Poleward migration of tropical corals inhibited by future trends of seawater temperature and calcium carbonate (CaCO3) saturation.

Poleward range expansion of marine organisms is commonly attributed to anthropogenic ocean warming. However, the extent to which a single species can migrate poleward remains unclear. In this study, we used molecular data to examine the current distribution of the Pocillopora damicornis species complex in Taiwan waters and applied niche modeling to predict its potential range through the end of the 21st Century. The P. damicornis species complex is widespread across shallow, tropical and subtropical waters of the Indo-Pacific regions. Our results revealed that populations from subtropical nonreefal coral communities are P. damicornis, whose native geographical ranges are approximately between 23°N and 35°N. In contrast, those from tropical reefs are P. acuta. Our analysis of 50 environmental data layers demonstrated that the concentrations of CaCO3 polymorphs had the greatest contributions to the distributions of the two species. Future projections under intermediate shared socioeconomic pathways (SSP) 2-4.5 and very high (SSP5-8.5) scenarios of greenhouse gas emissions showed that while sea surface temperature (SST) isotherms would shift northwards, saturation isolines of two CaCO3 polymorphs, calcite (Ωcal) and aragonite (Ωarag), would shift southwards by 2100. Subsequent predictions of future suitable habitats under those conditions indicated that distinct delimitation of geographical ranges for the two species would persist, and neither would extend beyond its native geographical zones, indicating that tropical Taiwan waters are the northern limit for P. acuta. In contrast, subtropical waters are the southern limit for P. damicornis. We concluded that the decline in CaCO3 saturation would make high latitudes less inhabitable, which could be one of the boundary elements that limit poleward range expansion driven by rising SSTs and preserve the latitudinal diversity gradient (LDG) on Earth. Consequently, poleward migration of tropical reef corals to cope with warming oceans should be reevaluated.

Potential PCR amplification bias in identifying complex ecological patterns: Higher species compositional homogeneity revealed in smaller-size coral reef zooplankton by metatranscriptomics.

PCR-based high-throughput sequencing has permitted comprehensive resolution analyses of zooplankton diversity dynamics. However, significant methodological issues still surround analyses of complex bulk community samples, not least as in prevailing PCR-based approaches. Marine drifting animals-zooplankton-play essential ecological roles in the pelagic ecosystem, transferring energy and elements to higher trophic levels, such as fishes, cetaceans and others. In the present study, we collected 48 size-fractionated zooplankton samples in the vicinity of a coral reef island with environmental gradients. To investigate the spatiotemporal dynamics of zooplankton diversity patterns and the effect of PCR amplification biases across these complex communities, we first took metatranscriptomics approach. Comprehensive computational analyses revealed a clear pattern of higher/lower homogeneity in smaller/larger zooplankton compositions across samples respectively. Our study thus suggests changes in the role of dispersal across the sizes. Next, we applied in silico PCR to the metatranscriptomics datasets, in order to estimate the extent of PCR amplification bias. Irrespective of stringency criteria, we observed clear separations of size fraction sample clusters in both metatranscriptomics and in silico datasets. In contrast, the pattern-smaller-fractioned communities had higher compositional homogeneity than larger ones-was observed in the metatranscriptomics data but not in the in silico datasets. To investigate this discrepancy further, we analysed the mismatches of widely used mitochondrial CO1 primers and identified priming site mismatches likely driving PCR-based biases. Our results suggest the use of metatranscriptomics or, although less ideal, redesigning the CO1 primers is necessary to circumvent these issues.

A molecular census of early-life stage scleractinian corals in shallow and mesophotic zones.

The decline of coral reefs has fueled interest in determining whether mesophotic reefs can shield against disturbances and help replenish deteriorated shallower reefs. In this study, we characterized spatial (horizontal and vertical) and seasonal patterns of diversity in coral recruits from Dabaisha and Guiwan reefs at Ludao, Taiwan. Concrete blocks supporting terra-cotta tiles were placed at shallow (15m) and mesophotic (40m) depths, during 2016-2018. Half of the tiles were retrieved and replaced biannually over three 6-month surveys (short-term); the remainder retrieved at the end of the 18-month (long-term) survey. 451 recruits were located using fluorescent censusing and identified by DNA barcoding. Barcoding the mitochondrial cytochrome oxidase I (COI) gene resulted in 17 molecular operational taxonomic units (MOTUs). To obtain taxonomic resolution to the generic level, Pocillopora were phylotyped using the mitochondrial open reading frame (ORF), resolving eight MOTUs. Acropora, Isopora, and Montipora recruits were identified by the nuclear PaxC intron, yielding ten MOTUs. Overall, 35 MOTUs were generated and were comprised primarily of Pocillopora and, in fewer numbers, Acropora, Isopora, Pavona, Montipora, Stylophora, among others. 40% of MOTUs recruited solely within mesophotic reefs while 20% were shared by both depth zones. MOTUs recruiting across a broad depth distribution appear consistent with the hypothesis of mesophotic reefs acting as a refuge for shallow-water coral reefs. In contrast, Acropora and Isopora MOTUs were structured across depth zones representing an exception to this hypothesis. This research provides an imperative assessment of coral recruitment in understudied mesophotic reefs and imparts insight into the refuge hypothesis.

Strong horizontal and vertical connectivity in the coral Pocillopora verrucosa from Ludao, Taiwan, a small oceanic island.

Mesophotic habitats could be sheltered from natural and anthropogenic disturbances and act as reproductive refuges, providing propagules to replenish shallower populations. Molecular markers can be used as proxies evaluating the connectivity and inferring population structure and larval dispersal. This study characterizes population structure as well as horizontal and vertical genetic connectivity of the broadcasting coral Pocillopora verrucosa from Ludao, a small oceanic island off the eastern coast of Taiwan. We genotyped 75 P. verrucosa specimens from three sites (Gongguan, Dabaisha, and Guiwan) at three depth ranges (Shallow: 7-15 m, Mid-depth: 23-30 m, and Deep: 38-45 m), spanning shallow to upper mesophotic coral reefs, with eight microsatellite markers. F-statistics showed a moderate differentiation (FST = 0.106, p<0.05) between two adjacent locations (Dabaisha 23-30 and Dabaisha 38-45 m), but no differentiation elsewhere, suggesting high levels of connectivity among sites and depths. STRUCTURE analysis showed no genetic clustering among sites or depths, indicating that all Pocillopora individuals could be drawn from a single panmictic population. Simulations of recent migration assigned 30 individuals (40%) to a different location from where they were collected. Among them, 1/3 were assigned to deeper locations, 1/3 to shallower populations and 1/3 were assigned to the right depth but a different site. These results suggest high levels of vertical and horizontal connectivity, which could enhance the recovery of P. verrucosa following disturbances around Ludao, a feature that agrees with demographic studies portraying this species as an opportunistic scleractinian.

A new species of Synagoga (Crustacea, Thecostraca, Ascothoracida) parasitic in an antipatharian from Green Island, Taiwan, with notes on its morphology.

A new ascothoracidan species has been discovered off Taiwan in the north part of the west Pacific at SCUBA depths. Twelve specimens including both sexes of the new species, described herein as Synagoga arabesque sp. nov., were collected from colonies of the antipatharian Myriopathes cf. japonica Brook, 1889. Three previously described species of Synagoga, morphologically the least specialized ascothoracidan genus, have been found as ectoparasites of antipatharians and an alcyonarian, whereas all other records of this genus have been based on specimens collected from the marine plankton. This is the second study of a new form of Synagoga to be based on more than a few mature specimens of a single sex or on a single juvenile. Furthermore, it is the second in which SEM has been used to document the fine-scale external morphology. The position of terminal pores in the anterior pairs of the lattice organs is different in Synagoga arabesque sp. nov. than those in S. grygieri Kolbasov & Newman, 2018 and S. millipalus Grygier & Ohtsuka, 1995. Species of Synagoga are small, host-specific predators or ectoparasites of antipatharians. This genus exhibits a major Tethyan reliction pattern.

The influence of tourism-based provisioning on fish behavior and benthic composition.

Distribution of non-natural food (provisioning) to attract fish, though popular in coral reef tourism, has often been discouraged due to its assumed adverse effects on fish health and behavior. However, the effects of provisioning on community structure, anti-predator, and foraging behavior of teleost fishes, as well as their potential to indirectly affect benthic organisms, are not yet clear. Here, we compared fish composition, wariness, foraging behavior of herbivorous fishes, and the benthic cover between provisioned and control sites. We found significant differences in fish abundance, species number, and composition at some locations, but not all. Although most provisioned herbivorous fish did not reduce their biting rates of benthic algae, provisioned sites still had higher coverage of green macroalgae. Our results dispute widely held presumptions on the effects of tourism-based provisioning on the ecology and behavior of teleost fishes, as well as the benthic cover. These findings suggest that while regulation of provisioning is necessary to manage and mitigate any deleterious outcomes, when moderated and monitored, it could still provide an educationally beneficial tool for coral reef ecotourism.

Molecular assessment of Pocillopora verrucosa (Scleractinia; Pocilloporidae) distribution along a depth gradient in Ludao, Taiwan.

It can be challenging to identify scleractinian corals from the genus Pocillopora Lamarck 1816 in the field because of their large range of inter- and intra-specific morphological variation that co-occur with changes in the physical environment. This task is made more arduous in the context of a depth gradient, where light and water current could greatly affect the morphology of the corallum. Pocillopora verrucosa (Ellis & Solander 1786) in Taiwan was previously reported exclusively from shallow waters (<10 m in depth), but a recent observation of this species in the mesophotic zone (>40 m in depth) questions this bathymetric distribution. We used the mitochondrial open reading frame and the histone 3 molecular markers to investigate the vertical and horizontal spatial distribution of P. verrucosa around Ludao (Green Island), Taiwan. We genotyped 101 P. verrucosa-like colonies collected from four depth zones, ranging from 7 to 45 m, at three sites around the island. Of the 101 colonies sampled, 85 were genotyped as P. verrucosa, 15 as P. meandrina, and one specimen as an undescribed Pocillopora species. P. verrucosa was found at all depths, while P. meandrina and the undescribed Pocillopora specimen were limited to 15 m depth. P. verrucosa has a large bathymetric distribution around Ludao and could benefit from the refuge that the mesophotic zone offers. This study illustrates the difficulty of identifying Pocillopora corals in the field and emphasizes the relevance of molecular taxonomy as an important and complementary tool to traditional taxonomy for clarifying vertical and horizontal species distribution. Our results also illustrate the need in conservation biology to target species genetic diversity rather than just species diversity.

Spatial variation in the morphological traits of Pocillopora verrucosa along a depth gradient in Taiwan.

Pocillopora verrucosa is a widely distributed depth-generalist coral that presents plasticity in its skeletal macro- and microstructure in response to environmental gradients. Light and water movement, which covary with depth, are the main environmental drivers of morphological plasticity in this genus; however, assessing environmentally-induced plasticity may be confounded by the extent of interspecific variation in Pocillopora. We examine the morphology of 8 typed P. verrucosa specimens collected along a depth gradient ranging from 7 to 45 meters and comprising 3 sites throughout Ludao, Taiwan. We measured 36 morphological characters, 14 which are novel, in 3 regions on the corallum-the apex, branch and base-in order to quantify their relationship to site and depth. We found significant correlation between depth and 19 morphological characters, notably branch verruca area, branch verruca height, base verruca spacing, base spinule length, and branch corallite area. 60% of microstructural characters and 25% of macrostructural characters showed a correlative relation to depth, suggesting that depth acclimatization is manifested primarily at the microstructural level. Canonical discriminant analysis of all morphometric characters by depth supports clustering into 3 groups: an overlapping 7m and 15m group, a 23-30m group, and a 38-45m group. Canonical discriminant analysis by site supports clustering into low- and high-current sites, differentiated primarily by branch septa width, base septa width, pre-terminal branch width, terminal branch maximum length, and terminal branch minimum length. We conclude that distinctive patterns of morphological variation in mesophotic specimens of P. verrucosa could reflect the effects of abiotic parameters such as light and water flow. Elucidating the mechanisms behind the morphological changes that occur in response to environmental gradients can help clarify the role that physiological plasticity plays in the acclimatization of corals to the unique environmental settings of mesophotic coral ecosystems.

Four anchimolgid copepods (Poecilostomatoida: Anchimolgidae) associated with the scleractinian coral Pavona explanulata (Lamarck, 1816) in Taiwan.

Several species of copepods are known to live in association with the coral genus Pavona Lamarck, 1801. In this paper, four poecilostomatoid copepods, including one new genus, two new species, and one species new to Taiwan, are described, i.e. Alienigena triangula gen. et sp. nov., Odontomolgus cognatus sp. nov., O. mucosus Kim, 2006 and Sociellus subgeminus sp. nov. All species were found together in a single washing of the scleractinian coral Pavona explanulata (Lamarck, 1816), collected from shallow water reefs in northern Taiwan. All of them appear closely related to the genera of the Odontomolgus-group in the family Anchimolgidae due to the possession of a large process on the convex margin of the mandible. The present report brings the number of copepod species that live in symbiosis with members of the coral genus Pavona to 17.