Open access peer-reviewed chapter

Ecology, Biology and Genetics of Millepora Hydrocorals on Coral Reefs

Written By

Caroline E. Dubé, Chloé A.F. Bourmaud, Alexandre Mercière, Serge Planes and Emilie Boissin

Submitted: October 8th, 2018 Reviewed: August 9th, 2019 Published: December 2nd, 2019

DOI: 10.5772/intechopen.89103

From the Edited Volume


Edited by Sajal Ray, Genaro Diarte-Plata and Ruth Escamilla-Montes

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Coral reefs are one of the most productive and diverse ecosystems on Earth. However, climate warming is occurring at an unprecedented rate and has negatively affected coral reefs worldwide. Evaluating the life history of reef-building species carries important implications for coral reef conservation. This chapter examines the taxonomy, biogeography, ecology, symbiosis, morphology and reproductive biology of Millepora hydrocorals, an important but relatively unstudied component of coral reefs. An emphasis is also placed on the influence of variable reef environments on Millepora life history traits, providing a fascinating opportunity to study the interplay between ecology and evolution. Special attention is given to ecological and evolutionary benefits of asexual versus sexual reproduction in the maintenance of genetic and phenotypic diversity. Lastly, this chapter discusses whether life-history strategies of Millepora hydrocorals and tolerance to different stressors can influence their ability to adapt and survive to future climate change, and other natural and anthropogenic disturbances.


  • Millepora
  • coral reefs
  • taxonomy
  • biogeography
  • symbiosis
  • morphology
  • reproduction
  • population genetics

1. Introduction

1.1 Coral reefs: biodiversity and threats

Coral reefs were formed only 230 million years ago and are largely limited to warm shallow waters [1], yet they are among the most biologically diverse and economically important marine ecosystems. Coral reefs do not only shelter thousands of species; they also provide critical services to humans, including fisheries, coastal protection, medicines and tourism activities [2, 3, 4]. The economic value of coral reefs worldwide has been estimated to be around 30 billion US$ of net benefit per year [5]. Often called the rainforest of the sea due to their outstanding biodiversity, coral reefs only cover less than 0.1% of the ocean seafloor [6, 7] or approximately 5% that of rainforest areas [8]. Coral reefs thrive under nutrient-poor and oligotrophic waters [9, 10, 11], but yet harbour more than 25% of all known marine species [12, 13]. This ecosystem is sustained through efficient nutrient recycling strategies developed by corals [14] and algae [15], the primary reef producers, and other key organisms, i.e., microbes [16] and sponges [17]. In coral reef ecosystems, many calcifying benthic organisms contribute to reef accretion and build the complex and massive three-dimensional structure of reefs, including scleractinian corals, the major habitat architects, and hydrocorals [18]. These reef-builders are key components of coral reef health and biodiversity as they offer food, shelter and nurseries for thousands of reef-dwelling organisms and fishes [19].

Reefs are dynamic systems that are frequently punctuated by perturbations [20]. For instance, human activities can alter both global (climate change associated with CO2 emissions) and local reef health (e.g. coastal habitat loss, pollution, sewage, overfishing and invasive species) [21, 22]. As a consequence, several reports of coral reef declines have been recorded, averaging 30–50% reductions in reef cover globally [4, 23, 24], including recent losses of coral cover following the multiple global bleaching events that occurred between 2014 and 2017 [25, 26, 27]. Since coral reefs are integrated ecosystems, declines in reef-building corals are often accompanied with declines of other species, such as many coral reef fishes [28], further hampering their capacity to deliver important ecosystem services to more than 500 million people [23, 29]. Yet, reef corals and the ecosystem they create can recover and a key factor underpinning such recovery is the ability of coral species to grow back, to maintain or renew their populations. Such an ability to respond to acute and chronic stressors in coral species is often linked to morphological traits, reproductive strategies and symbiont partners (among others). As we progress further into the Anthropocene, understanding and predicting these stress responses require prior knowledge on the life history traits of keystone reef corals, and some assessment of the influence that environmental changes may have on those traits.

1.2 Millepora hydrocorals

To date, the vast majority of studies on species’ life history traits in coral reefs have mainly focused on scleractinian corals due to their key role in providing much of the habitat framework and structural complexity of reefs [30, 31, 32, 33, 34]. The extent to which other non-scleractinian reef-building organisms might rescue reef populations in response to environmental change is largely unknown. More information on such organisms is therefore needed. Millepora hydrocorals, known as fire corals because of their painful sting via toxic nematocysts [35, 36], are important components of reef communities where they, similar to scleractinian corals, contribute to reef accretion and community dynamics [37, 38]. Millepora species are Hydrozoans (Medusozoans), and together with hermatypic corals (Anthozoans), belong to the phylum Cnidaria [39]. Millepora spp. are members of the monogeneric family Milleporidae, the sub-order Capitata and the order Anthomedusae [40, 41, 42]. Milleporidae and Stylasteridae are the only two Hydrozoan families producing skeletons of calcium carbonate. The first scientific report of Millepora spp. was from Linnaeus in 1758 [43], with subsequent species reports and descriptions by several authors (e.g. [44, 45]), and the seminal work of Boschma [46, 47]. There has been a surge of interest in fire corals over the last two decades (Figure 1), and especially in the last 7 years. These recent studies focused on genetics and coincided with the development of new molecular markers [48, 49, 50]. While there is much known now about fire corals (reviewed in [51]), the literature is scattered, particularly that of biogeography and population genetic research, and needs to be summarized. In this chapter, we will document what is known about taxonomy, biogeography, ecology, symbiosis, morphology and reproductive biology of Millepora hydrocorals, using both published and unpublished information, and will highlight areas where knowledge is especially lacking.

Figure 1.

The literature search in web of science identified 326 publications referring to Millepora hydrocorals, wherein only 29 were using genetic approaches.


2. Biodiversity and biogeography

2.1 Fossil records

Hydrocorals have a relatively long evolutionary history since many fossils from Tertiary deposits have been assigned to Millepora. However, Boschma [52] recognized only two species, Millepora tornquisti from Eocene rocks (56–33 mA) of Madagascar and M. alcicornis in Pleistocene deposits (2.58 mA–11,700 ya) from the Panama Canal zone [53]. Other branching milleporids were also reported from the Upper Cretaceous (100–66 mA) in northern Spain [54]. Recently, fossils of M. alcicornis have been recorded in deposits from the Early Miocene (∼23 mA) [55]. M. exaesa fossils were also recorded in more recent deposits in the Seychelles, dating from the last interglacial sea-level high-stand, ∼129,000–116,000 ya [56].

2.2 Species delimitation

As in many corals, the morphological species concept was traditionally applied to the species delimitation of Millepora, which is based on colony growth forms. Millepora species have a great diversity of growth forms and can be encrusting, branching, plate-like, massive or even columnar (Figure 2). Interestingly, the typical growth forms of Millepora species are broadly the same in the Red Sea and the Indo-Pacific. Arrigoni and colleagues [57] hypothesized a morphological convergence for these species. Similarly, in the Atlantic, there is also one plate-like and one branching species, as well as other massive/encrusting forms. As these growth forms do not form monophyletic groups on the phylogenetic reconstructions [57], they seem to have appeared independently and likely evolved in relation to the hydrodynamic conditions of their environment.

Figure 2.

Growth forms, pores and polyps of three Millepora species. (A–C) M. cf. exaesa encrusting growth form, pores and polyps, respectively; (D–F) for the massive M. cf. platyphylla and (G–I) for the branching M. cf. tenera. D photograph is courtesy of Gilles Siu.

This group is also known for its great phenotypic plasticity [46], and environmental factors are known to greatly influence the morphology of Millepora colonies. Recently, Dubé and colleagues [58] demonstrated phenotypic plasticity among clonal colonies distributed in habitats with different hydrodynamic characteristics (see Section 4). To further complicate the matter, fire corals have been shown to overgrow stony corals, hydrocorals and gorgonians, which gives them additional peculiar growth forms (Figure 3) [59, 60]. Consequently, about 100 nominal species were described [61]. While Duchassaing and Michelotti [44, 62] identified 24 Millepora species based on trivial morphological differences, Hickson [45, 63] reckoned that there was only one Millepora species, M. alcicornis, and that all other morphological growth forms were only ecological variations. There is a true ‘species boundary problem’ within Millepora and it has been subject to much debate for over 150 years [45, 46, 47, 64, 65].

Figure 3.

Millepora hydrocorals overgrowing living reef corals at Europa Island (Indian Ocean), including massive Porites (A, C and D), Distichopora sp. (B) and Astrea sp. (D). M. cf. platyphylla can overgrow giant clam shells (C).

Apart from colony growth forms, pore traits are the most widely used characters in Millepora species delimitation. The pores in Millepora are like the corallites for the scleractinian corals, accommodating the polyps. There are two types of polyps in Millepora species: feeding polyps (gastrozoids) which are provided with a gastrovascular cavity opening by a mouth, and defensive polyps (dactylozoids) without a mouth. The gastropores and the dactylopores, from which the gastrozoids and the dactylozoids are able to extend outside to catch food, are organized in cyclosystems formed by a circle of dactylopores surrounding a single gastropore (Figure 2). While Boschma [46] concluded that the colony growth form was the most important character for the distinction of species, and that the other characters were not sufficient delimiting criteria, subsequent studies have used pore characters. Using a more elaborate quantitative approach on pore characters, Moschenko [66] considered 11 traits (e.g. numbers and diameters of gastropores and dactylopores, distances between dactylopores and gastropores, number of dactylopores per gastropore) in one plate-like (M. platyphylla Hemprich and Ehrenberg 1834) and five branching Millepora species (M. cruzi Nemenzo 1975, M. dichotoma Forskal 1775, M. intricata Milne Edwards 1860, M. murrayi Quelch 1884 and M. tenera Boschma 1949). His results distinguished only M. platyphylla, while all branching species shared important overlap in trait values with gradual transition from one species to another [66]. However, M. cruzi and M. murrayi have been subsequently synonymized (with M. tenera and M. intricata, respectively) and this could explain some of the trait overlaps between species. More recently, Razak and Hoeksema [65], based on colony growth forms and pore characters, revised the Indonesian Millepora species and synonymized 6 of the 13 recognized Indo-Pacific species. In particular, the gastropore and dactylopore diameters were shown to be discriminant among many Millepora species [57, 67, 68]. Boissin and colleagues (submitted) analyzed 13 pore characters and could distinguish the three species present in Reunion Island. This latest study showed that gastropore and dactylopore numbers, as well as diameters, were informative and should be used as standard traits in future Millepora studies. This study also showed that polyp features were discriminant, such as the presence or absence of capitate tentacles or capitations, and the presence, absence or abundance of Symbiodiniaceae. Additional biological traits seem to be helpful to delineate milleporid species, such as reproductive periods, medusoid features and nematocyst morphology [36, 57, 69, 70].

The advent of DNA barcoding greatly helped delimiting species of many marine invertebrates [71, 72, 73, 74]. Consequently, the more recent works on Millepora spp. used a combination of morpho and molecular characterization. Mitochondrial sequence data were successfully used to delineate milleporid species from the Caribbean, revealing two genetic entities: M. squarrosa Lamarck 1816 and a species complex composed of M. alcicornis Linnaeus 1758–M. complanata Lamarck 1816 [67]. Similarly, the four Millepora species from the Brazilian province were discriminated using the 16S mitochondrial gene coupled with morphological characters [68]. Recently, a study on milleporids from the Red Sea successfully distinguished three species M. platyphylla, M. dichotoma and M. exaesa Forskal 1775, using both morphological and molecular characterization [57]. Similarly, Boissin and colleagues (submitted) successfully used 16S sequences to delineate the three Millepora species from Reunion Island.

2.3 Biogeography

Fire corals are found in tropical/subtropical regions around the globe, nearly ubiquitous on reefs in the Atlantic, Indian and Pacific Oceans (Figure 4). Currently, 10 species are considered valid in the Indo-Pacific and 6 in the Atlantic Ocean [57, 61, 65, 68, 75]. The species status of two other Indo-Pacific species, M. nodulosa Nemenzo 1984 and M. latifolia Boschma 1948, are still unclear [65]. Several Indo-Pacific species show an extensive geographic distribution from west of the Indian Ocean to west (M. dichotoma, M. tenera), centre (M. platyphylla) or east of the Pacific Ocean (M. exaesa, M. intricata), while M. foveolata Crossland 1952 and M. boschmai de Weerdt and Glynn 1991 have restricted distributions (Philippines and Indonesia, respectively, Figure 4). In the Atlantic, two species are endemic to the Caribbean province (M. complanata, M. squarrosa) and three species are endemic to the Brazilian province (M. braziliensis Verrill 1868, M. nitida Verrill 1868, M. laboreli Amaral 2008), while M. alcicornis is present in both provinces as well as in the Canary Islands, Cape Verde and Ascension Island (Figure 4) [46, 76].

Figure 4.

Geographic distribution of the 16 recognized species of Millepora in the Atlantic and Indo-Pacific Oceans.

However, with recent morpho-molecular re-evaluations of species boundaries in this group, our understanding of the biogeographic patterns is still evolving. The recent highlight of cryptic species between the Red Sea and the rest of the Indo-Pacific provinces [57] pointed out that M. platyphylla, M. dichotoma and M. exaesa in the Indo-Pacific need taxonomic re-description. The number of Indo-Pacific species was thus raised from 7 to 10 in the last few months. This number is likely to grow in future years, as M. cf. exaesa for instance includes several lineages over its Indo-Pacific range and likely represents another case of species complex (Boissin et al., unpublished).

Additionally, the range of M. platyphylla (now M. cf. platyphylla) was recently extended back to the eastern Pacific [77] from where it was documented as extirpated decades ago [78]. In the Atlantic, M. alcicornis has recently established in the Canary Islands (Macaronesia), far north of its tropical distribution [79], possibly by means of drifting material from the Caribbean Sea or transportation through ballast waters of large vessels and fouling of hulls [79, 80, 81]. Long-distance dispersals in milleporids have also been demonstrated in the Pacific, with Millepora colonies recorded on drifting pumice [80]. This alternative mode of dispersal can explain such a wide geographic distribution for a species with a short pelagic stage (see Section 5.3). However, as noticed by Lewis [51], it is surely remarkable that a family of worldwide distribution, with a long geological history and apparent ecological success, is represented by less than 20 species.


3. Ecology and symbiosis

3.1 Distribution, abundance and ecological roles

Fire corals occur worldwide in tropical seas and are limited in distribution from the intertidal zone to depths of approximately 50 m [51, 82, 83]. Although fire corals can be abundant locally [84, 85, 86] and dominate shallow water communities in some coral reef ecosystems [87, 88, 89, 90], they usually cover less than 10% of the overall reef substratum [51, 91]. Millepora spp. are also found in many environments and waves, water movement, light intensity and habitat depth were identified as key factors influencing their distribution and growth forms [51, 82, 91, 92, 93]. On barrier reefs, the amount of wave energy is highest on the reef crest, where wave breaking first occurs and subsequently attenuates towards fore reef and lagoonal environments (Figure 5) [94, 95]. This gradient in wave energy, combined with Millepora’s sensitivity to wave-induced breakage, were showed to strongly influence colony and size distributions of M. cf. platyphylla at Moorea (French Polynesia), with highest densities recorded on the fore reef and larger colonies on nearshore reefs [91]. M. cf. platyphylla colonies occurred in a contagious pattern of distribution (i.e. colonies close to one another), as described for other Caribbean species [96], and colony breakage and subsequent fragment re-attachment were suggested as explanations for such colony aggregations [58]. Three Millepora species were also identified on the reefs of Reunion Island [97], where each species is distributed according to their proximity with the shore and reef crest, mostly related to the wave energy dispersal. M. cf. exaesa is the first species encountered close to shore on the shallow reef flat (2 m depth), replaced by M. tenera when approaching the reef crest, and M. cf. platyphylla colonies live from the crest to 35 m depth on the outer slope.

Figure 5.

Wave energy dispersal on a barrier reef (modified from [94, 95]). The fore reef experiences strong wave action from incoming waves that break on the reef crest, near the upper slope, with a significant decrease in swell exposure towards deeper waters. The reef crest dissipates ∼70% of the incident swell wave energy with gradual wave attenuation from the back reef to nearshore fringing reefs.

Millepores are important reef framework builders, second only after scleractinian hard corals [51, 82]. Their complex structure is a habitat for other species adapted to stinging cells, including scavenger crustaceans (e.g. crabs, shrimps and barnacles, [51, 98, 99, 100]), as well as fish [38, 101, 102, 103], serpulids [104, 105], spionid polychaetes [51] and scleractinian corals [106]. Interestingly, high fire coral cover on Caribbean reefs was associated with increased fish richness species [86]. Many studies have described hydrocorals as opportunistic species that show rapid growth rates with high fecundity [51] and the ability for clonal propagation through fragmentation [58]. Fire corals are capable of colonizing both natural and artificial substrates, including dead gorgonians, rocks and ships [107, 108], as well as living seagrass stems, hydrocorals, gorgonians, scleractinian corals and other reef invertebrates (e.g. giant clams) through pursuit, contact and overgrowth (Figure 3) [59, 60]. This ability to inhabit different substrates and its rapid colonization rates [79] provide a competitive advantage for potential habitat expansions. Although fire corals compete with other corals, they also contribute to coral survival during Acanthaster outbreaks [106], highlighting their key ecological role in reef resilience. In fact, the corallivorous predator Acanthaster planci tends to avoid Millepora species [109], thus providing predator-free sanctuaries to nearby scleractinian corals.

3.2 Endosymbiosis with photosynthetic dinoflagellates (Symbiodiniaceae)

Many members of the phylum Cnidaria, including corals, octocorals, sea anemones and hydrocorals, host unicellular dinoflagellate endosymbionts (i.e. zooxanthellae) belonging to the family Symbiodiniaceae [110]. These associations are often obligatory and of fundamental importance to coral reef ecosystems as they enhance the growth of calcifying corals that form the reef. For instance, the zooxanthellae contribute to host nutrition (up to 95% of the energy requirements in scleractinian corals [111]) and skeletogenesis by providing photosynthetically fixed carbon, while the cnidarian host provides inorganic nutrients and refuge from herbivory to its symbionts [112, 113, 114]. Previous studies have demonstrated that the association of Cnidaria–Symbiodiniaceae is not stochastic, but mostly determined by host phylogeny and geography [115, 116]. Like scleractinian corals, hydrocorals feed heterotrophically on a variety of resources (mostly planktonic feeders [51, 117]) and rely on a mutualistic symbiosis with Symbiodiniaceae algae for autotrophic nutrition and calcification [118, 119]. While coral-Symbiodiniaceae associations have been extensively studied over the last decades (reviewed in [120]), only two studies have recently investigated hydrocoral-Symbiodiniaceae associations on Caribbean reefs [121, 122]. Rodriguez and colleagues [122] showed that Symbiodiniaceae species that associate with M. alcicornis vary as a function of its geography, with Symbiodinium sp. (formerly clade A) found in samples from Mexico and Breviolum sp. (formerly clade B) in the eastern Atlantic, with the exception of samples from the Canary Island and Cape Verde Islands that comprised Cladocopium sp. (formerly clade C). Unpublished data collected across M. cf. platyphylla Indo-Pacific range showed that this species can associate with the genera Symbiodinium (dominant symbiont), Cladocopium and more rarely with Brevolium in French Polynesia, Papua New Guinea and the south-western Indian Ocean (Dubé et al. in prep.; Boissin et al. in prep.). The other Indo-Pacific species (M. cf. dichotoma and M. cf. exaesa) investigated so far show the same Symbiodiniaceae associations (Boissin et al. in prep.).

3.3 Bleaching susceptibility

One of the most devastating consequences of global warming is coral bleaching. Bleaching occurs when scleractinian corals, hydrocorals and octocorals lose their photosynthetic symbiotic algae or pigments [21, 111, 123, 124, 125], which leads to the white calcium carbonate skeleton being visible through the transparent host tissue. The frequency and severity with which coral bleaching occurs have increased in recent years [126]. Numerous investigations have demonstrated that coral bleaching events are a serious threat to coral reefs worldwide, where they have caused a severe deterioration in reef health (e.g. increase in coral disease, decrease in reef calcification and loss of habitat for related reef organisms [25, 123, 127, 128, 129]. The severity of coral bleaching depends on several factors, including specific coral species impacted [130], symbiotic algae assemblages [131] and thermal history [132].

Zooxanthellate hydrocorals are thought to be extremely sensitive to bleaching [130, 133] and can be threatened by future climate change. Millepora spp. have been reported to be among the first cnidarians to lose their zooxanthellae symbionts during widespread bleaching events [134] and they have suffered local or regional extinctions from bleaching in the Pacific [78, 85, 135]. Numerous investigations of bleaching events on Caribbean and Florida Keys reefs have reported bleaching of Millepora colonies [133, 136, 137, 138, 139], with M. alcicornis, a finely branched species, being the most severely affected reef corals. Such coral morphology has been described to be more susceptible to bleaching than encrusting and massive species [140]. Yet, bleached colonies of M. alcicornis remained alive during a bleaching event affecting a north-eastern Brazilian reef [133], which is in accordance with previous reports that Millepora species are also the first to recover from short-term bleaching [136, 137]. In the Maldives Archipelago (Indian Ocean), Millepora was reported to be the major reef-building coral in shallow reefs (7 m depth), producing some ‘Millepora zones’ [141]. Three species were well documented, the massive species M. cf. platyphylla [46, 142] and two branching ones, M. tenera [51, 143, 144] and M. latifolia [143]. However, many recent surveys of the Maldivian reefs have identified another pattern of distribution, where none to low abundances of Millepora species were recorded (1–2 depending on the species) [145, 146, 147, 148]. Gravier-Bonnet and Bourmaud [148] suggested that milleporids were extirpated from several Maldives atolls, following the 1997–1998 El-Nino Southern Oscillation event (ENSO). ENSO has induced a strong bleaching and massive coral mortality (of up to 90%) in the tropical Indian Ocean, including the Maldives [145, 149]. On the Great Barrier Reef, Millepora spp. were also the most susceptible taxa to the mass bleaching event of 1998, with 85% of mortality [130], while they showed no evidence of bleaching at Moorea, although scleractinian corals were severely bleached at this location [150]. During 2014–2017, the worst documented bleaching event observed [26, 27], M. cf. platyphylla showed no sign of bleaching at Moorea, although about 60% of scleractinian corals were bleached on the fore reefs (Figure 6A). Since February 2019, Moorea’s reefs are suffering from another mass bleaching event, with colonies of M. cf. platyphylla showing sign of bleaching and mortality (Figure 6B). Differential susceptibilities to this bleaching event were also observed between M. cf. platyphylla colonies (Figure 6C). Ongoing surveys will help quantifying bleaching susceptibility and mortality among coral taxa and locations, as well as between fire coral growth forms and genotypes (Dubé et al. in prep). Nevertheless, a previous study has shown that temperature is the primary factor related to bleaching in M. alcicornis, but that synergism with exposure to solar radiation may play a key role in hydrocoral bleaching [151]. Also, multifocal bleaching in hydrocorals, consisting of numerous scattered bleached spots, has been first described as a syndrome caused by an infectious disease affecting several colonies of M. dichotoma in the Red Sea [152]. 16S rRNA gene sequencing showed that affected tissues match sequences of bacteria belonging to Alphaproteobacteria and Bacteroidetes members previously associated with various diseases in scleractinian corals [153]. Yet the mechanisms of multifocal bleaching, its aetiology and mode of transmission remain unknown. Nevertheless, many studies have addressed the aetiology and effects of bleaching in Anthozoan species, wherein changes in the expression of genes and proteins were observed, and particularly heat shock proteins and transcription factors [154, 155, 156, 157, 158, 159]. A recent study demonstrated that bleached specimens of M. alcicornis in Mexican Caribbean undergo a moderate decrease in symbiont’s density and photosynthetic pigments, in addition to differential expression of 17 key proteins, such as calmodulin, actin and collagen often coupled with calcium homeostasis, exocytosis and cytoskeleton organization in Anthozoan species [139].

Figure 6.

Bleaching susceptibility of M. cf. platyphylla during massive bleaching events occurring on the fore reefs at Moorea Island (French Polynesia). (A) View of the fore reef at Moorea during the bleaching event of 2016, showing healthy colonies of M. cf. platyphylla and bleached colonies of scleractinian corals, mostly of the Pocillopora genus. M. cf. platyphylla was sensitive to the recent bleaching event of 2019 at Moorea, where colonies bleached and died (B) from the rise in temperature, while other colonies showed sign of resistance to bleaching on the same reef (C). Photographs are courtesy of Yannick Chancerelle (A) and Yann Lacube (B and C).

Coral reefs are also threatened by ocean acidification associated with the increasing CO2 partial pressure, which depresses net calcification of corals and hydrocorals [160, 161]. Physiological responses of reef organisms to ocean acidification are relatively well known [162, 163]. Examples include changes in gene expression consistent with metabolic suppression, increased oxidative stress, antioxidant system, apoptosis and symbiont loss [164, 165]. Yet little information on the effects of ocean acidification on the physiology of fire corals is available in the current literature. Luz and colleagues [166] demonstrated that the antioxidant defense system of M. alcicornis is capable of coping with acidic conditions for a short period of time, while long-term exposure induces oxidative stress with consequent oxidative damage to lipids and proteins, which could compromise hydrocoral health and influence negatively the zooxanthellae-coral symbiosis and ultimately lead to bleaching [167].


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, 175, 176, 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].

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.

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 wave-tolerant growth forms in such dynamic reefs. Such phenotypic responses suggest that fire corals being susceptible to wave-induced breakage have benefits in terms of reproduction outweighing the costs of getting injured.

Figure 8.

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.


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, 184, 185, 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, 195, 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, 200, 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, 208, 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.

Figure 10.

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

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.

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/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/cm2. 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.


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, 230, 231, 232] that are within the range reported in Acroporidae corals from western Atlantic region [233].

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 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.

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.


8. Conclusions

In recent decades, declines in scleractinian coral cover have challenged their role as key ecosystem engineers of coral reefs [25, 26, 27, 249, 250, 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.



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 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.


Conflict of interest

The authors declare no conflict of interest.


  1. 1. Veron JEN. Corals in Space and Time: The Biogeography and Evolution of the Scleractinia. Sydney: UNSW Press; 1995
  2. 2. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, et al. Coral reefs under rapid climate change and ocean acidification. Science. 2007;318(5857):1737-1742
  3. 3. Srividhya S, Chellaram C. Role of marine life in nanomedicine. Indian Journal Innovations and Developments. 2012;1(S8):31-33
  4. 4. Moritz C, Vii J, Lee Long W, Tamelander J, Thomassin A, Planes S. Status and Tends of Coral Reefs of the Pacific. France: Global Coral Reef Monitoring Network; 2018. 218 p
  5. 5. Cesar H, Burke L, Pet-Soede L. The Economics of Worldwide Coral Reef Degradation. Cesar Environmental Economics Consulting: Arnhem; 2003
  6. 6. Copper P. Ancient reef ecosystem expansion and collapse. Coral Reefs. 1994;13:3-11
  7. 7. Spalding MD, Grenfell AM. New estimates of global and regional coral reef areas. Coral Reefs. 1997;16:225-230
  8. 8. Reaka-Kudla ML. The global biodiversity of coral reefs: A comparison with rain forests. In: Reaka-Kudla ML, Wilson DE, Wilson EO, editors. Biodiversity II: Understanding and Protecting our Biological Resources. Washington DC: Joseph Henry Press; 1997. pp. 83-108
  9. 9. Odum HT, Odum EP. Trophic structure and productivity of a windward coral reef community on Eniwetok atoll. Ecological Monographs. 1955;25:291-320
  10. 10. Hatcher BG. Coral reef primary productivity. A hierarchy of pattern and process. Trends in Ecology & Evolution. 1990;5:149-155
  11. 11. Atkinson MJ, Falter JL. In: Black KD, Shimmield GB, editors. Biogeochemistry of Marine Systems. Oxford: Blackwell Publishing; 2003. pp. 40-64
  12. 12. McAllister DE. What is the status of the world’s coral reef fishes? Sea Wind. 1991;5:14-18
  13. 13. Knowlton N, Brainard RE, Fisher R, Moews M, Plaisance L, Caley MJ. Coral reef biodiversity. In: McIntyre A, editor. Life in the World’s Oceans: Diversity Distribution and Abundance. Scotland, UK: John Wiley & Sons; 2010. pp. 65-74
  14. 14. Wild C, Huettel M, Klueter A, Kremb SG, Rasheed MY, Jørgensen BB. Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature. 2004;428:66-70
  15. 15. Haas AF, Naumann MS, Struck U, Mayr C, el-Zibdah M, Wild C. Organic matter release by coral reef associated benthic algae in the northern Red Sea. Journal of Experimental Marine Biology and Ecology. 2010;389:53-60
  16. 16. Azam F, Fenchel T, Field JG, Gray JS, Meyer-Rei LA, Thingstad F. The ecological role of water-column microbes in the sea. Marine Ecology Progress Series. 1983;10:257-263
  17. 17. De Goeij JM, Van Oevelen D, Vermeij MJ, Osinga R, Middelburg JJ, De Goeij AF, et al. Surviving in a marine desert: The sponge loop retains resources within coral reefs. Science. 2013;342(6154):108-110
  18. 18. Buddemeier RW, Baker AC, Fautin DG, Jacobs JR. The adaptive hypothesis of bleaching. In: Rosenberg E, Loya Y, editors. Coral Health and Disease. Berlin: Springer; 2004. pp. 427-444
  19. 19. Bellwood DR, Hughes TP, Hoey AS. Sleeping functional group drives coral-reef recovery. Current Biology. 2006;16(24):2434-2439
  20. 20. Connell JH. Diversity in tropical rain forests and coral reefs. Science. 1978;199(4335):1302-1310
  21. 21. Lesser MP. Coral reef bleaching and global climate change: Can corals survive the next century? Proceedings of the National Academy of Sciences of the United States of America. 2007;104:5259-5260
  22. 22. Lough JM, Anderson KD, Hughes TP. Increasing thermal stress for tropical coral reefs: 1871–2017. Scientific Reports. 2018;8(1):6079
  23. 23. Wilkinson C. Status of Coral Reefs of the World: 2008. Australia, Townsville: Global Coral Reef Monitoring Network and Reef and Rainforest Research Center; 2008
  24. 24. Selig ER, Casey KS, Bruno JF. Temperature-driven coral decline: The role of marine protected areas. Global Change Biology. 2012;18(5):1561-1570
  25. 25. Hughes TP, Barnes ML, Bellwood DR, Cinner JE, Cumming GS, Jackson JB, et al. Coral reefs in the Anthropocene. Nature. 2017;546(7656):82
  26. 26. Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, et al. Global warming and recurrent mass bleaching of corals. Nature. 2017;543(7645):373
  27. 27. Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science. 2018;359(6371):80-83
  28. 28. Graham NA, Wilson SK, Jennings S, Polunin NV, Robinson JA, Bijoux JP, et al. Lag effects in the impacts of mass coral bleaching on coral reef fish, fisheries, and ecosystems. Conservation Biology. 2007;21(5):1291-1300
  29. 29. Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, et al. Biodiversity loss and its impact on humanity. Nature. 2012;486(7401):59
  30. 30. Hughes TP, Tanner JE. Recruitment failure, life histories, and long-term decline of Caribbean corals. Ecology. 2000;81:2250-2263
  31. 31. Vermeij MJA. Early life-history dynamics of Caribbean coral species on artificial substratum: The importance of competition, growth and variation in life-history strategy. Coral Reefs. 2006;25:5-71
  32. 32. Darling ES, Alvarez-Filip L, Oliver TA, McClanahan TR, Côté IM. Evaluating life-history strategies of reef corals from species traits. Ecology Letters. 2012;15:1378-1386
  33. 33. Darling ES, McClanahan TR, Côté IM. Life histories predict coral community disassembly under multiple stressors. Global Change Biology. 2013;19:1930-1940
  34. 34. Kayal M, Vercelloni J, Wand MP, Adjeroud M. Searching for the best bet in life-strategy: A quantitative approach to individual performance and population dynamics in reef-building corals. Ecological Complexity. 2015;23:73-84
  35. 35. García-Arredondo A, Rojas A, Iglesias-Prieto R, Zepeda-Rodriguez A, Palma-Tirado L. Structure of nematocysts isolated from the fire corals Millepora alcicornis and Millepora complanata (Cnidaria: Hydrozoa). Journal of Venomous Animals and Toxins Including Tropical Diseases. 2012;18(1):109-115
  36. 36. Rojas-Molina A, García-Arredondo A, Ibarra-Alvarado C, Bah M. Millepora (“fire corals”) species: Toxinological studies until 2011. Advances in Environmental Research. 2012;26:133-148
  37. 37. Nagelkerken I, Nagelkerken WP. Loss of coral cover and biodiversity on shallow Acropora and Millepora reefs after 31 years on Curaçao, Netherlands Antilles. Bulletin of Marine Science. 2004;74:213-223
  38. 38. Coni EO, Ferreira CM, de Moura RL, Meirelles PM, Kaufman L, Francini-Filho RB. An evaluation of the use of branching fire-corals (Millepora spp.) as refuge by reef fish in the Abrolhos Bank, eastern Brazil. Environmental Biology of Fishes. 2013;96(1):45-55
  39. 39. Kayal E, Roure B, Philippe H, Collins AG, Lavrov DV. Cnidarian phylogenetic relationships as revealed by mitogenomics. BMC Evolutionary Biology. 2013;13(1):5
  40. 40. Bouillon J. Essai de classification des hydropolypes-hydroméduses (Hydrozoa-Cnidaria). Indo-Malayan Zoology. 1985;1:29-243
  41. 41. Schuchert P. The Hydrozoa Directory [Internet]. 2005. Available from: [Accessed 2019-02-09]
  42. 42. Bouillon J, Gravili C, Pagès F, Gili J-M, Boero F. An introduction to Hydrozoa. Mémoires du Muséum National d’Histoire Naturelle Paris. 2006;194:1-591
  43. 43. Linnaeus C. Systema Naturae. Vol. I. Laurentii Salvii: Holmiae; 1758
  44. 44. Duchassaing P, Michelotti J. Mémoire sur les Coralliaires des Antilles. Mémoire sur les coralliaires des Antilles 2. 1860;19:279-365
  45. 45. Hickson SJ. Notes on the collection of specimens of the genus Millepora, obtained by Mr. Stanley Gardiner at Funafuti and Rotuma. In: Proceedings of the Zoological Society of London. Vol. 66. 1898. pp. 828-833
  46. 46. Boschma H. The species problem in Millepora. Zoologische Verhandelingen. 1948;1:1-115
  47. 47. Boschma H. On a new species of Millepora from Mauritius, with notes on the specific characters of Millepora exaesa. In: Proceedings of the Koninklijke Nedderlandse Akademie van Wetenschappen. Vol. 69. 1966. pp. 409-419
  48. 48. Heckenhauer J, Schweinsberg M, Elbrecht V, John U, Tollrian R, Lampert KP. Isolation, characterization and cross amplification of eleven novel microsatellite loci for the hydrozoan coral Millepora. Conservation Genetics Resources. 2015;7:215-217
  49. 49. Tepper CS, Gaynor SC. Ribosomal internal transcribed spacer (ITS) DNA variation in Millepora. Journal of Marine Science Research and Development. 2015;6:1
  50. 50. Dubé CE, Planes S, Zhou Y, Berteaux-Lecellier V, Boissin E. Genetic diversity and differentiation in reef-building Millepora species, as revealed by cross-species amplification of fifteen novel microsatellite loci. PeerJ. 2017;5:e2936
  51. 51. Lewis JB. Biology and ecology of the hydrocoral Millepora on coral reefs. Marine Biology. 2006;50:1-53
  52. 52. Boschma H. Milleporina and Stylasterina. In: Moore RC, editor. Treatise on Invertebrate Paleontology. Part F, Coelenterata. London: Geological Society of America and University of Kansas Press; 1956
  53. 53. Vaughan TW. Fossil corals from Central America, Cuba and Puerto Rico, with an account of the American tertiary, Pleistocene, and recent coral reefs. United States National Museum Bulletin. 1919;103:189-524
  54. 54. Rehfeld U, Ernst G. Hydrozoan build-ups of Millepora irregularis sp. nov. and fungiid coral meadows of Cunnolites Alloiteau (Anthozoa) - Palaeoecological and palaeoceanographical implications for the upper cretaceous of North Cantabria (northern Spain). Facies. 1998;39:125-138
  55. 55. Florez P, Zapata-Ramirez P, Klaus JS. Early Miocene shallow-water corals from La Guajira, Colombia: Part II, Mussidae-Siderastreidae and Milleporidae. Journal of Paleontology. 2019;93:416-436
  56. 56. Vyverberg K, Dechnik B, Dutton A, Webster JM, Zwartz D, Portell RW. Episodic reef growth in the granitic Seychelles during the last interglacial: Implications for polar ice sheet dynamics. Marine Geology. 2018;399:170-187
  57. 57. Arrigoni R, Maggioni D, Montano S, Hoeksema BW, Seveso D, Shlesinger T, et al. An integrated morpho-molecular approach to delineate species boundaries of Millepora from the Red Sea. Coral Reefs. 2018;37(4):967-984
  58. 58. Dubé CE, Boissin E, Maynard JA, Planes S. Fire coral clones demonstrate phenotypic plasticity among reef habitats. Molecular Ecology. 2017;26:3860-3869
  59. 59. Dubé CE, Boissin E, Planes S. Overgrowth of living scleractinian corals by the hydrocoral Millepora platyphylla in Moorea, French Polynesia. Marine Biodiversity. 2016;46(2):329-330
  60. 60. Wegener C, Martin B, Didden C, Edmunds PJ. Overgrowth of Caribbean octocorals by milleporid hydrocorals. Invertebrate Biology. 2018;137(1):29-37
  61. 61. WoRMS 2019. Millepora Linnaeus [Internet]. 1758. Available from: [Accessed 2019-02-09]
  62. 62. Duchassaing P, Michelotti J, et al. Supplément au Mémoire sur les coralliaires des Antilles 2. 1864;23:1-256
  63. 63. Hickson SJ. Report on the specimens of the genus Millepora collected by Dr. Willey. Journal of Zoology. 1902;119:661-672
  64. 64. Duchassaing P. Animaux radiaires des Antilles. Paris: Typographie Plon Fréres; 1850. 48 p
  65. 65. Razak TB, Hoeksema BW. The hydrocoral genus Millepora (Hydrozoa: Capitata: Milleporidae) in Indonesia. Zoologische Verhandelingen Leiden. 2003;345:313-336
  66. 66. Moschencko AV. Anatomy and morphology of skeleton and soft tissues of Millepora spp. (Hydrozoa, Athecata, Milleporidae). Zoologicheskiĭ Zhurnal. 1993;72:5-14
  67. 67. Ruiz-Ramos DV, Weil E, Schizas NV. Morphological and genetic evaluation of the hydrocoral Millepora species complex in the Caribbean. Zoological Studies. 2014;53:15
  68. 68. De Souza JN, Nunes FL, Zilberberg C, Sanchez JA, Migotto AE, Hoeksema BW, et al. Contrasting patterns of connectivity among endemic and widespread fire coral species (Millepora spp.) in the tropical Southwestern Atlantic. Coral Reefs. 2017;36(3):701-716
  69. 69. Bourmaud CA-F, Leung JKL, Bollard S, Gravier-Bonnet N. Mass spawning events, seasonality and reproductive features in Milleporids (Cnidaria, Hydrozoa) from Reunion Island. Marine Ecology. 2013;34:14-24
  70. 70. Shlesinger T, Loya Y. Mass medusae release and temporal reproductive segregation among the three Red Sea fire coral species. Bulletin of the Ecological Society of America. 2019;100(2):1-3
  71. 71. Hebert PDN, Ratnasingham S, de Waard JR. Barcoding animal life: Cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London B: Biological Sciences. 2003;270:S96-S99
  72. 72. Hoareau TB, Boissin E. Design of phylum-specific hybrid primers for DNA barcoding: Addressing the need for efficient COI amplification in the Echinodermata. Molecular Ecology Resources. 2010;10:960-967
  73. 73. Bucklin A, Steinke D, Blanco-Bercial L. DNA barcoding of marine Metazoa. In: Carlson CA, Giovannoni SJ, editors. Annual Review of Marine Science. Vol. 3. Palo Alto: Annual Reviews; 2011. pp. 471-508
  74. 74. Geller J, Meyer C, Parker M, Hawk H. Redesign of PCR primers for mitochondrial cytochrome c oxidase subunit I for marine invertebrates and application in all-taxa biotic surveys. Molecular Ecology Resources. 2013;13:851-861
  75. 75. Amaral FD, Steiner AQ, Broadhurst MK, Cairns SD. An overview of the shallow-water calcified hydroids from Brazil (Hydrozoa: Cnidaria), including the description of a new species. Zootaxa. 1930;2008:56-68
  76. 76. Hoeksema BW, Nunes FLD, Lindner A, De Souza JN. Millepora alcicornis (Hydrozoa: Capitata) at Ascension Island: Confirmed identity based on morphological and molecular analyses. Journal of the Marine Biological Association of the United Kingdom. 2017;97:709-712
  77. 77. Boissin E, Pogoreutz C, Pey A, Gravier-Bonnet N, Planes S. Millepora platyphylla (Cnidaria, Hydrozoa) range extended back to the eastern Pacific, thanks to a new record from Clipperton atoll. Zootaxa. 2019;4668:599-600
  78. 78. Glynn PW, de Weerdt WH. Elimination of 2 reef-building hydrocorals following the 1982-83 El-Nino warming event. Science. 1991;253:69-71
  79. 79. Clemente S, Rodríguez A, Brito A, Ramos A, Monterroso Ó, Hernández JC. On the occurrence of the hydrocoral Millepora (Hydrozoa: Milleporidae) in the subtropical eastern Atlantic (Canary Islands): Is the colonization related to climatic events? Coral Reefs. 2011;30(1):237-240
  80. 80. Jokiel PL. Rafting of reef corals and other organisms at Kwajalein atoll. Marine Biology. 1989;101:483-493
  81. 81. López C, Clemente S, Almeida C, Brito A, Hernández M. A genetic approach to the origin of Millepora sp. in the eastern Atlantic. Coral Reefs. 2015;34(2):631-638
  82. 82. Lewis JB. The ecology of Millepora. Coral Reefs. 1989;8:99-107
  83. 83. Cairns SD. Worldwide distribution of the Stylasteridae (Cnidaria: Hydrozoa). Scientia Marina. 1992;56:125-130
  84. 84. Dustan P, Halas JC. Changes in the reef-coral community of Carysfort reef, Key largo, Florida: 1974 to 1982. Coral Reefs. 1987;6(2):91-106
  85. 85. Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, van Woesik R. Coral bleaching: The winners and the losers. Ecology Letters. 2001;4(2):122-131
  86. 86. Arias-González JE, Legendre P, Rodríguez-Zaragoza FA. Scaling up beta diversity on Caribbean coral reefs. Journal of Experimental Marine Biology and Ecology. 2008;366(1–2):28-36
  87. 87. Loya Y. Recolonization of Red Sea corals affected by natural catastrophes and man-made perturbations. Ecology. 1976;57(2):278-289
  88. 88. Richard C, Benzoni F, Dutrieux E, Chaîneau CH. Marine Sensitivity Mapping of the Southern Coast of Yemen: From Balhaf to Mukallah, Creocean. Montpellier: UMR 227 Coreus 2, Labex CORAIL, Institut de Recherche pour le Développement; 2011. 101 p
  89. 89. Andréfouët S, Benzoni F, Payri C. A monospecific Millepora reef in Marquesas Island, French Polynesia. Coral Reefs. 2014;33:463
  90. 90. Rioja-Nieto R, Álvarez-Filip L. Coral reef systems of the Mexican Caribbean: Status, recent trends and conservation. Marine Pollution Bulletin. 2019;140:616-625
  91. 91. Dubé CE, Mercière A, Vermeij MJ, Planes S. Population structure of the hydrocoral Millepora platyphylla in habitats experiencing different flow regimes in Moorea, French Polynesia. PLoS One. 2017;12:e0173513
  92. 92. Strömgren T. Skeleton growth of the hydrocoral Millepora complanata Lamarck in relation to light. Limnology and Oceanography. 1976;21(1):156-160
  93. 93. Meroz-Fine E, Brickner I, Loya Y, Ilan M. The hydrozoan coral Millepora dichotoma: Speciation or phenotypic plasticity? Marine Biology. 2003;143:1175-1183
  94. 94. Monismith SG. Hydrodynamics of coral reefs. Annual Review of Fluid Mechanics. 2007;39:37-55
  95. 95. Ferrario F, Beck MW, Storlazzi CD, Micheli F, Shepard CC, Airoldi L. The effectiveness of coral reefs for coastal hazard risk reduction and adaptation. Nature Communications. 2014;13:5
  96. 96. Lewis JB. Spatial distributions of the calcareous hydrozoans Millepora complanata and Millepora squarrosa on coral reefs. Bulletin of Marine Science. 1996;59(1):188-195
  97. 97. Faure G. Recherches sur le peuplement de scléractiniaires des récifs coralliens de l’archipel des Mascareignes (Ocean Indien occidental) [thesis]. Marseille: Université Aix-Marseille II; 1982
  98. 98. Garcia TM, Matthews-Cascon H, Franklin-Junior W. Millepora alcicornis (Cnidaria: Hydrozoa) as substrate for benthic fauna. Brazilian Journal of Oceanography. 2009;57:153-155
  99. 99. Stella JS, Jones GP, Pratchett MS. Variation in the structure of epifaunal invertebrate assemblages among coral hosts. Coral Reefs. 2010;29(4):957-973
  100. 100. Glynn PW, Enochs IC. Invertebrates and their roles in coral reef ecosystems. In: Coral Reefs: An Ecosystem in Transition. Dordrecht: Springer; 2011. pp. 273-325
  101. 101. Pereira PHC, Leal ICS, de Araújo ME, Souza AT. Feeding association between reef fishes and the fire coral Millepora spp. (Cnidaria: Hydrozoa). Marine Biodiversity Records. 2012;5:e42
  102. 102. Leal ICS, Pereira PHC, De Araujo ME. Coral reef fish association and behaviour on the fire coral Millepora spp. in north-East Brazil. Journal of the Marine Biological Association of the United Kingdom. 2013;93:1703-1711
  103. 103. Vermeij MJ, DeBey H, Grimsditch G, Brown J, Obura D, DeLeon R, et al. Negative effects of gardening damselfish Stegastes planifrons on coral health depend on predator abundance. Marine Ecology Progress Series. 2015;528:289-296
  104. 104. Hoeksema BW, Ten Hove HA. Attack on a Christmas tree worm by a Caribbean sharpnose pufferfish at St. Eustatius, Dutch Caribbean. Bulletin of Marine Science. 2017;93(4):1023-1024
  105. 105. Perry O, Sapir Y, Perry G, Ten Hove H, Fine M. Substrate selection of Christmas tree worms (Spirobranchus spp.) in the Gulf of Eilat, Red Sea. Journal of the Marine Biological Association of the United Kingdom. 2018;98(4):791-799
  106. 106. Kayal M, Kayal E. Colonies of the fire coral Millepora platyphylla constitute scleractinian survival oases during Acanthaster outbreaks in French Polynesia. Marine Biodiversity. 2017;47(1):255-258
  107. 107. Bertelsen E, Ussing H. Marine tropical animals carried to the Copenhagen Sydhavn on a ship from the Bermudas. Vidensk Medd Dansk Naturhist Foren Kobenhavn. 1936;100:237-245
  108. 108. Wahle CM. Detection, pursuit, and overgrowth of tropical gorgonians by milleporid hydrocorals: Perseus and Medusa revisited. Science. 1980;209:689-691
  109. 109. Glynn PW. Feeding ecology of selected coral-reef macroconsumers: Patterns and effects on coral reef community structure. In: Dubinsky Z, editor. Ecosystems of the World: Coral Reefs. New York: Elsevier; 1990. pp. 365-400
  110. 110. LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD, Voolstra CR, et al. Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Current Biology. 2018;28(16):2570-2580
  111. 111. Hoegh-Guldberg O. Climate change, coral bleaching and the future of the world’s coral reefs. Marine and Freshwater Research. 1999;50(8):839-866
  112. 112. Weis V, Reynolds W, de Boer M, Krupp D. Host-symbiont specificity during onset of symbiosis between the dinoflagellates Symbiodinium spp. and planula larvae of the scleractinian coral Fungia scutaria. Coral Reefs. 2001;20:301-308
  113. 113. Yellowlees D, Rees TAV, Leggat W. Metabolic interactions between algal symbionts and invertebrate hosts. Plant, Cell and Environment. 2008;31:679-694
  114. 114. Davy SK, Allemand D, Weis VM. Cell biology of cnidarian-Dinoflagellate symbiosis. Microbiology and Molecular Biology Reviews. 2012;76:229-261
  115. 115. Mieog JC, Olsen JL, Berkelmans R, Bleuler-Martinez SA, Willis BL, van Oppen MJH. The roles and interactions of symbiont, host and environment in defining coral fitness. PLoS One. 2009;4:e6364
  116. 116. Parkinson JE, Banaszak AT, Altman NS, LaJeunesse TC, Baums IB. Intraspecific diversity among partners drives functional variation in coral symbioses. Scientific Reports. 2015;5:1-12
  117. 117. Lewis JB. Heterotrophy in corals: Zooplankton predation by the hydrocoral Millepora complanata. Marine Ecology Progress Series. 1993;90:251
  118. 118. Banaszak AT, Santos MGB, LaJeunesse TC, Lesser MP. The distribution of mycosporine-like amino acids (MAAs) and the phylogenetic identity of symbiotic dinoflagellates in cnidarian hosts from the Mexican Caribbean. Journal of Experimental Marine Biology and Ecology. 2006;332:31-146
  119. 119. van Oppen MJ, Baker AC, Coffroth MA, Willis BL. Bleaching resistance and the role of algal endosymbionts. In: Coral Bleaching. Berlin: Heidelberg; 2009. pp. 83-102
  120. 120. Baker AC. Flexibility and specificity in coral-algal symbiosis: Diversity, ecology, and biogeography of Symbiodinium. Annual Review of Ecology, Evolution, and Systematics. 2003;34:661-689
  121. 121. Samayoa A, Reyes S, Karim YB, Roge-Jones L, Rueth M, Tepper C. Patterns of Millepore-Symbiodinium associations at two Caribbean locations: San Salvador, the Bahamas and south water Caye, Belize. In: Proceedings of the First Joint Natural History and Geology Symposium. 2017
  122. 122. Rodríguez L, López C, Casado-Amezua P, Ruiz-Ramos DV, Martínez B, Banaszak A, et al. Genetic relationships of the hydrocoral Millepora alcicornis and its symbionts within and between locations across the Atlantic. Coral Reefs. 2019;38(2):255-268
  123. 123. Lesser MP. Coral bleaching: Causes and mechanisms. In: Dubinsky Z, Stambler N, editors. Coral Reefs: An Ecosystem in Transition. Dordrecht: Springer; 2011. pp. 405-419
  124. 124. Bonesso JL, Leggat W, Ainsworth TD. Exposure to elevated sea-surface temperatures below the bleaching threshold impairs coral recovery and regeneration following injury. PeerJ. 2017;5:e3719
  125. 125. Neal BP, Khen A, Treibitz T, Beijbom O, O’Connor G, Coffroth MA, et al. Caribbean massive corals not recovering from repeated thermal stress events during 2005-2013. Ecology and Evolution. 2017;7(5):1339-1353
  126. 126. Oliver JK, Berkelmans R, Eakin CM. Coral bleaching in space and time. In: Coral Bleaching. Cham: Springer; 2018. pp. 27-49
  127. 127. Baker AC, Glynn PW, Riegl B. Climate change and coral reef bleaching: An ecological assessment of long-term impacts, recovery trends and future outlook. Estuarine, Coastal and Shelf Science. 2008;80(4):435-471
  128. 128. Grottoli AG, Warner ME, Levas SJ, Aschaffenburg MD, Schoepf V, McGinley M, et al. The cumulative impact of annual coral bleaching can turn some coral species winners into losers. Global Change Biology. 2014;20(12):3823-3833
  129. 129. Okazaki RR, Towle EK, Van Hooidonk R, Mor C, Winter RN, Piggot AM, et al. Species-specific responses to climate change and community composition determine future calcification rates of Florida keys reefs. Global Change Biology. 2016;23(3):1023-1035
  130. 130. Marshall PA, Baird AH. Bleaching of corals on the great barrier reef: Differential susceptibilities among taxa. Coral Reefs. 2000;19:155-163
  131. 131. Rowan R, Knowlton N, Baker A, Jara J. Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature. 1997;388(6639):265
  132. 132. Guest JR, Baird AH, Maynard JA, Muttaqin E, Edwards AJ, Campbell SJ, et al. Contrasting patterns of coral bleaching susceptibility in 2010 suggest an adaptive response to thermal stress. PLoS One. 2012;7(3):e33353
  133. 133. Dias TL, Gondim AI. Bleaching in scleractinians, hydrocorals, and octocorals during thermal stress in a northeastern Brazilian reef. Marine Biodiversity. 2016;46(1):303-307
  134. 134. Glynn PW. Coral reef bleaching: Ecological perspectives. Coral Reefs. 1993;12(1):1-7
  135. 135. Glynn PW, Feingold JS. Hydrocoral species not extinct. Science. 1992;257(5078):1845-1847
  136. 136. Cook CB, Logan A, Ward J, Luckhurst B, Berg CJ. Elevated temperatures and bleaching on a high latitude coral reef: The 1988 Bermuda event. Coral Reefs. 1990;9(1):45-49
  137. 137. Williams EH Jr, Bunkley-Williams L, et al. Atoll Research Bulletin. 1990;335:1-71
  138. 138. Wagner DE, Kramer P, van Woesik R. Species composition, habitat, and water quality influence coral bleaching in southern Florida. Marine Ecology Progress Series. 2010;408:65-78
  139. 139. Olguín-López N, Hérnandez-Elizárraga VH, Hernández-Matehuala R, Cruz-Hernández A, Guevara-González R, Caballero-Pérez J, et al. Impact of El Niño-southern oscillation 2015-2016 on the soluble proteomic profile and cytolytic activity of Millepora alcicornis (“fire coral”) from the Mexican Caribbean. PeerJ. 2019;7:e6593
  140. 140. van Woesik R, Sakai K, Ganase A, Loya Y. Revisiting the winners and the losers a decade after coral bleaching. Marine Ecology Progress Series. 2011;434:67-76
  141. 141. Morri C, Bianchi CN, Aliani S. Coral reefs at Gangehi (north Ari atoll, Maldive Islands). Publications du Service Géologique du Luxembourg. 1995;29:3-12
  142. 142. Coleman FC, Dennis GD, Jaap WC, Schmahl GP, Koenig CC, Reed SA, et al. Final Report to the National Oceanic and Atmospheric Administration Coral Reef Conservation Program. Part 1, Status and Trends in Habitat Characterization of the Florida Middle Grounds; 2004
  143. 143. Wells JW, Davies PS. Preliminary list of stony corals from Addu atoll. Atoll Research Bulletin. 1966;116:43-55
  144. 144. Coleman N. Marine Life of the Maldives. Sea Challengers. Appollo Bay: Atoll Editions; 2000
  145. 145. McClanahan TR. Bleaching damage and recovery potential of Maldivian coral reefs. Marine Pollution Bulletin. 2000;40(7):587-597
  146. 146. Bianchi CN, Morri C, Pichon M, Benzoni F, Colantoni P, Baldelli G, et al. Dynamics and pattern of coral recolonization following the 1998 bleaching event in the reefs of the Maldives. In: Proceedings of the 10th International Coral Reef Symposium, Okinawa, Japan. Vol. 1. 2006. pp. 30-37
  147. 147. Bianchi CN, Morri C, Colantoni P, Sandrini M. Italian research in the Maldives. Reef Encounter. 2009;37:17
  148. 148. Gravier-Bonnet N, Bourmaud CA-F. Hydroids (Cnidaria, Hydrozoa) of Baa atoll (Indian Ocean, Maldives archipelago). In: Biodiversity, Resources, and Conservation of Baa Atoll (Republic of Maldives): A Unesco Man and Biosphere Reserve. 2012
  149. 149. Wilkinson C, Linden O, Cesar H, Hodgson G, Rubens J, Strong AE. Ecological and socioeconomic impacts of 1998 coral mortality in the Indian Ocean: An ENSO impact and a warning of future change? Ambio. 1999;28(2):188-196
  150. 150. Gleason MG. Effects of disturbance on coral communities: Bleaching in Moorea, French Polynesia. Coral Reefs. 1993;12(3–4):193-201
  151. 151. Banaszak AT, Ayala-Schiaffino BN, Rodríguez-Román A, Enríquez S, Iglesias-Prieto R. Response of Millepora alcicornis (Milleporina: Milleporidae) to two bleaching events at Puerto Morelos reef, Mexican Caribbean. Revista de Biología Tropical. 2003;51(4):57-66
  152. 152. Zvuloni A, Armoza-Zvuloni R, Shaked Y. Multifocal bleaching of Millepora dichotoma in the Gulf of Aqaba (Eilat), Red Sea. Marine Ecology Progress Series. 2011;441:25-32
  153. 153. Paramasivam N, Ben-Dov E, Arotsker L, Kramarsky-Winter E, Zvuloni A, Loya Y, et al. Bacterial consortium of Millepora dichotoma exhibiting unusual multifocal lesion event in the Gulf of Eilat, Red Sea. Microbial Ecology. 2013;65(1):50-59
  154. 154. Bay RA, Palumbi SR. Rapid acclimation ability mediated by transcriptome changes in reef-building corals. Genome Biology and Evolution. 2015;7(6):1602-1612
  155. 155. Pinzón JH, Kamel B, Burge CA, Harvell CD, Medina M, Weil E, et al. Whole transcriptome analysis reveals changes in expression of immune-related genes during and after bleaching in a reef-building coral. Royal Society Open Science. 2015;2(4):140214
  156. 156. Seneca FO, Palumbi SR. The role of transcriptome resilience in resistance of corals to bleaching. Molecular Ecology. 2015;24(7):1467-1484
  157. 157. Ruiz-Jones LJ, Palumbi SR. Tidal heat pulses on a reef trigger a fine-tuned transcriptional response in corals to maintain homeostasis. Science Advances. 2017;3(3):e1601298
  158. 158. Huang Y, Yuan J, Zhang Y, Peng H, Liu L. Molecular cloning and characterization of calmodulin-like protein CaLP from the Scleractinian coral Galaxea astreata. Cell Stress & Chaperones. 2018;23(6):1329-1335
  159. 159. Mayfield AB, Chen Y-J, Lu C-Y, Chen C-S. The proteomic response of the reef coral Pocillopora acuta to experimentally elevated temperatures. PLoS One. 2018;13(1):e0192001
  160. 160. Brown D, Edmunds PJ. Differences in the responses of three scleractinians and the hydrocoral Millepora platyphylla to ocean acidification. Marine Biology. 2016;163(3):62
  161. 161. Marangoni LFB, Calderon EN, Marques JA, Duarte GAS, Pereira CM, Castro CB, et al. Effects of CO2-driven acidification of seawater on the calcification process in the calcareous hydrozoan Millepora alcicornis (Linnaeus, 1758). Coral Reefs. 2017;36:1133-1141
  162. 162. Kroeker KJ, Kordas RL, Crim R, Hendriks IE, Ramajo L, Singh GS, et al. Impacts of ocean acidification on marine organisms: Quantifying sensitivities and interaction with warming. Global Change Biology. 2013;19(6):1884-1896
  163. 163. Chan NCS, Connolly SR. Sensitivity of coral calcification to ocean acidification: A meta-analysis. Global Change Biology. 2013;19(1):282-290
  164. 164. Kaniewska P, Campbell PR, Kline DI, Rodriguez-Lanetty M, Miller DJ, Dove S, et al. Major cellular and physiological impacts of ocean acidification on a reef building coral. PLoS One. 2012;7:e34659
  165. 165. Soriano-Santiago OS, Liñán-Cabello MA, Delgadillo-Nuño MA, Ortega-Ortiz C, Cuevas-Venegas S. Physiological responses to oxidative stress associated with pH variations in host tissue and zooxanthellae of hermatypic coral Pocillopora capitata. Marine and Freshwater Behaviour and Physiology. 2013;46(5):275-286
  166. 166. Luz DC, Zebral YD, Klein RD, Marques JA, de Barros Marangoni LF, Pereira CM, et al. Oxidative stress in the hydrocoral Millepora alcicornis exposed to CO2-driven seawater acidification. Coral Reefs. 2018;37(2):571-579
  167. 167. Downs CA, Fauth JE, Halas JC, Dustan P, Bemiss J, Woodley CM. Oxidative stress and seasonal coral bleaching. Free Radical Biology and Medicine. 2002;33:533-543
  168. 168. Todd PA. Morphological plasticity in scleractinian corals. Biological Reviews of the Cambridge Philosophical Society. 2008;83:315-337
  169. 169. Denny MW. Biology and the Mechanics of the Wave-Swept Environment. New Jersey: Princeton University Press; 2014
  170. 170. Swierts T, Vermeij MJA. Competitive interactions between corals and turf algae depend on coral colony form. PeerJ. 2016;4:e1984
  171. 171. Baird AH, Hughes TP. Competitive dominance by tabular corals: An experimental analysis of recruitment and survival of understorey assemblages. Journal of Experimental Marine Biology and Ecology. 2000;251:117-132
  172. 172. Madin JS. Mechanical limitations of reef corals during hydrodynamic disturbances. Coral Reefs. 2005;24:630-635
  173. 173. Madin JS, Baird AH, Dornelas M, Connolly SR. Mechanical vulnerability explains size-dependent mortality of reef corals. Ecology Letters. 2014;17:1008-1015
  174. 174. Ayre DJ, Willis BL. Population structure in the coral Pavona cactus: Clonal genotypes show little phenotypic plasticity. Marine Biology. 1988;99:495-505
  175. 175. West JM, Harvell CD, Walls AM. Morphological plasticity in a gorgonian coral (Briareum asbestinum) over a depth cline. Marine Ecology Progress Series. 1993;94:61-69
  176. 176. Bruno JF, Edmunds PJ. Clonal variation for phenotypic plasticity in the coral Madracis mirabilis. Ecology. 1997;78:2177-2190
  177. 177. Hill MS, Hill AL. Morphological plasticity in the tropical sponge Anthosigmella varians: Responses to predators and wave energy. The Biological Bulletin. 2002;202:86-95
  178. 178. Pineda-Krch M, Lehtilä K. Costs and benefits of genetic heterogeneity within organisms. Journal of Evolutionary Biology. 2004;17:1167-1177
  179. 179. Agrawal AA. Phenotypic plasticity in the interactions and evolution of species. Science. 2001;294:321-326
  180. 180. Beaman JE, White CR, Seebacher F. Evolution of plasticity: Mechanistic link between development and reversible acclimation. Trends in Ecology & Evolution. 2016;31:237-249
  181. 181. Edmunds PJ. The role of colony morphology and substratum inclination in the success of Millepora alcicornis on shallow coral reefs. Coral Reefs. 1999;18:133-140
  182. 182. Jackson JBC. Morphological strategies of sessile animals. In: Larwood G, Rosen BR, editors. Biology and Systematics of Colonial Organisms. London: Academic Press; 1979. pp. 499-555
  183. 183. Highsmith RC. Reproduction by fragmentation in corals. Marine Ecology Progress Series. 1982;7:207-226
  184. 184. Jackson JBC. Modes of dispersal of clonal benthic invertebrates: Consequences for 4 species’ distributions and genetic structure of local populations. Bulletin of Marine Science. 1986;39:588-605
  185. 185. Sherman CDH, Ayre DJ, Miller KJ. Asexual reproduction does not produce clonal populations of the brooding coral Pocillopora damicornis on the great barrier reef, Australia. Coral Reefs. 2006;25:7-18
  186. 186. Foster NL, Baums IB, Sanchez JA, Paris CB, Chollett I, Agudelo CL, et al. Hurricane-driven patterns of clonality in an ecosystem engineer: The Caribbean coral Montastraea annularis. PLoS One. 2013;8(1):e53283
  187. 187. Harrison PL. Sexual reproduction of scleractinian corals. In: Zvy D, Stambler N, editors. Coral Reefs: An Ecosystem in Transition. Dordrecht: Springer Netherlands; 2011. pp. 59-85
  188. 188. Gravier-Bonnet N, Bourmaud CA-F. Cloning by releasing specialized frustules in a successful epiphytic zooxanthellate halecid (Cnidaria, Hydrozoa, Haleciidae), with comments on stolonization and frustulation. Journal of Invertebrate Reproduction and Development. 2005;48:63-69
  189. 189. Pearson EA, Murray SN. Patterns of reproduction, genetic diversity, and genetic differentiation in California populations of the geniculate coralline alga Lithothrix aspergillum (Rhodophyta). Journal of Phycology. 1997;33:753-763
  190. 190. Sherman CDH, Ayre DJ. Fine-scale adaptation in a clonal sea anemone. Evolution. 2008;62:1373-1380
  191. 191. Hoareau TB, Boissin E, Conand C. First record of asexual reproduction of Holothuria hilla in a fringing reef of Reunion Island. SPC Beche-de-Mer Information Bulletin. 2010;27:24
  192. 192. Kahng SE, Benayahu Y, Lasker HR. Sexual reproduction in octocorals. Marine Ecology Progress Series. 2011;443:265-283
  193. 193. Whalan S, Johnson MS, Harvey E, Battershill C. Mode of reproduction, recruitment, and genetic subdivision in the brooding sponge Haliclona sp. Marine Biology. 2005;146:425-433
  194. 194. Miller KJ, Ayre DJ. The role of sexual and asexual reproduction in structuring high latitude populations of the reef coral Pocillopora damicornis. Heredity. 2004;92:557-568
  195. 195. Gorospe KD, Karl SA. Genetic relatedness does not retain spatial pattern across multiple spatial scales: Dispersal and colonization in the coral Pocillopora damicornis. Molecular Ecology. 2013;22:3721-3736
  196. 196. Baums IB, Devlin-Durante M, Laing BA, Feingold J, Smith T, Bruckner A, et al. Marginal coral populations: The densest known aggregation of Pocillopora in the Galápagos archipelago is of asexual origin. Frontiers in Marine Science. 2014;1:59
  197. 197. Rice WR, Chippindale AK. Sexual recombination and the power of natural selection. Science. 2001;294:555-559
  198. 198. Williams GC. Sex and Evolution. Princeton University Press: Princeton; 1975
  199. 199. Brazeau DA, Lasker HR. Sexual reproduction and external brooding by the Caribbean gorgonian Briareum asbestinum. Marine Biology. 1990;104:465-474
  200. 200. Ereskovsky AV, Tokina DB. Asexual reproduction in homoscleromorph sponges (Porifera; Homoscleromorpha). Marine Biology. 2007;151:425-434
  201. 201. Reitzel AM, Burton PM, Krone C, Finnerty JR. Comparison of developmental trajectories in the starlet sea anemone Nematostella vectensis: Embryogenesis, regeneration, and two forms of asexual fission. Invertebrate Biology. 2007;126:99-112
  202. 202. Gutiérrez-Rodríguez C, Lasker HR. Reproductive biology, development, and planula behavior in the Caribbean gorgonian Pseudopterogorgia elisabethae. Invertebrate Biology. 2004;123:54-67
  203. 203. Nakajima Y, Chuang PS, Ueda N, Mitarai S. First evidence of asexual recruitment of Pocillopora acuta in Okinawa Island using genotypic identification. PeerJ. 2018;6:e5915
  204. 204. Oury N, Gélin P, Massé L, Magalon H. First study of asexual planulae in the coral Pocillopora damicornis type β SSH05c from the southwestern Indian Ocean. Coral Reefs. 2019;38(3):499-503
  205. 205. Nomura J. Sexual Reproduction of Millepora intricata and Millepora tenella (Hydrozoa : Milleporidae) [Thesis]. Okinawa: University of the Ryukyus; 1998
  206. 206. Soong K, Cho LC. Synchronized release of medusae from three species of hydrozoan fire corals. Coral Reefs. 1998;17:145-154
  207. 207. Boschma H. The ampullae of Millepora. In: Proceedings Koninklijke Nederlandse Akademie van Wetenschappen Amsterdam. Vol. 3. 1949. pp. 2-3
  208. 208. Boschma H. Further notes on the ampullae of Millepora. Zoologische Mededelingen Leiden. 1950;31:49-61
  209. 209. de Weerdt WH. Taxonomic characters in Caribbean Millepora species (Hydrozoa, Coelenterata). Bijdragen tot de Dierkunde. 1984;54:243-262
  210. 210. Quelch JJ. The Milleporidae. Nature. 1884;30:539
  211. 211. Quelch JJ. Report of the reef-corals collected by H. M. S. challenger during the years 1873-76. Reports of the Challenger, Zoology. 1886;6:189-194
  212. 212. Boschma H. Notes on the ampullae of two colonies of Millepora. In: Proceedings Koninklijke Nederlandse Akademie van Wetenschappen Amsterdam. Vol. 67. 1964. pp. 195-200
  213. 213. Gili J-M, Hughes RG. The ecology of marine benthic hydroids. Oceanography and Marine Biology: An Annual Review. 1995;33:351-426
  214. 214. Tsounis G, Rossi S, Aranguren M, Gili JM, Arntz W. Effects of spatial variability and colony size on the reproductive output and gonadal development cycle of the Mediterranean red coral (Corallium rubrum L.). Marine Biology. 2006;148:513-527
  215. 215. Gaines SD, Gaylord B, Largier JL. Avoiding current oversights in marine reserve design. Ecological Applications. 2003;13:32-46
  216. 216. Ayre DJ, Hughes TP. Climate change, genotypic diversity and gene flow in reef-building corals. Ecology Letters. 2004;7:273-278
  217. 217. Steneck RS. Staying connected in a turbulent world. Science. 2006;311:480-481
  218. 218. Adjeroud M, Guérécheau A, Vidal-Dupiol J, Flot JF, Arnaud-Haond S, Bonhomme F. Genetic diversity, clonality and connectivity in the scleractinian coral Pocillopora damicornis: A multi-scale analysis in an insular, fragmented reef system. Marine Biology. 2014;161(3):531-541
  219. 219. Combosch DJ, Vollmer SV. Population genetics of an ecosystem-defining reef coral Pocillopora damicornis in the tropical eastern Pacific. PLoS One. 2011;6:e21200
  220. 220. Pinzón JH, Reyes-Bonilla H, Baums IB, Lajeunesse TC. Contrasting clonal structure among Pocillopora (Scleractinia) communities at two environmentally distinct sites in the Gulf of California. Coral Reefs. 2012;3:765-777
  221. 221. Dubé CE, Boissin E, Mercière A, Planes S. Dispersal limitations of early life stages and sibling aggregations in a broadcasting Millepora hydrocoral, as revealed by parentage analysis. bioRxiv. 2018;1:413963
  222. 222. Hughes RN. Lessons in modularity: The evolutionary ecology of colonial invertebrates. Scientia Marina. 2005;69:169-179
  223. 223. Jackson JBC. Competition on marine hard substrata: The adaptive significance of solitary and colonial strategies. American Naturalist. 1977;111:743-767
  224. 224. Jackson JBC. Distribution and ecology of clonal and aclonal benthic invertebrates. In: Jackson JBC, Buss LW, Cook RE, editors. Population Biology and Evolution of Clonal Organisms. New Haven: Yale University Press; 1985. pp. 297-355
  225. 225. Hughes TP, Jackson JBC. Do corals lie about their age? Some demographic consequences of partial mortality, fission and fusion. Science. 1980;209:713-715
  226. 226. Hughes RN. A Functional Biology of Clonal Animals. New York: Chapman and Hall; 1989
  227. 227. Hall VR, Hughes TP. Reproductive strategies of modular organisms: Comparative studies of reef-building corals. Ecology. 1996;77:950-963
  228. 228. Wood R. Reef Evolution. Oxford: Oxford University Press; 1999
  229. 229. de Weerdt WH. Transplantation experiments with Caribbean Millepora species (Hydrozoa, Coelenterata), including some ecological observations on growth forms. Bijdragen tot de Dierkunde. 1981;51:1-19
  230. 230. Witman JD. Effects of predation by the fireworm Hermodice carunculata on milleporid hydrocorals. Bulletin of Marine Science. 1988;42(3):446-458
  231. 231. Rahav O, Ben-Zion M, Achituv Y, Dubinsky Z. A photographic, computerized method for in situ growth measurements in reef-building cnidarians. Coral Reefs. 1991;9(4):204
  232. 232. Lewis JB. Banding, age and growth in the calcareous hydrozoan Millepora complanata Lamarck. Coral Reefs. 1991;9(4):209-214
  233. 233. Glynn PW. Acanthaster: Effect on coral reef growth in Panama. Science. 1973;180(4085):504-506
  234. 234. Schweinsberg M, Tollrian R, Lampert KP. Inter- and intra-colonial genotypic diversity in hermatypic hydrozoans of the family Milleporidae. Marine Ecology. 2017;38(1):e12388
  235. 235. Dubé CE, Planes S, Zhou Y, Berteaux-Lecellier V, Boissin E. On the occurrence of intracolonial genotypic variability in highly clonal populations of the hydrocoral Millepora platyphylla at Moorea (French Polynesia). Scientific Reports. 2017;7(1):14861
  236. 236. Puill-Stephan E, van Oppen MJH, Pichavant-Rafini K, Willis BL. High potential for formation and persistence of chimeras following aggregated larval settlement in the broadcast spawning coral, Acropora millepora. Proceedings of the Royal Society of London B: Biological Sciences. 2012;279:699-708
  237. 237. Amar KO, Chadwick NE, Rinkevich B. Coral kin aggregations exhibit mixed allogeneic reactions and enhanced fitness during early ontogeny. BMC Evolutionary Biology. 2008;8:126
  238. 238. Puill-Stephan E, Willis BL, Abrego D, Raina J-B, van Oppen MJH. Allorecognition maturation in the broadcast spawning coral Acropora millepora. Coral Reefs. 2012;31:1019-1028
  239. 239. D’Aloia CC, Bogdanowicz SM, Majoris JE, Harrison RG, Buston PM. Self-recruitment in a Caribbean reef fish: A method for approximating dispersal kernels accounting for seascape. Molecular Ecology. 2013;22:2563-2572
  240. 240. Cuif M, Kaplan DM, Fauvelot C, Lett C, Vigliola L. Monthly variability of self-recruitment for a coral reef damselfish. Coral Reefs. 2015;34:759-770
  241. 241. Galzin R, Pointier JP. Moorea Island, society archipelago. In: Proceedings of the Fifth International Coral Reef Symposium. Vol. 1. 1985. pp. 73-102
  242. 242. Kayal M, Vercelloni J, De Loma TL, Bosserelle P, Chancerelle Y, Geoffroy S, et al. Predator crown-of-thorns starfish (Acanthaster planci) outbreak, mass mortality of corals, and cascading effects on reef fish and benthic communities. PLoS One. 2012;7(10):e47363
  243. 243. Holbrook SJ, Adam TC, Edmunds PJ, Schmitt RJ, Carpenter RC, Brooks AJ, et al. Recruitment drives spatial variation in recovery rates of resilient coral reefs. Scientific Reports. 2018;8(1):7338
  244. 244. Bengtsson BO. Genetic variation in organisms with sexual and asexual reproduction. Journal of Evolutionary Biology. 2003;16:189-199
  245. 245. Harrison PL, Wallace CC. Reproduction, dispersal and recruitment of scleractinian corals. Ecosystems of the World. 1990;25:133-207
  246. 246. Harrison PL, Booth DJ. Coral reefs: Naturally dynamic and increasingly disturbed ecosystems. In: Marine Ecology, Connell SD and Gillanders BM editors. Melbourne: Oxford University Press; 2007. pp. 316-377
  247. 247. Courchamp F, Clutton-Brock T, Grenfell B. Inverse density dependence and the Allee effect. Trends in Ecology & Evolution. 1999;14:405-410
  248. 248. Randall RH, Cheng YM. Shallow water hydrozoan corals. Acta Geologica Taiwanica. 1984;22:35-99
  249. 249. Bellwood DR, Hughes TP, Folke C, Nyström M. Confronting the coral reef crisis. Nature. 2004;429:827-833
  250. 250. Bruno JF, Selig ER. Regional decline of coral cover in the indo-Pacific: Timing, extent, and subregional comparisons. PLoS One. 2007;2:e711
  251. 251. De’ath G, Fabricius KE, Sweatman H, Puotinen M. The 27–year decline of coral cover on the great barrier reef and its causes. Proceedings of the National Academy of Sciences of the United States of America. 2012;109:17995-17999
  252. 252. Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, et al. Anthropogenic Ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature. 2005;437(7059):681
  253. 253. Norström AV, Nyström M, Lokrantz J, Folke C. Alternative states on coral reefs: Beyond coral–macroalgal phase shifts. Marine Ecology Progress Series. 2009;376:295-306
  254. 254. Glynn PW, Maté JL, Baker AC, Calderón MO. Coral bleaching and mortality in Panama and Ecuador during the 1997–1998 El Niño-southern oscillation event: Spatial/temporal patterns and comparisons with the 1982–1983 event. Bulletin of Marine Science. 2001;69:79-109
  255. 255. Brown D, Edmunds PJ. Long-term changes in the population dynamics of the Caribbean hydrocoral Millepora spp. Journal of Experimental Marine Biology and Ecology. 2013;441:62-70

Written By

Caroline E. Dubé, Chloé A.F. Bourmaud, Alexandre Mercière, Serge Planes and Emilie Boissin

Submitted: October 8th, 2018 Reviewed: August 9th, 2019 Published: December 2nd, 2019