Molecules Clarify a Cnidarian Life Cycle – The “Hydrozoan” Microhydrula limopsicola Is an Early Life Stage of the Staurozoan Haliclystus antarcticus

Background: Life cycles of medusozoan cnidarians vary widely, and have been difficult to document, especially in the most recently proposed class Staurozoa. However, molecular data can be a useful tool to elucidate medusozoan life cycles by tying together different life history stages. Methodology/Principal Findings: Genetic data from fast-evolving molecular markers (mitochondrial 16S, nuclear ITS1, and nuclear ITS2) show that animals that were presumed to be a hydrozoan, Microhydrula limopsicola (Limnomedusae, Microhydrulidae), are actually an early stage of the life cycle of the staurozoan Haliclystus antarcticus (Stauromedusae, Lucernariidae). Conclusions/Significance: Similarity between the haplotypes of three markers of Microhydrula limopsicola and Haliclystus antarcticus settles the identity of these taxa, expanding our understanding of the staurozoan life cycle, which was thought to be more straightforward and simple. A synthetic discussion of prior observations makes sense of the morphological, histological and behavioral similarities/congruence between Microhydrula and Haliclystus. The consequences are likely to be replicated in other medusozoan groups. For instance we hypothesize that other species of Microhydrulidae are likely to represent life stages of other species of Staurozoa.45Fundacao de Amparo a Pesquisa do Estado de Sao Paulo (FAPESP)[2004/09961-4]Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq)[55.7333/2005-9]Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq)[490348/2006-8]Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq)[305735/2006-3]Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq)[474672/2007-7]National Science Foundation (NSF) [0531779

Lipkea ruspoliana Vogt, 1886 (Cnidaria: Staurozoa) in Portugal: the contribution of citizen science to range extension and taxonomic discussion of rare species

Citizen science online platforms are increasingly making important sources of biological information available at the click of a button, allowing the interaction of volunteers and scientists to report and identify the world's diversity. In this work, we combined the data available in citizen science platforms (iNaturalist and GelAvista) and the effort and collaboration of a diverse team of scuba-divers, scientists, and underwater photographers to report for the first time the presence of the stauromedusa Lipkea (Cnidaria: Staurozoa) in Portugal. Based on DNA (COI and 16S), we identified the species as Lipkearuspoliana. However, the marginal lappets of some Portuguese specimens are similar to those of Lipkeasturdzii, a species described based on a single specimen in 1893 and never reported again. These results suggest that L.sturdzii is a synonym of L.ruspoliana, although further taxon and habitat sampling for genetic studies and investigations of intraspecific morphological variation are necessary. In addition, we provided data on species ecology, reviewed the records of Staurozoa from Portugal, and mapped the world geographic distribution of Lipkea. Staurozoa is a cryptic group of cnidarians, and Lipkea seems to be a particularly rare genus. Citizen science has proved to be a valuable contribution to studies on the group, enabling biological discussions that otherwise would be more challenging.BIOMARES20212023; UID/MAR/04292/2018/2019; BiodivAMP Grant FA_06_2017_045; BiodivRestore ERA-NET Cofund (GA N°101003777); POCI-01-0247-FEDER-033889info:eu-repo/semantics/publishedVersio

Description of a common stauromedusa on the Pacific Coast of the United States and Canada, Haliclystus sanjuanensis new species (Cnidaria: Staurozoa)

Haliclystus “sanjuanensis” nomen nudum is the most common staurozoan on the west coast of the United States and Canada. This species was described in the M.S. Thesis by Gellermann (1926) and although that name has been in use nearly continuously since that time, no published description exists. Furthermore, the most popular operative name for this species has varied between several related species names over time, resulting in confusion. Herein, we provide a detailed description and synonymy of Haliclystus sanjuanensis n. sp., whose distribution is verified from Unalaska Island in the Aleutians (53.4° N, 166.8° W) in the northwest, to Santa Barbara County, California, just north of Point Conception (34.5° N, 120.5° W), in the south. Haliclystus sanjuanensis n. sp. is compared with the twelve other described species of Haliclystus and illustrations of both macroscopic and microscopic anatomy are provided. Haliclystus sanjuanensis n. sp. is unique among species of Haliclystus in the arrangement of the bright-white nematocyst spots in its calyx and the pattern of dark stripes running the length of the stalk and up the outside of the calyx

Putative scheme of the life cycle of <i>H. antarcticus</i>, including the “microhydrula” phase.

<p>The main life cycle was based on <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0010182#pone.0010182-Wietrzykowski1" target="_blank">[6]</a>, for <i>H. octoradiatus</i>. Stauropolyp stage and its ability to create frustules (white arrows) are hypothesized based on observations of <i>Stylocoronella </i><a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0010182#pone.0010182-Kikinger1" target="_blank">[7]</a>. Dotted gray arrows corresponding to the “microhydrula” stage, derived from this study. Figures modified from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0010182#pone.0010182-Wietrzykowski1" target="_blank">[6]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0010182#pone.0010182-Kikinger1" target="_blank">[7]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0010182#pone.0010182-Jarms1" target="_blank">[11]</a>.</p

Phylogenetic hypothesis (MP) based on mitochondrial 16S, nuclear ITS1+ITS2 and combined data.

<p>AN (King George Island, Antarctica), AK (Akkeshi, Hokkaido, Japan), CA (Franklin Point, California, USA), CH (Valdivia, Chile), MU (Muroran, Hokkaido, Japan), WA (San Juan Island, Washington, USA).“1” and “2” refers to the different haplotypes found for each species. Bootstrap indices under both MP and ML (respectively) at each node. Topologies are congruent under MP and ML analysis.</p

Comparisons between the <i>M. limopsicola</i> polyp and the <i>H. octoradiatus</i> settled planula.

<p><i>(A–C) different stages of M. limopsicola </i><a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0010182#pone.0010182-Jarms1" target="_blank">[11]</a>: A) newly settled “polyp”; B) closely attached “polyps”, with expansions provided with nematocysts; C) later stage, with a cauliflower-shaped head. <i>(D–E) process of frustulation observed in both species</i>: D) planula of <i>H. octoradiatus</i> producing lateral protuberances, which become frustules <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0010182#pone.0010182-Wietrzykowski1" target="_blank">[6]</a>; E) frustules <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0010182#pone.0010182-Jarms1" target="_blank">[11]</a>. <i>(F–G) possible correspondences of stages of both species</i>: F) a group of <i>H. octoradiatus</i> larvae, capturing a nauplius <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0010182#pone.0010182-Wietrzykowski1" target="_blank">[6]</a>; G) superior view of a settled planula of <i>H. octoradiatus</i> at an advanced stage, showing four lobes <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0010182#pone.0010182-Wietrzykowski2" target="_blank">[8]</a>.The hemispherical shape and the production of frustules (A, D, E) are similar in settled planulae of <i>H. octoradiatus</i> and “polyps” of <i>M. limopsicola</i>. The same gregarious behavior to feeding was observed in both species (B, F). At a more advanced stage, the larva of <i>H. octoradiatus</i> presents four lobes (G), that might be associated with the cauliflower structure seen in later stages of <i>M. limopsicola</i> (C), which possibly is an aggregation of more than one individual. Figures modified from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0010182#pone.0010182-Wietrzykowski1" target="_blank">[6]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0010182#pone.0010182-Wietrzykowski2" target="_blank">[8]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0010182#pone.0010182-Jarms1" target="_blank">[11]</a>.</p

Intraspecific variation for three species of Staurozoa in 16S, ITS1 and ITS2, highlighting the number of specimens, the number of haplotypes found and the range of divergence of each molecular marker; the linear distance refers to the distance between populations.

<p>Intraspecific variation for three species of Staurozoa in 16S, ITS1 and ITS2, highlighting the number of specimens, the number of haplotypes found and the range of divergence of each molecular marker; the linear distance refers to the distance between populations.</p

Map of Antarctica and southernmost part of Chile.

<p>Stars are records of <i>Haliclystus antarcticus</i>: South Georgia Island, Paulet Island, King George Island (Polish “Arctowski” Station, US “Copacabana” Refuge and Argentinean Antarctic Station “Jubany”) and Chile (Valdivia).</p

Living specimens of <i>Haliclystus antarcticus</i> in the field.

<p>A and B) Side view, attached to rock; C) Side view attached to rock and algae (Rhodophyta <i>Iridaea cordata</i>). Pictures from Morandini, AC. Scale = 1.2 cm.</p