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.
Zoobank: http://zoobank.org/urn:lsid:zoobank.org:pub:19B47378-B015-401D-B011-AD48AFE8F8DD
Introduction
Natural history collections play a crucial societal role as reservoirs of biological information, spanning multiple generations of researchers. The information derived from biological collections impacts a large range of disciplines and provides a solid baseline for evolutionary and biodiversity studies (Suarez & Tsutsui, 2004). Natural history museums generally follow the prime directive to archive and document the diversity of species and their distributions on Earth. In this context, they are an irreplaceable tool for the scientific community, and the value of such collections can only increase with time (Krell & Wheeler, 2014; Rocha et al., 2014; Connelly et al., 2024). Each specimen in a collection is unique and represents a “snapshot” of the environment, location and the taxonomy that was understood at the time it was collected and/or used in a description or analysis (Winker, 2004). Furthermore, with the advances in technology and development of scientific knowledge, museum specimens are increasingly recognized as a unique source of unexplored information (Winker, 2004; Bakker et al., 2020; Nakahama, 2021). In recent years museum collections have been gaining attention as an abundant, convenient, and often unique snapshots in time, source of genetic data (Card et al., 2021; Sampaio et al., 2023), and as a stock of undescribed diversity. They also provide baselines to study changes in the species composition of biota in areas that undergo anthropogenic stress (Hoeksema & Koh, 2009; Van der Meij et al., 2010; Hoeksema et al., 2012; Richards et al., 2014; Drew, 2017).
One of the taxonomic groups that has been demonstrated to have unknown diversity represented in natural history collections is the order Zoantharia Rafinesque, 1815 (Reimer et al., 2014). Zoantharians are benthic hexacorals most closely related to actiniarians (sea anemones) and include taxa from shallow waters to the deep sea. Zoantharians are also recognized as an important components of nearshore cnidarian communities, and as such have a long history of research (Donati, 1765; Ellis, 1768; Fujii & Reimer, 2013; Low, 2016; Montenegro et al., 2020). Valuable and ground-breaking discoveries on zoantharian ecology, systematics and diversity have often stemmed from collections targeting other organisms, with associated zoantharians becoming unintended “bycatch” of this collection (Swain & Wulff, 2007; Montenegro et al., 2020; Kise et al., 2022). This has been particularly true in Porifera (sponge) collections, with sponges often establishing symbiotic associations with at least four genera of zoantharians in two families; Epizoanthus Gray, 1867 in the family Epizoanthidae Delage & Hérouard, 1901 and Parazoanthus Haddon & Shackleton, 1891, Bergia Duchassaing de Fonbressin & Michelotti, 1860, and Umimayanthus Montenegro, Sinniger & Reimer, 2015 in the family Parazoanthidae Delage & Hérouard, 1901. By targeting Porifera collections, scientists have discovered species new to science, described emerging ecological and evolutionary patterns in this symbiosis, and made significant progress in the understanding of the systematics and phylogenetics of sponge-zoantharian associations (Swain & Wulff, 2007; Montenegro et al., 2020; Kise et al., 2022).
Within the family Parazoanthidae, the genus Umimayanthus has recently been one of the most actively studied groups. First erected by Montenegro et al. (2015), the genus originally consisted of four species; the type species, U. chanpuru Montenegro, Sinniger & Reimer, 2015, along with U. miyabi Montenegro, Sinniger & Reimer, 2015, U. nakama Montenegro, Sinniger & Reimer, 2015, and U. parasiticus (Duchassaing de Fonbressin & Michelotti, 1860). Subsequently, Fujii et al. (2021) described U. kanabou Fujii, dos Santos & Reimer, 2021 from Amami-Oshima Island in southern Japan. Thus, currently Umimayanthus includes five formally described valid species, but it is expected that the diversity of this genus remains largely underestimated. For instance, Sinniger & Häussermann (2009) reported an undescribed species of Umimayanthus from the Indian Ocean, and Montenegro et al. (2020) reported another unknown species from the Caribbean Sea. Furthermore, considering that the taxonomy of the genus Parazoanthus, a sister group to Umimayanthus, has undergone extensive revisions in recent years (Sinniger & Häussermann, 2009; Low & Reimer, 2011; Montenegro et al., 2015, 2016), it is likely that after re-examination, several additional Parazoanthus species reported from the South Pacific and Indo-Pacific oceans may be transferred into the genus Umimayanthus, such as P. lividum Cutress, 1971 and P. aruensis Pax, 1911.
In this study we present the results of a survey aiming to describe the hidden diversity of zoantharians within the Porifera collections of the Western Australia Museum (WAM), Naturalis Biodiversity Center (NBC), The Netherlands, and other institutions, which are listed below. Specimens were independently analysed by taxonomists with expertise in sponges and zoantharians using a multidisciplinary approach, including traditional morphological analyses, histological dissections, and DNA sequencing analyses. The results of our survey highlight the value of biological collections not only as archives of reference biological material for comparative analyses, but also as a repository of significant undescribed diversity yet to be revealed. In this study we discover and formally describe six new species within the genus Umimayanthus from voucher specimens in the Porifera collections of WAM and NBC. We also discuss the implications of these discoveries on the systematics and taxonomy of the genus Umimayanthus, provide a key for identification of Umimayanthus species, and give insights into possible future research directions on this genus.
Materials and methods
Abbreviations of museum collections
| MV | Museums Victoria Natural History Museum (Melbourne, Australia) |
| NBC | Naturalis Biodiversity Center (Leiden, The Netherlands) |
| NHMUK | Natural History Museum (London, UK) |
| RMNH | Rijksmuseum van Natuurlijke Historie (now at NBC) |
| SMF | Forschungsinstitut und Natur-Museum Senckenberg |
| WAM | Western Australian Museum (Perth, Australia) |
| ZMA | Zoological Museum of Amsterdam (now at NBC) |
Specimens
WAM specimens were collected by SCUBA diving, by trawl, or by epibenthic sled beyond diving depths, from several localities along the Western Australian coast between 2007–2018 and preserved in 70–100% ethanol. Additional preserved specimens were loaned from the MV and NHMUK. Specimens were also examined at NBC (RMNH and ZMA collections) in the Netherlands, and SMF in Germany.
DNA extraction, PCR, and sequencing
Total DNA was extracted using the Qiagen DNeasy Blood & Tissue Kit (Qiagen, Hilden, Germany) following the manufacturer’s instructions for all zoantharian specimens. PCR amplification was performed using a Taq PCR Master Mix Kit (Qiagen, Hilden, Germany) for partial sequences of cytochrome oxidase subunit I (COI-mtDNA) using primers LCO1490: 5’-GGT CAA CAA ATC ATA AAG ATA TTG G-3’ and HCO2198: 5’-TAA ACT TCA GGG TGA CCA AAA AAT CA-3’ (Folmer et al., 1994), and thermal cycling conditions of 35 cycles of 1 min at 94 °C, 1 min at 40 °C, and 90 sec at 72 °C, with a final elongation of 7 min at 72 °C (Reimer et al., 2007a); mitochondrial 16S ribosomal DNA (16S-rDNA) with primers 16SarmL: 5’-GGC CTC GAC TGT TTA CCA AA-3’ and 16SBmoH: 5’-CGA ACA GCC AAC CCT TGG-3’ (Sinniger et al., 2005; Fujii & Reimer, 2011), and thermal cycling conditions of 35 cycles of 1 min at 95 °C, 1 min at 52 °C, 2 min at 72 °C and followed by a 7 min extension at 72 °C (Fujii & Reimer, 2011); and the nuclear internal transcribed spacer region of ribosomal DNA (ITS-rDNA) using primers Zoan-f: 5’-CTT GAT CAT TTA GAG GGA GT-3’ and Zoan-r: 5’-CGG AGA TTT CAA ATT TGA GCT-3’, and thermal cycling conditions of 35 cycles of 1 min at 94 °C, 1 min at 50 °C, and 2 min at 72 °C, with a final elongation of 10 min at 72 °C (Reimer et al., 2007b). Successful amplifications were confirmed by 2% agarose gel electrophoresis, cleaned by a mix of ExoI and SAP (cat. 2650A and 2660A, TaKaRa, Japan), and sent for external sequencing in both directions to Fasmac, Kanagawa, Japan.
Phylogenetic analyses
The nucleotide sequences were initially aligned using Geneious Prime 2024.04 (https://www.geneious.com) with the algorithm “Global alignment with free end gaps” and default settings, thereafter sequences were manually curated and flaking positions were trimmed. 127 additional sequences were downloaded from GenBank following Montenegro et al. (2016, 2020) and included in this study (table 1). All sequences were then aligned using the Geneious plugin MAFFT (Katoh & Standley, 2013) with the algorithm L-INS-I. Resultant alignments were trimmed, realigned using the plugin MUSCLE (Edgar, 2004) and manually checked.
Maximum likelihood (ML) and Bayesian posterior probability (BPP) phylogenetic hypothesis were estimated using raxml-ng v0.9.0 (Kozlov et al., 2019), and Mr. Bayes v3.2.6 (Ronquist & Huelsenbeck, 2003), respectively. Phylogeny reconstructions were performed for the concatenated alignment of the regions ITS-rDNA, 16S-rDNA and COI-mtDNA, and with Epizoanthus arenaceus as the outgroup. Epizoanthidae it is in a clade sister to Parazoanthidae within Macrocnemina Haddon & Shackleton, 1891 (Sinniger et al., 2005; Reimer et al., 2019), thus giving sufficient resolution to establish if all specimens’ sequences truly belong within genus Umimayanthus, confirming that the genus remains a cohesive taxonomic and evolutionary unit (monophyly).
Newly generated and downloaded sequences used in the phylogenetic reconstructions, along with their corresponding GenBank accession numbers.
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
For each of the molecular markers, the best-fitting model was selected using ModelTest-NG v0.2 (Darriba et al., 2020) for ML reconstructions and MrModeltest2 (Nylander, 2004) for BBP. In both cases the lowest AIC score was used as the selecting criteria. The best-fitting models for ML were TPM3uf+I+G4 for ITS-rDNA, TrN+G4 for 16S-rDNA, and TrN+I for COI- mtDNA. The best-fitting models for BPP were HKY+I+G for ITS-rDNA, SMY+G for 16S-rDNA, and HKY+I for COI-mtDNA.
ML phylogenies were estimated using a 100 initial parsimony trees, 1000 bootstraps, and the evolutionary models selected by ModelTest-NG; distinct substitution rates across partitions, automated optimization of model parameters and branch lengths were allowed. BPP trees were estimated following the models and parameters as indicated by MrModeltest2, 4 MCMC heated chains were run for 10,000,000 generations with a temperature for the heated chain of 0.2. Chains were sampled every 200 generations. Burn-in length was set to 25% at which point the average standard deviation of split frequency (ASDOSF) was steadily below 0.01.
Specimen identification
All zoantharian specimens were identified by JM, HK or JDR, while associated sponges from MV and WAM were identified by JF. ZMA sponges were identified by B. Alvarez, N.J. de Voogd and R.W.M. van Soest (ZMA. POR.9139, ZMA.POR.20704) in previous publications (Alvarez et al., 2016). NHMUK specimens were identified by E. Hentschel (NHMUK 1931.8.4.57) and H. John Carter (Carter, 1882) (NHMUK 1887.5.21.1865), and reexamined by J. Hooper and JF. Sponge subsamples were cut at right angles to the surface and processed using a graded ethanol dehydration and histolene clearing procedure, sectioned at right angles to the sponge surface either with a Leitz slide microtome or hand cut with a razor blade, and mounted on glass slides with EZ-Mount mountant (Fisher Scientific) to determine the skeletal arrangement (Fromont et al., 2011). Spicule preparations were made with nitric acid or bleach, washed in distilled water, mounted on glass slides and examined with an Olympus BX50 microscope. A calibrated micrometer eyepiece was used to measure skeletal details and spicule sizes (Fromont et al., 2011). Skeletal layout and spicule complements were examined and compared with relevant sponge literature to identify genera and species. (Hooper, 1984,1991, 1996; Van Soest et al., 2012; Alvarez et al., 2016; de Voogd et al., 2023).
Zoantharian specimens were preliminarily grouped based on molecular similarities across the three DNA markers. For all species, where possible, three polyps were randomly selected to measure diameter and height, and the presence or absence of coenenchyma connecting polyps was recorded. Cnidae analyses were performed; one polyp was dissected per species group and undischarged nematocysts from tentacles, column, actinopharynx, and mesenterial filaments were counted and measured under a Nikon Eclipse80i stereomicroscope (Nikon, Tokyo, Japan). Cnidae sizes were measured using ImageJ ver. 1.45s (Rasband, 2012), and classified according to England (1991) and Ryland & Lancaster (2004), to the exception of basitrichs and microbasic mastigophores, which were treated as a single type following Kise et al. (2019). Thus, six cnidae categories were quantified; spirocysts, bastrichs & microbasic b-mastigophores, holotrichs-(L), holotrichs-(M), holotrichs- (S), and microbasic p-mastigophores; additionally special microbasic b-mastigophores were also counted when present.
Serial sections from preserved specimens were also examined for internal morphology. Whole polyps of the specimens were embedded in paraplast after decalcification with Morse solution for 48 h (1:1 vol; 20% citric acid: 50% formic acid) and desilication with 20% hydrofluoric acid for 18–24 h. 10–15 mm thick serial sections were made with a microtome (LEICA RM2145; Leica, Germany) and stained with haematoxylin and eosin. Classification of marginal muscle shapes followed Swain et al. (2015). However serial sectioning was not successful and therefore the internal morphology of the polyps was characterized by direct observation using a dissection stereomicroscope.
Results
Phylogenetic analyses
In total, 34 zoantharian specimens were analysed in this study; 26 from WAM, three from MV, two from NHMUK, two from NBC, and one from SMF (table 2). The specimens were collected from 26 different localities in Australia and Indonesia (table 2, fig. 1). The final concatenated alignment included data from 26 out of the 34 analysed specimens, and included 191 sequences, out of which 64 were newly generated in this study: 23 sequences for ITS-rDNA, 17 sequences for 16S-rDNA, and 24 sequences for COI-mtDNA. The total length of the final concatenated alignments was 1843 bp; consisting of 864 bp for ITS-rDNA, 533 bp of 16S-rDNA, and 446 bp of COI-mtDNA (supplementary data S1–S4).
Collection location for all samples analyzed. Numbers indicate unique locations. Details in table 2 (*) indicate approximated locations
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
Samples and collection metadata for all samples analysed in this study
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
The genus Umimayanthus was supported as a member of the family Parazoanthidae, and was presented as a moderately supported monophyly in ML analyses, and well supported in BPP with a >0.98 posterior probability. All specimens analysed in this study were included within the Umimayanthus clade, and grouped into three major clades; designated as clades I, II and III in fig. 2.
Phylogenetic reconstruction based on the concatenated alignments of the ITS-rDNA, 16S-rDNA, and COI-mtDNA. Values at branches indicate ML bootstrap support ≥ 50% and black circles at nodes represent BPP ≥ 0.95. Numbers in brackets correspond to the unique number per taxonomic unit in table 1.
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
Clade III was sister to all other species in the genus Umimayanthus while the phylogenetic positions of Clades I and II were less certain. Nonetheless, each of these three clades was well supported in both ML analyses, with bootstrap values of 76–89% for ML and posterior probabilities of ≥0.95 for BPP for Clades II and III. The lack of support from BPP analyses for Clade I may stem from multiple individuals having missing ITS-rDNA or 16S-rDNA sequence data.
Clade III included three closely related clades corresponding to Umimayanthus discolor sp. nov., Umimayanthus lynherensis sp. nov., and Umimayanthus raksasa sp. nov. The clades of U. discolor sp. nov. and U. lynherensis sp. nov. were strongly supported as sister species, while U. raksasa sp. nov. was found to be basal within Clade III. The relationships between these three sibling species were supported by bootstrap value of 76% for ML and a posterior probability of ≥ 0.95 for BPP in phylogenetic analyses. Interestingly, U. discolor sp. nov. was found in association with two distantly related sponge species in families Microcionidae (specimens WAM Z88616 and WAM Z88626) and Raspiliidae (specimens NHMUK-1887.5.21.1865 and NHMUK-1931.8.4.57), while each of its sibling species seems to be restricted to a single family and genus of host sponges.
The monophyly formed by Clade I was strongly supported in ML analyses with a bootstrap value of 89%, however support from BPP was lacking. While minor subclades were present within Clade I their support was weak in ML and not existent in BPP analyses. Clade I was formed by multiple specimens of Umimayanthus cf. aruensis.
In a similar fashion, Clade II was well supported in ML analyses with a bootstrap value of 89% and posterior probabilities of ≥ 0.95 for BPP in the phylogenetic analysis. However, in contrast to Clade I, Clade II internal subclades were well supported with values ranging from 65% to 89%, and posterior probabilities ≥ 0.95 for BPP for some of these clades. Of these subclades, the most supported monophyly was formed by three specimens of Umimayanthus mirnangga sp. nov., followed by a clade formed by four specimens of Umimayanthus wunanggu sp. nov., and finally a single specimen of Umimayanthus jebarra sp. nov. Specimens in this complex were all hosted by sponges in the genera Endectyon and/or Ectyoplasia in the family Raspaillidae, supporting the phylogenetic hypothesis of close evolutionary relatedness among these three species.
Systematics
Phylum Cnidaria Hatschek, 1888
Subphylum Anthozoa Ehrenberg, 1831
Class Hexacorallia Haeckel, 1896
Order Zoantharia Rafinesque, 1815
Family Parazoanthidae Delage & Hérouard, 1901
Genus Umimayanthus Montenegro, Sinniger and Reimer 2015
urn:lsid:zoobank.org:act:A7C6F356-9128-41EA-B108-271EC70B82F
The genus Umimayanthus was initially diagnosed by a unique insertion of 9 bp in length and one 14 bp deletion in the mt 16S-rDNA region. However, relying on deletions, or alignment gaps, as a diagnostic character can be problematic when analysing relationships between distantly related taxa. Therefore, here we revise the generic diagnosis and propose to use a combination of unique insertions and substitutions across the ITS-rDNA and 16S-rDNA molecular markers as follows.
The genus Umimayanthus can be distinguished from all other sponge-associated zoantharians by multiple conservative positions across the ITS-rDNA region in our concatenated alignment, as follows: two conservative and unique substitutions in base pair positions 22–23 bp as “TG”, and multiple unique combinations of substitutions between positions 20–24 bp as “GTTGT”, 52–54 bp as “GAC” and 663–664 bp as “CA”. Furthermore, between positions 1351–1354 bp in the 16S-rDNA region of our alignment a highly conservative insertion of four base pairs, “AAGG”, was also found to be unique to genus Umimayanthus (fig. 3).
Summary chart for the alignments showing relevant nucleotide positions for the molecular diagnosis of genus Umimayanthus. Positions in green are unique to genus Umimayanthus. Positions in grey indicate regions with a unique combination of nucleotides for Umimayanthus.
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
Umimayanthus cf. aruensis (Pax, 1911)
urn:lsid:zoobank.org:act:9310A989-B76E-4096-8BB5-09E348935394
Here we transfer Parazoanthus aruensis to the genus Umimayanthus based on its general morphology and position of the sphincter muscle, as well as corresponding geographical location, and gross external morphology of the host sponge. P. aruensis was originally described by Pax (1911) as a zoantharian “that lives in sponges and forming loose colonies. Polyps 8 mm high, 5 mm wide, connected to each other by narrow flat stolon. Tissue walls incrusted with sponge spicules, 18 septs, sphincter muscle diffuse, endodermal and poorly developed”. The holotype specimen of P. aruensis, SMF museum, GUID = SeSam 42611, Catalog #86, had polyps of 4.15 mm ± 0.402 mm (
Specimens of Umimayanthus cf. aruensis and holotype of Umimayanthus aruensis; (A) WAM Z88819 and (B) WAM Z88820 specimens of U. cf. aruensis. (C) SeSam 42611 Cat.86 picture of U. aruensis holotype taken by Saskia Dimter, and (D) in situ image of U. cf. aruensis. Scale bars: 5 mm
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
The specimens newly analysed in this study that are attributable to U. cf. aruensis have polyps that are on average 2.66 mm ± 0.89 mm (
The U. cf. aruensis colonies were found to be primarily formed by interconnected polyp chains extending over the surface of the host sponge in a reticulated pattern; exceptionally the polyps were found to be solitary or arranged in groups of two or three. The coenenchyma is clearly visible over the sponge surface and firmly connects multiple polyps by the stolon. Polyps preserved in ethanol are white or cream in color. Capitulary ridges not visible. Tentacles approximately up to 24 in number, in two rows. Preserved tentacles light brown in coloration. Capitulum and scapus heavily encrusted by various particles comprised of sand and silica (spicules of host sponges). The sphincter muscle located in the endoderm. Mesenterial arrangement macrocnemic (fifth mesenteries from dorsal directive complete). Mesenteries approximately up to 24 in number. Ectoderm and mesoglea of capitulum and scapus heavily encrusted by various sand and silica particles. Single siphonoglyph.
In synthesis, U. aruensis and U. cf. aruensis strongly resemble each other in multiple aspects. Both U. aruensis and U. cf. aruensis present colonies form by chains of polyps extending over the surface of the host sponge in a reticulated manner, with a clearly visible coenenchyma. Both were collected from the same region of the Indo-Pacific Ocean and are associated to host sponges of arborescent/branching shapes. Both have sphincter muscle located in the endoderm, and tissue walls incrusted with sponge spicules. However, differences were observed regarding the dimensions of the polyps, U. aruensis was 4.15 mm ± 0.402 mm in diameter and 4.72 mm ± 0.89 mm in height, while for U. cf. aruensis polyps were 2.66 mm ± 0.89 mm in diameter and 0.79 mm ± 0.5 mm in height. It is important to note that differences in height could be related to the level of retraction of the specimens in preservation. Therefore, we consider these facts, along with the fact that no Parazoanthus is known from this region of the Indo-Pacific Ocean, sufficient to support that U. aruensis should be transferred into Umimayanthus. However, given the evident species diversity of Umimayanthus in the region as illuminated by the current work, we feel the evidence is not strong enough to be fully ascertain that our relevant specimens represent U. aruensis, and conservatively we therefore have decided to use the “confer” denomination (cf.) for these specimen’s identification (= U. cf. aruensis).
Molecular characterization. At the molecular level, U. cf. aruensis can be distinguished from other species in Umimayanthus using multiple unique nucleotide substitutions across the ITS-rDNA region as follows: an “A” in positions 49 bp, 378 bp, 387 bp and 441 bp; a “G” in positions 97 bp, 338 bp, 340 bp, 359 bp and 390 bp; a “C” at 113 bp and 128 bp, and “T” at 373 bp. Additionally, unique combinations of nucleotides and deletions were found from 128 bp to 341 bp; and 408 bp to 437 bp (fig. 5).
Summary chart of the alignments showing nucleotide positions and deletions characteristics to U. cf. aruensis. across the ITS-rDNA region. Positions in green are unique to U. cf. aruensis sp. nov. in genus Umimayanthus. Positions in grey indicate regions with a unique combination of nucleotides insertion and deletions for U. cf. aruensis
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
Cnidae. All cnidae categories were found, but they were differentially distributed across tissues. Spirocysts were numerous and only found in the tentacles, with bastrichs and microbasic b-mastigophores also present. The column presented few cnidae and exclusively (M) and (L) type holotrichs. The pharynx had holotrichs (M) and microbasic b-mastigophores. Filaments presented the largest variety of cnidae with special microbasic b-mastigophores, bastrichs and microbasic b-mastigophores, and microbasic p-mastigophores. For details on sizes, lengths, and widths of each cnidocyte type see table 3 and fig. 6.
Diversity of cnidae found in U. cf. aruensis across tissues in specimen WAM Z88819. (S) spriocysts, (O) basitrichs and microbasic b-mastigophores, (HM) holotrich medium, (HL) holotrich large, (PM) microbasic p-mastigophores and special (SBM) microbasic b-mastigophores
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
Results for the cnidocyte analyses for Umimayanthus cf. aruensis, holotype specimen WAM Z88819
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
Material examined. WAM Z88819, loc. 16 (−15.376306 °S, 124.139547 °E), Camden Sound, Western Australia, 39 m depth, March 21, 2015 by J. Fromont & L. Kirkendale, WAM Z88820, loc. 6 (−21.596111 °S, 115.060556 °E), near Wheatstone, Onslow, Western Australia, 12.3 m depth, July 7, 2015 by J. Fromont & M.A. Wahab, WAM Z88840, loc. 5 (−21.606944 °S, 114.933056 °E), Wheatstone, Onslow, Western Australia, 12.2 m depth, March 29, 2013 by J. Fromont & C.L. Schoenberg, WAM Z88847, loc. 11 (−20.474722 °S, 116.307222 °E), Bare Rock, Pilbara Shelf, Western Australia, 37 m depth, June 25, 2013 by E. Morello, G. Fry, M. Miller, D. Thomson & D. Bearham, WAM Z88841, loc. 7 (−21.4 °S, 115.089722 °E), Sultan Reef, Pilbara Shelf, Western Australia, 18 m depth, June 13, 2013 by E. Morello, G. Fry, M. Miller, D. Thomson & D. Bearham, WAM Z88839, loc. 5 (−21.606944 °S, 114.933056 °E), Wheatstone, Onslow, Western Australia, 12.2 m depth, March 29, 2013 by J. Fromont & C.L. Schoenberg, WAM Z88867, loc. 8 (−21.312222 °S, 115.369167 °E), West Reef, Pilbara Shelf, Western Australia, 14 m depth, June 14, 2013 by E. Morello, G. Fry, M. Miller, D. Thomson & D. Bearham, WAM Z88837, loc. 6 (−21.596111 °S, 115.060556 °E), Wheatstone, Onslow, Western Australia, 12.2 m depth on March 26, 2013 by J. Fromont & E. Buettner, WAM Z88870, loc. 10 (−20.499167 °S, 115.589722 °E), Ah Chong I., Montebello Is., Western Australia, 14.5 m depth on April 16, 2015 by A.M. Hosie & A. Hara, WAM Z88865, loc. 9 (−20.978333 °S, 115.552222 °E), West Reef , Pilbara Shelf, Western Australia, 14 m depth, June 14, 2013 by E. Morello, G. Fry, M. Miller, D. Thomson & D. Bearham, WAM Z88861, loc. 9 (-20.978333 °S, 115.552222 °E), The Man in the Boat, Pilbara Shelf, Western Australia, 18 m depth, June 21, 2013 by E. Morello, G. Fry, M. Miller, D. Thomson & D. Bearham, WAM Z88863, loc. 7 (−21.4 °S, 115.089722 °E), Sultan Reef, Pilbara Shelf, Western Australia, 18 m depth, June 13, 2013 by E. Morello, G. Fry, M. Miller, D. Thomson & D. Bearham, and WAM Z88853, loc. 25, (−21.080278 °S, 115.18 °E), Poivre Reef, Pilbara Shelf, Western Australia, 21 m depth, June 16, 2013 by E. Morello, G. Fry, M. Miller, D. Thomson & D. Bearham.
Associated host. Umimayanthus cf. aruensis was found to be host specific, only associated with the host sponge Trikentrion flabelliforme (family Raspailiidae). Interestingly, the paralectotype of T. flabelliforme (NHMUK 1931.8.4.57, from Aru Islands, Indonesia) and another historical specimen (NHMUK 1887.5.21.1865, precise location unknown, southwest Western Australia) were found associated with Umimayanthus discolor sp. nov., described below, rather than with U. cf. aruensis.
Remarks. Specimen WAM Z88865 has an abnormally small polyp diameter and height for U. cf. aruensis, 0.9 mm in diameter and 0.1 mm in height. It is worth noting that only two polyps were available for examination from this specimen. Nonetheless, molecular evidence clearly determined specimen WAM Z88865 to belong to U. cf. aruensis (fig. 5).
U. cf. aruensis has polyp sizes similar to those of U. kanabou as described in Fujii et al. (2021), however U. kanabou has been reported to be exclusively in association with gorgonians while U. cf. aruensis exclusively associates with sponges, and appears to be specific to Trikentrion flabelliforme.
Specimen NHMUK 1887.5.21.1865 was referred to Trikentrion laeve Carter, 1879 by Carter (1882), being a species described from South Africa. Although the specimen number was not given in the publication, Carter’s (1899) description is of a fan-shaped sponge with an anastomosing zoantharian over its surface. Hooper (1991) used Carter’s name for the specimen NHMUK 1887.5.21.1865, namely Trikentrion laeve var. flabelliforme, but Van Soest et al. (2012) noted that the specimen was never formerly described. Re-examination of a fragment of the specimen by J.N.A. Hooper and JF confirmed that this specimen is T. flabelliforme based on the spicule complement and skeletal characters. Therefore, the locality of this specimen as southwest Western Australia is potentially incorrect as no specimens of T. flabelliforme have since been collected south of Red Bluff near Ningaloo (−24.043611 °S, 113.026944 °E) in Western Australia.
Hooper (1991) redescribed T. flabelliforme and commented on the heavy infestation of a white zoantharian that regularly occurs on this species. He noted it was previously referred to as Bergia in Carter (1882). Trikentrion flabelliforme is common in shallow subtidal tropical waters and has been reported from the Arafura Sea (type locality), and Northern and Western Australia.
Umimayanthus mirnangga sp. nov. Montenegro, Kise & Reimer
urn:lsid:zoobank.org:act:50E0D7DC- D383-45EE-B921-1140F1E29347
Etymology. The specific epithet “mirnangga” is derived from the phoneme used to refer to a young single woman in the Wunambal language. This in reference to the fact that the colonies of U. mirnangga sp. nov. are exclusively composed of solitary polyps. “mɨrnangga binya” n., B-class young woman. Syn: munangga. See Bengmoro et al. (1971) and Boona (2022).
Material examined. Type locality: Maret Is. [loc. 19], Western Australia, -14.35445 °S, 124.9488 °E. Holotype: WAM Z88824 (−14.35445 °S, 124.9488 °E, loc. 19, Maret Is., Western Australia, 61 m depth, December 16, 2015 by O.A. Gomez & J.A. Ritchie). Paratype: WAM Z88823 (−14.424417 °S, 125.040933 °E, loc. 17, Maret Is., Western Australia, 55 m depth, December 9, 2015 by O.A. Gomez & J.A. Ritchie).
Other material. Other examined specimens belong to the Western Australian Museum; WAM Z88817 (−15.446442 °S, 124.083022 °E, loc. 15, Camden Sound, Western Australia, 61 m depth, March 20, 2015 by J. Fromont & L. Kirkendale).
Type specimens of Umimayanthus mirnangga sp. nov; (A) WAM Z88824 (holotype), (B) WAM Z88823 (paratype). Scale bars: 5 mm
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
Diagnosis. U. mirnangga sp. nov. can be distinguished from other species in the genus Umimayanthus by having colonies exclusively formed of solitary polyps, and by having symbiotic associations with sponges in genus Endectyon Topsent, 1920 and Ectyoplasia Topsent, 1931; current known hosts are Endectyon (Endectyon) fruticosum (Dendy, 1887) and Ectyoplasia vannus Hooper, 1991. Additionally, U. mirnangga sp. nov. can be differentiated from all other species in genus Umimayanthus by three unique nucleotide substitutions across the ITS-rDNA region as follows: “C” in positions 88 bp and 418 bp, and “G” at position 438 bp (fig. 8).
Summary chart of the alignments showing nucleotide positions characteristics to U. mirnangga sp. nov. across the ITS-rDNA and COI-mtDNA region. Positions in green are unique to U. mirnangga sp. nov. in genus Umimayanthus. Positions in grey are characteristic but not unique to U. mirnangga sp. nov
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
Description. Size. Preserved polyps were on average 2.41 mm ± 0.23 mm (
Morphology. The type specimens are associated with Ectyoplasia vannus. The species has solitary polyps spread all over the surface of the sponges. The inter-polyp distance is variable, with a minimum distance of 2.35 mm between polyps, and an average of 4.27 mm ± 0.91 mm (
Distribution. All specimens analysed were collected along the west coast of Australia. Camden Sound [loc. 15] and Maret Is. [loc. 17, 19] (fig. 1). Specimens were found at depths of 55–61 m.
Associated host. Umimayanthus mirnangga sp. nov. was found associated with two different sponge species, Ectyoplasia vannus and Endectyon (Endectyon) fruticosum, both in the family Raspailiidae.
Remarks. Umimayanthus mirnangga sp. nov., U. wunanggu sp. nov., and U. jebarra sp. nov. are sibling species based on our phylogenetic analyses. Key diagnostic molecular and morphological characters, including the general external morphology of the colonies and the height of the polyps, as well as the different host species, clearly separate these three species from each other.
Out of all the species in Umimayanthus the closest resemblances can be found between the sibling species U. wunanggu sp. nov., and U. jebarra sp. nov., which have similar polyp diameters as U. mirnangga sp. nov. Nonetheless, the heights of polyps in U. mirnangga sp. nov. are 2.41 mm ± 0.23 mm, twice as large as U. wunanggu sp. nov. (0.92 mm ± 0.36 mm), and smaller than U. jebarra sp. nov. (3.09 mm ± 0.63 mm). Furthermore, the morphological differences between U. mirnangga sp. nov. and U. wunanggu sp. nov. are present even though both species were found to establish associations with the same sponge species, Endectyon (Endectyon) fruticosum. Out of the three sibling species, U. mirnangga sp. nov. is the only species composed exclusively of solitary polyps.
The type locality of Ectyoplasia vannus, the host sponge of Umimayanthus mirnangga sp. nov., is Port Essington in the Northern Territory, Australia, and this sponge species has otherwise only been reported from other areas in the Northern Territory and tropical Western Australia.
Umimayanthus jebarra sp. nov. Montenegro, Kise & Reimer
urn:lsid:zoobank.org:act:557A4CDC-8805-4626-854E-C591DB88598C
Etymology. The specific epithet “jebarra” is derived from the phoneme used to refer to the emu in Wunambal language. This in reference to the elongated shape of the polyps in U. jebarra sp. nov., which resemble the neck of an emu. As well, the name can act as a memorial to all the emus killed during the Great Emu Wars of 1932 in Western Australia. “jebarra anya” n., A-class. emu. Dromaius novaehollandiae. Syn: garnanganyja; jeebarra. See Mangglamarra (1991) and Karadada et al. (2011).
Material examined. Type locality: Eclipse Is. [loc. 21], −13.493782 °S, 125.851633 °E. Holotype: WAM Z88825 (−13.493782 °S, 125.851633 °E, loc. 21, Eclipse Is., Western Australia, 41 m depth, March 2, 2016 by O.A. Gomez & J.A. Ritchie). No other material was available.
Holotype of Umimayanthus jebarra sp. nov.; (A) WAM Z88825 (holotype). Scale bars: 5 mm
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
Diagnosis. U. jebarra sp. nov. can be distinguished from other species in the genus Umimayanthus by having colonies with polyps connected to each other in a linear fashion, and establishing symbiotic associations with sponges in the genus Endectyon. Additionally, three unique substitutions in the ITS-rDNA region differentiate U. jebarra sp. nov. from all other species in the genus Umimayanthus, as follows: “G” in position 367 bp, “C” in position 417 bp and “A” in position 760 bp. Furthermore, a unique combination of nucleotides can be found between positions 417 bp to 425 bp in the ITS-rDNA region (fig. 10).
Summary chart of the alignments showing nucleotide positions characteristics to U. jebarra sp. nov. across the ITS-rDNA region. Positions in green are unique to U. jebarra sp. nov. in genus Umimayanthus. Positions in grey are characteristic but not unique to U. jebarra sp. nov
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
Description. Size. Preserved polyps were on average 2.34 mm ± 0.02 mm (
Morphology. The holotype specimen is associated with a sponge in the genus Endectyon. The colony is formed by a chain of polyps that branches and extends linearly over the surface of the sponge. The coenenchyma connecting the polyps is thin but clearly visible. All polyps were clearly spread over the sponge matrix and the coenenchyma tissue by 3.09 mm ± 0.63 mm on average. Capitulary ridges were visible, and approximately 16 in number. Polyps preserved in ethanol were orange in colour. No cnidae or internal morphological data are available for this species due to the poor condition of the preserved specimen.
Distribution. The specimen analysed was collected along the west coast of Australia. Eclipse Is. [loc. 21] (fig. 1). The specimen was found at a depth of 41 m.
Associated host. Umimayanthus jebarra sp. nov. was found in association with a sponge in the genus Endectyon.
Remarks. U. mirnangga sp. nov., U. wunanggu sp. nov., and U. jebarra sp. nov. are closely related sibling species. Nonetheless, key diagnostic molecular and morphological characters, including the external morphology of the colonies and the height of the polyps, as well as the different host species, clearly separate these three species from each other.
The sponge specimen voucher WAM Z94791 could only be identified as Endectyon sp. The acanthostyles are “cladotylote-like”. For now, we have retained this specimen in Endectyon but this interesting specimen requires further study for a species-level identification.
While no other species in the genus Umimayanthus quite resemble U. jebarra sp. nov., the closest similarity is to one of the specimens WAM Z88817 of U. mirnangga sp. nov. associated with the sponge Endectyon (Endectyon) fruticosum (sponge voucher WAM Z87200). However, the polyps of U. mirnangga sp. nov. are solitary, while the polyps of U. jebarra sp. nov. are clearly connected to each other in a linear fashion by a coenenchyma, which is not as well developed as in U. cf. aruensis or in U. discolor sp. nov.
Umimayanthus wunanggu sp. nov. Montenegro, Kise & Reimer
urn:lsid:zoobank.org:act:E0D67C58-5506-4700-9F44-98C4789A27F7
Etymology. The specific epithet “wunanggu” is derived from the phoneme used to refer to the hill white gum tree in Wunambal language. This in reference to U. wunanggu sp. nov. forming colonies of white polyps connected by a thin coenenchyma that extends on a linear branching pattern over the sponge surface. “wunanggu winya” n., W-class. /wunaŋgu/. hill white gum, tropical red box, Eucalyptus brachyandra von Mueller, 1859. See Capell (1941) and Karadada (2011).
Material examined. Type locality: Eclipse Is. [loc. 20], −13.794197 °S, 126.11881 °E, Western Australia (fig. 1).
Holotype. WAM Z88826 (−13.794197 °S, 126.11881 °E, loc. 20, Eclipse Is., Western Australia, 59 m depth, March 7, 2016 by O.A. Gomez & J.A. Ritchie). Paratype 1: WAM Z88822 (−14.401883 °S, 124.944067 °E, loc. 18, Maret Is. Western Australia, 50 m depth, December 8, 2015 by O.A. Gomez & J.A. Ritchie). Paratype 2: WAM Z88818 (−15.446442 °S, 124.083022 °E, loc. 15, Camden Sound, Western Australia, 61 m depth, March 20, 2015 by J. Fromont & L. Kirkendale).
Other material. One additional examined specimen belonging to the Western Australian Museum; WAM Z88827 (−15.6233 °S, 121.972233 °E, loc. 13, Lynher Bank, Western Australia, 61 m depth, October 28, 2016 by J. Fromont & J.A. Ritchie).
Specimens of Umimayanthus wunanggu sp. nov.; (A) WAM Z88826 (holotype), (B) WAM Z88822 (paratype), (C) WAM Z88818 (paratype), and (D) WAM Z88827. Scale bars: 5 mm
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
Diagnosis. U. wunanggu sp. nov. can be distinguished from all other sponge-associated zoantharians by its symbiotic associations with sponges in the genus Endectyon, and forming colonies of polyps connected by a thin coenenchyma that extends linearly over the host sponge surface; currently known to establish associations with Endectyon (Endectyon) fruticosum and Endectyon (Endectyon) thurstoni (Dendy, 1887). Additionally, unique substitutions across the ITS-rDNA region set this species apart from other species in the genus Umimayanthus, as follows: “C” in positions 360 bp, 421 bp, and 426 bp; “TTAC” from positions 423–426 bp; “A” in position 704 bp; and a unique combination of nucleotides, “AA” between position 704–705 bp, and “CG” in 816–817 bp (fig. 12).
Summary chart of the alignments showing nucleotide positions characteristics to U. wunanggu sp. nov. across the ITS-rDNA and 16S-rDNA region. Positions in green are unique to U. wunanggu sp. nov. in genus Umimayanthus. Positions in grey are characteristic but not unique to U. wunanggu sp. nov
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
Description. Size: Preserved polyps are on average 2.4 mm ± 0.22 mm (
Morphology. The holotype specimen is associated with Endectyon (Endectyon) thurstoni. The polyp diameter of U. wunanggu sp. nov. is remarkably constant, 2.2~2.8 mm across all analysed specimens. All specimens were colonies with polyps extended well over the sponge surface. Most specimens had polyps connected by a well-developed coenenchyma, forming chains of polyps in branches rather than in a reticulate pattern, different from U. cf. aruensis. Capitulary ridges were visible, 14–18 in number. Tentacles were approximately up to 36 in number. Preserved tentacles were light brown in coloration. Capitulum and scapus were heavily encrusted by various particles of sand and silica (= spicules of host sponges). Polyps preserved in ethanol were white or cream in color.
Cnidae. Except for holotrich (S), all categories of cnidae were found. The cnidae composition across tentacles and pharynx was similar and made up of spirocysts, holotrichs (L) and (M), bastrichs and microbasic b-mastigophores. The column had the lowest diversity of cnidae with only holotrichs (L) and (M). In contrast the mesenterial filaments had the largest diversity of cnidae, including holotrichs (L) and (M), microbasic p-mastigophores, bastrichs and microbasic b-mastigophores and special microbasic b-mastigophores. For details on sizes, lengths, and widths of each cnidae type, see table 4 and fig. 13.
Diversity of cnidae found in Umimayanthus wunanggu sp. nov. across tissues in specimen WAM Z88826. (S) spriocysts, (O) basitrichs and microbasic b-mastigophores, (HM) holotrich medium, (HL) holotrich large, (PM) microbasic p-mastigophores and (SBM) special microbasic b-mastigophores
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
Results for the cnidocyte analyses for Umimayanthus wunanggu sp. nov., holotype specimen WAM Z88826
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
Internal morphology. Sphincter muscle was located in the endoderm. Mesenterial arrangement was macrocnemic. Mesenteries were approximately up to 28 in number. Ectoderm and mesoglea of capitulum and scapus were heavily encrusted by various sand and silica particles. Single siphonoglyph.
Distribution. All specimens analysed were collected along the west coast of Western Australia. Lynher Bank [loc. 13], Camden Sound [Loc. 15], Maret Is. [loc. 18] and Eclipse Is. [loc. 20] (fig. 1). Specimens were found at depths of 50–61 m.
Associated host. Umimayanthus wunanggu sp. nov. was associated with four sponges in two species in the family Raspailiidae Nardo, 1833, Endectyon (Endectyon) thurstoni (n = 3) and Endectyon (Endectyon) fruticosum (n = 1). The type locality of Endectyon (Endectyon) thurstoni is India, and this species has also been reported from the Arabian Sea and Western Australia. The type locality of Endectyon (Endectyon) fruticosum is also India and it has additionally been reported from the Aru Islands, Indonesia, the south Andaman Sea, Thailand (Hooper, 1991), and now from the Kimberley region, Western Australia. Based on this wide host sponge distribution, it may be that the distribution of U. wunanggu sp. nov. is wider than currently known.
Remarks. Umimayanthus wunanggu sp. nov., Umimayanthus mirnangga sp. nov. and Umimayanthus jebarra sp. nov. are sibling species that were shown to be closely related in our phylogenetic analyses. Nonetheless, key diagnostic molecular and morphological characters, including the general external morphology of the colonies and the height of the polyps, as well as the different host species, clearly separate these three species from each other. For details refer to each of the species formal description.
Umimayanthus discolor sp. nov. Montenegro, Kise & Reimer
urn:lsid:zoobank.org:act:7A022F55-32F9-49FA-A395-081BA7240FF3
Synonymy. This specimen was misidentified as Parazoanthus lividum, specimen F67954 in the collection of Museum Victoria.
Etymology. The specific epithet “discolor” means multiple colors in Latin. This is in reference to U. discolor sp. nov. forming colonies of polyps with contrasting colorations between the oral disk and the column, stolon, and coenenchyma.
Type specimens of Umimayanthus discolor sp. nov.; WAM Z88616 (holotype) voucher specimen (A) and in-vivo pictures (B), WAM Z88626 (paratype) voucher specimen (C) and in-vivo pictures (D). Scale bars: 5 mm
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
Material examined. Type locality: Albany [loc. 3], −35.093889 °S, 117.963889 °E. Holotype: WAM Z88616 (−35.093889 °S, 117.963889 °E, loc. 3, Murray Road boat ramp, Albany, Western Australia, 6.4 m depth, April 10, 2018 by O.A. Gomez). Paratype: WAM Z88626 (−35.049722 °S, 117.693611 °E, loc. 4, Shelter Is., Albany, Western Australia, 8.5 m depth, April 11, 2018 by O.A. Gomez).
Other material (n =3). Other examined specimens belong to the Museum of Natural History and Museums Victoria; NHMUK-1887.5.21.1865 (precise location unknown, southwestern part of Western Australia), NHMUK-1931.8.4.57 (−6.164028 °S, 134.944667 °E, loc. 24, east coast of Aru Is., Maluku, Indonesia, 4–15 m depth), MV-F67954 (−39.016306 °S, 146.442917 °E, loc. 1, South Wall, Sealer Cove, Wilsons Promontory, Victoria, Australia, 10 m depth, April 16, 1987 by Dept. Conservation of Environment).
Diagnosis. U. discolor sp. nov. can be distinguished from other species in the genus Umimayanthus by combining the growing pattern and coloration of colonies. U. discolor has polyps connected in chains following a branching pattern, but branches are not connected to each other. Different from all other species of Umimayanthus in the Indo-Pacific Ocean, U. discolor sp. nov. has a disruptive coloration pattern when observed in-vivo, with polyps having a dark brown oral disk clearly contrasting against the white-coloured column, stolon, and coenenchyma (fig. 14B–D). Currently known to establish associations with sponges in the genera Trikentrion Ehlers, 1870 and Clathria Schmidt, 1862; known host species are Trikentrion flabelliforme and Clathria (Thalysias) cactiformis (Lamarck, 1814).
Additionally, multiple unique substitutions across the ITS-rDNA, 16S-rDNA and COI-mtDNA markers clearly differentiate this species from all other members of genus Umimayanthus in the concatenated alignment, as follows: in the ITS-rDNA there is a “A” in position 9 bp, “TCA” between 42 bp to 44 bp, “T” at 74 bp, 344 bp and 665 bp, “G” at 87 bp, 430 bp, 652 bp, 710 bp, and unique deletions at 51 bp and 455 bp; remarkably substitutions were found in the 16S-rDNA region, “T” at position 1337bp, and COI-rDNA region, “T” at position 1654bp . As well, a unique combination of substitutions and deletions/gabs is present between 132–339 bp in the ITS-rDNA region (fig. 15).
Description. Size. Preserved polyps were on average 2.1 mm ± 0.26 mm (
Morphology. The holotype specimen is associated with Clathria (Thalysias) cactiformis (Lamarck, 1814). Colonies formed by polyps tightly connected by stoloniferous chains in a branching pattern extending over the surface of the host sponge. Polyp chains branch continuously with branches interconnected. The coenenchyma is clearly visible over the sponge surface and connects multiple polyps by the stolon. Polyps preserved in ethanol are white or cream in color. Capitulary ridges were not visible. Tentacles were approximately up to 22–24 in number. Capitulum and scapus were moderately encrusted by small sand particles.
Cnidae. The diversity of cnidae was relatively low across tissues. Spirocysts, bastrichs and microbasic b-mastigophores were numerous in the tentacles and pharynx. Additionally, holotrichs (L) were found in the pharynx. Mesenterial filaments were populated by numerous microbasic p-mastigophores, while cnidae were rare in the column with only holotrichs (L) found. See table 5 and fig. 16.
Internal morphology. Sphincter muscle was located in the endoderm. Mesenterial arrangement was macrocnemic. Mesenteries were approximately up to 22–24 in number.
Distribution. Analysed specimens were collected from Australia and Indonesia. In Australia, specimens were from Albany [loc. 3, 4] and Wilson’s Promontory [loc. 1], and in Indonesia from the Aru Islands [loc. 24] (fig. 1). Specimens were found at depths of 4–15 m.
Summary chart of the alignments showing nucleotide positions characteristics to U. discolor sp. nov. across the ITS-rDNA, 16S-rDNA and COI-mtDNA region. Positions in green are unique to U. discolor sp. nov. in genus Umimayanthus. Positions in grey are characteristic but not unique to U. discolor sp. nov
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
Diversity of cnidae found in Umimayanthus discolor sp. nov. across tissues in specimen WAM Z88616. (S) spriocysts, (O) basitrichs and microbasic b-mastigophores, (HL) holotrich large and (PM) microbasic p-mastigophores
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
Results for the cnidocyte analyses for Umimayanthus discolor sp. nov., holotype specimen WAM Z88616
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
Associated host. Umimayanthus discolor sp. nov. was found to be associated with two sponge species; Clathria (Thalysias) cactiformis, family Microcionidae Carter, 1875, and Trikentrion flabelliforme, family Raspailiidae.
As with Umimayanthus cf. aruensis, only historic specimens (collected in 1887 and 1931) of Trikentrion flabelliforme were shown to host Umimayanthus discolor sp. nov., and all more recently collected specimens of this sponge species available to us instead hosted Umimayanthus cf. aruensis.
Clathria (Thalysias) cactiformis is in a different sponge family (Microcionidae) from Trikentrion flabelliforme (Raspailiidae). The other Umimayanthus species described in this study are specific to the same host family, often to the same genus, and in one instance to a single species. Thus, Umimayanthus discolor sp. nov. is a more ‘host-generalist’ species, and the exception among these newly described Umimayanthus species.
Remarks. Molecular data and the arrangement of polyps in specimens BMNH-1887.5.21.1865 and BMNH-1931.8. 4.57 led us to identify these specimens as Umimayanthus discolor sp. nov., and further morphological analyses will be helpful to confirm this decision.
Specimen MV-F67954 was initially identified as P. lividum, however based on the general morphology of the colony, with polyps arranged in branching chains, and the association with Clathria (Thalysias) cf. cactiformis, we have amended the identification of this specimen to Umimayanthus discolor sp. nov.
U. discolor sp. nov. has polyp diameter sizes similar to those reported for U. chanpuru, U. miyabi, and U. nakama, all from southern Japan. In contrast to these species, U. discolor sp. nov. has a well-developed coenenchyma firmly connecting polyps in chains in a branching pattern. These branches remain unlinked and do not form a reticulate pattern over the surface of the host sponge, unlike as in U. cf. aruensis, and do not form a mat as in Parazoanthus lividum.
Umimayanthus lynherensis sp. nov. Montenegro, Kise & Reimer
urn:lsid:zoobank.org:act:5047277C-8846- 4965-81E1-53A2D5268A56
Etymology. The specific epithet “lynherensis” is derived from the locality where the type specimen was collected, the Lynher Bank sea country north Kimberley, Western Australia, Australia.
Material examined. Type locality: Lynher Bank [loc. 14], −15.493683 °S, 121.636233 °E. Holotype: WAM Z88821 (−15.493683 °S, 121.636233 °E, loc. 14, Lynher Bank, Western Australia, 95 m depth, October 25, 2016 by J. Fromont & J.A. Ritchie). No other material was available.
Diagnosis. U. lynherensis sp. nov. can be differentiated from all other species in the genus Umimayanthus by combining polyp size, colony morphology and identity of the host sponges. U. lynherensis sp. nov. have comparatively the smallest polyp diameter of all the species described in here, 1.58 mm ± 0.17 mm, colonies exclusively composed of solitary polyps, and associate with sponges in Sigmaxinella soelae Hooper, 1984 of the order Biemnida Morrow, 2013.
Umimayanthus lynherensis sp. nov. specimen WAM Z88821 (holotype). Scale bars: 5 mm
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
Additionally, there are multiple unique nucleotide substitutions and insertions across ITS-rDNA and COI-mtDNA in the concatenated alignment, as follows: for ITS-rDNA an “A” in positions 47 bp and 135 bp, a “C” at 65 bp and 354 bp, a “G” at 403 bp, 411bp, 426 bp and 705 bp, a “T” at 756 bp, and one unique insertion of 8 nucleotides “GGTGGGGT” between 695–702 bp. As well, multiple unique substitutions were also found in the COI region: a “G” at positions 1442 bp and 1446 bp, a “C” at 1804 bp, and an “A” at 1835 bp (fig. 18).
Summary chart of the alignments showing nucleotide positions characteristics to U. lynherensis sp. nov. across the ITS-rDNA, 16S-rDNA and COI-mtDNA region. Positions in green are unique to U. lynherensis sp. nov. in genus Umimayanthus. Positions in grey are characteristic but not unique to U. lynherensis sp. nov
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
Description. Size. Preserved polyps were on average 1.58 mm ± 0.17 mm (
Morphology. The holotype specimen is associated with Sigmaxinella soelae. Colonies formed of solitary polyps, barely extending out from the surface of the sponge. The polyps were distributed all over the surface of the sponge, and inter-polyp distances were relatively constant, 3.58 mm ± 0.44 mm (
Cnidae. All dissected tissues had a unique composition of cnidae compared to other species examined in this study (table 6). Spirocysts were only present in tentacles. Bastrichs and microbasic b-mastigophores were found across most tissues except for the column. Special microbasic b-mastigophores were found only in the pharynx. Holotrichs (L) were found in the column and filaments. Microbasic p-mastigophores were only present in filaments (fig. 19).
Diversity of cnidae found in Umimayanthus lynherensis sp. nov. across tissues in specimen WAM Z88821. (S) spriocysts, (O) basitrichs and microbasic b-mastigophores, (HL) holotrich large, (SBM) special microbasic b-mastigophores and (PM) microbasic p-mastigophores
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
Internal morphology. The sphincter muscle was located in the endoderm. Mesenterial arrangement was macrocnemic. Mesenteries were approximately 20–24 in number. Single siphonoglyph.
Distribution. The single available specimen was collected from Lynher Bank, Australia [loc. 14] (fig. 1). This specimen was found at a depth of 95 m.
Associated host. U. lynherensis sp. nov. is associated with Sigmaxinella soelae in the family Biemnidae Hentschel, 1923. The type locality of Sigmaxinella soelae is off Port Hedland with originally distribution reported between Exmouth and Broome (Hooper, 1984) in tropical Western Australia. Sigmaxinella soelae is now known to be more widespread in Western Australia and occurs between Lynher Bank, Kimberley (−15.493611 °S, 121.63611 °E) in the north and Point Cloates, Ningaloo (−22.603333 °S, 113.609444 °E) on the upper central west coast of Western Australia.
Remarks. Only a single specimen of U. lynherensis sp. nov. was available, and the inter-polyp distances and polyp diameters were very consistent across the colony.
The colonies of U. lynherensis sp. nov. are formed by solitary polyps spread homogenously across the surface of the host sponge, different from the arrangement of polyps in chains, as in U. discolor sp. nov. The diameter of the polyps of U. lynherensis sp. nov. are similar to those observed for U. chanpuru, U. nakama, U. miyabi, and U. parasiticus. Out of these four species, U. lynherensis sp. nov. most closely resembles U. parasiticus, however U. parasiticus has only been reported from the Atlantic Ocean while U. lynherensis sp. nov. was collected from Western Australia in the Indian Ocean. Furthermore, U. parasiticus has only been reported in association with sponges in the orders Clionaida Morrow & Cárdenas, 2015, Haplosclerida Topsent, 1928, Scopalinida Morrow & Cárdenas, 2015, and Tetractinellida Marshall, 1876 (Montenegro et al., 2020; Swain & Wulff, 2007), while U. lynherensis sp. nov. is associated with Sigmaxinella soelae in the order Biemnida.
Results for the cnidocyte analyses for Umimayanthus lynherensis sp. nov., holotype specimen WAM Z88821
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
Umimayanthus raksasa sp. nov. Montenegro, Kise & Reimer
urn:lsid:zoobank.org:act:01BCCB92-17CE-4768-AB0E-186C31653238
Synonymy. Parazoanthus sp. 3 in Reimer et al. (2014) and Parazoanthus in Alvarez et al. (2016).
Etymology. The specific epithet “raksasa”, which means “giant” or “gigantic” in Indonesian, refers to the large size of the polyps of this species in comparison to the other members of its genus.
Material examined. Type locality: NE coast of Sumba, Nusa Tenggara Timur, Indonesia [loc. 22], −9.891694 °S, 120.711694 °E.
Holotype. RMNH.COEL.46520 in ZMA. POR.9139, Phakellia cf. tropicalis Alvarez & Hooper, 2009, (−9.891694 °S, 120.711694 °E, loc. 22, east of Melolo, NE coast of Sumba, Nusa Tenggara Timur, Indonesia, 75–90 m depth, September 13, 1984. Collected by R.W.M. van Soest, Snellius-II Expedition). Paratype: RMNH.COEL.46521 in ZMA.POR.20704, Phakellia spec., (−8.468333 °S, 119.6175 °E, loc. 23, east of Komodo Field #100, Nusa Tenggara Timur, Indonesia, 91 m depth, September 19, 1984 Collected by R.W.M. van Soest, Snellius-II Expedition).
Other material (n =2). Other examined specimens belong to the collection of the Western Australian Museum; WAM Z88815 (−16.7525 °S, 121.046667 °E, loc. 12, Broome L25, Broome, Western Australia, 108-100 m depth, June 30, 2007 by M.P. Salotti), WAM Z88828 (−15.6233 °S, 121.972233 °E, loc. 13, Lynher Bank, Western Australia, 61 m depth, October 28, 2016 by J. Fromont & J.A. Ritchie).
Diagnosis. U. raksasa sp. nov. can be differentiated from other members of the genus Umimayanthus by presenting comparatively large polyps, colonies with a unique growth pattern, and the identity of host sponge. U. raksasa sp. nov. has an average polyp diameter of 2.83 mm ± 0.42 mm and polyp height of 6.53 mm ± 5.58 mm, colonies primarily extended along the edges of the sponge and this species has only been found in association with sponges in the genus Phakellia Bowerbank, 1862 (fig. 20A). Additionally, there are multiple unique nucleotide substitution across the ITS-rDNA and 16S-rDNA regions in the concatenated alignment, as follows: for the ITS-rDNA region a “G” in positions 47 bp, 131 bp, 454 bp and 860 bp, a “T” at 51 bp, 130 bp, 634 bp, 650 bp, 716 bp, 835 bp and 850 bp, an “A” at 648 bp, and a unique combination of substitutions and deletion/gaps between 130–340 bp; and for the 16S-rDNA region there is a “T” at position 1036 bp, a “C” at 1132 bp, and a unique combination of substitutions and deletion/gaps between 1348–1381 bp (fig. 21).
Specimens of Umimayanthus raksasa sp. nov.; (A) RMNH.COEL.46520 (holotype), (B) RMNH.COEL.46521 (Paratype), (C) WAM Z88815, and (D) WAM Z88828. White bars represent 5mm scales. Note that specimens C and D are tightly contracted in comparation to specimens A and B
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
Summary chart of the alignments showing nucleotide positions characteristics to U. raksasa sp. nov. across the ITS-rDNA and 16S-rDNA region. Positions in green are unique to U. raksasa sp. nov. in genus Umimayanthus. Positions in grey are characteristic, but not unique, to U. raksasa sp. nov
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
Description. Size. Preserved polyps were on average 2.83 mm ± 0.42 mm (
Morphology. The holotype specimen is associated with Phakellia cf. tropicalis Alvarez & Hooper, 2009. Colonies formed by polyps tightly connected in a single chain, although small branches with 2~3 polyps were also found. All polyps were conspicuously spread over a well-developed coenenchyma. Capitulary ridges were visible, 16 in number. Tentacles were 32 in number. Preserved tentacles were brown in coloration. Capitulum and scapus were heavily encrusted by various particles of sand and silica (spicules of host sponges). The colony developed primarily on the outer edge of the host sponge, and most of the sponge surface remained free of polyps. Polyps preserved in ethanol were brown or white in color.
Cnidae. Tentacles and pharynx had similar cnidae compositions, with spirocysts, bastrichs and microbasic b-mastigophores commonly found. In the column only holotrichs (L) were found at a low frequency. In the mesenterial filaments bastrichs and microbasic b-mastigophores, and microbasic p-mastigophores were found in low frequency. See table 7 and fig. 22.
Diversity of cnidae found in Umimayanthus raksasa sp. nov. across tissues in specimen RMNH.COEL.46521. (S) spriocysts, (O) basitrichs and microbasic b-mastigophores, (HL) holotrich large and (PM) microbasic p-mastigophores
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
Results for the cnidocyte analyses for Umimayanthus raksasa sp. nov., holotype specimen RMNH.COEL.46520
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
Internal morphology. Sphincter muscle was located in the endoderm. Mesenterial arrangement was macrocnemic. Mesenteries were approximately up to 32 in number. Ectoderm and mesoglea of capitulum and scapus were heavily encrusted by various sand and silica particles. Single siphonoglyph.
Distribution. The analysed specimens were collected from Australia and Indonesia. In Australia, from Broome [loc. 12], and Lynher Bank [loc. 13], while in Indonesia off Sumba [loc. 22] and Komodo [loc. 23] islands (fig. 1). Specimens were found at depths of 61–108 m.
Associated host. Umimayanthus raksasa sp. nov. appears to be exclusively associated with sponges in the genus Phakellia, within the family Bubaridae Topsent, 1894. One of the ZMA specimens was identified as P. cf. tropicalis (Alvarez et al., 2016), while the WAM sponge specimens were not P. tropicalis.
Remarks. Molecular data, identity of the host sponge, and polyp diameter group all specimens here analysed as Umimayanthus raksasa sp. nov. It is worth noting that in specimens WAM Z88815 and WAM Z88828 polyps are tightly contracted and therefore it will appear to have smaller heights (1.67 mm ± 0.52 mm,
The large size of the polyps of U. raksasa sp. nov. clearly set it apart from the other species in the genus Umimayanthus (fig. 20A–D). U. aruensis as described in Pax (1911) is the only species that slightly resembles U. raksasa sp. nov. Nonetheless, the maximum height of polyps of U. raksasa sp. nov. was found to be 15.7 mm in preserved specimens, approximately four times the height of polyps reported in U. aruensis. As well, colonies of U. raksasa sp. nov. primarily extended along the edges of host sponges, while U. aruensis colonies extended indiscriminately across the whole surface of sponges in a reticulate pattern.
Key to the valid species of Umimayanthus
This key is provided to aid field workers in identification of formally described Umimayanthus species, and is thus largely based on gross morphological attributes along with associated organisms and occasionally geography. More detailed identification can be made using supplementary table 1. This key should not be used as a basis to erect new species.
Citation: Contributions to Zoology 93, 5 (2024) ; 10.1163/18759866-bja10069
Discussion
Importance of museum collections
In this survey we examined 31 voucher specimens of sponges with associated zoantharians, and three type specimens of sponge-associated zoantharians, gathering data on morphological and molecular traits that could lead to their identification. Surprisingly, our results led to the discovery of six species new to science in the genus Umimayanthus, highlighting the importance of proper maintenance and curation of biological collections.
Museum collections have played a crucial role on the study of the ecology, taxonomy and systematics of sponge-associated zoantharians in families Epizoanthidae and Parazoanthidae. For instance, Swain & Wulff (2007), after a meticulous examination of the Porifera collection in the United States National Museum of Natural History in Washington, DC, USA (NMNH), published the first comprehensive analyses of host specificity in sponge-Zoantharia associations for the Caribbean region. The results of Swain & Wulff (2007) played a crucial role in the study of Montenegro et al. (2020) for the identification of extensive legacy material from the RMNH and ZMA collections of NBC in the Netherlands, and specimens recently collected in the Dutch Caribbean. The study published by Montenegro et al. (2020) remains to date the most comprehensive revision of the diversity of zoantharians in the Caribbean region and includes the original description of Parazoanthus atlanticus and the first record for four potentially undescribed species for the region. The work of Swain & Wulff (2007) also set the basis for later reexamination of P. tunicans (Duerden, 1900) by Sinniger et al. (2010), who transferred P. tunicans into the newly created genus Hydrozoanthus. Similarly, Kise et al. (2022) reexamined voucher specimens from the coelenterate collection in NHMUK and the Porifera collections of NBC, and revealed the existence of two new genera and three new species within the family Parazoanthidae.
It is important to note that the oldest specimen analysed by Kise et al. (2022) was collected in 1963 during the “Equalant II Expedition” to the Gulf of Guinea, while some of the specimens from the Dutch Caribbean analysed by Montenegro et al. (2020) were collected in Curaçao by C.J. van der Horst in 1920 (Pax, 1924), and the oldest specimens analysed in the current study can be traced back to 1908 (table 2). Therefore, biological collections not only play a crucial role as reference materials for the identification of species, but also as time capsules for future generations of scientists to access information in light of modern technological developments such as molecular data, thus collecting data in ways beyond the imagination of scientists at the original time of collection, preservation and curation of specimens. Furthermore, the representation of species in old collections also offers the opportunity to return to the same localities where they were originally found and examine whether they still occur there or may have disappeared (Hoeksema & Koh, 2009; van der Meij et al., 2009, 2010). This information is vital to document possible local species extinctions.
Host specificity in the genus Umimayanthus
The specificity of host-zoantharian associations in Umimayanthus has not been thoroughly studied, primarily because of the taxonomic uncertainty of the groups involved in the symbioses. This study provided a rare situation where taxonomists with specialties in both taxa worked in collaboration to provide a more complete picture of associations (see also Swain & Wulff, 2007).
Earlier work on host-zoantharian associations concluded that it is relatively common for a single zoantharian species to associate with multiple host species, but it is more unusual to find one host associated with more than one zoantharian species (Swain & Wulff, 2007). It is worth noting that multiple exceptions are known for host sponges in the genera Agelas Duchassaing & Michelotti, 1864, Cribrochalina Schmidt, 1870, Xestospongia de Laubenfels, 1932, Svenzea Alvarez, van Soest & Rützler, 2002 and Hymeniacidon Bowerbank, 1858 (Swain & Wulff, 2007; Montenegro et al., 2020). However, in general terms, this pattern first observed by Swain & Wulff (2007) appears to be valid for host-Umimayanthus associations (table 2). For instance, U. wunanggu sp. nov. was found in association with two different sponge species in the genus Endectyon; U. mirnangga sp. nov. was in association with two species in two genera, as was U. discolor sp. nov.; and U. raksasa sp. nov. is likely associated with more than one species in the genus Phakellia. Remarkably, Caribbean U. parasiticus has been reported in association with 23 species of sponges across 10 different genera of host sponges (Swain & Wulff, 2007; Montenegro et al., 2020). Other species such as U. chanpuru, U. miyabi and U. nakama are likely associated with multiple genera of encrusting and calcareous sponges, but no detailed taxonomic data are yet available on the identity of their host sponges (Montenegro, pers. observ.).
The only confirmed exceptions to this generalized pattern are U. cf. aruensis, which appears to have a specialized association with Trikentrion flabelliforme, and U. kanabou consistently found in association with a gorgonian in the genus Ellisella, although the identity of the species remains unknown (Fujii et al., 2021). Other species such as U. jebarra sp. nov. and U. lynherensis sp. nov. are only known from a single record, and thus is not possible to draw conclusions on the specificity of the associations for these species.
On the other hand, the host sponges in this study appear to be quite restricted to the specific Umimayanthus species, with most of them associated with a single zoantharian species. Two exceptions were found: Trikentrion flabelliforme, which had associations with two phylogenetically distinct species, U. cf. aruensis and U. discolor sp. nov.; and Endectyon (Endectyon) fruticosum, which was associated with U. wunanggu sp. nov. and U. mirnangga. sp. nov. Given that the latter two sibling species are closely phylogenetically related, we speculate that some level of overlap in host preference is to be expected (Brändle et al., 2000; Blomberg & Garland, 2002).
Based on the results of our phylogenetic analyses, it is clear that these species represent a large radiation of sponge-associated Umimayanthus, with species and clades having generally different niches, based on host species and depth. For instance, Clade I was found inhabiting depths of 12–39 m, Clade II between 41–59 m, and Clade III overlapping all other depth ranges with records from depths of 4–100 m. However, a closer look revealed stratification by depth within Clade III, with U. raksasa sp. nov. and U. lytherensis sp. nov. restricted to deeper waters while U. discolor sp. nov. inhabits shallow waters.
Many studies have shown the Central Indo-Pacific (the Coral Triangle) to be the center of marine biodiversity for a variety of marine taxa such as algae, larger benthic forams, crustaceans, fishes, molluscs, and scleractinian corals (Hoeksema, 2007; Förderer et al., 2018); but whether the region also harbors high diversities of many less studied taxa, including zoantharians, still needs to be examined (Reimer et al., 2014). The current study, focused on species associated with only four families of sponges, indicates that zoantharians may also follow the Coral Triangle centre of biodiversity, and further studies are needed to better confirm this.
Systematics and phylogeny within genus Umimayanthus
Fujii et al. (2021) recently described U. kanabou from Amamioshima Island in southern Japan, and established three subgenera within Umimayanthus based on the results of their phylogenetic analyses. However, as revealed by our study, the evolutionary independence of these “subgeneric” lineages is brought into question. Our results cannot establish with certainty the phylogenetic position of U. parasiticus, U. chanpuru, and U. kanabou, with a lack of support in both ML and BPP phylogenetic analyses. This result renders the phylogenetic distinction between the subgenera Gorgoniazoanthus and Umimayanthus to possibly be invalid. The remaining subgenus proposed by Fujii et al. (2021) was Paraumimayanthus and included the species U. miyabi and U. nakama. This lineage remains well-supported in our analyses, but its position within the genus Umimayanthus is uncertain.
In Fujii et al. (2021) the primary characters used to tell apart subgenera were insertions and deletions across the ITS-rDNA and 16S-rDNA regions, but alignments were extensively masked using GBlock (Castresana, 2000) previous to the phylogenetic reconstructions; the masking resulted in the exclusion of 61.7% of the positions, 556 bp out of 901 bp, from the ITS-rDNA region (Fujii et al., 2021). This calls the diagnostic genetic characters used to differentiate the subgenera into question. Furthermore, the best-fitting model seems to have been only evaluated for the ITS region, and extrapolated to the 16S-rDNA and COI regions. Therefore, in light of the phylogenetic results presented here (fig. 2), the issues mentioned above in Fujii et al. (2021), and the fact that the diversity within the genus Umimayanthus remains clearly underestimated as demonstrated by our results, in this study we refrain from using subgeneric categories within Umimayanthus. Furthermore, we recommend a comprehensive census of the diversity within Umimayanthus to achieve a better understanding of the relationships among all Umimayanthus species; at this point a reassessment of subgeneric or possibly generic divisions can be conducted.
Conclusions
Currently, the genus Umimayanthus includes three well supported subclades and four well supported monophylies formed by single species. The single species monophylies are U. chanpuru, U. parasiticus, U. kanabou, and U. cf. aruensis (fig. 2), while the lineages forming well supported subclades are: (A) U. miyabi and U. nakama (Montenegro et al., 2015; Fujii et al., 2021), (B) U. wunanggu sp. nov., U. mirnangga sp. nov., and U. jebarra sp. nov. (Clade II in fig. 2), and (C) U. discolor sp. nov., U. lynherensis sp. nov., and U. raksasa sp. nov. (Clade III in fig. 2). Additionally, the genus also includes two potentially undescribed species Umimayanthus sp. Madagascar in Sinniger & Häussermann (2009), and Umimayanthus sp. MISE JDR170619‐20‐ 94 (Reimer et al., 2018; Montenegro et al., 2020).
This study highlights the need for further examining in detail the Porifera collections at museums around the world to better expose the undescribed diversity of sponge-associated zoantharians, which effectively remain hidden in plain sight on their host species. It would also be advantageous to conduct genome-wide analyses to further clarify the phylogenetic position of Umimayanthus species, and identify potential hotspots of genetic variation that may have fueled the diversification of this genus in the central Indo-Pacific region as uncovered in this study. Genome-wide comparative analyses may also offer clues on the genetic regions linked to the evolution of symbiotic associations, capitalizing on the fact that the genus Umimayanthus is an obligate symbiont with the rare evolutionary capacity of switching across phylogenetically unrelated host species, as demonstrated by the association of U. kanabou with gorgonians (Fujii et al., 2021).
Acknowledgements
We would like to thank the following institutions for their funding, project support and collection of specimens: The Western Australian Marine Science Institution (WAMSI) and partners, Western Australian Museum (WAM), Australian Institute of Marine Science (AIMS) for the following Kimberley Surveys: WAMSI Survey 1B Camden Sound March 2015 (Permit numbers: DoF – 2547, DPW-CE004795, SF010234); WAMSI Survey 2 Maret Islands December 2015 (Permit numbers: SF010627, (DoF) 2677 ) and WAMSI Survey 4 Lynher Bank Oct–Nov 2016 (Permit numbers: AU-COM2016-326), WAMSI Dredging Surveys: WAMSI Onslow Survey I March 2013 (Permit numbers: DEC SF008483, WAFi 2183); WAMSI Onslow Survey II July 2015 (Permit numbers: DEC SF008483, WAFi2442). The CSIRO and J. Keesing for the following CSIRO survey: Pilbara MCP: Seabed Biodiversity Characterisation & Mapping 2013, A. Hosie WAM for his Albany Sponge Barnacle Survey 2018 (Permit numbers: WA Fisheries Exemption #2756), CSIRO Tasmania and its survey: RV “Southern Surveyor” Cruise SS0507 June/July 2007, WAM Gorgon Project’s Barrow Island Net Conservation Benefit Fund survey: NCB Murions and Montebellos Islands April 2015 (Permit Numbers: Fisheries Exemption 2550, DpaW CE004584 Reg 4 and SF010218 Reg 17). Thanks to museum staff who organized specimen loans; Melanie McKenzie MV and Tom White NHMUK. Thanks to Saskia Dimter at the Forschungsinstitut und Natur-Museum Senckenberg (SMF) in Germany. We thank Dhugal Lindsay at JAMSTEC in Japan, and Alan Jamieson at the Minderoo-UWA Deep-Sea Research Centre in Australia for kindly providing the logistics and support to write this manuscript. JM and JDR were supported in part by fellowships to visit the Naturalis collection hosted by BWH. JDR’s visit to WAM was supported via a Curtin University fellowship hosted by Joseph DiBattista and Michael Bunce. The authors would particularly like to thank the Wunambal Gaambera community including Tom Vigilante and Jason Lee but especially Lillian Karadada and Jeremy Kowan for the Wunambal names used for new species from Wunambal Gaambera Country. We are very grateful to the anonymous reviewers and the editorial team for significantly improving the quality of this study with very accurate comments and recommendations.
Supplementary material
Supplementary material is available online at:
References
Alvarez, B., de Voogd, N.J. & van Soest, R.W.M. (2016). Sponges of the family Axinellidae (Porifera: Demospongiae) in Indonesia. Zootaxa, 4137, 451–477. https://doi.org/10.11646/zootaxa.4137.4.1.
Bakker, F.T., Antonelli, A., Clarke, J.A., Cook, J.A., Edwards, S.V., Ericson, P.G.P., Faurby, S., Ferrand, N., Gelang, M., Gillespie, R.G., Irestedt, M., Lundin, K., Larsson, E., Matos- Maraví, P., Müller, J., von Proschwitz, T., Roderick, G.K., Schliep, A., Wahlberg, N., Wiedenhoeft, J. & Källersjö, M. (2020). The Global Museum: Natural history collections and the future of evolutionary science and public education. PeerJ, 8, e8225. https://doi.org/10.7717/peerj.8225.
Bengmoro, C., Utemorrah, L., Bird, J., Lulpundah, P. & Wati, F. (1971). VASZOLYI_E01 Wunambal language elicitation with some Mangarla, W.A. in Wunambal Gaambera Aboriginal Corporation (2023). Wunambal Gaambera dictionary (Version 1.0). Mobile App: https://apps.apple.com/au/app/wunambal-gaambera-dictionary/.
Boona, A. (2022). Lee J Wunambal recordings, Kalumburu, WA. in Wunambal Gaambera Aboriginal Corporation (2023). Wunambal Gaambera dictionary (Version 1.0). Mobile App: https://apps.apple.com/au/app/wunambal-gaambera-dictionary/.
Blomberg, S.P. & Garland, T. Jr. (2002). Tempo and mode in evolution: Phylogenetic inertia, adaptation and comparative methods. J. Evol. Biol., 15, 899–910. https://doi.org/10.1046/j.1420-9101.2002.00472.x.
Brändle, M., Stadler, J. & Brandl, R. (2000). Body size and host range in European Heteroptera. Ecography, 23, 139–147. https://doi.org/10.1111/j.1600-0587.2000.tb00269.x.
Capell, A. (1941). Notes on the Wunambal language. Oceania, 11(3), 295–308. https://doi.org/10.1002/j.1834-4461.1941.tb00325.x.
Card, D.C., Shapiro, B., Giribet, G., Moritz, C. & Edwards, S.V. (2021). Museum genomics. Annu. Rev. Genet., 55, 633–659. https://doi.org/10.1146/annurev-genet-071719-020506.
Carter, H.J. (1882). New sponges, observations on old ones, and a proposed new group. Ann. Mag. Nat. Hist. 10, 106–125. https://doi.org/10.1080/00222938209459681.
Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol., 17, 540–552. https://doi.org/10.1093/oxfordjournals.molbev.a026334.
Connelly, M.T., Catapang, M.G., Quattrini, A.M. (2024). Unlocking the treasure trove: leveraging dry coral specimens for museum genomics. Coral Reefs, 1–7. https://doi.org/10.1007/s00338-024-02525-5.
Cutress, C.E. (1971). Port Phillip Bay Survey Pt 2. Corallimorpharia, Actiniaria and Zoanthidea. Mem. Mus. Vic., 32, 83–92, pl. 9.
Darriba, D., Posada, D., Kozlov, A.M., Stamatakis, A., Morel, B. & Flouri, T. (2020). ModelTest-NG: A new and scalable tool for the selection of DNA and protein evolutionary models. Mol. Biol. Evol., 37, 291–294. https://doi.org/10.1093/molbev/msz189.
Donati, V. (1765). Storia naturale dell’ Antipate, o corallo nero dell’Adriatico. Giornale d’Italia, spettante all scienza naturale, e principalmente all’ agricoltura, alle aru, ed al commercio, 1: 51–56, 60–64, 2 pl. [pp. 51–56, 1 pl. (issue no. 6, session of 18 August 1764); pp. 60–64, 1 pl. (issue no. 8, session of 25 August 1764)].
de Voogd, N.J., Alvarez, B., Boury-Esnault, N., Cárdenas, P., Díaz, M.C., Dohrmann, M., Downey, R., Goodwin, C., Hajdu, E., Hooper, J.N.A., Kelly, M., Klautau, M., Lim, S.C., Manconi, R., Morrow, C., Pinheiro, U., Pisera, A.B., Ríos, P., Rützler, K., Schönberg, C., Turner, T., Vacelet, J., van Soest, R.W.M. & Xavier, J. (2023). World Porifera Database. Available at: https://www.marinespecies.org/porifera/porifera.php?p=taxdetails&id=167950 (Accessed 21 March 2023).
Drew, J. (2011). The role of natural history institutions and bioinformatics in conservation biology. Conserv. Biol., 25, 1250–1252. https://doi.org/10.1111/j.1523-1739.2011.01725.x.
Edgar, R.C. (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nuc. Acids Res., 32, 1792–1797. https://doi:10.1093/nar/gkh340.
Ellis, J. (1768). An account of the Actinia sociata, or clustered animal-flower, lately found on the sea-coasts of the new-ceded islands. Philos. Trans. R. Soc. London, 57, 428–437.
England, K.W. (1991). Nematocysts of sea anemones (Actiniaria, Ceriantharia and Corallimorpharia: Cnidaria): nomenclature. Hydrobiologia, 216–217, 691–697. https://doi.org/10.1007/bf00026532.
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol., 3, 294–299.
Förderer, M., Rödder, D. & Langer, M.R. (2018). Patterns of species richness and the center of diversity in modern Indo-Pacific larger Foraminifera. Sci. Rep., 8, 8189. https://doi.org/10.1038/s41598-018-26598-9.
Fujii, T. & Reimer, J.D. (2013). A new family of diminutive zooxanthellate zoanthids (Hexacorallia: Zoantharia). Zool. J. Linn. Soc., 169, 509–522. https://doi.org/10.1111/zoj.12075.
Fujii, T., Alves Dos Santos, M.E. & Reimer, J.D. (2021). A new species of sea whip gorgonian-associated Zoantharian (Cnidaria: Anthozoa: Hexacorallia: Parazoanthidae) from the Ryukyu Islands, Japan, with subgeneric subdivision of genus Umimayanthus. Zool. Sci. 38, 466–480. https://doi.org/10.2108/zs200172.
Fujii, T. & Reimer, J.D. (2011). Phylogeny of the highly divergent zoanthid family Microzoanthidae (Anthozoa, Hexacorallia) from the Pacific. Zool. Scr., 40, 418–431. https://doi.org/10.1111/j.1463-6409.2011.00479.x.
Fromont, J., Alvarez, B., Gomez, O. & Roberts, E. (2011). Tetrapocillon (Demospongiae: Poecilosclerida: Guitarridae) in Australia, with the description of a new species. Rec. West. Aust. Mus., 26: 70–89.
Hoeksema, B.W. (2007). Delineation of the Indo-Malayan centre of maximum marine biodiversity: the Coral Triangle. In: Renema, W. (Ed.) Biogeography, Time, and Place: Distributions, Barriers, and Islands, pp. 117–178. Springer, Dordrecht.
Hoeksema, B.W., & Koh, E.G. (2009). Depauperation of the mushroom coral fauna (Fungiidae) of Singapore (1860s–2006) in changing reef conditions. Raffles Bull. Zool. Suppl., 22, 91–101.
Hoeksema, B.W., van der Land, J., van der Meij, S.E.T., van Ofwegen, L.P., Reijnen, B.T., van Soest, R.W.M. & de Voogd, N.J. (2011). Unforeseen importance of historical collections as baselines to determine biotic change of coral reefs: the Saba Bank case. Mar. Ecol., 32, 135–141. https://doi.org/10.1111/j.1439-0485.2011.00434.x.
Hooper, J.N.A. (1984). Sigmaxinella soelae and Desmacella ithystela, two new desmacellid sponges (Porifera, Axinellida, Desmacellidae) from the Northwest shelf of western Australia, with a revision of the family Desmacellidae. N. Terr. Mus. Arts Sci. Monogr. Ser., 2, 1–158.
Hooper, J.N.A. (1991). Revision of the family Raspailiidae (Porifera : Demospongiae), with description of Australian species. Invertebr. Syst., 5, 1179–1481. https://doi.org/10.1071/it9911179.
Hooper, J.N.A. (1996). Revision of Microcionidae (Porifera: Poecilosclerida: Demospongiae), with description of Australian species. Mem. Queensl. Mus., 40: 1–626.
Hooper, J.N.A. (2002). Family Raspailiidae Hentschel, 1923. In: J.N.A. Hooper & R.W.M. Van Soest (Eds.) Systema Porifera. Guide to the Classification of Sponges. Vol. 1, pp. 469–510. Kluwer Academic/Plenum Publishers, New York, Dordrecht.
Karadada, J., Karadada, L., Goonack, W., Mangolamara, G., Bunjuck, W., Karadada, L., Djanghara, B., Mangolamara, S., Oobagooma, J., Charles, A., Williams, D., Karadada, R., Saunders, T. & Wightman, G. (2011). Uunguu plants and animals: Aboriginal biological knowledge from Wunambal Gaambera Country in the north-west Kimberley, Australia. Wunambal Gaambera Aboriginal Corporation.
Katoh, K., & Standley, D.M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Bio. and Evo., 30(4), 772–780. https://doi.org/10.1093/molbev/mst010.
Krell, F.T. & Wheeler, Q.D. (2014). Specimen collection: plan for the future. Science 344: 815–816. https://doi.org/10.1126/science.344.6186.815.
Kise, H., Maeda, T. & Reimer, J.D. (2019). A phylogeny and the evolution of epizoism within the family Hydrozoanthidae with description of a new genus and two new species. Mol. Phylogenet. Evol., 130, 304–314. https://doi.org/10.1016/j.ympev.2018.10.011.
Kise, H., Montenegro, J., Santos, M.E.A., Hoeksema, B.W., Ekins, M., Ise, Y., Higashiji, T., Fernandez-Silva, I. & Reimer, J.D. (2022). Evolution and phylogeny of glass-sponge-associated zoantharians, with a description of two new genera and three new species. Zool. J. Linn. Soc., 194, 323–347. https://doi.org/10.1093/zoolinnean/zlab068.
Kozlov, A.M., Darriba, D., Flouri, T., Morel, B., Stamatakis, A. & Wren, J. (2019). RAxML-NG: A fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics, 35, 4453–4455. https://doi.org/10.1093/bioinformatics/btz305.
Low, M.E.Y. & Reimer, J.D. (2011). Parazoanthus Haddon & Shackleton, 1891, and Parazoanthidae Delage & Hérouard, 1901: Conservation of usage by reversal of precedence with Bergia Duchassaing & Michelotti, 1860, and Bergiidae Verrill, 1869 (Cnidaria: Anthozoa: Hexacorallia). Zootaxa, 2995, 64–68. https://doi.org/10.11646/zootaxa.2995.1.5.
Low, M.E., Sinniger, F. & Reimer, J.D. (2016). The order Zoantharia Rafinesque, 1815 (Cnidaria, Anthozoa: Hexacorallia): supraspecific classification and nomenclature. Zookeys, 14, 1–80. https://doi.org/10.3897/zookeys.641.10346.
Mangglamarra, G., Burbidge, A.A. & Fuller, P.J. (1991). Wunambal words for rainforest and other Kimberley plants and animals. In: N.L. McKenzie, R.B. Johnston & P.G. Kendrick (Eds.) Kimberley Rainforests of Australia, pp. 413–421. Surrey Beatty & Sons Pty Ltd, Chipping Norton.
Montenegro, J., Sinniger, F., Reimer, J.D. & Davis, J. (2015). Unexpected diversity and new species in the sponge-Parazoanthidae association in southern Japan. Mol. Phylogenet. Evol., 89, 73–90. https://doi.org/10.1016/j.ympev.2015.04.002.
Montenegro, J., Low, M.E.Y.Y. & Reimer, J.D. (2016). The resurrection of the genus Bergia (Anthozoa, Zoantharia, Parazoanthidae). Syst. Biodivers., 14, 63–73. https://doi.org/10.1080/14772000.2015.1101028.
Montenegro, J., Hoeksema, B.W., Santos, M.E.A., Kise, H. & Reimer, J.D. (2020). Zoantharia (Cnidaria: Hexacorallia) of the Dutch Caribbean and one new species of Parazoanthus. Diversity, 12, 190. https://doi.org/10.3390/d12050190.
Morrow, C.C., Redmond, N.E., Picton, B.E., Thacker, R.W., Collins, A.G., Maggs, C.A., Sigwart, J.D. & Allcock, A.L. (2013). Molecular phylogenies support homoplasy of multiple morphological characters used in the taxonomy of Heteroscleromorpha (Porifera: Demospongiae). Integr. Comp. Biol., 53, 428–446. https://doi.org/10.1093/icb/ict065.
Nakahama, N. (2021). Museum specimens: An overlooked and valuable material for conservation genetics. Ecol. Res., 36, 13–23. https://doi.org/10.1111/1440-1703.12181.
Nylander, J.A.A. (2004). MrModeltest Version 2. Evolutionary Biology Centre, Uppsala University, Uppsala. https://github.com/nylander/MrModeltest2/releases.
Pax, F.A. (1911). Aktinien der Aru-Inseln. Abh. Senckenberg. Naturforsch. Gesellsch., 33, 300–302.
Pax, F.A. (1924). Actiniarien, Zoantharien und Ceriantharien von Curaçao. Bijdr. Dierk. 23(1), 93–121.
Rafinesque, C.S. (1815). Analyse de la Nature, ou Tableau de l’Univers et des Corps Organisés. Self-published, Palerme, 224 pp.
Rasband, W.S. (2012). ImageJ. U.S. National Institutes of Health, Bethesda, MD, USA.
Reimer, J.D., Kise, H., Santos, M.E.A., Lindsay, D.J., Pyle, R.L., Copus, J.M., Bowen, B.W., Nonaka, M., Higashiji, T. & Benayahu, Y. (2019). Exploring the biodiversity of understudied benthic taxa at mesophotic and deeper depths: Examples from the order Zoantharia (Anthozoa: Hexacorallia). Front. Mar. Sci., 6, 305. https://doi.org/10.3389/fmars.2019.00305.
Reimer, J.D., Sinniger, F., Fujiwara, Y., Hirano, S. & Maruyama, T. (2007a). Morphological and molecular characterisation of Abyssoanthus nankaiensis, a new family, new genus and new species of deep-sea zoanthid (Anthozoa: Hexacorallia: Zoantharia) from a north-west Pacific methane cold seep. Invertebr. Syst., 21, 255–262. https://doi.org/10.1071/IS06008.
Reimer, J.D., Takishita, K., Ono, S., Tsukahara, J. & Maruyama, T. (2007b). Molecular evidence suggesting interspecific hybridization in Zoanthus spp. (Anthozoa: Hexacorallia). Zool. Sci., 24, 346–359. https://doi.org/10.2108/zsj.24.346.
Reimer, J.D., Poliseno, A. & Hoeksema, B.W. (2014). Shallow-water zoantharians (Cnidaria, Hexacorallia) from the Central Indo-Pacific. ZooKeys, 1–57. https://doi.org/10.3897/zookeys.444.7537.
Reimer, J.D., Wee, H.B., García-Hernández, J.E. & Hoeksema, B.W. (2018). Zoantharia (Anthozoa: Hexacorallia) abundance and associations with Porifera and Hydrozoa across a depth gradient on the west coast of Curaçao. Syst. Biodivers., 16, 820–830. https://doi.org/10.1080/14772000.2018.1518936.
Richards, Z.T., Sampey, A. & Marsh, L. (2014). Kimberley marine biota. Historical data: scleractinian corals. Rec. West. Aust. Mus. Suppl., 84: 111–132. https://doi.org/10.18195/issn.0313-122x.84.2014.111-132.
Rocha, L.A., Aleixo, A., Allen, G., Almeda, F., Baldwin, C.C., Barclay, M.V. & Berumen, M.L. (2014). Specimen collection: An essential tool. Science 344: 814–815. https://doi.org/10.1126/science.344.6186.81.
Ronquist, F.R. & Huelsenbeck, J.P. (2003). MRBAYES: Bayesian inference of phylogeny. Bioinformatics, 19, 1572–1574. https://doi.org/10.1093/bioinformatics/17.8.754.
Ryland, J.S. & Lancaster, J.E. (2004). A review of zoanthid nematocyst types and their population structure. Hydrobiologia, 530–531, 179–187. https://doi.org/10.1007/s10750-004-2685-1.
Sampaio, F.L., Day, J.J., Mendis Wickramasinghe, L.J., Cyriac, V.P., Papadopoulou, A., Brace, S., Rajendran, A., Simon-Nutbrown, C., Flouris, T., Kapli, P., Ranga Vidanapathirana, D., Kotharambath, R., Kodandaramaiah, U. & Gower, D.J. (2023). A near-complete species-level phylogeny of uropeltid snakes harnessing historical museum collections as a DNA source. Mol. Phylogenet. Evol., 178, 107651. https://doi.org/10.1016/j.ympev.2022.107651.
Sinniger, F. & Häussermann, V. (2009). Zoanthids (Cnidaria: Hexacorallia: Zoantharia) from shallow waters of the southern Chilean fjord region, with descriptions of a new genus and two new species. Org. Divers. Evol., 9, 23–36. https://doi.org/10.1016/j.ode.2008.10.003.
Sinniger, F., Montoya-Burgos, J.I., Chevaldonné, P. & Pawlowski, J. (2005). Phylogeny of the order Zoantharia (Anthozoa, Hexacorallia) based on the mitochondrial ribosomal genes. Mar. Biol., 147, 1121–1128. https://doi.org/10.1007/s00227-005-0016-3.
Sinniger, F., Reimer, J.D. & Pawlowski, J. (2010). The Parazoanthidae (Hexacorallia: Zoantharia) DNA taxonomy: description of two new genera. Mar. Biodivers., 40, 57–70. https://doi.org/10.1007/s12526-009-0034-3.
Suarez, A.V. & Tsutsui, N.D. (2004). The value of museum collections for research and society. BioScience, 54, 66–74. https://doi.org/10.1641/0006-3568(2004)054[0066:TVOMCF]2.0.CO;2.
Swain, T.D. & Wulff, J.L. (2007). Diversity and specificity of Caribbean sponge – zoanthid symbioses: a foundation for understanding the adaptive significance of symbioses and generating hypotheses about higher-order systematics. Biol. J. Linn. Soc. Lond., 92, 695–711. https://doi.org/10.1111/j.1095-8312.2007.00861.x.
Swain, T.D., Schellinger, J.L., Strimaitis, A.M., and Reuter, K.E. (2015). Evolution of anthozoan polyp retraction mechanisms: convergent functional morphology and evolutionary allometry of the marginal musculature in order Zoanthidea (Cnidaria: Anthozoa: Hexacorallia). BMC Evol. Biol., 15, 123. https://doi.org/10.1186/s12862-015-0406-1.
van der Meij, S.E.T, Moolenbeek, R.G., & Hoeksema, B.W. (2009). Decline of the Jakarta Bay molluscan fauna linked to human impact. Mar. Pollut. Bull., 59, 101–107. https://doi.org/10.1016/j.marpolbul.2009.02.021.
van der Meij, S.E.T, Suharsono, & Hoeksema, B.W. (2010). Long-term changes in coral assemblages under natural and anthropogenic stress in Jakarta Bay (1920–2005). Mar. Pollut. Bull., 60, 1442–1454. https://doi.org/10.1016/j.marpolbul.2010.05.011.
van Soest, R.W.M., Carballo, J.L. & Hooper, J.N.A. (2012). Polyaxone monaxonids: revision of raspailiid sponges with polyactine megascleres (Cyamon and Trikentrion). ZooKeys, 239, 1–70. https://doi.org/10.3897/zookeys.239.3734.
Winker, K. (2004). Natural history museums in a postbiodiversity era. BioScience, 54, 455–459. https://doi.org/10.1641/0006-3568(2004)054[0455:NHMIAP]2.0.CO;2.
