Zoantharian Species Research Articles

Museum collections as untapped sources of undescribed diversity of sponge-zoantharian associations with the description of six new species of Umimayanthus (Zoantharia: Parazoanthidae) from Western Australia and eastern Indonesia

Abstract The zoantharian genus Umimayanthus consists largely of species that live in obligate symbioses with sponges. Although zoantharians have often been overlooked in field collecting campaigns and in research, sponges are usually well-collected, and many natural history museums harbor numerous sponge specimens. Thus, these sponge collections may also include previously overlooked zoantharian species. Such is the case in this research, in which we examined sponge specimens in museum collections from Western Australia and eastern Indonesia. Based on our morphological and molecular analyses, we herein describe six species of Umimayanthus new to science, and redescribe another species described over a century ago. These species can be distinguished by their sponge associations, gross polyp and colony morphology, and depth ranges. Based on these findings, it appears that the Central Indo-Pacific region of Western Australia and Indonesia can be considered a hotspot for sponge-associated zoantharian diversity. We provide a key for the identification of all formally described species in the genus, but caution that there are likely more Umimayanthus species awaiting discovery.

Effects of macroalgae and sea urchin grazing pressure on zoantharians growth under laboratory conditions

In the context of ocean warming, thermophilic organisms such as zoantharians are expanding and altering shallow benthic habitats. Here, a four-month laboratory experiment was performed to examine the influence of three types of macroalgae morphotypes common in the Canary Islands (turf algae, Lobophora spp., and crustose coralline algae) on the growth of two zoantharian species, Palythoa caribaeorum and Zoanthus pulchellus. Additionally, the grazing effects of echinoids Diadema africanum and Paracentrotus lividus were assessed as facilitators of substrate colonization by means of controlling macroalgae cover. Colony and algal coverages were measured at the beginning, middle and end of the experiment, and increments were calculated. Results indicated a general decrease in zoantharian colony sizes in contact with different algal types in the absence of sea urchins. However, P. caribaeorum colonies showed significant growth in the presence of D. africanum, highlighting the ecological importance of sea urchins in zoantharian population proliferation and subsequent community modification. This study represents the first investigation into zoantharian-macroalgae interactions under controlled conditions.

Genome sizes and repeatome evolution in zoantharians (Cnidaria: Hexacorallia: Zoantharia).

Across eukaryotes, large variations of genome sizes have been observed even between closely related species. Transposable elements as part of the repeated DNA have been proposed and confirmed as one of the most important contributors to genome size variation. However, the evolutionary implications of genome size variation and transposable element dynamics are not well understood. Together with phenotypic traits, they are commonly referred to as the "C-value enigma". The order Zoantharia are benthic cnidarians found from intertidal zones to the deep sea, and some species are particularly abundant in coral reefs. Despite their high ecological relevance, zoantharians have yet to be largely studied from the genomic point of view. This study aims at investigating the role of the repeatome (total content of repeated elements) in genome size variations across the order Zoantharia. To this end, whole-genomes of 32 zoantharian species representing five families were sequenced. Genome sizes were estimated and the abundances of different repeat classes were assessed. In addition, the repeat overlap between species was assessed by a sequence clustering method. The genome sizes in the dataset varied up to 2.4 fold magnitude. Significant correlations between genome size, repeated DNA content and transposable elements, respectively (Pearson's correlation test R2=0.47, p=0.0016; R2=0.22, p=0.05) were found, suggesting their involvement in the dynamics of genome expansion and reduction. In all species, long interspersed nuclear elements and DNA transposons were the most abundant identified elements. These transposable elements also appeared to have had a recent expansion event. This was in contrast to the comparative clustering analysis which revealed species-specific patterns of satellite elements' amplification. In summary, the genome sizes of zoantharians likely result from the complex dynamics of repeated elements. Finally, the majority of repeated elements (up to 70%) could not be annotated to a known repeat class, highlighting the need to further investigate non-model cnidarian genomes. More research is needed to understand how repeated DNA dynamics relate to zoantharian evolution and their biology.

Tropicalization alert: new species of mat-forming zoantharian (Zoanthus pulchellus) arrives on Madeira Island (NE Atlantic)

The first record of a mat-forming zoantharian species, Zoanthus pulchellus (Duchassaing and Michelotti, 1860), in Madeira Island, Portugal (NE Atlantic).

Genome-wide SNPs data provides new insights into the population structure of the Atlantic-Mediterranean gold coral Savalia savaglia (Zoantharia: Parazoanthidae)

Savalia savaglia is an Atlantic-Mediterranean zoantharian species with a patchy geographic and bathymetric distribution. Due to its longevity, S. savaglia may form large-sized colonies which play a crucial role in the ecosystem as habitat formers. Despite its ecological importance, little is known about the population structure and intraspecific genetic diversity of this species. Using ddRAD-Seq genotyping, we obtained genome-wide single nucleotide polymorphisms (SNPs) from 50 S. savaglia individuals collected at different depths (8–60 m) and localities across the Mediterranean Sea (Marseille, Sardinia, Puglia and Montenegro) and eastern Atlantic (Portugal). Our molecular observations were discussed with the reproductive behaviour of the species to understand the observed patterns of connectivity and gene flow. These results highlight the presence of three main genetic clusters (Marseille; Sardinia; and Montenegro + Portugal + Puglia), with some of the Mediterranean individuals being genetically closer to the Atlantic population rather than to other Mediterranean populations. The strong linkage disequilibrium recorded across loci and the detection of clonal individuals in the shallow populations suggest that asexual reproduction seems to be the dominant reproductive strategy among the S. savaglia populations sampled at lower depths. Our work highlights the potential of genome-wide SNP data to study the reproductive behaviour in species such as S. savaglia that are difficult to investigate in the field. The genetic connectivity data obtained in this study can be used in the future to better guide the development of effective management and conservation plans.

Biogeography of endosymbionts (Symbiodiniaceae) associated with zoantharian species (Hexacorallia: Anthozoa) from the Macaronesia and Cape Verde ecoregions

Populations of some zoantharian species (Cnidaria: Anthozoa) have been able to proliferate in locations where abiotic conditions hinder scleractinian corals’ survival. One of the contributing factors might be the advantageous host-symbiont associations that could lead holobionts to be more resilient to environmental variation, even in marginal-environments. However, few studies have addressed these Zoantharia–Symbiodiniaceae associations, especially little is known about their nature and distribution in the Atlantic Ocean. In this study, we use the large ribosomal subunit (LSU-rDNA) and Internal Transcribed Spacer 2 (ITS2) to examine the biodiversity and distribution of Symbiodiniaceae species within zoantharians that inhabit along the latitudinal gradient Madeira (40ºN)—Cape Verde (16ºN). Moreover, we determine the number of different endosymbionts genera inhabiting the same specimen, in order to estimate their ability to face alterations in the environment. The results showed that Symbiodiniaceae diversity increases towards the tropics, with a total of six ITS2 types belonging to Symbiodinium and Cladocopium, the latter being the most frequent genus. Furthermore, we have found a possible undescribed species inhabiting P. aff. clavata collected at Madeira Island, the northernmost limit of brachycnemic zoantharian distributions in the East Atlantic. These results, combined with the literature reviewed, constitute the first mention of the genus Symbiodinium in a species host that is not Zoanthus spp and for the archipelago of the Canary Islands. An appendix summarizing Zoantharia–Symbiodiniaceae distributions around the Atlantic is included to facilitate future research on these holobiont associations.

Same but different? Zoantharian assemblages (Anthozoa: Hexacorallia) in Bonaire and Curaçao, southern Caribbean

Marine community datasets are key to the effective management and conservation of marine ecosystems, including coral reefs, which are increasingly threatened by a myriad of stressors. Although community information exists for many comparatively well-studied taxa, other common groups remain to be examined for even such basic information. In this study, we report on the zoantharian communities (Cnidaria: Anthozoa: Hexacorallia: Zoantharia) on the reefs of Bonaire in the southern Caribbean, and compare current results from 30, 20, 10, and 5 m depths to recent similar surveys from nearby Curaçao. The surveys revealed a total of 17 zoantharian species and epibiotic associations on the reefs of Bonaire. Additionally, results showed that while zoantharian assemblages around Bonaire at shallow 5 and 10 m depths, dominated by Palythoa spp., were similar to those found on Curaçao, diversity and numbers of zoantharians were higher at 20 and 30 m due to more abundant epibiotic Parazoanthidae species associated with sponges. Differences in assemblage structure were seen in deeper 20 and 30 m depths between the two islands, implying that conservation of deeper reef slopes, or along depth gradients, may need to be independently considered and addressed for each location. Analyses with environmental parameters on the Bonaire dataset indicate the potential importance of coral reef rugosity and physical structure in shaping these zoantharian communities, aspects that should be focused on in more detail in future research.

Unexpected high abundance of aragonite-forming Nanipora (Octocorallia: Helioporacea) at an acidified volcanic reef in southern Japan

Nanipora Miyazaki & Reimer, 2015 is a recently discovered genus of aragonite-skeleton producing octocorals closely related to the blue coral genus Heliopora de Blainville, 1830. Since its discovery, Nanipora has been reported from coral reefs in Okinawa, Japan, and Thailand, and from seagrass beds in the northern South China Sea. However, it remains little known and studied. Here, we report on the unexpected discovery of an abundance of Nanipora colonies in shallow waters less than 2-m deep around a CO2 vent from the uninhabited volcanic island of Iwotorishima, Okinawa, in southern Japan. Nanipora colonies were found covering both coral rubble and hard substrates, alongside a few soft coral and zoantharian species. Polyps were pale white in color with none brown or darker in coloration as in some recent reports. As the original description of N. kamurai from Zamami Island in Okinawa describes the species as azooxanthellate, as the current Iwotorishima specimens also appear to be, and recently reported specimens from Thailand, Dongsha Atoll, and Yaeyama are zooxanthellate, it may be that there are more than one Nanipora species; the type species N. kamurai that is also likely at Iwotorishima, and a zooxanthellate species that constitutes the other records. Although Nanipora is not well studied, its presence at this volcanic CO2 seep suggests it has the ability to survive under unique and extreme environmental conditions, rendering it as a potentially important subject of study in the face of increasing ocean acidification.

Zoantharia (Cnidaria: Hexacorallia) of the Dutch Caribbean and One New Species of Parazoanthus

Species of the anthozoan order Zoantharia (=Zoanthidea) are common components of subtropical and tropical shallow water coral reefs. Despite a long history of research on their species diversity in the Caribbean, many regions within this sea remain underexamined. One such region is the Dutch Caribbean, including the islands of St. Eustatius, St. Maarten, Saba, Aruba, Bonaire, and Curaçao, as well as the Saba Bank, for which no definitive species list exists. Here, combining examinations of specimens housed in the Naturalis Biodiversity Center collection with new specimens and records from field expeditions, we provide a list of zoantharian species found within the Dutch Caribbean. Our results demonstrate the presence at least 16 described species, including the newly described Parazoanthus atlanticus, and the additional potential presence of up to four undescribed species. These records of new and undescribed species demonstrate that although the zoantharian research history of the Caribbean is long, further discoveries remain to be found. In light of biodiversity loss and increasing anthropogenic pressure on declining coral reefs, documenting the diversity of zoantharians and other coral reef species to provide baseline data takes on a new urgency.

Comparison of Symbiodiniaceae diversities in different members of a Palythoa species complex (Cnidaria: Anthozoa: Zoantharia)-implications for ecological adaptations to different microhabitats.

In this study we compared genotypes of zoantharian host-associating algal symbionts among Palythoa species, which are among the dominant benthic reef organisms in the Ryukyu Archipelago, Japan, and evaluated Symbiodiniaceae diversities of closely related congeneric Palythoa species. We targeted a species complex of the zoantharian genus Palythoa (P. tuberculosa, P. sp. yoron, P. mutuki) living among different microhabitats in a narrow reef area of Tokunoshima Island. For phylogenetic analyses, we used two DNA marker regions; nuclear internal transcribed spacer (ITS) and plastid mini-circle non-coding region (psbAncr), both of which have previously been used to determine Symbiodiniaceae genotypes of zoantharian species. Our results showed that all Palythoa species hosted symbionts of the genus Cladocopium, with genotypic compositions of this genus showing some variations among the three different Palythoa species. Additionally, we found that the Cladocopium genotypic composition was statistically different among Palythoa species, and among P. tuberculosa specimens in different microhabitats. Our results suggest that ecological divergence among these three Palythoa species may be related to differing Symbiodiniaceae diversities that may in turn contribute to eco-physiological adaptation into different microhabitats on coral reefs.

A molecular phylogeny of carcinoecium-forming Epizoanthus (Hexacorallia: Zoantharia) from the Western Pacific Ocean with descriptions of three new species

Many cnidarians have been reported in association with hermit crabs from shallow waters to the deep sea. Some of these actiniarians and zoantharians produce a carcinoecium, a chitin-like pseudo-shell. Many studies have been conducted on hermit crab–actiniarian symbioses, while hermit crab–zoantharian symbioses have received less attention due to the difficulty of specimen collection as they are exclusively found in the deep sea. In this study, 11 carcinoecium-forming specimens associated with hermit crabs of several genera were collected from the western Pacific Ocean. We formally described the collected specimens as Epizoanthus xenomorphoideus sp. nov., E. australis sp. nov., and E. gorgonus sp. nov. based on results of molecular phylogenetic analyses (COI, mt 12S-rDNA, mt 16S-rDNA, 18S-rDNA, ITS-rDNA) and morphological observations. Our phylogenetic results showed that there are two different subclades within a carcinoecium clade, and these subclades have different external morphologies. Further studies with more taxon sampling will enable a more comprehensive evaluation of the evolution and phylogenetic relationships of carcinoecium-forming zoantharian species.

Diversity of Saint Helena Island and zoogeography of zoantharians in the Atlantic Ocean: Jigsaw falling into place

Diversity surveys in isolated sites, such as oceanic islands, provide biogeographic data that can improve our analyses and knowledge of evolutionary processes in the oceans. Zoantharians (Cnidaria: Anthozoa) are common and widespread components of shallow-water reefs, but distributional analyses are scarce for this group. In this study, we collected Zoantharia specimens from around Saint Helena Island (STH) in the mid-Atlantic and identified species using external morphology and molecular data. Moreover, we compiled and analysed the most comprehensive distributional data for zoantharian species in the subtropical and tropical Atlantic Ocean to date. Our results show eight zoantharian species in STH, which includes seven new records for STH waters. Furthermore, all families and genera of the suborder Brachycnemina recorded are widespread in the Atlantic Ocean, including at least four amphi-Atlantic species. The Caribbean is the richness centre in the Atlantic Ocean for zoantharian species, a pattern similar to that observed for many other subtropical/tropical marine taxa. However, Zoantharia may have a lower endemism rate in some areas than other common reef animals, for example zooxanthellate scleractinian corals and reef fishes. Moreover, zoantharian species have a more extensive distribution than close-related taxa such as zooxanthellate scleractinian corals and hydrocorals in the Atlantic Ocean.

Diversity of zoantharian species and their symbionts from the Macaronesian and Cape Verde ecoregions demonstrates their widespread distribution in the Atlantic Ocean

Zooxanthellate zoantharians (Cnidaria: Anthozoa) are commonly found in tropical and subtropical marine regions around the world. However, due to the low genetic variability of commonly used DNA markers combined with high levels of intraspecific morphological variation, misidentifications and species synonyms are commonly found in the literature. In this study, zoantharians from the suborder Brachycnemina collected in the Macaronesia and Cape Verde ecoregions were studied combining morphological, molecular and ecological data, in order to comprehensively assess the species diversity of the region. Moreover, molecular analyses of endosymbiotic Symbiodiniaceae zooxanthellae were also performed to provide more information on each holobiont. Our integrative results demonstrate that Brachycnemina species diversity increases as seawater temperature rises toward the tropics with a total of nine species recorded: one from waters around northern Madeira, five in the Canary Islands and seven in the southernmost Cape Verde Archipelago. All species were seen to host either Symbiodiniaceae of the genera Symbiodinium (former Symbiodinium ‘Clade A’) or Cladocopium (former Symbiodinium ‘Clade C’). Moreover, this study records for the first time the presence of Palythoa grandis, P. aff. clavata, P. grandiflora, an unknown Zoanthus species and Z. pulchellus in the East Atlantic Ocean. These results show no endemic zooxanthellate zoantharians in the East Atlantic, with all species shared with the West Atlantic.

Spatial partitioning of Zoantharian species (Suborder Brachycnemina) at intertidal rocky platforms of the Canary Islands

Spatial partitioning of Zoantharian species (Suborder Brachycnemina) at intertidal rocky platforms of the Canary Islands

Distribution patterns of intertidal zoantharian species in the Canary Islands and their relation with ocean temperature

Distribution patterns of intertidal zoantharian species in the Canary Islands and their relation with ocean temperature

Zoantharia (Anthozoa: Hexacorallia) abundance and associations with Porifera and Hydrozoa across a depth gradient on the west coast of Curaçao

Despite much research on zoantharians, little work has been done on the abundance of these animals in depths greater than 5 m. In this study, we examined the abundance of zoantharian species and their associated fauna at four depths (5, 10, 20, and 30 m) at multiple sites on the leeward west side of Curaçao in the southern Caribbean in order to provide baseline data. We aimed to quantify zoantharian-host associations in Curaçao to examine if the associations present vary according to different sites and across depths. Results showed that zooxanthellate Palythoa and Zoanthus were most common in shallow waters (5 m), although perhaps less common than observed 35–45 years ago, while sponge-associated species of Macrocnemina were commonly observed at greater depths. There was increasing zoantharian abundance and diversity with greater depth, and two major clusters of zoantharian assemblages in multi-dimensional scaling analyses, one cluster of shallow 5-m datasets, and the other of the large majority of 10-, 20-, and 30-m datasets, demonstrating that assemblages differed significantly by depth (5 m vs. 10, 20, 30 m). In contrast, no significant differences in zoantharian abundance or assemblage were seen across different sites. The data from this study establish a baseline of zoantharian assemblage data that can be compared with other regions and to datasets from Curaçao in the future, which will be of importance in tracking ecological shifts in the face of on-going climate change.

Rafting in Zoantharia: a hitchhiker's guide to dispersal?

The increasing availability of human-made structure in the oceans coupled with climate changes may lead to the range expansion of species able to disperse by rafting. In this study, we report on zoantharian species of genera Isaurus, Palythoa, Umimayanthus and Zoanthus covering artificial substrates in locations in both the Atlantic and Pacific oceans. Moreover, we reviewed observations of additional zoantharians as macrofouling organisms, and discuss the possible role of rafting in the dispersal of this cosmopolitan group. Traits reported to some zoantharian species, such as hermaphroditism and resistance to desiccation, support their dispersal potential by drifting attached to floating objects. Further reports of zoantharian species covering floating artificial structures and natural debris are needed to increase our knowledge of dispersal mechanisms in the oceans. Additionally, this information is essential to monitor and manage possible exotic species invasions, especially for zoantharian species that are common in the aquarium trade.

Zoantharian mitochondrial genomes contain unique complex group I introns and highly conserved intergenic regions

Complex group I introns represent hallmarks of hexacoral mitochondrial genomes (mtDNAs). These intron elements are expected to influence the gene organization and gene expression. We sequenced the mitochondrial genome and transcriptome of Zoanthus sansibariscus and Palythoa heliodiscus, two zoantharian species (colonial anemones) representing different families within the suborder Brachycnemina. The circular and approximately 21kb mtDNAs contained two group I introns, one in ND5 and another in COI. The ND5-717 intron harbored two conventional mitochondrial genes (ND1 and ND3) within its structure and revealed several conserved features compared to ND5-717 in sea anemones. The COI intron, however, was inserted at a unique location (after position 867), which was different from that in sea anemones (position 884) and stony corals (position 720). COI-867 contained a homing endonuclease gene (HEG) with remarkable features, including species-specific length variations and only one copy of the essential LAGLIDADG motif. Whereas transcriptome analysis indicated that all conventional mtDNA genes were expressed, HEG expression appeared significantly repressed. Finally, we identified absolutely conserved non-coding repeat motifs with antisense features and potential regulatory functions.

Diversity of Zoantharia (Anthozoa: Hexacorallia) at Dongsha Atoll in the South China Sea

Dongsha Atoll is the largest coral atoll in the South China Sea (SCS), and is expected to harbor high levels of biodiversity as the SCS is located adjacent to the recognized center of maximum marine biodiversity in the central Indo-Pacific (CIP). However, due to its relative isolation, the biodiversity of Dongsha Atoll has not yet been well investigated for most marine taxa. In this study, we report on findings from our survey in 2016 that focused on the order Zoantharia, for which only sporadic previous reports exist from the SCS. Our results indicate some species such as Palythoa tuberculosa are very common around Dongsha Atoll, as well as the presence of at least three undescribed species, including one species only found thus far at the atoll. Overall, we recorded 16 species of Zoantharia from Dongsha Atoll, bringing the total number of zoantharian species in the SCS to 22, close to numbers reported from the CIP (=24 spp.) and southern Japan (=28 spp.). These findings demonstrate the importance of protecting the biodiversity of Dongsha Atoll, and also, given the limited survey coverage, the potential for undiscovered biodiversity in the SCS.

Phylogeny of Symbiodinium populations in zoantharians of the northern Persian Gulf

Zoantharians of the Persian Gulf (PG) experience periods of anomalous high temperature, irradiance and desiccation. Their survival largely relies on the symbiotic relationship with single celled dinoflagellates of the genus Symbiodinium. However, the phylogeny of symbionts of zoantharians has not been investigated in the region. In this study, the second internal transcribed spacer region of ribosomal DNA (ITS2) was used to recognize in hospite populations of Symbiodinium in Palythoa aff. mutuki, Palythoa tuberculosa and Zoanthus sansibaricus colonies from Hengam, Kish, Larak, and Qeshm Islands, in the PG. The results showed subclade D1–4 and a variant of A1, were the most prevalent subclades of Symbiodinium. Predominance of stress tolerant subclade D1–4 and putatively radiation tolerant variant of A1 of Symbiodinium in zoantharian species might suggest an adaptation strategy to the extreme physical environment of the PG.