A clear distinction and presence of Acropora divaricata within Acropora solitaryensis species complex along their biogeographic distribution in East-Asia

doi:10.21203/rs.3.rs-5001575/v1

Download PDF

Article

A clear distinction and presence of Acropora divaricata within Acropora solitaryensis species complex along their biogeographic distribution in East-Asia

https://doi.org/10.21203/rs.3.rs-5001575/v1

This work is licensed under a CC BY 4.0 License

You are reading this latest preprint version

In the Anthropocene, scleractinian corals face unprecedented threats from synergistic stressors, including rising seawater temperatures that surpass critical thresholds that lead to global coral reef degradation. With over 1,698 coral species in the order Scleractinia, their conservation is increasingly complex due to their morphological plasticity and the challenge of accurate species identification. The genus Acropora, with approximately 400 nominal species, exemplifies these challenges, as morphological traits often vary within and among species, complicating taxonomic efforts. Traditional methods based on skeletal characteristics are insufficient for delineating Acropora species, prompting the use of integrative approaches combining morphology, reproduction, and molecular data. In this study, we employ multi-locus phylogenetic analyses and morphometric measurements to distinguish different growth forms of Acropora solitaryensis as distinct species and delineate the species range boundaries of A. divaricata and A. solitaryensis in East Asian coral ecosystems. We identify arborescent and intermediate morphotypes belonging to A. divaricata, which is distributed from tropical reefs in southeastern Taiwan to temperate non-reefal communities in Shikoku, Japan. Conversely, the solid-plate morphotype aligns with A. solitaryensis from the holotype locality in Solitary Island, Australia, found primarily in subtropical non-reefal regions in northern Taiwan and Japan. The distinct distribution patterns of A. divaricata and A. solitaryensis underscore the necessity for biogeographic sampling in Acroporataxonomy, considering the Kuroshio Current's impact on coral distributions, and a re-evaluation of poleward coral migration or expansion due to climate change. Our findings challenge the traditional taxonomy of A. divaricata and A. solitaryensis, revealing that they may instead encompass multiple species. This has significant implications for coral conservation strategies, as accurate species identification is crucial for understanding coral responses to environmental changes and for informing conservation efforts in the face of climate change.

Biological sciences/Evolution/Taxonomy

Biological sciences/Ecology/Biodiversity

Biological sciences/Ecology/Climate change ecology

Earth and environmental sciences/Climate sciences/Ocean sciences/Marine biology

Biological sciences/Ecology/Biooceanography/Coral reefs

Acropora solitaryensis

Acropora divaricata

species

complex

coral ecosystems in East Asia

Taiwan

climate change.

Scleractinian corals (hereafter referred to as corals) are under threat in the Anthropocene due to the synergistic effects of stressors, natural and man-made ¹. As we progress into uncertainty, including the likelihood of seawater temperatures breaching a 1.5 ºC threshold ² and frequent and prolonged seawater temperature anomalies below and above threshold limits for coral survival ^1,3–5, there is increased awareness and pressure for coral and coral reef conservation worldwide ^7–12. While the conservation of corals is a top priority, planning for it can be confusing and overwhelming due to diverse species composition. With 1698 coral species in the order Scleractinia ¹³ distributed from the tropics to high-latitude non-reefal communities ¹⁴, working toward their protection is very difficult as they are morphologically plastic and challenging to identify genetically due to the lack of efficient molecular markers ^15,16. Nevertheless, recent studies on coral taxonomy using integrative approaches (morphology, reproduction, and molecular) have gradually advanced our understanding of coral species ^17–21.

The most dominant group, the genus Acropora, with approximately 400 nominal species being abundant in tropical and subtropical reefs and high-latitudinal non-reefal communities in the three ocean provinces, represents a typical showcase for demonstrating integrative approaches to understanding coral taxonomy ^14,22. Traditional methods for describing species that include the use of morphological characteristics such as growth form, corallite, and corallum structure^22,23, have not been effective in delineating species within Acropora as its morphological traits are often unstable and subject to variation, either interspecifically or interspecifically ²⁴. For instance, skeletal characteristics such as size and shape of corallites can differ dramatically due to genetics, environmental factors ²⁵, or even the location of corallites within the same colony^14,22. ²³ divided Acropora into 14 “species groups” based on skeletal morphology to assist in classification and subsequent research. ²² recognized 19 Indo-Pacific and one Caribbean species group within the genus. Nevertheless, only 122 of approximately 400 nominal species were considered valid in the latest revision of the genus ²⁶, and the phylogenetic implications of Acropora species groups remain challenging ^{20,21,27–29}.

Inferring Acropora species phylogeny using conventional single-locus markers has shown intertwined patterns of mitochondrial and nuclear gene trees since the late 20^th Century ^24,30–33. This has been widely interpreted as evidence supporting either ongoing hybridization between coral species ^34,35 or incomplete lineage sorting due to recent diversification of species groups as well as in species with large effective population sizes ³⁶. In addition, the incorrect identification of specimens, which is highly likely in morphologically diverse groups such as Acropora, could also result in polyphyletic patterns observed in gene trees ^37,38. Nevertheless, cryptic lineages of Acropora morphospecies complexes that have a broad geographic distribution in the Indo-Pacific region have recently been identified by multi-locus (microsatellites) and single-nucleotide polymorphism (SNP) genetic data in combination with the genotypic cluster species definition ^{20,21,28,29,39–42}. ³⁹ use DNA sequence data from 12 genomic regions to clarify that A. hyacinthus collections from the Indo-Pacific region comprise at least four cryptic lineages. Two of the A. hyacinthus lineages have an unusual distributional pattern in East Asia, with one dominating marginal locations in Japan and Taiwan and the other dominating reefs of the Ryukyus Archipelago, Japan ⁴⁰. Using microsatellites and single nucleotide polymorphisms (SNPs) derived from 2b-RAD sequencing, one lineage of A. hyacinthus identified in temperate Japan showed distinct bottleneck pressures, including higher clonality, increased linkage disequilibrium, and lower genetic diversity compared to subtropical populations ^41,42. Combining morphological examination, genetic data of conventional single-locus markers, SNPs derived from the ultraconserved elements (UCEs) of hexacorallian genomes ^27,43, and breeding trials successfully delineate distinct species boundaries among A. bifurcata, A. cytherea, and A. hyacinthus ²⁸. The application of UCEs to examine species phylogeny in the A. tenuis clade derived from Cowman et al. ²⁷ show this clade contains over 11 distinct lineages, only four of which correspond to then-accepted species based on morphological and geographical evidence, and allowed the description of two new species, A. rongi and A. tenuissima ²⁰. Population structure and principal component analyses with SNPs (>60,000) indicate that A. cf bifurcata, A. cf cytherea, A. cf hyacinthus, and A. cf subulata are genetically distinct and do not show signs of introgression ²¹.

In this study, we apply molecular phylogenetic and morphological approaches to delineate species boundaries for Acropora divaricata ⁴⁴ and A. solitaryensis ²³ collected from coral ecosystems in East Asia. Based on morphology, both species have previously been categorized into the divaricata species group ^14,22. The holotype of A. divaricata was described by Dana in 1846 from Fiji with nariform radial corallites characterized by large, open calices and possessing a reticulate coenosteum, despite variations in the density and arrangement of spinules (Table 1). At the colony level, A. divaricata exhibits an open caespitose-corymbose branching pattern, forming branching colonies with tapering branches that can curve and anastomose to create a network within the colony ²². Acropora solitaryensis is a relatively new species described by ²³ with a similar growth form with respect to branching patterns, corallite, and corallum structures as A. divaricata, but with a tendency to fuse into solid plates along basal branches ^{22,23,45–47}. Acropora solitaryensis is abundant in high-latitude coral ecosystems, including the low-latitude Flinders Reef (Moreton Bay), Middleton Reef, and Solitary Islands in Australia. However, specimens of A. solitaryensis has also been reported and collected from the tropical Murray Reef, Martha Ridgeway Reef, and Palam Islands in the Great Barrier Reef ²³. This unusual geographic distribution and its morphological variabilities leads to a suspicion that A. solitaryensis might be readily divisible into five geographic subspecies that are widely separated spatially and environmentally ²³. On the other hand, morphological plasticity also results in the sympatric and continuous occurrences of colony morphs, including arborescent (AR), solid plate (PL), and intermediate (IM) forms of A. solitaryensis, mainly in high-latitude coral ecosystems ^{14,22,46–48}.

Both A. divaricata and A. solitaryensis have broad geographic distributions in the Pacific and Indian Oceans, with the former extending more to the Red Sea and the Persian/ Arabian Gulf ^14,22,49,50. While ²² confirms the occurrence of A. solitaryensis in the central and west Indian Ocean, ¹⁴ confines its distribution to Sumatra and Indonesia in the east Indian Ocean. Both species are recorded from the island chain of East Asia, including Taiwan, Ryukyus Archipelago, and mainland Japan, with A. divaricata more in tropical and subtropical coral reefs and A. solitaryensis distributed further into high-latitude non-reefal coral ecosystems ^{14,22,46,48,51}. Molecular phylogeny and cross-fertilization experiments was used to examine the relationships of the three morphs, namely arborescent (AR), intermediate (IM), and solid plate (PL), of A. solitarynensis in the high-latitude non-reefal region in Japan ⁴⁷. Their results showed that AR is clearly distinct from PL, suggesting an absence of gene flow between the morphs. In their cross-fertilization experiments, gametic compatibility between AR and PL was extremely low, suggesting pre-zygotic isolation of these morphs. They concluded that AR and IM forms are variations of A. solitaryensis, whereas the PL form may be an undescribed species. Interestingly, the AR and IM types formed a monophyletic group in the molecular phylogenetic trees with samples of A. divaricata collected from the subtropical islands Ishigaki and Miyako of the Ryukyus Archipelago ⁴⁷. In contrast, applying morphometric, molecular phylogenetic, and cross-fertilization experiments to examine the cryptic boundary of two morphs of A. divaricata, “slender” and “robust,” in the central Ryukyus, show that although inter-morphotype gamete compatibility was high in the year of overlapping spawning seasons for these two distinct morphotypes, population genetics analyses and molecular phylogenetic analysis show that they are genetically distinct and rarely hybridize ⁵². The molecular phylogenetic tree grouped the “slender” form into the clade containing mitochondrial control region DNA sequences of A. divaricata and the AR of A. solitaryensis. On the other hand, the “robust” form was grouped with the PL of A. solitaryensis from the high-latitude non-reefal region in Japan ^47,52.

We hypothesized that the different growth forms of these two Acropora species collected from different geographical localities in the island groups of East Asia might represent two distinct lineages of the A. divaricata species group, one being A. divaricata and the other A. solitaryensis. To test this hypothesis, we collected A. solitaryensis from the holotype locality in the north Solitary Island, Australia, and extended the sampling of both species to the waters off Taiwan, the largest continental island in East Asia with distinct development of tropical reefs to the southeast and subtropical non-reefal coral communities to the northeast of mainland Taiwan and Penghu Archipelago in the Taiwan Strait ⁵³ and high-latitude coral communities in Shikoku, Japan ⁵⁴. By applying multi-locus molecular phylogenetic and morphological analyses, we confirm the species status of A. divaricata and A. solitaryensis in the island chain of East Asia. While both species have sympatric occurrences in the subtropical reefs of the Ryukyus Archipelago and high-latitude non-reefal coral communities in mainland Japan, they have discrete distributions following a boundary separating tropical coral reefs and subtropical non-reefal coral communities in Taiwan.

DNA sequence variation of molecular markers

Acropora samples (n=124) collected from Taiwan, Japan, and Australia were sequenced for mtCR, MC, exon4706, and PMCA. Published mtCR (n=59) ^24,47,52 and MC (n=12) ^47,55,56 DNA sequences were downloaded from DDBJ and GenBank. In total, 111 mtCR, 112 MC, 108 exon4706, and 108 PMCA sequences were utilized in phylogenetic analyses (Table 2). The aligned mtCR produced 80 bp of variable sites, but only 47.5% (48 bp) were phylogenetic informative sites. In contrast, the three markers derived from the nuclear genome provided high proportions of phylogenetically informative sites ranging from 75.8% in PMCA to 81.6% in MC (Table 2).

Molecular phylogenetic inferences

The phylogenetic trees arebased on mtCR with Acropora species from tropical reefs and subtropical non-reefal coral communities in Taiwan, subtropical coral reefs (Ryukyus), high-latitude coral communities (Shikoku, Japan), and non-reefal coral communities (Solitary Island, Australia) (Fig. 2A; Fig. 1S-A). Three major clades, namely A. divaricata (clade I), A. solitaryensis (clade II), and A. japonica/ tumida (clade III), are supported by high ML bootstrapping and Bayesian inferences. Clade I is composed of mtCR sequencesfrom tropical reefs (Kenting and Green Island) in Taiwan, the “slender” form of A. divaricata (AdivSlender) from subtropical reefs of Ryukyus, Japan ⁵², and the “arborescent” form of A. solitaryensis (AsolAR)and A. pruinosa from high-latitude coral communities in Otuski, Shikoku, Japan ⁴⁷. Clade II contains mtCR sequences from subtropical non-reefal coral communities (Keelung and Penghu) in Taiwan, the “robust” form of A. divaricata (AdivRobust) from subtropical reefs of Ryukyus, and the “solid plate” form of A. solitaryensis (AsolPL) from high-latitude coral communities in Otuski, Shikoku, Japan. Two A. solitaryensis (5010, 5015) collected from Solitary Island, Australia, are grouped in clade II. The other two from Australia (5028, 5083) and seven from high-latitude Japan show a paraphyletic relationship with the three major clades (Fig. 2A); however, later analyses using nuclear genes support their grouping in clade II (Fig. 2B, C). Clade III is consistently composed of A. japonica and A. tumida.

Phylogenetic inferences based on nuclear genes support the relationship of three major clades (Fig. 2B, C; Fig1S-B). The MC tree shows that clade I contains sequences of “AsolAR” published by ⁴⁷, samples from tropical reefs at Green Island and Kenting, Taiwan, and high-latitude coral communities in Otuski, Shikoku, Japan. Clade II, on the other hand, contains sequences of “AsolPL” published by ⁴⁷, samples from subtropical non-reefal coral communities in Penghu and Keelung, Taiwan, and high-latitude coral communities in Otuski, Shikoku, Japan. The four A. solitaryensis collected from Solitary Island are grouped within clade II. Clade III composed of A. japonica/tumida branches out the monophyletic group of clades I and II (Fig. 2B). The tree generated by the combination of nuclear genes, MC, exon4706, and PMCA, shows a similar topology to the MC tree with increasing ML bootstrapping and Bayesian support at the major nodes of the three clades (Fig 2C).

Morphological differences between A. divaricata and A. solitaryensis

Our observations show various skeletal structures, including corallites, coenosteum, and spinules in A. divaricata (Fig. 3A-C) and A. solitaryensis (Fig. 3D-F). However, these descriptive variations are not variable enough to distinguish between the two species (Fig. 3). The axial corallite of both species shares similar diameters ranging from 2.3 to 3.0 mm, calices diameters between 0.7 to 1.1 mm, and incomplete primary septa cycles with 1/2R to 1/4R (Fig. 3). The radial corallite is tubular on branch tips, with tubo-nariform to nariform and sub-immersed shapes on basal branches (Fig. 3). The coenosteum is costate in form, with spinules densely arranged between intercorallite regions (Fig. 3). In contrast, A. divaricata and A. solitaryensis can be distinguished by their colony growth forms (Fig. 1). Acropora solitaryensis grows dominantly in the solid plate (PL) form, with colonies having anastomosed lower branches developing into flat basal plates, complemented by upright short branchlets (Fig. 1, A-D; E-H; M-P). Interestingly, juvenile colonies in the PL form show an additional characteristic: a semi-fused plate with an elongated, anastomosing, and upwardly curving branching pattern (Fig. 1, M, O, P). Acropora divaricata, on the other hand, dominantly has an arborescent (AR) form that is distinctively characterized by an open caespitose-corymbose structure with tapering branches and bowl/bracket-shaped colonies, either centrally or laterally attached. The AR form exhibits stacked tables with spaced, anastomosing, and upwardly curving branchlets, which form an intricate network within the colony (Fig. 1, I-L; Q-T). A notable differentiation in some AR specimens from Lyudao (Fig. 1 K) and Shikoku (Fig. 1 Q, R, S) is the flattening of branchlets, leading the colony into a prostrate form and eventually fusing into thin plates (Fig. 1 Q, R, S).

Overall branch widths (5 mm below axial corallites) and outer axial corallite diameters are significantly larger in A. solitaryensis than in A. divaricata (Fig. 4a, b; branch width, A. divaricata: 4.767 ± 1.196 mm, A. solitaryensis: 5.650 ±1.046 mm, Tukey’s HSD, p < 0.001; outer diameter of axial corallites, A. divaricata: 1.833 ± 0.362 mm, A. solitaryensis: 2.029 ± 0.318 mm, Wilcoxon signed rank test, p < 0.001; mean ± SD), suggesting that A. divaricata and A. solitaryensis are morphometrically distinct. Intraspecific variations also occur in both the branch width and outer diameter of axial corallites in both species collected from Taiwan and Japan. In pairwise comparisons (Fig. S2), A. divaricata in Taiwan has smaller branch widths (4.585 ± 1.176 mm) and smaller axial corallite outer diameters (1.732 ± 0.287 mm) than those from Japan (branch width: 5.525 ± 0.971 mm, Tukey’s HSD, p <0.001; corallite diameter: 2.290 ± 0.308 mm, Wilcoxon signed rank test, p <0.001). In contrast, there are no differences in A. solitaryensis branch widths collected from Japan and Taiwan (Japan: 5.793 ± 0.930 mm; Taiwan: 5.515 ± 1.150 mm, Tukey’s HSD, p >0.05) or in axial corallite outer diameters (Japan: 2.049 ± 0.323 mm; Taiwan: 2.003 ± 0.314 mm Wilcoxon signed rank test, p >0.05).

Our study utilized multi-locus phylogenetic approaches and morphometric measurements of skeletal structures to demonstrate that different growth forms of Acropora solitaryensis are distinct species in East Asian coral ecosystems. Those with arborescent or intermediate growth morphotypes belong to A. divaricata, which has a distribution range from tropical reefs in southeastern Taiwan to high-latitude temperate non-reefal coral communities in Shikoku, Japan. The solid plate morphotype, clustering with A. solitaryensis collected from the holotype locality at Solitary Island, Australia, is distributed mainly in the subtropical non-reefal coral communities of the Penghu Islands, northern Taiwan, and Shikoku, Japan. The distinct distribution pattern of A. divaricata and A. solitaryensis found in this study highlights the urgent need to reconsider (1) biogeographic sampling when examining the taxonomy and systematics of Acropora, (2) the influence of the Kuroshio Current on the biogeographic patterns of corals, and (3) cautious interpretation of poleward migration and range expansion of corals in East Asia.

Skeletal structures, including colony growth forms and corallite structures, are important traits for species identification and taxonomy in the genus Acropora ²². It has been suggested that morphological variation among biogeographic locations and habitats and ambiguity of taxonomic characters make the delineation of species extremely difficult; therefore, morphotypes (or types) are used to describe the variants within species ^40,47,52. In the case of A. divaricata and A. solitaryensis, extending biogeographic sampling of morphotypes helps clarify the morphological variation within and between species in high-latitude Japan and Taiwan. Based on molecular phylogeny and morphological measurements, A. divaricata is diagnosedas arborescent with stacked tables and anastomosing, upwardly curving branchlets that show intricate networks within colonies in the populations of tropical (Taiwan) and subtropical reefs (Ryukyus). In non-reefal coral communities (Shikoku), the branchlets of A. divaricata colonies become thicker and sturdier, and their network bases become fused in comparison to their reefal counterparts. This is a characteristic of corals adapted to harsher environmental conditions such as colder water temperatures and lower light levels in the high latitudes ⁵⁷. Adaptations to harsh environments are also seen in A. solitaryensis collected from non-reefal coral communities in Taiwan and Shikoku, where colonies consistently have thick solid plates with anastomosing lower branches developing into flat basal plates, complemented by short upright branchlets. Interestingly, juvenile A. solitaryensis show an additional semi-fused plate with an elongated, anastomosing, and upwardly curving branching pattern that can be confused with sympatric IM and AR forms of A. divaricata during field surveys and sample collections ^{47,48,58–60}. This confusion is enhanced by the fact that the holotype of A. solitaryensis described from Solitary Island ^22,23 is an IM form, leading ⁴⁷ to hypothesize that the IM and AR forms are A. solitaryensis and the PL form is likely an undescribed species in the non-reef region of Japan. Our A. solitaryensis samples collected from Solitary Island are IM morphotypes, but molecular phylogeny does not show them grouping with A. divaricata, thus rejecting the hypothesis proposed by ⁴⁷.

In addition, the slender and robust morphotypes of A. divaricata in the subtropical Ryukyus are unambiguously assigned to A. divaricata and A. solitaryensis, respectively, based on mtCR phylogeny and STRUCTURE analyses ⁵². Several lines of evidence suggest that slender and robust morphotypes of A. divaricata are likely distinct species. Firstly, branch sizes and axial diameters are significantly different. Secondly, the two species are reproductively isolated. Reproductive isolation is also observed in the AR (=A. divaricata) and PL forms of A. solitaryensis in high-latitude Japan ⁴⁷, indicating that premating and postzygotic isolation mechanisms operate effectively in maintaining species boundaries, as seen in other sympatric Acropora species ^{21,28,61–64}. Additional surveys, collections, and examinations of NGS markers of both morphotypesthroughout the Ryukyus Archipelago are currently underway to confirm their affiliations with East Asian A. divaricata and A. solitaryensis.

Our study shows that both A. divaricata and A. solitaryensis are sympatric in subtropical reefs (Ryukyus) and the high-latitude non-reefal region (Shikoku) in Japan, but have a segregated distribution around the waters of Taiwan. Acropora divaricata is found in the tropical reefs of its southeastern coast and islets, and A. solitaryensis is restricted to the non-reefal communities along the northeastern coast, islets, and Penghu Archipelago in the Taiwan Strait. This unusual pattern might be related to the paleoceanography of the Kuroshio Current (KC) and environmental changes since the last glacial maximum (LGM, 20,000 yrs. BP) that have shaped the coral phylogeography in East Asia ⁶⁵. The KC passes through Orchid Island and Green Island off the east coast of Taiwan, across the Yonaguni Depression via the East Taiwan Channel into the East China Sea and follows the edge of the continental shelf in the Okinawa Trough with a deep break between the ECS continental slope and the Ryukyu Archipelago. It flows along the western part of the Okinawa Trough, and leaves the continental slope via the Tokara Strait, reaching the southern island of Japan at ~31 °N (reviewed in ⁵³). During the LGM, the sea level dropped 100-120 m, obstructingthe KC from entering the Okinawa Trough, resulting in the KC flowing westward at a lower latitude than today ^66,67. SST around the Japanese mainland was 5–6 °C lower than at present, which might have hindered reef development at the higher latitude. Fossil records have shown that coral reefs had retreated from their current locations at southern Kyushu near Tanegashima to the southern Ryukyus near Miyazakijima-Ishigakijima (reviewed in ⁶⁵). During the same period, the non-reefal regions of Taiwan that include the Penghu Archipelago and most of the north and northeast coast of Taiwan Island were exposed to air and remained part of the Asian landmass ⁶⁸. The southern Ryukyus, therefore, likely served as a refugia for corals (and other reef organisms) that included A. divaricata and A. solitaryensis during the LGM in East Asia. After the LGM, the KC resumed its current position, temperatures gradually increased and peaked 2–3 °C higher at ~6,000 yrs. BP, and sea-level rose 2-3 m higher than at present in Japan and Taiwan ^68,69. Sea surface temperature warming during this period enabled coral populations to extend their ranges northward to reach the Japanese mainland, as did non-reefal coral communities to northern Taiwan and the Penghu Archipelago. Fossil records indicate that tropical fauna, including hermatypic corals, were distributed at higher latitudes (~35°N) 6,000 yrs. BP ^70,71. Similar fossil coral and crustose coralline algae (CCA) assemblages are recorded along the coast of Taoyuan City, northwest Taiwan (~25°N) 7500-6000 yrs. BP ^68,72. After global cooling occurred 4000 yrs. BP, also known as the Little Ice Age in the Northern Hemisphere (LIANH⁷³), reef development in Japan retreated from higher latitudes to its current position near Tanegashima (30 ^oN ⁶⁵). Along the coast of Taoyuan City, Taiwan, most corals could not survive lower temperatures, freshwater intrusion, and highly sedimented surroundings during LIANH. CCA became the dominant reef-builders and have continuously constructed unprecedented algal reefs unto the present ^72,74,75. During this period, the benthic communities of high-latitude coasts in Japan were dominated by kelp (Ecklonia spp.) and fucoid seaweed (Sargassum spp.) until the early 21st Century, being gradually replaced by corals and CCA due to SST rising caused by climate change ⁷⁶. An examination of museum collections since the 1930s suggests that three Acropora species including A. solitaryensis have responded to rising SST by range expansions to the high-latitude non-reefal region in Japan ⁷⁷.Similar speculation of the influence of KC on coral distribution along East Asia is also made for A. hyacinthus ⁴⁰.

The alternative hypothesis explaining the segregated distribution pattern of Acropora divaricata and A. solitaryensis in Taiwan is that the sources for repopulating these species differ after post-GLM seawater reemerged in the Taiwan Strait. During the GLM, A. divaricata could have maintained its occurrence on the coast and islets of southeast Taiwan in the Pacific. Acropora solitaryensis, on the other hand, needed to repopulate the Penghu Archipelago in the Taiwan Strait and northern Taiwan from sources further south, such as Dongsha Atoll in the South China Sea ⁷⁸, which served as a southern refugia for corals and reef-associated organisms during the LGM. Future surveys, collections, and phylogeographic genomic analyses of both species in the South China Sea are needed to test these two hypotheses.

Taxonomy plays an important role in conservation planning for coral species and theoretical inferences such as poleward range expansion. Our findings for Acropora solitaryensis, composed of two distinct species at the high latitudes of Japan, highlight the need to revisit the scenario of tropical coral poleward migration and/ or range expansion in East Asia ⁷⁷. Based on literature reviews and examination of museum collections, it is suggested that Acropora species, including A. solitaryensis, A. hyacinthus, and A. muricata, have expanded from previous northern distribution limits within the East Asian region, Tokara and Tanegashima, to higher latitudes in Japan since the 1930s, with the speed of these expansions reaching up to 14 km/yr. However, reader need to take note of ever-changing taxonomical analysis of corals due to their morphological and genetic complexities within and between locations. Projects such as “Project Phoenix” (https://coralprojectphoenix.org) are working towards resolving issues related to coral taxonomy across the oceans (For example, see ²⁸). Nevertheless, our study demonstrates that A. solitaryensis in high latitudes is indeed mixed with A. divaricata, questioning not only which of the two species is expanding its range but also risking mixing expansion speed calculations for these two species. Nevertheless, clarification of the species status of A. divaricata and A. solitaryensis allows us to establish a diagnostic framework for differentiating them in the field and lab and provides a good species pair for reexamining the hypothesis of poleward migration and range expansion of Acropora in East Asia in response to rising SST caused by climate change.

Coral Sampling and Identification

Sampling for Acropora solitaryensis was conducted by SCUBA diving primarily in Taiwan and Japan between 2013 and 2023 (Fig. 1 and Table 1S). Additionally, samples were collected in 2016 from Solitary Island, Australia (Permit No. P12/0050-1.0), the locality from where the holotype of A. solitaryensis was described ²³. This was to confirm the phylogenetic status of A. solitaryensis in the northern hemisphere. The identification of coral species followed ²² and ²³. Due to the high resemblance of morphological characters that easily confuses in-situ underwater identifications of A. solitaryensis and A. divaricata (Table 1), we targeted colonies fitting the descriptions of corallum characters, including branching pattern, size, and arrangement. Additional Acropora species, A. cf. japonica, A. cf. pruinosa, and A. cf. tumida, which occur sympatrically with A. cf solitaryensis ⁴⁸, were also sampled from the non-reefal coral communities of Penghu Island (Permit No. 03751) and Keelung (Permit No. 1090225216), Taiwan (Permit No. 11258843900), and Otsuki, Shikoku, Japan (Permit No. 768). The outgroup, A. tenuis, was collected from the tropical reef in Kenting National Park, southern Taiwan. Growth form, branch pattern, and a close-up of radial corallites of each sampled colony were photographed with an Olympus TG-6 camera. Samples containing at least three branches of coral colonies were chiseled off, returned to the shore, and preserved in 80% EtOH before cutting off small pieces (5 cm long) for DNA extraction. The remaining samples were bleached in 10% sodium hypochlorite solution for morphological examination. The bleached skeletons were deposited in the Biodiversity Research Museum, Academia Sinica, with voucher numbers listed in Table 1S. Formal identification of coral samples were done by Chaolun Allen Chen in Taiwan, Chaolun Allen Chen and Takuma Mezaki in Japan, and Andrew H. Baird in Australia

Molecular phylogenetic analysis

Total genomic DNA was extracted using NautiaZ Tissue DNA Extraction Mini Kit (Nautia Gene, Taiwan) following the manufacturer’s protocol. Four genetic markers, the mitochondrial control region (mtCR), the intron region of the nuclear mini-collagen (MC) gene, nuclear gene Exon 4706 (4706), and exon plasma membrane calcium-transporting ATPase (PMCA), were subjected to polymerase chain (PCR) reactions to obtain DNA sequences for phylogenetic analyses. A total volume of 25 µl PCR recipe contained 0.5 µL of genomic DNA template, 0.5 µL of each primer (10 µM), 12.5 µL of Taq DNA Polymerase Master Mix RED (Ampliqon, Denmark), and 10.5 µL of ddH₂O. PCR primers, temperature settings, and cycle numbers are listed in Table 2S.

PCR products were Sanger sequenced for forward and reverse strands by Genomics Biotech (Taipei, Taiwan). Forward and reverse strands of DNA sequences were assembled and trimmed by Geneious Prime 2023.2.1 (https://www.geneious.com). DNA sequences of all markers obtained in this study were submitted to the NCBI Genbank under accession numbers listed in Table 1S. DNA sequences were aligned using Clustal Omega v 1.2.3 ⁷⁹ before phylogenetic construction.

Phylogenetic tree constructions were based on (1) mtCR, (2) MC, and (3) a combination of three nuclear genes (4706, PMCA, and MC). Firstly, we compiled our data with the previously published mtCR and MC DNA sequences of other Acropora species to visualize the overall phylogenetic relationships ^24,56. As expected, the phylogenetic trees (Fig. 1S) showed reticulate patterns of other non-divaricata-solitaryensis species that complicated the interpretation of the relationship between A. divaricata and A. solitaryensis. We then reduced the taxa containing only A. cf. divaricata, A. cf. solitaryensis, A. cf. japonica, and A.cf. tumida for further phylogenetic analyses with the early-spawning clade of A. tenuis, A. longicyathus, and A. austera, as outgroups ^24,47,52,56. The analyses employed maximum likelihood (ML, 1000 bootstrap replicates) and Bayesian inferences (1000 replicates). Nucleotide substitution models were selected using Modeltest-NG v0.1.7 ⁸⁰. The substitution models, information on gamma distribution, and proportion of invariable sites for the ML inference and models selected for Bayesian inference are listed in Table 2S. ML trees were constructed using RAxMLGUI V2.0 v8 ⁸¹, and Bayesian inferences were executed in BEAST2 v2.5.0 ⁸². The final trees were imported into FigTree V.1.4.4 (http://tree.bio.ed.ac.uk/software/figtree/) and Affinity Designer V1.0.8 to refine tree shapes, labels, and tags.

Morphological variation analyses

Morphological characters were obtained through photographs of bleached skeleton samples. Coral branches and branching patterns were photographed using a Nikon Coolpix P6000 digital camera. Corallites and septa were captured with Olympus Stereomicroscope System SZ51 with OLYMPUS DP72 CCD camera. All images were processed using cellSens Standard 1.6 imaging software (Evident Corporation, Japan). Synapticular rings and coenostea were visualized and documented using scanning electron microscopy (FEI Quanta 200 equipped with a Quorum PP2000TR FEI system). Descriptive growth forms and skeletal characteristics of the coral samples, including coral branching patterns, growth form, corallites, septa, and coenostea, were used in species identification ^14,22,23,83. We compared branch widths and axial corallites by the methods modified by Furukawa et al. ^21,52 to determine whether skeletal differences exist among samples collected from different geographical locations. Branch widths (5 mm below the axial corallites) and outer diameters of axial corallites, which are specific to the species level (A. divaricata and A. solitaryensis) and the geographic level (Japan and Taiwan), were measured. The Shapiro-Wilk normality test ⁸⁴ showed that branch widths conformed to a normal distribution; thus, ANOVA and Tukey's HSD were applied ⁸⁵ to examine the difference in branch widths across the different localities (Japan and Taiwan). In contrast, Shapiro-Wilk normality testing showed that the outer diameter of axial corallites had a high W value (0.98354) but low P-value (<0.05). We applied the Wilcoxon signed rank test ⁸⁶ to examine the difference in corallite diameter between A. divaricata and A. solitaryensis. All analyses were done in R-package (version 4.3.2).

Acknowledgements

We thank members of the Coral Lab, Biodiversity Research Center, Academia Sinica (BRCAS) for support in field sampling, molecular technique and analysis. Special thanks to Dr. Silvia Fontana for field sampling, species identification, and DNA extraction of specimens in Otsuki. This work was funded by NSTC 111-2740-M-001-004 in Lyudao field work; AS-4010-PI, AS-100-TP2-A02-SUB in Japan field work; AS-TP-111-L03 in Kenting field work; AS-4010-PI in Penghu field work; MOST 109-2621-B-001-002-MY2 in Keeling field work; all to CAC. Postdoctroal Research Fellowship to SK is funded by Ministry of Science and Technology, Taiwan. SWC is supported by the doctorate fellowship of the Taiwan International Graduate Program, Academia Sinica of Taiwan.

Conflict of Interest

The authors declare no conflict of interest.

Authors Contributions

SWC- Sample processing, Molecular and statistical analysis, wrote the manuscript with contributions from CAC and SK. CHC- Morphology, morphometry and statistical analysis. DYT - Logistics, sampling and statistical analysis. TM and SKu - Samples from Japan, morphology and permits. AHB - holotype from Australia and permits. HJH - Sampling logistics, permit and funding in Penghu. SK- Supervision, manuscript revision and guidance. CAC -Conceived and oversaw project development, overall logistics and funding. All authors contributed to the final draft manuscript. All authors edited and approved the final version.

Data availability statement

The data that supports the findings of this study are available in the supplementary material of this article.

Declaration of interests

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Hughes, T. P. et al. Coral reefs in the Anthropocene. Nature 546, 82–90 (2017).
Intergovernmental Panel on Climate Change (IPCC). Global Warming of 1.5°C: IPCC Special Report on Impacts of Global Warming of 1.5°C above Pre-Industrial Levels in Context of Strengthening Response to Climate Change, Sustainable Development, and Efforts to Eradicate Poverty. (Cambridge University Press, Cambridge, 2022). doi:10.1017/9781009157940.
Hoegh-Guldberg, O., Poloczanska, E. S., Skirving, W. & Dove, S. Coral Reef Ecosystems under Climate Change and Ocean Acidification. Front. Mar. Sci. 4, 158 (2017).
Hughes, T. P. et al. Global warming transforms coral reef assemblages. Nature 556, 492–496 (2018).
Zande, R. M. van der et al. Paradise lost: End‐of‐century warming and acidification under business‐as‐usual emissions have severe consequences for symbiotic corals. Glob. Chang. Biol. 26, 2203–2219 (2020).
Beyer, H. L. et al. Risk‐sensitive planning for conserving coral reefs under rapid climate change. Conserv. Lett. 11, (2018).
Hoegh-Guldberg, O., Kennedy, E. V., Beyer, H. L., McClennen, C. & Possingham, H. P. Securing a Long-term Future for Coral Reefs. Trends Ecol. Evol. 33, 936–944 (2018).
Anthony, K. R. N. et al. Interventions to help coral reefs under global change—A complex decision challenge. PLoS ONE 15, e0236399 (2020).
Chauka, L. J. & Nyangoko, B. P. Climate change impacts outweigh conservation efforts in coral reefs that are highly exposed to thermal stresses in Zanzibar, Tanzania. Ocean Coast. Manag. 238, 106575 (2023).
Hilmi, N. et al. The pressures and opportunities for coral reef preservation and restoration in the Maldives. Front. Environ. Econ. 2, 1110214 (2023).
Gove, J. M. et al. Coral reefs benefit from reduced land–sea impacts under ocean warming. Nature 621, 536–542 (2023).
Battaglia, F.-M. Blue Planet Law, The Ecology of our Economic and Technological World. Sustain. Dev. Goals Ser. 121–130 (2023) doi:10.1007/978-3-031-24888-7_10.
Bernot, J. et al. World Register of Marine Species (WoRMS). (2024).
Veron, J. E. N. Corals of the World. Vol. 1–3. Australian Institute of Marine Science and CRR, Queensland, Australia (2000).
Fukami, H. Short review: molecular phylogenetic analyses of reef corals. Galaxea, J. Coral Reef Stud. 10, 47–55 (2008).
Fukami, H., Tachikawa, H., Suzuki, G., Nagata, S. & Sugihara, K. Current status and problems with the identification and taxonomy of zooxanthellate scleractinian corals in Japan. J. Jpn. Coral Reef Soc. 12, 17–31 (2010).
Kitahara, M. V., Fukami, H., Benzoni, F. & Huang, D. The Cnidaria, Past, Present and Future. 41–59 (2016) doi:10.1007/978-3-319-31305-4_4.
Arrigoni, R. et al. An integrated morpho-molecular approach to delineate species boundaries of Millepora from the Red Sea. Coral Reefs 37, 967–984 (2018).
Terraneo, T. I., Benzoni, F., Baird, A. H., Arrigoni, R. & Berumen, M. L. Morphology and molecules reveal two new species of Porites (Scleractinia, Poritidae) from the Red Sea and the Gulf of Aden. Syst. Biodivers. 17, 491–508 (2019).
Bridge, T. C. L. et al. A tenuis relationship: traditional taxonomy obscures systematics and biogeography of the ‘Acropora tenuis’ (Scleractinia: Acroporidae) species complex. Zoöl. J. Linn. Soc. zlad062 (2023) doi:10.1093/zoolinnean/zlad062.
Furukawa, M. et al. Integrative taxonomic analyses reveal that rapid genetic divergence drives Acropora speciation. Mol. Phylogenetics Evol. 195, 108063 (2024).
Wallace, C. Staghorn Corals of the World. (1999) doi:10.1071/9780643101388.
Veron, J. E. N. (John E. N. & Wallace, C. C. Scleractinia of eastern Australia. Part V. Family Acroporidae. Scleractinia of eastern Australia. Part V 6, 1–485 (1984).
Fukami, H., Niimura, A., Nakamori, T. & Iryu, Y. Species composition and mitochondrial molecular phylogeny of Acropora corals in Funakoshi, Amami-Oshima Island, Japan: A proposal for its new taxonomic grouping. Galaxea, J. Coral Reef Stud. 23, 17–35 (2021).
Todd, P. A. Morphological plasticity in scleractinian corals. Biol. Rev. 83, 315–337 (2008).
Wallace, C., Done, B. & Muir, P. Revision and catalogue of worldwide staghorn corals Acropora and Isopora (Scleractinia: Acroporidae) in the Museum of Tropical Queensland. Mem. Qld. Mus. - Nat. 57, 1–255 (2012).
Cowman, P. F. et al. An enhanced target-enrichment bait set for Hexacorallia provides phylogenomic resolution of the staghorn corals (Acroporidae) and close relatives. Mol. Phylogenetics Evol. 153, 106944 (2020).
Ramírez-Portilla, C. et al. Solving the Coral Species Delimitation Conundrum. Syst. Biol. 71, 461–475 (2021).
Ramírez-Portilla, C. et al. Quantitative three-dimensional morphological analysis supports species discrimination in complex-shaped and taxonomically challenging corals. Front. Mar. Sci. 9, 955582 (2022).
Odorico, D. M. & Miller, D. J. Variation in the ribosomal internal transcribed spacers and 5.8S rDNA among five species of Acropora (Cnidaria; Scleractinia): patterns of variation consistent with reticulate evolution. Mol. Biol. Evol. 14, 465–473 (1997).
Oppen, M. J. H. van, McDonald, B. J., Willis, B. & Miller, D. J. The Evolutionary History of the Coral Genus Acropora (Scleractinia, Cnidaria) Based on a Mitochondrial and a Nuclear Marker: Reticulation, Incomplete Lineage Sorting, or Morphological Convergence? Mol. Biol. Evol. 18, 1315–1329 (2001).
Márquez, L. M., Oppen, M. J. H. V., Willis, B. L., Reyes, A. & Miller, D. J. The highly cross‐fertile coral species, Acropora hyacinthus and Acropora cytherea, constitute statistically distinguishable lineages. Mol. Ecol. 11, 1339–1349 (2002).
Richards, Z. T., Berry, O. & Oppen, M. J. H. van. Cryptic genetic divergence within threatened species of Acropora coral from the Indian and Pacific Oceans. Conserv. Genet. 17, 577–591 (2016).
Veron, J. E. N. Corals in Space and Time: The Biogeography and Evolution of the Scleractinia. (Cornell University Press, 1995).
Willis, B. L., Oppen, M. J. H. van, Miller, D. J., Vollmer, S. V. & Ayre, D. J. The Role of Hybridization in the Evolution of Reef Corals. Ecol., Evol., Syst. 37, 489–517 (2006).
Fukami, H., Omori, M. & Hatta, M. Phylogenetic Relationships in the Coral Family Acroporidae, Reassessed by Inference from Mitochondrial Genes. Zoöl. Sci. 17, 689–696 (2000).
Wolstenholme, J. K., Wallace, C. C. & Chen, C. A. Species boundaries within the Acropora humilis species group (Cnidaria; Scleractinia): a morphological and molecular interpretation of evolution. Coral Reefs 22, 155–166 (2003).
Richards, Z. T., Miller, D. J. & Wallace, C. C. Molecular phylogenetics of geographically restricted Acropora species: Implications for threatened species conservation. Mol. Phylogenetics Evol. 69, 837–851 (2013).
Ladner, J. T. & Palumbi, S. R. Extensive sympatry, cryptic diversity and introgression throughout the geographic distribution of two coral species complexes. Mol. Ecol. 21, 2224–2238 (2012).
Suzuki, G. et al. Genetic evidence of peripheral isolation and low diversity in marginal populations of the Acropora hyacinthus complex. Coral Reefs 35, 1419–1432 (2016).
Nakabayashi, A. et al. The potential role of temperate Japanese regions as refugia for the coral Acropora hyacinthus in the face of climate change. Sci. Rep. 9, 1892 (2019).
Fifer, J. E., Yasuda, N., Yamakita, T., Bove, C. B. & Davies, S. W. Genetic divergence and range expansion in a western North Pacific coral. Sci. Total Environ. 813, 152423 (2022).
Quattrini, A. M. et al. Universal target‐enrichment baits for anthozoan (Cnidaria) phylogenomics: New approaches to long‐standing problems. Mol. Ecol. Resour. 18, 281–295 (2018).
Dana, J. D. Zoophytes. United States Exploring Expedition during the years 1838-1842. (1846).
Veron, J. E. N. (John E. N. Hermatypic Corals of Japan . vol. (Australian Institute of Marine Science, Townsville, Qld, 1992).
Dai, C. & Horng, S. Scleractinia Fauna of Taiwan I. The Complex Group.,(National Taiwan University: Taipei, Taiwan.). (2009).
Suzuki, G. & Fukami, H. Evidence of Genetic and Reproductive Isolation between Two Morphs of Subtropical-Dominant Coral Acropora solitaryensis in the Non-Reef Region of Japan. Zoöl. Sci. 29, 134–140 (2012).
Nishihira, M. & Veron, J. E. N. 日本の造礁サンゴ類 Hermatypic Corals of Japan. (Kaiyusha, Tokyo, 1995).
Veron, J. E. N. (John E. N., M., Marsh, Loisette & Museum, W. A. Hermatypic Corals of Western Australia : Records and Annotated Species List. vol. (Western Australian Museum, Perth, 1988).
Veron, J. E. N. (John E. N. A Biogeographic Database of Hermatypic Coral Species of the Central Indo-Pacific, Genera of the World . (Australian Institute of Marine Science, Townsville, Qld, 1993).
Dai, C. & Cheng, Y.-R. Corals of Taiwan: Scleractinia Fauna. vol. Vol. 1 (Owl Publishing House Co., LTD, 2020).
Furukawa, M., Ohki, S., Kitanobo, S., Fukami, H. & Morita, M. Differences in spawning time drive cryptic speciation in the coral Acropora divaricata. Mar. Biol. 167, 163 (2020).
Kuo, C.-Y. et al. Coral Reefs of Eastern Asia under Anthropogenic Impacts. Coral Reefs World 7–35 (2023) doi:10.1007/978-3-031-27560-9_2.
Keshavmurthy, S., Mezaki, T., Reimer, J. D., Choi, K.-S. & Chen, C. A. Coral Reefs of Eastern Asia under Anthropogenic Impacts. Coral Reefs World 53–71 (2023) doi:10.1007/978-3-031-27560-9_4.
Hatta, M. et al. Reproductive and genetic evidence for a reticulate evolutionary history of mass-spawning corals. Mol. Biol. Evol. 16, 1607–1613 (1999).
Fukami, H., Omori, M., Shimoike, K., Hayashibara, T. & Hatta, M. Ecological and genetic aspects of reproductive isolation by different spawning times in Acropora corals. Mar. Biol. 142, 679–684 (2003).
Chong, F. et al. High‐latitude marginal reefs support fewer but bigger corals than their tropical counterparts. Ecography 2023, (2023).
Sugihara, K. et al. Zooxanthellate Scleractinian Corals of Tanegashima Island, Japan. 1–197 (2015).
Nomura, K. The illustrated zooxanthellate scleractinian corals of Kushimoto I REFERTINA. Marine Pavilion 1–56 (2016).
Nomura, K. et al. Revision of the zooxanthellate scleractinian corals in Kushimoto, Wakayama, Japan. Marine Pavilion (2016).
Mrquez, L. M., Oppen, M. J. H. van, Willis, B. L. & Miller, D. J. Sympatric populations of the highly cross-fertile coral species Acropora hyacinthus and Acropora cytherea are genetically distinct. Proc. R. Soc. Lond. Ser. B: Biol. Sci. 269, 1289–1294 (2002).
Wei, N. V. et al. Reproductive isolation among Acropora species (Scleractinia: Acroporidae) in a marginal coral assemblage. Zoological Studies 51, 85–92 (2012).
Ohki, S., Kowalski, R. K., Kitanobo, S. & Morita, M. Changes in spawning time led to the speciation of the broadcast spawning corals Acropora digitifera and the cryptic species Acropora sp. 1 with similar gamete recognition systems. Coral Reefs 34, 1189–1198 (2015).
Kitanobo, S., Isomura, N., Fukami, H., Iwao, K. & Morita, M. The reef-building coral Acropora conditionally hybridize under sperm limitation. Biol. Lett. 12, 20160511 (2016).
Gallagher, S. J. et al. The Pliocene to recent history of the Kuroshio and Tsushima Currents: a multi-proxy approach. Prog. Earth Planet. Sci. 2, 17 (2015).
Ujiié, H., Tanaka, Y. & Ono, T. Late Quarternary paleoceanographic record from the middle Ryukyu Trench slope, northwest Pacific. Mar. Micropaleontol. 18, 115–128 (1991).
Ujiié, Y., Ujiié, H., Taira, A., Nakamura, T. & Oguri, K. Spatial and temporal variability of surface water in the Kuroshio source region, Pacific Ocean, over the past 21,000 years: evidence from planktonic foraminifera. Mar. Micropaleontol. 49, 335–364 (2003).
Dai, C., Wang, S. & Chang, J. Handbook for Ecological Tours of Guanyin Algae Reef. (Liquefied Natural Gas Engineering Office, CPC Corporation, Taiwan, Taiwan, 2009).
Schöne, B. R. et al. Holocene seasonal environmental trends at Tokyo Bay, Japan, reconstructed from bivalve mollusk shells—implications for changes in the East Asian monsoon and latitudinal shifts of the Polar Front. Quat. Sci. Rev. 23, 1137–1150 (2004).
Hoshino, M. The Absolute Age of the Numa Coral Reef, Chiba Prefecture. 14C-Age of the Quaternary Deposits in Japan XXXVI 21, 38–39 (1967).
Matsushima, Y. Shallow marine molluscan assemblages of postglacial period in the Japan Islands-Its historical and geographical changes induced by the environmental changes. Bull. Kanagawa Prefectural Museum 15, 37–109 (1984).
Liou, C.-Y., Yang, S.-Y. & Chen, C. A. Unprecedented calcareous algal reefs in northern Taiwan merit high conservation priority. Coral Reefs 36, 1253–1253 (2017).
Chen, M. et al. Enhanced Monsoon‐Driven Upwelling in Southeast Asia During the Little Ice Age. Paleoceanogr. Paleoclimatology 38, (2023).
Kuo, C.-Y. et al. Lonely giant on the sand: unexpected massive Taiwanese coral, Polycyathus chaishanensis in the Datan algal reef demands a conservation focus. Galaxea, J. Coral Reef Stud. 21, 11–12 (2019).
Kuo, C.-Y. et al. Demographic census confirms a stable population of the critically-endangered caryophyllid coral Polycyathus chaishanensis (Scleractinia; Caryophyllidae) in the Datan Algal Reef, Taiwan. Sci. Rep. 10, 10585 (2020).
Serisawa, Y., Imoto, Z., Ishikawa, T. & Ohno, M. Decline of the Ecklonia cava population associated with increased seawater temperatures in Tosa Bay, southern Japan. Fish. Sci. 70, 189–191 (2004).
Yamano, H., Sugihara, K. & Nomura, K. Rapid poleward range expansion of tropical reef corals in response to rising sea surface temperatures. Geophys. Res. Lett. 38, n/a-n/a (2011).
Tkachenko, K. S. & Soong, K. Dongsha Atoll: A potential thermal refuge for reef-building corals in the South China Sea. Mar. Environ. Res. 127, 112–125 (2017).
Sievers, F. et al. Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539–539 (2011).
Darriba, D. et al. ModelTest-NG: A New and Scalable Tool for the Selection of DNA and Protein Evolutionary Models. Mol. Biol. Evol. 37, 291–294 (2020).
Edler, D., Klein, J., Antonelli, A. & Silvestro, D. raxmlGUI 2.0: A graphical interface and toolkit for phylogenetic analyses using RAxML. Methods Ecol. Evol. 12, 373–377 (2021).
Suchard, M. A. et al. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol. 4, vey016 (2018).
Wallace, C. C. & Dai, C.-F. Scleractinia of Taiwan (IV): review of the coral genus Acropora from Taiwan. ZOOLOGICAL STUDIES-TAIPEI 36, 288–324 (1997).
Royston, P. Approximating the Shapiro-Wilk W-test for non-normality. Stat. Comput. 2, 117–119 (1992).
Tukey, J. Multiple comparisons. Journal of the American Statistical Association 48, 624–625 (1953).
Trawiński, B., Smętek, M., Telec, Z. & Lasota, T. Nonparametric statistical analysis for multiple comparison of machine learning regression algorithms. Int. J. Appl. Math. Comput. Sci. 22, 867–881 (2012).

Table 1. Identification criteria based on morphological characters used for distinguishing Acropora solitaryensis and A. divaricata. Due to the high resemblance of morphological characters that often complicate in-situ underwater identification of Acropora solitaryensis and A. divaricata, we conducted a comparative table of specific corallum characteristics, including branch pattern, size, and arrangement, to clarify the distinguishing features and similarities between these two species as referenced by Veron and Wallace (1984) ²³, Wallace (1999)²².

	*Acropora divaricata*		*Acropora solitaryensis*
References	Veron and Wallace, 1984{ Veron and Wallace 1984}	Wallace, 1999²²	Veron and Wallace, 1984²³	Wallace, 1999²²
Corallum
Branching Pattern	Thick tables or bowl/bracket-shaped with central or lateral attachment, 1m or more in height and diameter	Open caespito-corymbose with tapering branches	A. divaricata-like branching pattern, basal branches fused into a perforated or solid plate	Tabulate, table tops formed by anastomosing and upwardly curving, tapering branches
Branch Size	Caespitose branching, distal branches 6-12mm diameter	Branches 5-15 mm in diameter, up to 70 mm		Branches 5-15 mm in diameter, up to 45 mm
Branch Arrangement	Branching pattern and colony shape varying greatly	Curving and anastomosing to form a network within the colony		Anastomosing and upwardly curving
Growth Type		Determinate		Determinate
Corallites
Axial Corallites	Usually 2.3-3.0mm diameter, with calices 0.8-1.1mm diameter	Outer diameter 1.8-3.0 mm, inner diameter 0.7-1.1 mm	Up to 3 mm exsert, 3.4 mm diameter with calices 0.7-1.0 mm diameter	Outer diameter 1.6-3.4 mm, inner diameter 0.5-1.1 mm
Primary Septa	Two cycles up to 1/2R and 1/4R, the latter frequently incomplete	Present up to 1/R	Usually in complete cycles of 1/2R	Present up to 1/2R
Secondary Septa		Absent or some to all present to 1/4R	Usually incomplete to absent	Absent or a few just visible, up to 1/4R
Radial Corallites	Change in shape and size along branches, from prominent on upper branchlets extending at from 45° to 90°, tubular on branch tips, passing through tubo-nariform to nariform, then rounded to sub-immersed proximally	Evenly sized and spaced on branches, nariform, with large, open calices	Tubular appressed on branchlets, becoming immersed on basal branches. Circular to nariform, diameter 1.0-1.3 mm	Evenly sized and arranged, nariform or tubo-nariform, with large, open calices
Primary Septa	Extremely variable septal development, some corallites with only rudimentary septa, others with two well-developed cycles	Present up to 1/2R with obvious directives	Septal development varies, both cycles may be present up to 2/3R	Present up to 1/3R
Secondary Septa		Present up to 1/4R	Usually incomplete to absent	Absent or a few just visible, up to 1/4R
Distally Radial Corallites		Tubo-nariform; towards the base, appressed tubular, sometimes walls extended by prostrate development		Tubo-nariform; towards the base, appressed tubular, sometimes walls extended by rostrate development
Coenosteum
Texture	Consists of rows of laterally flattened or forked spinules, spongy between corallites	Reticulate	Usually the same on and between corallites	Reticulate
Radial Corallites		Dense arrangement of laterally flattened or forked spinules	Covered with rows of fine spinules, may develop into distinct costae	Dense arrangement of laterally flattened or forked spinules
Intercorallite Areas		Spinules less densely arranged		Spinules less densely arranged
Other Systematic Information and Remarks
Similarity to Other Species	Have similar radial corallites and a coenosteum with A. clathrata but can be differ by growth forms. Acropora secale may be confused with A. divaricata but is readily distinguished by having radial corallites of two sizes, the larger having a tubular form.	Very similar to Acropora solitaryensis, distinguished mainly by growth form	Superficially, does not resemble any other species. Closest affinities are with A. divaricata	Looks like a flattened form of A. divaricata, with branches sometimes forming a solid plate
Syntype Information	-	Syntype of Acropora stoddarti Pilai & Scheer, 1976 is a flattened colony, growing on a wreck
Growth Form Variation	Wide range of skeletal variation within single biotopes, seldom develops well-defined, environment-related ecomorphs. One exception is sometimes found in coralla growing on soft substrates, or in turbid water where branchlets become flattened and the colony prostrate (viz. A. stoddarti Pillai & Scheer, 1976). In extreme cases, branchlets become fused into thin plates. Some skeletal developments (e.g. various types of corallite wall-thickening and the development of naked branchlets) appear to be commonly associated with particular populations rather than particular environments.			Varies greatly in thickness of branches, can appear quite delicate or very sturdy
Growth Form Variation
Distribution			Abundant at specific locations but rare elsewhere. Divisible into five geographic subspecies, widely separated spatially and environmentally	Very common species in the Indian Ocean, Indonesia, and the South China Sea. Surprisingly rare on the Great Barrier Reef proper as reported in Veron & Wallace, 1984
Geographic Subspecies			Indicates five geographic subspecies, needing experimental verification to confirm as a single species unit

Table 2. Overview of genetic markers, genomic locations, and sequence characteristics. The table summarizes the genetic markers used in this study, detailing their genomic locations, number of taxa analyzed for each marker, sequence length before alignment (L), sequence length after alignment (AL), number of variable sites (VS), and number of parsimony-informative sites (PI).

Marker	genome	Taxa	L (bp)	AL	VS	PI
Control Region	mitochondrial	111	778-989	742	80	38
Mini-collagen	nuclear	112	462-508	210	49	40
4706	nuclear	108	413-461	401	5	4
PMCA	nuclear	108	542-608	487	33	25
Nuclear Combined	4706-PMCA-Mini Collagen	108	1078-1097	1100	89	68

L = sequence length before alignment; AL = sequence length after alignment; VS= variable sites; PI=parsimony informative sites

No competing interests reported.

Download PDF

Editorial decision: Revision requested
30 Oct, 2024
Reviews received at journal
26 Oct, 2024
Reviews received at journal
22 Oct, 2024
Reviews received at journal
19 Oct, 2024
Reviewers agreed at journal
09 Oct, 2024
Reviewers agreed at journal
09 Oct, 2024
Reviewers agreed at journal
08 Oct, 2024
Reviews received at journal
03 Oct, 2024
Reviewers agreed at journal
23 Sep, 2024
Reviewers agreed at journal
22 Sep, 2024
Reviewers invited by journal
20 Sep, 2024
Editor assigned by journal
17 Sep, 2024
Editor invited by journal
02 Sep, 2024
Submission checks completed at journal
30 Aug, 2024
First submitted to journal
30 Aug, 2024

You are reading this latest preprint version

A clear distinction and presence of Acropora divaricata within Acropora solitaryensis species complex along their biogeographic distribution in East-Asia

Status:

Version 1

Abstract

Figures

INTRODUCTION

RESULTS

DISCUSSION

METHODS

Declarations

References

Table

Additional Declarations

Supplementary Files

Status:

Version 1