support coral, to further characterize


46 those corals that can utilize mangrove habitat, and to investigate potential connectivity between

47 coral populations in mangroves and nearby reef habitats.

48


49 Introduction

50 Mangroves can promote the health and taxonomic richness of nearby coral reefs through a

51 number of mechanisms, including stabilizing sediments, increasing water clarity, and serving as

52 a nursery for juvenile fishes and invertebrates that will migrate to the reef as adults [1, 2].

53 Additionally, mangrove prop roots support diverse communities of sessile epibionts, some of

54 which can co-occur in nearby reef habitats [2]. For example, at seven Caribbean localities, coral

55 reefs and nearby mangrove ecosystems were found to support overlapping but distinctive

56 assemblages of sponges, implying that some sponge species can disperse between reef and

57 mangrove [3], representing yet another mechanism whereby mangroves impact the biodiversity

58 of nearby coral reefs.

59 To date, the abundance and distribution of scleractinians in mangroves has received

60 relatively little study [4], but based on recent published reports from the U.S. Virgin Islands [5-7]

61 and Cuba [8], there is emerging evidence to suggest that mangroves could represent a significant

62 habitat for corals. Rogers reported 28 coral species growing on or among mangrove prop roots in

63 Hurricane Hole, St. John (Table 1) [5]. A follow-up study quantified the abundance of two reef-

64 building corals — Colpophyllia natans and Diploria labrynthiformis — revealing that some

65 specimens in the mangroves survived an outbreak of disease and bleaching that caused high

66 mortality in nearby reef habitats [6]. Based on this finding, the authors suggested that mangroves

67 may provide a refuge from conditions that promote bleaching on the reef because of differences

68 in key environmental parameters e.g., shading from mangrove trees [7]. Alternatively, corals

69 could become locally adapted to conditions in the mangroves. As poorly flushed mangrove

70 habitats tend to experience higher temperatures than nearby reefs, mangroves could harbor

71 populations of heat tolerant individuals whose larvae could replenish nearby reefs following


72 heat-related coral mortality [7]. More recently, Hernández-Fernández reported 11 species of

73 hermatypic corals living on mangrove roots at Jardines de la Reina National Park in Cuba, all

74 inhabiting roots that were also occupied by crustose coralline algae [8].

75 To evaluate the potential importance of mangroves as a habitat for corals, we conducted a

76 systematic survey for corals on the prop roots of Rhizophora mangle at Calabash Caye, Turneffe

77 Atoll, Belize. Here, we present data on the abundance, distribution, size, colony morphology, and

78 year-to-year survival of corals along 1858 meters of mangrove prop roots fringing both banks of

79 a high-flow channel, a moderate-flow creek, and a low-flow mangrove pond. In all, we found

80 127 coral colonies occupying mangrove roots at Calabash, all branching members of the genus

81 Porites. Their distribution was highly clustered, with 108 colonies located in a single 178-meter

82 stretch of shoreline. An incipient longitudinal study of 60 randomly sampled mangrove roots at

83 Calabash revealed that roots bearing corals are relatively rare, but that corals inhabiting

84 mangrove roots exhibit a high survival rate over a year’s time. Given that the coral fauna we

85 characterized at Calabash was substantially less diverse than that reported in the U.S. Virgin

86 Islands and Cuba, we also investigated coral species richness at Crooked Creek, a high flow

87 environment along the western edge of Turneffe Atoll—there, we found representatives of eight

88 scleractinian genera, in contrast to the single genus we found at Calabash. We discuss the

89 implications of these findings for the importance of mangroves as a coral habitat in Turneffe

90 Atoll, and for the hypothesis that mangroves may represent a refuge for reef corals suffering

91 from the impacts of climate change.

92

93 Methods

94 Study sites


95 In November and December of 2013 and 2014, we surveyed the mangrove roots fringing three

96 contiguous bodies of water at Calabash Caye, a small mangrove on the eastern (windward) face

97 of Turneffe Atoll (Fig. 1). From north to south, these sites were: (1) a mangrove pond in the

98 interior of Little Calabash (17°17'18.87"N, 87°48'43.46"W); (2) the channel separating Little

99 Calabash from Calabash Caye (17°17'12.88"N, 87°48'41.86"W); and (3) a narrow creek

100 connecting the channel with a mangrove pond in the interior of Calabash (17°17'10.50"N,

101 87°48'44.94"W). These three sites—henceforth referred to as (1) Seahorse Pond, (2) Calabash

102 Channel, and (3) Calabash Creek— differed qualitatively with respect to current judged by in-

103 water observers: the pond exhibited the lowest current, the channel exhibited the highest current,

104 and the creek exhibited an intermediate current. At all three sites, the banks were continuously

105 lined with prop roots of Rhizophora mangle, and the roots located furthest from the bank were

106 densely occupied by a diverse epibiont community including macroalgae, sponges, tunicates,

107 bivalves, anemones, and corals. From November 16-December 15, 2014, nine data loggers

108 (HOBO Pendant® model 8K) were deployed to record hourly measurements of water

109 temperature at seven locations along the survey site (Fig. 1B, a-g). We also performed visual

110 surveys for corals on mangrove prop roots at Crooked Creek (17°19'45.00"N, 87°55'4.10"W), for

111 comparison with the mangroves at Calabash (Fig. 1C). Crooked Creek is a high-flow channel on

112 the western edge of Turneffe Atoll located approximately 12 km WNW of Calabash. The

113 research was conducted under Aquatic Scientific Research Permit 000047-13 issued by the

114 Belize Fisheries Department and signed by Fisheries Officer James Azueta.

115

116 Targeted coral surveys


117 In November of 2014, along three discontinuous sections of shoreline at Calabash Caye spanning

118 1858 meters (Fig. 1; red lines), the mangroves were systematically inspected for the presence of

119 corals by three observers who slowly snorkeled in sequence past the fringing prop roots. Each

120 root that harbored at least one coral was marked above the waterline using colored zip ties, and

121 its location was determined using a handheld GPS device (Garmin; GPSmap 76CSx). Every

122 coral colony was photographed from above and from one side using an underwater digital

123 camera (Pentax WG-10). In each photograph, a centimeter rule was held in approximately the

124 same plane as the center of the coral, so that each colony’s dimensions could be estimated from

125 the photographs.

126

127 Transect-based sampling of mangrove roots

128 In November 2013, we established six 30m transects along the shorelines of Calabash Channel

129 and Calabash Creek (Fig. 1B; 1-6). On each transect, a unique combination of colored zip ties

130 was used to mark ten mangrove prop roots at regular intervals (3, 6, 9, 12, 15, 18, 21, 24, 27 and

131 30 m from the start of the transect). Video and still photography were used to record the

132 macroscopic epibionts inhabiting each of these 60 marked roots. The same 60 roots were

133 photographically re-sampled in November 2014. The still photos and videos were analyzed by

134 five independent observers to identify corals living on the roots.

135

136 Species identification

137 Corals were identified based on gross colony morphology by observers on site and from

138 photographs. In the case of the branching Porites, which proved to be the only type of coral we

139 observed at Calabash, we did not attempt to identify individual colonies to species. Caribbean


140 branching Porites are thought to compose a monophyletic group, but the number of species

141 constituting the complex is unclear. A recent molecular phylogenetic analysis of this clade based

142 on the mitochondrial control region and 10 nuclear loci failed to resolve the three nominal

143 species: P. divaricata, P. furcata, and P. porites [9]. Given this uncertainty, we refer to all of

144 these specimens as branching Porites, to differentiate them from sympatric crustose/massive

145 congeners such as P. astreoides.

146

147 Characterization of colony size and morphology

148 The length, width, and height of each branching Porites found at Calabash Caye were measured

149 on site. From these linear dimensions, the ecological volume of each colony was calculated

150 according to the formula of Shaish et al. [10]. Branch tips were counted from photographs aided

151 by ImageJ [11]. Branch density was then calculated by dividing the number of branch tips by the

152 ecological volume.

153

154 Analysis of spatial distribution

155 Distances between corals were estimated from GPS coordinates. Using the estimated distances

156 between colonies within each contiguous stretch of shoreline, we applied the Clark-Evans test

157 [12] modified for dispersion along one dimension [13] to determine if the average distance

158 between nearest neighbors differed from null expectations.

159

160 Results

161 Number and distribution of corals at Calabash Caye


162 Representative photographs of coral colonies on red mangrove prop roots at Calabash Caye are

163 shown in Fig. 2. In all, 127 coral colonies were identified along the 1858 meters of shoreline

164 surveyed at Calabash Caye (Fig. 3). All of the corals identified appeared to be branching

165 members of the genus Porites. However, twenty (15.7%) of the colonies were recent recruits that

166 did not yet have any branches.

167 The corals exhibited a highly clustered distribution, with 85% (108/127) of the Porites

168 colonies occurring on 26 prop roots in a 178-meter stretch along the north side of Calabash

169 Channel (Fig. 3A, B). Single colonies were found on 9 of these roots, but multiple colonies were

170 found on the other 17 roots, with as many as 18 colonies on a single root (Fig. 3B). Along the

171 eastern edge of Calabash Creek and the southern side of Calabash Channel (Fig. 3A; blue line),

172 corals were identified on 11 prop roots. Most of these roots bore a single coral, but three colonies

173 were found on one root and five on another (Fig. 3C). Only two coral-bearing roots were found

174 on the western edge of Calabash Creek (Fig. 3A; green line), each with only 1 colony per root.

175 No corals were found along the 821 m of shoreline surveyed within Seahorse Pond. According to

176 the Clark-Evans test, the corals along the 1110 m shoreline encompassing Seahorse Pond and the

177 north side of Calabash Channel were more tightly clustered than would be expected by chance

178 (p<0.001; Table 2), while those located along the 550 m shoreline encompassing the south side

179 of Calabash channel and the eastern edge of Calabash Creek were not (p=0.184).

180 We determined the size of the colonies using two metrics: the number of branch tips and

181 the ecological volume [10]. The number of branch tips ranged from zero to 120 (mean = 9.9),

182 with more than half of all corals having ≤3 branch tips (Fig. 4A). The ecological volume ranged

183 from 0.25 to 8008 cm3 (mean = 366.3; Fig. 4B). The two parameters were positively correlated

184 (r2=0.39; p<0.0001; Fig. 4C), but the number of branch tips varied substantially among colonies


185 at higher ecological volumes. For example, the colony in Fig. 4D occupies about 73% of the

186 ecological volume of the colony in Figure 4E (960 vs. 1320 cm3), but it has over 8x as many

187 branch tips (65 vs. 8).

188 To examine the distribution of Porites colonies by size, we divided all corals into four

189 size categories based on branch number (0; 1-10; 11-40; >40) and four categories based on

190 ecological volume (1-10; 10-100; 100-1000; 1000-10000 cm3; Fig. 5). Regardless of whether

191 colonies were categorized according to branch number or ecological volume, the categories were

192 not distributed equally among shoreline regions (for branch number: (6) = 40.05, p<0.005; for

193 ecological volume: (6) = 25.49, p<0.005). Nearly all of the colonies lacking branches (19/20)

194 were found in the western section of the north shore of Calabash channel (Fig. 5A, B). By

195 contrast, nearly all of the colonies with >40 branches (4/5) were found in the stretch of shoreline

196 encompassing the eastern bank of the creek and the southern bank of the channel (Fig. 5A, C).

197 In addition to our targeted search for corals living on mangrove roots, we undertook a

198 longitudinal, transect-based survey of mangrove roots at Calabash, which would allow us to

199 estimate the frequency of mangrove roots bearing corals along stretches of shoreline where

200 corals were observed. Of the 60 roots we surveyed in both 2013 and 2014 (labeled 1-6 in Fig.

201 1B), 57 did not bear any corals in either 2013 or 2014; the roots lacking corals included 20 of 20

202 roots sampled along the east bank of Calabash Creek, 20 of 20 along the south shore of Calabash

203 Channel, and 17 of 20 (85%) along the north shore of Calabash Channel. In both 2013 and 2014,

204 one root along the north shore of Calabash Channel was found to harbor a single coral colony

205 (Fig. 6A, B), while a second root was found to harbor 4 coral colonies (Fig. 6C-E). In our 2013

206 survey, we identified a single unbranched colony on root 2-7. This colony cannot be seen in the

207 images recorded in 2014.


208 Given their comparable locations on the same mangrove roots, we conclude the colonies

209 found in 2013 are the same colonies identified in 2014 (Fig. 6), and therefore, it is possible to

210 make inferences about change in colony shape and size in the intervening year. Among the five

211 corals we can compare between years, there are colonies that appear to have lost branches and

212 colonies that appear to have gained branches. In the single coral located on root 1-9 (the ninth

213 root sampled on transect one) a substantial section of the colony appears to have been lost

214 between 2013 and 2014 (see dashed line in Fig. 6A). By contrast, coral 1 on root 2-3 appears to

215 have erupted new branches near its point of attachment with the mangrove root (compare dashed

216 circles in Fig 6C and 6E).

217

218 Species diversity of corals at Crooked Creek

219 To determine whether the coral diversity on mangroves at Calabash Caye was representative of

220 Turneffe Atoll, we surveyed the mangroves lining Crooked Creek, a high-flow channel on the

221 western edge of Turneffe Atoll (Fig. 1C). In sharp contrast to Calabash Caye, at Crooked Creek,

222 we were able to tentatively identify nine coral species in addition to branching Porites (Table 1).

223 These included Porites astreoides, Dichocoenia stokesii, Orbicella faveolata and Siderastrea

224 siderea (Fig. 7). Fire coral (Millepora alcicornis), a member of the cnidarian class Hydrozoa,

225 was also abundant at Crooked Creek (Fig. 7) but absent from the mangroves we surveyed at

226 Calabash.

227228 Discussion

229 Mangroves are generally regarded as unsuitable habitat for scleractinians, and, as a result,

230 few studies have focused on the abundance and diversity of corals living on or among mangrove

231 prop roots [5, 7, 8]. There are a handful of references to corals occupying mangrove roots in


232 general studies on mangrove biodiversity [14-17]. For example, in their authoritative analysis of

233 mangrove epibionts at four cays off the coast of southern Belize, Farnsworth and Ellison

234 included two corals among the species list in the appendix (Porites astreoides and Diploria

235 strigosa), but they did not mention corals in the text [16]. In their biotic survey of the Pelican

236 Cays, McIntyre et al. reported corals inhabiting mangrove roots at five sites [4]. In one mangrove

237 pond, the prop roots supported a few colonies of Agaricia sp., while in another pond, a single

238 large colony of Siderastrea siderea was found inhabiting mangrove roots. In three other sites,

239 “corals” were listed among the members of the mangrove root community, but no species were

240 identified by name [4]. In a biotic survey of Twin Cays, also in southern Belize, Rützler and co-

241 workers reported corals occupying mangrove prop roots at three of 20 observation stations. The

242 species identified on mangrove roots were Diploria strigosa, Porites astreoides, and P. porites

243 [17].

244 In contrast to these general studies of mangrove biodiversity, recent studies in St. John and

245 Cuba have focused explicitly on corals. These studies have demonstrated that diverse coral

246 assemblages can thrive on and among mangroves [5-8], thus raising the question of how

247 important mangroves might be for particular coral species. Mangroves could prove critical to the

248 long term health of certain coral populations, perhaps especially during periods of extreme

249 environmental stress on nearby reef habitats [6, 7]. If this proves true, we may begin to regard

250 mangroves as part of the ecological niche for some coral species [18]. Alternatively, mangroves

251 may represent marginal habitat for corals with little impact on regional abundance or species’

252 resilience, even for those species that occur in mangroves regularly.

253 Understanding the importance of mangroves as coral habitat will require studies on coral

254 abundance and diversity from many more sites. Given the existing data (Table 1), it appears that


255 corals are widespread on mangroves, but mangrove coral assemblages can differ substantially

256 between sites. At Calabash Caye, all of the corals we identified were branching Porites,

257 representing at most two nominal species (P. divaricata and P. furcata), making it the least

258 diverse mangrove coral fauna so far described. The most diverse site described to date, Hurricane

259 Hole, boasts 34-36 distinct species (depending upon whether P. divaricata, furcata, and porites

260 prove to be valid species)[7]. Of note, the published studies from Hurricane Hole do not specify

261 in every instance whether a particular species was found attached directly to mangrove prop

262 roots, on the peat shelf immediately below mangrove prop roots, or on some other substratum in

263 one of the mangrove lined bays and creeks that were studied [7]. This distinction is potentially

264 important when identifying suitable habitat for a given species. Intermediate levels of coral

265 diversity were observed at five sites in Cuba (4-9 species; [5, 7]) and at Crooked Creek, where

266 we observed 10-12 different species (depending upon resolution of the branching Porites).

267 Branching Porites have been reported at every mangrove site where corals have been

268 systematically surveyed (Table 1), which suggests that this may among those corals most tolerant

269 of the mangrove forest environment.

270 With existing data we cannot ascertain definitively why some mangrove sites have high

271 coral diversity, some sites have low coral diversity, and some sites are lacking corals entirely.

272 The biodiversity of mangrove epibiont communities is driven by a combination of processes

273 operating at different scales [16]. Key environmental parameters such as light, flow, and the

274 abundance of predators can vary substantially between adjacent prop roots and even within a

275 single root.

276 However, based on this study and previous studies on mangrove epibiont communities, it

277 appears that flow is likely to be a major determinant of a mangrove site’s suitability for corals.


278 While a detailed analysis of water flow was beyond the scope of our study, we observed a

279 qualitative difference in the current between Seahorse Pond, where we found no corals, and

280 Calabash Channel, where we found 85% of the corals identified in our study. Within Seahorse

281 Pond, there was no perceptible current, at least none sufficient to displace a snorkeler or a small

282 buoy. The stillness of the water was further evidenced by a nearly ubiquitous layer of fine

283 sediment covering the sessile epibionts on the mangrove roots, a layer that was easily dislodged

284 by the current from a passing snorkeler. By contrast, in the channel, snorkelers had to actively

285 swim against the current to maintain their positions relative to the bank, and the sessile epibionts

286 inhabiting the mangrove roots were not covered in sediment. Other recent studies on low flow

287 mangrove sites are consistent with the absence of corals in the low-flow Seahorse Pond. Ruiz et

288 al. characterized more than 59,000 macroinvertebrate epibionts inhabiting prop roots in a low-

289 flow coastal mangrove pond in Mexico, and did not report a single coral specimen [19], and

290 Yates et al. reported finding no corals in the most interior portion of three embayments at

291 Hurricane Hole [7].

292 Another factor that we suspect is impacting coral diversity in the mangroves is the fine-

293 scale topography of the shoreline. Along the northern bank of Calabash Channel where we

294 observed many branching Porites but no other species, there was a pronounced undercut in the

295 peat bank, and the overhanging prop roots effectively shaded a habitat of mixed peat bank. By

296 contrast, at Crooked Creek, the coral-bearing areas were characterized by a shallow, well-lit peat

297 bank and carbonate platform that was occupied by numerous coral colonies, some of which

298 extended from the bank to the prop roots (Fig. 7A, F). This microhabitat is similar to that

299 depicted in the photographs of mangrove corals in St. John [5, 7] and Cuba [8]. We suspect that

300 the broad, shallow, well-lit shelf observed at these sites can support a more diverse coral


301 assemblage by providing a larger settlement area for corals and by allowing some species to

302 colonize the mangrove fringe that might not be well suited to settle and/or grow to substantial

303 size directly on the prop roots themselves.

304 To understand the importance of mangrove populations for the regional abundance of

305 corals—and whether mangroves might serve as refuges during periods of environmental stress—

306 we will require data on the growth, health, reproductive output, and temporal variability of coral

307 populations living in mangroves, as well as their relationship to populations in nearby reef

308 habitats. The current study begins to address these needs by obtaining baseline data on the size

309 and location of individual mangrove corals. By identifying a range of colony sizes, and

310 documenting the persistence of individual colonies from year-to-year, we have shown that

311 branching Porites can settle, survive, grow, and presumably reproduce in the channel and creek

312 habitats at Calabash Caye. We are in the process of acquiring additional longitudinal data (1) to

313 track the growth and survival of individual corals, (2) to determine how these life history traits

314 might be impacted by microhabitat, (3) to determine how this population fluctuates over time, (4)

315 to determine whether it is self-sustaining or requires constant immigration from adjacent “core”

316 habitats, and (5) to determine whether this site may export larvae to nearby reef and seagrass

317 habitats.

318 Branching Porites appear particularly adept at colonizing mangroves, and we suspect that

319 phenotypic plasticity is critical to their ability to tolerate a range of environments, from high

320 irradiance sites in shallow reefs, to shaded locations in the mangroves. The colony form of

321 branching corals has been shown to be strongly impacted by features of the physical

322 environment, particularly water flow and irradiance [20]. It is therefore noteworthy that our

323 study has detected substantial variation in colony form among branching Porites in the


324 mangroves at Calabash, namely a 10-fold difference in the number of branch tips found in corals

325 at a similar ecological volume. At this time, we lack the data necessary to determine the relative

326 contributions of fixed genetic differences and phenotypic plasticity to the range of colony forms

327 we observed. To address this question, we are currently working to determine the genetic

328 relatedness and characterize the microhabitat of colonies exhibiting alternative morphologies.

329 We are also monitoring the development of recent recruits to document their growth patterns,

330 and how growth relates to microhabitat. Finally, we are conducting reciprocal transplants to

331 directly test the capacity for phenotypic plasticity.

332 Going forward, we hope that this study will contribute to our understanding of the

333 importance of mangrove habitats for coral resilience. Future studies will be required to determine

334 if the utilization of mangroves by corals is predictable and deterministic or stochastic. If we

335 discover that mangrove populations make important contributions to the long-term survival of

336 some coral species, and that the type of mangrove habitat utilized by these corals is predictable,

337 this information could prove vitally important to marine resource managers in the design of

338 marine protected areas.

339

340 Acknowledgments

341 This research was conducted by students and faculty participating in the Marine Semester

342 offered by the Boston University Marine Program (BUMP) and Biology Department. The

343 research was conducted at the Calabash Caye Field Station (CCFS), Environmental Research

344 Institute, University of Belize. We are grateful to the staff of BUMP (D. Brown, J. Hammer-

345 Mendez, J. Perry, and J. Scace), the staff of CCFS (M. Alamina, V. Alamina, A. Cherrington, N.

346 Craig, C. Encalada, J. Hall, J. Morey) and colleagues from UB (L. Cho-Ricketts, E. Garcia) for


347 their technical expertise and logistical support. We are grateful to J. Azueta and I. Majil at the

348 Belize Fisheries Department for assistance in obtaining research permits. We thank J. Lang for

349 assistance in identifying corals. EAR was supported by a summer research fellowship from the

350 Undergraduate Research Opportunities Program at Boston University.

351

352


353 References

354 1. Martin TSH, Olds AD, Pitt KA, Johnston AB, Butler IR, Maxwell PS, et al. Effective protection 355 of fish on inshore coral reefs depends on the scale of mangrove-reef connectivity. Mar Ecol Prog Ser. 356 2015;527:157-65.357 2. Nagelkerken I, Blaber SJM, Bouillon S, Green P, Haywood M, Kirton LG, et al. The habitat 358 function of mangroves for terrestrial and marine fauna: A review. Aquat Bot. 2008;89:155-85.359 3. Diaz MC. Mangrove and coral reef sponge faunas: untold stories about shallow water Porifera in 360 the Caribbean. Hydrobiologia. 2012;687:179-90.361 4. Macintyre IG, Goodbody I, Rützler K, Littler DS, Littler MM. A general biological and 362 geological survey of the rims of ponds in the major mangrove islands of the Pelican Cays, Belize. Atoll 363 Res Bull. 2000;467:13-44.364 5. Rogers CS. High diversity and abundance of scleractinian corals growing on and near mangrove 365 prop roots, St. John, US Virgin Islands. Coral Reefs. 2009;28:909.366 6. Rogers CS, Herlan JJ, editors. Life on the edge: corals in mangroves and climate change. 12th 367 International Coral Reef Symposium; 2012; Cairns, Australia.368 7. Yates KK, Rogers CS, Herlan JJ, Brooks GR, Smiley NA, Larson RA. Diverse coral 369 communities in mangrove habitats suggest a novel refuge from climate change. Biogeosciences. 370 2014;11:4321-37.371 8. Hernández-Fernández. Stony corals on submerged mangrove roots of Rhizophora mangle L. in 372 Jardines de la Reina National Park, Cuba. unknown. 2015:in press.373 9. Prada C, DeBiasse MB, Neigel JE, Yednock B, Stake JL, Forsman ZH, et al. Genetic species 374 delineation among branching Caribbean Porites corals. Coral Reefs. 2014;33:1019-30.375 10. Shaish L, Abelson A, Rinkevich B. Branch to colony trajectory in a modular organism: pattern 376 formation in the Indo-Pacific coral Stylophora pistillata. Developmental dynamics : an official 377 publication of the American Association of Anatomists. 2006;235:2111-21.378 11. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat 379 Methods. 2012;9:671-5.380 12. Clark PJ, Evans FC. Distance to nearest neighbor as a measure of spatial relationships in 381 populations. Ecology. 1954;35:445-53.382 13. Clark PJ, Evans FC. Generalization of a nearest neighbor measure of dispersion for use in k-383 dimensions. Ecology. 1979;60:316-7.384 14. Nagelkerken I, Blaber SJM, Bouillon S, Green P, Haywood M, Kirton LG, et al. The habitat 385 function of mangroves for terrestrial and marine fauna: A review. Aquat Bot. 2008;89:155-85.386 15. Kathiresan K, Bingham B. Biology of mangroves and mangrove ecosystems. Adv Mar Biol. 387 2001;40:81–251.388 16. Farnsworth EJ, Ellison AM. Scale-dependent spatial and temporal variability in biogeography of 389 mangrove root epibiont communities. Ecol Monogr. 1996;66:45-66.390 17. Rützler K, Goodbody I, Diaz MC, Feller IC, Macintyre IG. The aquatic environment of Twin 391 Cays, Belize. Atoll Res Bull. 2004;512.392 18. Kawecki TJ. Adaptation to marginal habitats. Annu Rev Ecol Evol S. 2008;39:321-42.393 19. Ruiz M, López-Portillo J. Variación espacio-temporal de la comunidad de macroinvertebrados 394 epibiontes en las raíces del mangle rojo Rhizophora mangle (Rhizophoraceae) en la laguna costera de La 395 Mancha, Veracruz, México. Int J Trop Biol. 2014;62:1309-30.396 20. Todd PA. Morphological plasticity in scleractinian corals. Biol Rev Camb Philos Soc. 397 2008;83:315-37.

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Table 1(on next page)

Species diversity of corals in mangrove habitats of the Caribbean


Table 1. Species diversity of corals in mangrove habitats of the Caribbean Species HH BS LA M-n M-s Ni Ca CC TC

Acropora palmata X Agaricia agaricites X X X X Agaricia sp. X X X X Cladocora arbuscula X Colpophyllia amaranthus X Colpophyllia natans X Dendrogyra cylindrus X Dichocoenia stokesii X X X X X X Diploria labyrinthiformis X Eusmilia fastigiata X Favia fragum X X X X X Madracis auretenra X Manicina areolata X X Meandrina meandrites X Milleopora alcicornis X X X X Montastrea cavernosa X Mycetophillia species X X Oculina diffusa X Orbicella annularis X Orbicella faveolata1 X X Orbicella franksi X Phyllangia americana X Porites astreoides, X X X X X X X X Porites, branching P. divaricata X X X X X X X X P. furcata X X X X X P. porites X X X X X X Porites colonensis X Pseudodiploria clivosa X Pseudodiploria strigosa X X Scolymia cubensis X Scolymia lacera X Siderastrea radians X X Siderastrea siderea X X Solenastrea bournoni X Stephanocoenia intersepta X Stephanocoenia species X Tubastrea aurea X Tubastrea coccinea X TOTAL SPECIES2 34-36 5 4-5 6-7 7-9 6-7 1-2 10-12 3 1referred to as Montastrea faveolata; 2a range is given depending on whether branching Porites are counted as one species or multiple species; 3not all corals found on mangrove roots in this study were identified by species. US Virgin Islands [5]: HH=Hurricane Hole; Cuba [8]: BS=Boca Stone; LA=Las Auras, M-n=Mariflores north, M-s=Mariflores south, Ni=Nicola; Belize: TC=Twin Cays [4]; Ca=Calabash Caye [the current study]; CC=Crooked Creek [the current study].


Table 2(on next page)

Clark-Evans analysis of dispersion


Table 2. Clark-Evans analysis of dispersion

Shoreline Corals Span RA RE RA/RE σRE C p N. Channel1 108 1100m 1.66 m 5.09 m 0.33 0.49 6.99 <0.001 S. Channel2 14 550m 10.00 m 16.18 m 0.62 3.92 1.57 0.116

1includes Seahorse pond; 2includes eastern shore of Calabash Creek; RA = actual mean nearest-neighbor distance; RE = expected mean nearest-neighbor distance; σRE = the standard error of the mean distance to nearest neighbor in a randomly distributed population with a known density; c= the standard variate of the normal curve


1Overhead view of study sites

(A) The locations of mangrove roots that were inspected for the presence of corals are shown

for (B) Calabash Caye and (C) Crooked Creek. At Calabash Caye, the survey area was divided

between three discontinuous stretches of mangrove: (1) the shoreline of Seahorse Pond

which is contiguous with the northern shoreline of Calabash Channel; (2) the eastern edge of

Calabash Creek which is contiguous with the southern shore of Calabash Channel; (3) the

western edge of Calabash Creek. In panel B, the white diamonds labeled a-g indicate the

approximate locations of temperature loggers, and the white lines labeled 1-6 indicate the

approximate locations of 30m transects. In panel C, the red lines indicate the shoreline that

was surveyed for corals.


2Representative photographs of Porites inhabiting prop roots

The images depict a specimen that has not yet developed any branches (A) as well as larger

colonies with eight (B) or more than 20 (C) branches. A 5-cm scale bar is shown in each

photograph.


3Plot of coral locations

(A) Along three stretches of shoreline (yellow, blue, and green lines), we identified 40 prop

roots bearing corals (circles). (B-D) The graphs indicated the number of corals found at each

point along the three transects.


4Coral dimensions

(A) Number of corals with a given number of branches. (B) Number of corals with a given

ecological volume. (C) Linear regression of branch number versus ecological volume.

Photographs of two of the individual corals represented in this plot (red circles) are shown (D-

E).


5Geographic distribution of coral size classes at Calabash

(A) All corals along three stretches of shoreline (B-D) were placed into one of four size

categories based upon the number of branch tips and one of four size categories based upon

ecological volume. The pie charts indicate the proportion (and number) of corals in each size

category for branch tips and for ecological volume for each stretch of shoreline. The same

color scheme is used as in Fig. 3.


6Visual comparison of the same coral colonies in 2013 and 2014

The single coral observed on mangrove root 1-9 is shown in 2013 (A) and 2014 (B). The

corresponding sections of the coral colony are given the same number in each panel (1-3).

The arrow indicates what appears to be the identical sponge species in the same location

relative to the colony in both photographs. The dashed line in (A) indicates a region of the

colony that was lost between 2014 and 2014 (B). The five corals observed on root 2-3 are

shown for both 2013 (C, D) and 2014 (E). The presumed correspondence between colonies,

based on their relative locations along the root, is indicated by the numbering (1-5). The

dashed circles on colony 1 in 2013 (C) indicate protuberances near the base of the colony

that appear to be located in the same relative positions as the bases of two erupting

branches in 2014 (E). The asterisks (C, D) indicate branches that have experienced breakage.


7Coral diversity at Crooked Creek

Representative photos of corals observed at Crooked Creek. (A) PA: Porites astreiodes; (B)

bP: branching Porites; DS: Dichocoenia stokesii; (C) PA: Porites astreiodes; (D) OF: Orbicella

faveolata; SS: Siderastrea siderea; (E) MA: Milleopora alcicornis (a hydrozoan); (F) DS:

Dichocoenia stokesii;


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