4. Morphology and phenotypic plasticity

In coral reefs, some calcifying species, such as corals and hydrocorals, are known to have a high degree of morphological plasticity in response to hydrodynamic changes and light availability, which strongly influences their performance, including resource acquisition and light capture, thereby benefiting colony growth, reproduction and survival [168]. Branching and plating growth forms grow quickly into large arborescent colonies in shallow reef environments, where irradiance is high and water flow is low, which makes them effective competitors for space [169, 170], light and food [171]. However, this growth strategy renders them extremely vulnerable to breakage when large waves and storm events occur, often resulting in fragmentation or coral mortality [172, 173]. Intraspecific morphological variation has been reported in many colonial reef organisms in response to environmental gradients, which ultimately affect their survival and growth [174–177]. Such plastic developmental responses are often induced during ontogeny of modular organisms with persistent effect on adult phenotypes [178]. These phenotypic responses can also change independently from the genetic background of reef corals (acclimatization), but they often rely on a genetic basis (adaptation) [179, 180].

Fire coral species are also known for their extensive morphological variability and vulnerability to fragmentation varies greatly among their morphologies [51, 58, 91, 181]. Examples include variations in growth forms of M. cf. platyphylla colonies that were found in distinct reef environments at Moorea; the fore reef at 15 and 6 m depth (mid and upper slope, respectively), the back and fringing reefs [58, 91]. Colonies on the mid slope and back reef were mostly encrusting, while the massive morphology was dominant in the fringing and patch reefs (Figure 7A, B). The sheet tree morphology of M. cf. platyphylla [182], the most vulnerable to wave-induced breakage, was nearly exclusive to colonies encountered in the upper slope (Figure 7C), where waves can break the blades, while the encrusting bases remain intact [181].

that fire corals being susceptible to wave-induced breakage have benefits in terms

Graphical abstract showing the occurrence of phenotypic plasticity among fire coral clones, where clones of the same genotype display different morphologies across distinct reef habitats [58]. Geographic coordinates of each georeferenced colony collected in the three reef habitats are shown in meters on the x and y axes. On the left side: each genotype is represented by a unique color; on the right side: colonies with encrusting morphology are shown

Although only a few species are exclusively reproducing asexually, clonality has evolved repeatedly in many reef organisms (e.g. [183–186]). In coral reef ecosystems, there are many organisms that can reproduce through both sexual and asexual reproduction, including scleractinian corals [187], hydrocorals [58], hydroids [188], coralline algae [189], sea anemones [190], sea cucumbers [191], gorgonians [192] and sponges [193]. Asexual reproduction produces genetically identical offspring, often leading in local populations dominated by few adapted clones [194–196]. In the contrary, sexual reproduction enables genetic recombination and production of genetically diverse propagules, thus generating the genotypic variation required for adaptation [197] and colonization of new habitats [198]. In many colonial reef organisms, asexual reproduction can occur through fragmentation, fission, budding, polyp expulsion or polyp bail-out [187, 199–201], while sexual reproduction often involves a wide range of reproductive strategies, i.e. gonochorism, hermaphroditism, internal (brooders) and external (spawners) fertilization [187, 202].

Despite their ecological importance to the ecosystem functioning of coral reefs, Millepora hydrocorals have been relatively understudied and information regarding their reproduction and dispersal patterns remain scarce. Fire corals are gonochoric broadcast spawners that reproduce sexually by producing medusoids and planula larvae (Figure 9). They also rely on asexual reproduction through fragmentation [58, 181], but the production of asexual larvae has never been documented within

this genus though described for some Pocillopora species [203, 204].

of reproduction outweighing the costs of getting injured.

in orange, massive in green and the vulnerable sheet tree morphology in grey.

Ecology, Biology and Genetics of Millepora Hydrocorals on Coral Reefs

DOI: http://dx.doi.org/10.5772/intechopen.89103

5. Reproduction

Figure 8.

27

5.1 Reproductive strategies

To date, the flexibility for a single genotype to produce a range of phenotypic responses to distinct environmental conditions (i.e. phenotypic plasticity) has rarely been documented in natural marine populations, mostly because of the difficulty in identifying naturally occurring clonal genotypes across variable environments. Dubé and colleagues [58] have described the first example of phenotypic plasticity among fire coral clones, where clones of the same genotype display different morphologies across distinct reef habitats (Figure 8). The fire coral M. cf. platyphylla seems to invest in a vulnerable morphology that increases the contribution of asexual reproduction through fragmentation in high-energy reef habitats. This is a unique example of phenotypic plasticity as corals typically have wavetolerant growth forms in such dynamic reefs. Such phenotypic responses suggest

#### Figure 7.

Morphologies of M. cf. platyphylla colonies in habitats experiencing contrasting hydrodynamic regimes. (A) Massive wave-tolerant morphology in the patch reef, a lagoonal habitat (photograph is courtesy of Gilles Siu); (B) encrusting wave-tolerant morphology in the back reef, a lagoonal habitat at <1 m depth and (C) sheet tree morphology vulnerable to wave-induced breakage in the upper slope, a fore reef habitat at 6 m.

Ecology, Biology and Genetics of Millepora Hydrocorals on Coral Reefs DOI: http://dx.doi.org/10.5772/intechopen.89103

#### Figure 8.

4. Morphology and phenotypic plasticity

Invertebrates - Ecophysiology and Management

[179, 180].

Figure 7.

26

In coral reefs, some calcifying species, such as corals and hydrocorals, are known to have a high degree of morphological plasticity in response to hydrodynamic changes and light availability, which strongly influences their performance, including resource acquisition and light capture, thereby benefiting colony growth, reproduction and survival [168]. Branching and plating growth forms grow quickly into large arborescent colonies in shallow reef environments, where irradiance is high and water flow is low, which makes them effective competitors for space [169, 170], light and food [171]. However, this growth strategy renders them extremely vulnerable to breakage when large waves and storm events occur, often resulting in fragmentation or coral mortality [172, 173]. Intraspecific morphological variation has been reported in many colonial reef organisms in response to environmental gradients, which ultimately affect their survival and growth [174–177]. Such plastic developmental responses are often induced during ontogeny of modular organisms with persistent effect on adult phenotypes [178]. These phenotypic responses can also change independently from the genetic background of reef

corals (acclimatization), but they often rely on a genetic basis (adaptation)

Fire coral species are also known for their extensive morphological variability and vulnerability to fragmentation varies greatly among their morphologies [51, 58, 91, 181]. Examples include variations in growth forms of M. cf. platyphylla colonies that were found in distinct reef environments at Moorea; the fore reef at 15 and 6 m depth (mid and upper slope, respectively), the back and fringing reefs [58, 91]. Colonies on the mid slope and back reef were mostly encrusting, while the massive morphology was dominant in the fringing and patch reefs (Figure 7A, B). The sheet tree morphology of M. cf. platyphylla [182], the most vulnerable to wave-induced breakage, was nearly exclusive to colonies encountered in the upper slope (Figure 7C), where waves can break the blades, while the encrusting bases remain intact [181]. To date, the flexibility for a single genotype to produce a range of phenotypic responses to distinct environmental conditions (i.e. phenotypic plasticity) has rarely been documented in natural marine populations, mostly because of the difficulty in identifying naturally occurring clonal genotypes across variable environments. Dubé and colleagues [58] have described the first example of phenotypic plasticity among fire coral clones, where clones of the same genotype display different morphologies across distinct reef habitats (Figure 8). The fire coral M. cf. platyphylla seems to invest in a vulnerable morphology that increases the contribution of asexual reproduction through fragmentation in high-energy reef habitats. This is a unique example of phenotypic plasticity as corals typically have wavetolerant growth forms in such dynamic reefs. Such phenotypic responses suggest

Morphologies of M. cf. platyphylla colonies in habitats experiencing contrasting hydrodynamic regimes. (A) Massive wave-tolerant morphology in the patch reef, a lagoonal habitat (photograph is courtesy of Gilles Siu); (B) encrusting wave-tolerant morphology in the back reef, a lagoonal habitat at <1 m depth and (C) sheet tree

morphology vulnerable to wave-induced breakage in the upper slope, a fore reef habitat at 6 m.

Graphical abstract showing the occurrence of phenotypic plasticity among fire coral clones, where clones of the same genotype display different morphologies across distinct reef habitats [58]. Geographic coordinates of each georeferenced colony collected in the three reef habitats are shown in meters on the x and y axes. On the left side: each genotype is represented by a unique color; on the right side: colonies with encrusting morphology are shown in orange, massive in green and the vulnerable sheet tree morphology in grey.

that fire corals being susceptible to wave-induced breakage have benefits in terms of reproduction outweighing the costs of getting injured.

## 5. Reproduction

#### 5.1 Reproductive strategies

Although only a few species are exclusively reproducing asexually, clonality has evolved repeatedly in many reef organisms (e.g. [183–186]). In coral reef ecosystems, there are many organisms that can reproduce through both sexual and asexual reproduction, including scleractinian corals [187], hydrocorals [58], hydroids [188], coralline algae [189], sea anemones [190], sea cucumbers [191], gorgonians [192] and sponges [193]. Asexual reproduction produces genetically identical offspring, often leading in local populations dominated by few adapted clones [194–196]. In the contrary, sexual reproduction enables genetic recombination and production of genetically diverse propagules, thus generating the genotypic variation required for adaptation [197] and colonization of new habitats [198]. In many colonial reef organisms, asexual reproduction can occur through fragmentation, fission, budding, polyp expulsion or polyp bail-out [187, 199–201], while sexual reproduction often involves a wide range of reproductive strategies, i.e. gonochorism, hermaphroditism, internal (brooders) and external (spawners) fertilization [187, 202].

Despite their ecological importance to the ecosystem functioning of coral reefs, Millepora hydrocorals have been relatively understudied and information regarding their reproduction and dispersal patterns remain scarce. Fire corals are gonochoric broadcast spawners that reproduce sexually by producing medusoids and planula larvae (Figure 9). They also rely on asexual reproduction through fragmentation [58, 181], but the production of asexual larvae has never been documented within this genus though described for some Pocillopora species [203, 204].

#### Figure 9.

Millepora life cycle. Millepora hydrocorals are gonochoric broadcast spawners that reproduce sexually by producing medusoids and planula larvae. The medusoids release the gametes in the water column for external fertilization. The ciliate larvae sink and crawl on the reef substratum and metamorphose in a new calcifying polyp, founder of a new colony. Millepora also relies on clonal propagation through fragmentation and grow via asexual budding.

#### 5.2 Spawning, medusoids and larval development

Milleporid sexual reproduction is seasonal [69]. Millepora colonies become mature during the spring or summer (or austral summer for the southern hemisphere). Sexual reproduction period is usually correlated with the increase of the sea water temperature [69, 70, 205, 206], but some studies based on ampullae observations suggest a reproduction throughout the year [207–209]. Spawning occurs at different dates according to species, preventing hybridization [69, 70, 206]. The empty ampullae are visible during 1–2 months on the colonies (Figure 10D) before the skeleton reconstruction.

the ripe gametes in the water column. The spawning of gametes is therefore almost synchronous with the release of medusoids. Spawning always begins before dark, but is not correlated with the lunar or tidal cycles [69, 70, 206]. In shallow water of Reunion Island, Indian Ocean (reef flat), a unique massive spawning event was observed in situ for M. cf. exaesa and M. cf. platyphylla during the reproductive period, in December for the former species and in January for the later one [69]. Conversely, M. tenera seems to spawn regularly but not massively during 2 months

of the austral summer, resulting in the observation of both closed and open ampullae on fertile colonies during the reproduction season. Likewise, Nomura [205] and Soong and Cho [206] described several medusoid batches in different Millepora species in controlled conditions during the reproductive season in Japan and Taiwan, respectively. Recently, Shlesinger and Loya [70] described massive spawning events in the Red Sea (Gulf of Eilat/Aqaba) for three species, M. dichotoma, M. exaesa and M. platyphylla. Their field observations during the reproductive period (from June to September 2016–2018) also showed one or two spawning events per year for M. exaesa and M. platyphylla, while M. dichotoma colonies released their medusae massively, 4–6 times during the reproductive season. The higher reproductive output of M. dichotoma might be in relation with its

Before, during and after medusoid release in M. cf. exaesa in Reunion Island (modified from [69]). (A) Ampullae showing a small opening resulting in skeleton dissolution few days before the medusoid release. Notice that the cyclosystems have disappeared because of the high ampulla density; (B) medusoids protruding through the open ampullae and (C) male medusoid release with the umbrella opening towards the surface. Notice the big tentacular bulbs with refringent nematocyst and the sperm sac filling the subumbrellar cavity; (D) empty ampullae visible during 1–2 months after the massive medusoid release event. A, B and C

photographs were taken using a stereomicroscope; photograph D was taken underwater.

Ecology, Biology and Genetics of Millepora Hydrocorals on Coral Reefs

DOI: http://dx.doi.org/10.5772/intechopen.89103

Figure 10.

29

The sexual reproduction process begins with the growing of special cavities, called ampullae, developed in tissues and designing densely packed white dots on the coenosteum of the gonochoric colonies. These ampullae were first described by Quelch [210, 211] and further studied by Boschma [46, 207, 208, 212] and Moschencko [66]. Each ampulla contains one developing medusoid, i.e. a 'regressed'short-lived medusa, shed with mature gametes. Male and female medusoids are liberated after the disintegration of the dense network of the trabeculae covering the ampullae (Figure 10A–C). They have marginal bulbs but no tentacle, no circular or radial canal, no manubrium, no statocyst or any sense organ (Figures 10C and 11A), and they are not able to feed on zooplankton. On the contrary, as true medusae, they are able to actively swim with their muscle fibres distributed in the bell and display a velum. Gonads are attached to the short spadix and fill entirely the subumbrellar cavity. Female medusoids contain 2–5 zooxanthellate oocytes (Figure 11A) and male medusoids contain a spermatic mass (Figure 10C). The medusoids detach themselves from the fertile colonies by active bell pulsations in a few minutes and their swimming activity leads to the release of

Ecology, Biology and Genetics of Millepora Hydrocorals on Coral Reefs DOI: http://dx.doi.org/10.5772/intechopen.89103

#### Figure 10.

5.2 Spawning, medusoids and larval development

Invertebrates - Ecophysiology and Management

the skeleton reconstruction.

Figure 9.

28

via asexual budding.

Milleporid sexual reproduction is seasonal [69]. Millepora colonies become mature during the spring or summer (or austral summer for the southern hemisphere). Sexual reproduction period is usually correlated with the increase of the sea water temperature [69, 70, 205, 206], but some studies based on ampullae observations suggest a reproduction throughout the year [207–209]. Spawning occurs at different dates according to species, preventing hybridization [69, 70, 206]. The empty ampullae are visible during 1–2 months on the colonies (Figure 10D) before

Millepora life cycle. Millepora hydrocorals are gonochoric broadcast spawners that reproduce sexually by producing medusoids and planula larvae. The medusoids release the gametes in the water column for external fertilization. The ciliate larvae sink and crawl on the reef substratum and metamorphose in a new calcifying polyp, founder of a new colony. Millepora also relies on clonal propagation through fragmentation and grow

The sexual reproduction process begins with the growing of special cavities, called ampullae, developed in tissues and designing densely packed white dots on the coenosteum of the gonochoric colonies. These ampullae were first described by

'regressed'short-lived medusa, shed with mature gametes. Male and female medusoids are liberated after the disintegration of the dense network of the trabeculae covering the ampullae (Figure 10A–C). They have marginal bulbs but no tentacle,

Quelch [210, 211] and further studied by Boschma [46, 207, 208, 212] and Moschencko [66]. Each ampulla contains one developing medusoid, i.e. a

no circular or radial canal, no manubrium, no statocyst or any sense organ (Figures 10C and 11A), and they are not able to feed on zooplankton. On the contrary, as true medusae, they are able to actively swim with their muscle fibres distributed in the bell and display a velum. Gonads are attached to the short spadix and fill entirely the subumbrellar cavity. Female medusoids contain 2–5 zooxanthellate oocytes (Figure 11A) and male medusoids contain a spermatic mass (Figure 10C). The medusoids detach themselves from the fertile colonies by active bell pulsations in a few minutes and their swimming activity leads to the release of

Before, during and after medusoid release in M. cf. exaesa in Reunion Island (modified from [69]). (A) Ampullae showing a small opening resulting in skeleton dissolution few days before the medusoid release. Notice that the cyclosystems have disappeared because of the high ampulla density; (B) medusoids protruding through the open ampullae and (C) male medusoid release with the umbrella opening towards the surface. Notice the big tentacular bulbs with refringent nematocyst and the sperm sac filling the subumbrellar cavity; (D) empty ampullae visible during 1–2 months after the massive medusoid release event. A, B and C photographs were taken using a stereomicroscope; photograph D was taken underwater.

the ripe gametes in the water column. The spawning of gametes is therefore almost synchronous with the release of medusoids. Spawning always begins before dark, but is not correlated with the lunar or tidal cycles [69, 70, 206]. In shallow water of Reunion Island, Indian Ocean (reef flat), a unique massive spawning event was observed in situ for M. cf. exaesa and M. cf. platyphylla during the reproductive period, in December for the former species and in January for the later one [69]. Conversely, M. tenera seems to spawn regularly but not massively during 2 months of the austral summer, resulting in the observation of both closed and open ampullae on fertile colonies during the reproduction season. Likewise, Nomura [205] and Soong and Cho [206] described several medusoid batches in different Millepora species in controlled conditions during the reproductive season in Japan and Taiwan, respectively. Recently, Shlesinger and Loya [70] described massive spawning events in the Red Sea (Gulf of Eilat/Aqaba) for three species, M. dichotoma, M. exaesa and M. platyphylla. Their field observations during the reproductive period (from June to September 2016–2018) also showed one or two spawning events per year for M. exaesa and M. platyphylla, while M. dichotoma colonies released their medusae massively, 4–6 times during the reproductive season. The higher reproductive output of M. dichotoma might be in relation with its

In Hydrozoans, the reproductive output can vary between and within species, and can often depend on the colony size and environmental conditions [213, 214]. In Reunion Island, the ampulla density of M. cf. exaesa is positively correlated with the size of colonies, indicating that the reproductive output varies with the colony size. Global change also seems to influence the reproductive output of milleporids as the rate of fertile colonies have decreased considerably in the last 10 years at two

For most colonial reef species whose adults are sessile, their early life history includes a pelagic stage. These propagules represent the first step for successful recruitment and have profound implications for population dynamics and renewal, which ultimately affect their evolutionary history [215, 216]. Dispersal in colonial organisms is mostly mediated by the release of gametes and/or larvae during sexual reproduction events, together with the continuous supply in asexual propagules. In many reef species, the extent of dispersal is largely governed by the reproductive biology and early life history ecology. Molecular studies and oceanographic models have uncovered a wide range of dispersal patterns (i.e. dispersal kernels) in coral reefs, from populations primarily sustained by self-recruitment due to limited dispersal potential or retention, to ecologically significant gene flow and connectivity among adult populations [217]. In corals for instance, brooded larvae settle and metamorphose rapidly after being released, which is most likely to enhance local dispersal patterns, while broadcast larvae require a planktonic development phase and settle further away from the parental source [187]. On the other hand, clonal propagation can allow populations to expand locally under unfavorable conditions. Such conditions include fragmented [218], marginal [196] and highly disturbed habitats [186], where clonal reproduction reinforce local adaptation processes and population genetic heterogeneity due to restricted dispersal potential of asexual

Although local demography and self-recruitment have been shown to have major consequences on the genetic diversity and adaptive ability of reef organisms, empirical data of dispersal patterns in reef-building species remain scarce. Dubé and colleagues [221] documented the first genetic estimates of local dispersal and self-recruitment in a marine broadcasting species, the hydrocoral M. cf. platyphylla. They performed a parentage analysis that revealed a significant contribution from self-recruitment in addition to limited dispersal of sexual propagules on Moorea's reefs. Sexual propagules often settled at less than 10 m from their parents and dispersal events decreased with increasing geographic distances. Sibship analysis showed that full siblings recruit together on the reef, resulting in sibling aggregations. Such limited dispersal abilities in fire corals can be related to their early life history traits. Dispersion during the medusoid stage may not be as effective due to the short pre-competency period time of the hydromedusae in the water column [51, 181]. Other means of dispersal can occur through the propagation of asexual offspring, e.g. fragments that have broken and re-attached to the reef framework. Asexual reproduction through fragmentation in branching hydrocoral can be substantial during disturbances [51, 181] and may therefore contribute to dispersal. However, clonal fragments of the plate-like M. cf. platyphylla were found to be dispersed close to one another on a barrier reef (mean = 18 m), with clone distribution being perfectly aligned with wave energy dispersal [58]. The maximal distance between fragments of the same genotype in this plate-like species at

contrasting reef sites in Reunion Island (Bourmaud et al. in prep).

Ecology, Biology and Genetics of Millepora Hydrocorals on Coral Reefs

DOI: http://dx.doi.org/10.5772/intechopen.89103

5.3 Dispersal and recruitment

offspring [58, 219, 220].

Moorea Island was about 450 m.

31

#### Figure 11.

Gamete spawning, planula larva formation and settlement in Millepora spp. in Reunion Island (modified from [69]). (A) M. cf. platyphylla female medusoid releasing an oocyte through the velum while swimming. Notice the numerous zooxanthellae in the oocyte and spadix tissues; (B) M. cf. exaesa zooxanthellate (orange dots in endoderm) planula larva; (C) M. cf. exaesa larva finding a sustainable substrate to fix by the tapered pole before metamorphosis; (D) M. cf. exaesa recruit with the first pore. All photographs were taken using a stereomicroscope.

higher abundance in the Gulf of Eilat/Aqaba (i.e. M. dichotoma is the most abundant milleporid in the Gulf [70]).

The empty medusoids continue to swim for 1–3 h and die quickly while sinking and shrinking. Male and female medusoids are released synchronously (for a giving species), the spawning of the oocytes and spermatozoids is also simultaneous, and fertilization occurs rapidly. Embryogenesis and planula larvae formation occur in less than 12 h in aquarium [69]. Because of the presence of algal symbionts in oocytes, the planula larvae are zooxanthellate and have the potential to live for several weeks before settlement (more than 1 month in controlled conditions for M. cf. exaesa from Reunion Island). This feature is certainly a character to keep in mind to explain the large distribution of Millepora species in all oceans. M. cf. exaesa planula has been described as a bipolar ciliated larva with a wide anterior and tapered posterior, without a mouth and gastrovascular cavity (Figure 11B) [69]. The larva endoderm is full of lipid droplets and zooxanthellae. The larva sinks and crawls until it finds a sustainable substrate to fix and metamorphose (Figure 11C). This process leads to the formation of a calcareous structure surrounding the primary polyp, founder of a new colony by asexual budding (Figure 11D).

The reproductive output (ampulla density) is variable according to species and within species. Amaral and colleagues [75] found an average of 10 ampullae/ cm<sup>2</sup> for Millepora species occurring on Brazilian reefs, while the highest density was observed by Soong and Cho [206] in Taiwan with 84–120 ampullae/cm<sup>2</sup> .

Ecology, Biology and Genetics of Millepora Hydrocorals on Coral Reefs DOI: http://dx.doi.org/10.5772/intechopen.89103

In Hydrozoans, the reproductive output can vary between and within species, and can often depend on the colony size and environmental conditions [213, 214]. In Reunion Island, the ampulla density of M. cf. exaesa is positively correlated with the size of colonies, indicating that the reproductive output varies with the colony size. Global change also seems to influence the reproductive output of milleporids as the rate of fertile colonies have decreased considerably in the last 10 years at two contrasting reef sites in Reunion Island (Bourmaud et al. in prep).

#### 5.3 Dispersal and recruitment

For most colonial reef species whose adults are sessile, their early life history includes a pelagic stage. These propagules represent the first step for successful recruitment and have profound implications for population dynamics and renewal, which ultimately affect their evolutionary history [215, 216]. Dispersal in colonial organisms is mostly mediated by the release of gametes and/or larvae during sexual reproduction events, together with the continuous supply in asexual propagules. In many reef species, the extent of dispersal is largely governed by the reproductive biology and early life history ecology. Molecular studies and oceanographic models have uncovered a wide range of dispersal patterns (i.e. dispersal kernels) in coral reefs, from populations primarily sustained by self-recruitment due to limited dispersal potential or retention, to ecologically significant gene flow and connectivity among adult populations [217]. In corals for instance, brooded larvae settle and metamorphose rapidly after being released, which is most likely to enhance local dispersal patterns, while broadcast larvae require a planktonic development phase and settle further away from the parental source [187]. On the other hand, clonal propagation can allow populations to expand locally under unfavorable conditions. Such conditions include fragmented [218], marginal [196] and highly disturbed habitats [186], where clonal reproduction reinforce local adaptation processes and population genetic heterogeneity due to restricted dispersal potential of asexual offspring [58, 219, 220].

Although local demography and self-recruitment have been shown to have major consequences on the genetic diversity and adaptive ability of reef organisms, empirical data of dispersal patterns in reef-building species remain scarce. Dubé and colleagues [221] documented the first genetic estimates of local dispersal and self-recruitment in a marine broadcasting species, the hydrocoral M. cf. platyphylla. They performed a parentage analysis that revealed a significant contribution from self-recruitment in addition to limited dispersal of sexual propagules on Moorea's reefs. Sexual propagules often settled at less than 10 m from their parents and dispersal events decreased with increasing geographic distances. Sibship analysis showed that full siblings recruit together on the reef, resulting in sibling aggregations. Such limited dispersal abilities in fire corals can be related to their early life history traits. Dispersion during the medusoid stage may not be as effective due to the short pre-competency period time of the hydromedusae in the water column [51, 181]. Other means of dispersal can occur through the propagation of asexual offspring, e.g. fragments that have broken and re-attached to the reef framework. Asexual reproduction through fragmentation in branching hydrocoral can be substantial during disturbances [51, 181] and may therefore contribute to dispersal. However, clonal fragments of the plate-like M. cf. platyphylla were found to be dispersed close to one another on a barrier reef (mean = 18 m), with clone distribution being perfectly aligned with wave energy dispersal [58]. The maximal distance between fragments of the same genotype in this plate-like species at Moorea Island was about 450 m.

higher abundance in the Gulf of Eilat/Aqaba (i.e. M. dichotoma is the most abundant

Gamete spawning, planula larva formation and settlement in Millepora spp. in Reunion Island (modified from [69]). (A) M. cf. platyphylla female medusoid releasing an oocyte through the velum while swimming. Notice the numerous zooxanthellae in the oocyte and spadix tissues; (B) M. cf. exaesa zooxanthellate (orange dots in endoderm) planula larva; (C) M. cf. exaesa larva finding a sustainable substrate to fix by the tapered pole before metamorphosis; (D) M. cf. exaesa recruit with the first pore. All photographs were taken using a

mary polyp, founder of a new colony by asexual budding (Figure 11D).

The reproductive output (ampulla density) is variable according to species and within species. Amaral and colleagues [75] found an average of 10 ampullae/ cm2 for Millepora species occurring on Brazilian reefs, while the highest density was observed by Soong and Cho [206] in Taiwan with 84–120 ampullae/cm<sup>2</sup>

.

The empty medusoids continue to swim for 1–3 h and die quickly while sinking and shrinking. Male and female medusoids are released synchronously (for a giving species), the spawning of the oocytes and spermatozoids is also simultaneous, and fertilization occurs rapidly. Embryogenesis and planula larvae formation occur in less than 12 h in aquarium [69]. Because of the presence of algal symbionts in oocytes, the planula larvae are zooxanthellate and have the potential to live for several weeks before settlement (more than 1 month in controlled conditions for M. cf. exaesa from Reunion Island). This feature is certainly a character to keep in mind to explain the large distribution of Millepora species in all oceans. M. cf. exaesa planula has been described as a bipolar ciliated larva with a wide anterior and tapered posterior, without a mouth and gastrovascular cavity (Figure 11B) [69]. The larva endoderm is full of lipid droplets and zooxanthellae. The larva sinks and crawls until it finds a sustainable substrate to fix and metamorphose (Figure 11C). This process leads to the formation of a calcareous structure surrounding the pri-

milleporid in the Gulf [70]).

Invertebrates - Ecophysiology and Management

Figure 11.

stereomicroscope.

30

## 6. Modularity and growth

Modularity is a well-established life history strategy among colonial reef invertebrates, i.e. corals, gorgonians, sea anemones, hydroids, hydrocorals, bryozoans and sponges [222]. Modular organisms grow in size via the repeated, vegetative formation of genetically identical modules, referred to as asexual budding, whereby all modules are derived from the same initial zygote to form a colony [223, 224]. Colony size often correlates with many fitness advantages in response to both physical and biological stressors. For instance, larger colonies can survive better towards predation [225] and competition [226], and their fecundity is often increased due to the large number of polyps that contributes to sexual reproduction [227]. Modules usually remain physiologically interconnected, but may also separate from the colony through fission or fragmentation and persist as discrete units [228], thereafter reducing colony size. There are only few reports of growth rates in Millepora species [79, 92, 229–232] that are within the range reported in Acroporidae corals from western Atlantic region [233].

colony fragmentation contributed effectively to population growth (Figure 12), where a high number of clonal genotypes have the potential for phenotypic plasticity in response to environmental changes. Genetic data indicated that fragmentation is the dominant reproductive process generating the high abundance of fire corals at Moorea (80% of colonies were clones). Even small recruits were having multilocus genotypes identical to adults and were often positioned below the reef substratum, i.e. frequently on branches of dead coral colonies or side of crevices. These observations suggest that the successful recruitment of clones may be the result of clonal reproduction processes other than fragmentation, such as asexual planula larvae, because asexual fragments are less likely to re-attach on such inclined substrate. The release of ameiotic planula larvae was reported in a number of coral species [187], where larval behaviour allows the settlement of a new individual characterized by its mother genotype (clone mates). However, such clonal reproductive strategy has never been described for the Millepora genus, and requires further investigations. In Moorea, fire corals are sustained by a moderate degree of self-recruitment [221] suggesting that despite low gene flow, genetically diverse and locally adapted recruits can successfully establish high local population abundance via their subsequent growth, survival and fragmentation (as described in [244]). However, such populations are predicted to be vulnerable to severe disturbances owing to their isolation from potential source reefs and are often associated with increased extinction risks [245, 246]. A high potential for gene flow and connectivity has been revealed among islands of the Society Archipelago in French Polynesia for some scleractinian species (i.e. Moorea, Raiatea, Taha'a and Tahiti) [218]. Preliminary results from samples of M. cf. platyphylla collected in several islands from French

Ecology, Biology and Genetics of Millepora Hydrocorals on Coral Reefs

DOI: http://dx.doi.org/10.5772/intechopen.89103

Polynesia revealed significant genetic differentiation among archipelagos

ability.

Figure 12.

33

(Marquesas, Austral, Gambier, Society and Tuamotu, Boissin et al. unpublished), highlighting the importance of self-recruitment processes in population sustain-

Summary of life history strategies in M. cf. platyphylla at Moorea, French Polynesia. M. cf. platyphylla heavily relies on asexual reproduction through fragmentation for local replenishment (80% of the colonies are clones), allowing population growth and the persistence of a genotype over time. M. cf. platyphylla population is sustained via a significant contribution from self-recruitment (8–36% of juveniles are self-recruits). Mosaicism and chimerism also contribute in creating novel genotypic diversity at the population and individual levels.

Some marine modular organisms, e.g. corals and ascidians, can also grow larger and quicker via the fusion of distinct colonies [178], which results in genetically heterogeneous colony, also referred to chimera. In addition to chimerism, somatic mutations may arise within a colony, which also results in intracolonial genotypic variability. Both chimerism (fusion) and mosaicism (somatic mutation) were identified in fire corals [234, 235]. At Moorea, for instance, fusion between siblings is likely to occur as fire corals have limited dispersal abilities and are often aggregated due to the co-settlement of their larvae [221]. Puill-Stephan and colleagues [236] demonstrated that high levels of relatedness between juvenile corals correlated with late maturation of allorecognition. The fusion of siblings could thus be related to a low conspecific acceptance threshold and/or a delay in allorecognition maturation for Millepora hydrocorals, as described in some hermatypic corals [237, 238]. Considering the common occurrence of somatic mutations in fire coral species, modularity might be a promising strategy to increase genotypic variability in populations that are predominantly sustained through asexual reproduction [235].

## 7. Population genetics: a case study of Millepora cf. platyphylla at Moorea, French Polynesia

Recent genetic studies have uncovered that geographically isolated populations, such as those of Moorea, appear to be more dependent on self-recruitment for local replenishment and sustainability [239, 240], highlighting the importance of studying local patterns of life history traits in keystone species. Moorea is a high volcanic island surrounded by a barrier reef with extensive fringing reefs and lagoon systems [241]. Lagoons and deep interrupted channels separate the fore reefs from the island, and the lagoon is connected to the oceanic waters via deep passes through the barrier reef. Furthermore, coral reefs surrounding Moorea Island have undergone a massive decline in coral cover from a recent outbreak of Acanthaster planci and cyclone Oli [242, 243], which provides a unique perspective from which to comprehend how fire corals can survive and recover from such disturbances.

By gathering genotypic and phenotypic data, Dubé and colleagues [58, 221, 235] were able to produce a complete picture of ecological and evolutionary strategies involved in the population persistence of Millepora hydrocorals. On Moorea's reefs, M. cf. platyphylla displays a wide range of strategies that ensure its survival by maximizing the acquisition of local resources. Self-recruitment and mosaicism successfully established diverse genotypes within M. cf. platyphylla population, while

#### Ecology, Biology and Genetics of Millepora Hydrocorals on Coral Reefs DOI: http://dx.doi.org/10.5772/intechopen.89103

colony fragmentation contributed effectively to population growth (Figure 12), where a high number of clonal genotypes have the potential for phenotypic plasticity in response to environmental changes. Genetic data indicated that fragmentation is the dominant reproductive process generating the high abundance of fire corals at Moorea (80% of colonies were clones). Even small recruits were having multilocus genotypes identical to adults and were often positioned below the reef substratum, i.e. frequently on branches of dead coral colonies or side of crevices. These observations suggest that the successful recruitment of clones may be the result of clonal reproduction processes other than fragmentation, such as asexual planula larvae, because asexual fragments are less likely to re-attach on such inclined substrate. The release of ameiotic planula larvae was reported in a number of coral species [187], where larval behaviour allows the settlement of a new individual characterized by its mother genotype (clone mates). However, such clonal reproductive strategy has never been described for the Millepora genus, and requires further investigations. In Moorea, fire corals are sustained by a moderate degree of self-recruitment [221] suggesting that despite low gene flow, genetically diverse and locally adapted recruits can successfully establish high local population abundance via their subsequent growth, survival and fragmentation (as described in [244]). However, such populations are predicted to be vulnerable to severe disturbances owing to their isolation from potential source reefs and are often associated with increased extinction risks [245, 246]. A high potential for gene flow and connectivity has been revealed among islands of the Society Archipelago in French Polynesia for some scleractinian species (i.e. Moorea, Raiatea, Taha'a and Tahiti) [218]. Preliminary results from samples of M. cf. platyphylla collected in several islands from French Polynesia revealed significant genetic differentiation among archipelagos (Marquesas, Austral, Gambier, Society and Tuamotu, Boissin et al. unpublished), highlighting the importance of self-recruitment processes in population sustainability.

#### Figure 12.

Summary of life history strategies in M. cf. platyphylla at Moorea, French Polynesia. M. cf. platyphylla heavily relies on asexual reproduction through fragmentation for local replenishment (80% of the colonies are clones), allowing population growth and the persistence of a genotype over time. M. cf. platyphylla population is sustained via a significant contribution from self-recruitment (8–36% of juveniles are self-recruits). Mosaicism and chimerism also contribute in creating novel genotypic diversity at the population and individual levels.

6. Modularity and growth

Invertebrates - Ecophysiology and Management

Modularity is a well-established life history strategy among colonial reef invertebrates, i.e. corals, gorgonians, sea anemones, hydroids, hydrocorals, bryozoans and sponges [222]. Modular organisms grow in size via the repeated, vegetative formation of genetically identical modules, referred to as asexual budding, whereby all modules are derived from the same initial zygote to form a colony [223, 224]. Colony size often correlates with many fitness advantages in response to both physical and biological stressors. For instance, larger colonies can survive better towards predation [225] and competition [226], and their fecundity is often

increased due to the large number of polyps that contributes to sexual reproduction [227]. Modules usually remain physiologically interconnected, but may also separate from the colony through fission or fragmentation and persist as discrete units [228], thereafter reducing colony size. There are only few reports of growth rates in

Some marine modular organisms, e.g. corals and ascidians, can also grow larger and quicker via the fusion of distinct colonies [178], which results in genetically heterogeneous colony, also referred to chimera. In addition to chimerism, somatic mutations may arise within a colony, which also results in intracolonial genotypic variability. Both chimerism (fusion) and mosaicism (somatic mutation) were identified in fire corals [234, 235]. At Moorea, for instance, fusion between siblings is likely to occur as fire corals have limited dispersal abilities and are often aggregated due to the co-settlement of their larvae [221]. Puill-Stephan and colleagues [236] demonstrated that high levels of relatedness between juvenile corals correlated with late maturation of allorecognition. The fusion of siblings could thus be related to a low conspecific acceptance threshold and/or a delay in allorecognition maturation for Millepora hydrocorals, as described in some hermatypic corals [237, 238]. Considering the common occurrence of somatic mutations in fire coral species, modularity might be a promising strategy to increase genotypic variability in populations

Millepora species [79, 92, 229–232] that are within the range reported in

that are predominantly sustained through asexual reproduction [235].

Moorea, French Polynesia

32

7. Population genetics: a case study of Millepora cf. platyphylla at

Recent genetic studies have uncovered that geographically isolated populations, such as those of Moorea, appear to be more dependent on self-recruitment for local replenishment and sustainability [239, 240], highlighting the importance of studying local patterns of life history traits in keystone species. Moorea is a high volcanic island surrounded by a barrier reef with extensive fringing reefs and lagoon systems [241]. Lagoons and deep interrupted channels separate the fore reefs from the island, and the lagoon is connected to the oceanic waters via deep passes through the barrier reef. Furthermore, coral reefs surrounding Moorea Island have undergone a massive decline in coral cover from a recent outbreak of Acanthaster planci and cyclone Oli [242, 243], which provides a unique perspective from which to comprehend how fire corals can survive and recover from such disturbances.

By gathering genotypic and phenotypic data, Dubé and colleagues [58, 221, 235] were able to produce a complete picture of ecological and evolutionary strategies involved in the population persistence of Millepora hydrocorals. On Moorea's reefs, M. cf. platyphylla displays a wide range of strategies that ensure its survival by maximizing the acquisition of local resources. Self-recruitment and mosaicism successfully established diverse genotypes within M. cf. platyphylla population, while

Acroporidae corals from western Atlantic region [233].

Overall, the evaluation of the life history of M. cf. platyphylla suggests a competitive strategy, based on few locally produced sexual recruits and their ability of reaching large sizes (fusion [235] and stolonal spreading [59]), which allows them to pre-empt space on coral reefs, but also brought evidence of high susceptibility to fragmentation. This life strategy is well suited for population persistence in the absence of sexual recruitment, but can be risky in unstable environments [247]. Yet M. cf. platyphylla populations in Moorea have withstood severe disturbances, e.g. Acanthaster outbreaks, cyclones and mass bleaching events. Their recovery is foremost sustained by the rapid growth of remnant colonies, mostly those encrusting, and the subsequent local recruitment via both sexual and asexual reproduction. There is evidence that under pressure from environmental changes fire corals might be among the reef coral 'winners', joining some scleractinian species that have already been described as such [32, 85, 140]. Yet more information on how they respond to bleaching events is needed, as Millepora species have been reported to be highly vulnerable to thermal stress in other reefs [4, 130, 133]. Nevertheless, the life history of M. cf. platyphylla is most likely contributing to its colonization success in various reef environments in French Polynesia. Although M. cf. platyphylla is the only fire coral species reported in this geographic region [50], this species is also characterized by one of the widest ranges of distribution in the entire Indo-Pacific region within the Millepora genus [248], but similar to the branching species M. intricata. Evaluating the life history of other Millepora species with different growth forms will enable to determine whether these strategies are unique to M. cf. platyphylla or spread within the Millepora genus.

Biodiversity Federation (FRB), French Agency for Biodiversity (AFB),

Ecology, Biology and Genetics of Millepora Hydrocorals on Coral Reefs

DOI: http://dx.doi.org/10.5772/intechopen.89103

respectively, during expeditions, field work and data analysis.

Caroline E. Dubé1,2\*, Chloé A.F. Bourmaud2,3, Alexandre Mercière1,2,

1 PSL Research University, EPHE-UPVD-CNRS, USR 3278 CRIOBE,

2 Laboratoire d'Excellence "CORAIL", Moorea, French Polynesia

\*Address all correspondence to: caroline.dube.qc@gmail.com

3 UMR ENTROPIE 9220, Université de La Réunion, Saint-Denis Cedex,

© 2019 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium,

The authors declare no conflict of interest.

Conflict of interest

Author details

La Réunion, France

35

Serge Planes1,2 and Emilie Boissin1,2

provided the original work is properly cited.

Université de Perpignan, Perpignan Cedex, France

'Observatoire des Sciences de l'Univers' from Reunion Island (OSU-R) and the Ministry of French overseas territories. We are very grateful to N Gravier-Bonnet who firstly initiated milleporids studies in the south-west Indian Ocean. Further, several collaborations lead us to undergo marine biodiversity surveys in the Indo-Pacific region. N Gravier-Bonnet also provided valuable help with data gathering and species descriptions. We would like to thank numerous colleagues that allow us to participate to biodiversity or multidisciplinary research programs (S Andréfouët, L Bigot, P Chabanet, JL Join) and many students for contributing to the studies. CED also wishes to thank M Ziegler, B Hume and CR Voolstra for helping in the identification of Symbiodiniaceae species associated with M. cf. platyphylla at Moorea and Reunion Islands. CED and EB were financially supported by a FRQNT PhD scholarship and Marie-Curie Postdoctoral fellowship (MC-CIG-618480),

## 8. Conclusions

In recent decades, declines in scleractinian coral cover have challenged their role as key ecosystem engineers of coral reefs [25–27, 249–251]. Assuming rising sea temperatures and increased ocean acidification, climate change can interfere with a range of key processes in the life history of reef corals, including growth, calcification, development, reproduction and behavior [162, 252]. Despite the acclimatization and genetic adaptation of reef corals [2], such persistent physical and chemical conditions can lead to shifts in reef community composition. This phenomenon has already been reported in many reefs, where alternative organisms are dominating reef assemblages (reviewed in [253]). Only few studies have considered hydrocorals in ecological monitoring of coral reefs [130, 254, 255]. For instance, M. cf. platyphylla can dominate some reefs in the Indo-Pacific region [89] and also contribute to the survival of corals during Acanthaster outbreaks [106]. Therefore, it is crucial to gain insights into how populations of this keystone species can adapt and survive in the face of climate change, and other natural or anthropogenic disturbances. In this chapter, we established that fire corals possess a great variety of life history strategies that favor a high degree of genetic diversity and plasticity enabling these organisms to persist throughout environmental variations. Consequently, these Millepora species may become one of the major components in some modern reefs and requires more consideration in ecological monitoring.

#### Acknowledgements

Much of the information in this review has come from expeditions and field work we have made in the Indian and Pacific Oceans, courtesy of grants from the LabEx 'CORAIL', Regional Council of Reunion Island, ANR French funds, French Ecology, Biology and Genetics of Millepora Hydrocorals on Coral Reefs DOI: http://dx.doi.org/10.5772/intechopen.89103

Biodiversity Federation (FRB), French Agency for Biodiversity (AFB), 'Observatoire des Sciences de l'Univers' from Reunion Island (OSU-R) and the Ministry of French overseas territories. We are very grateful to N Gravier-Bonnet who firstly initiated milleporids studies in the south-west Indian Ocean. Further, several collaborations lead us to undergo marine biodiversity surveys in the Indo-Pacific region. N Gravier-Bonnet also provided valuable help with data gathering and species descriptions. We would like to thank numerous colleagues that allow us to participate to biodiversity or multidisciplinary research programs (S Andréfouët, L Bigot, P Chabanet, JL Join) and many students for contributing to the studies. CED also wishes to thank M Ziegler, B Hume and CR Voolstra for helping in the identification of Symbiodiniaceae species associated with M. cf. platyphylla at Moorea and Reunion Islands. CED and EB were financially supported by a FRQNT PhD scholarship and Marie-Curie Postdoctoral fellowship (MC-CIG-618480), respectively, during expeditions, field work and data analysis.
