Research Article |
Corresponding author: Jeremy Horowitz ( horowitzj@si.edu ) Academic editor: Bert W. Hoeksema
© 2024 Jeremy Horowitz, Dennis M. Opresko, Santiago Herrera, Colleen M. Hansel, Andrea M. Quattrini.
This is an open access article distributed under the terms of the CC0 Public Domain Dedication.
Citation:
Horowitz J, Opresko DM, Herrera S, Hansel CM, Quattrini AM (2024) Ameripathidae, a new family of antipatharian corals (Cnidaria, Anthozoa, Hexacorallia, Antipatharia). ZooKeys 1203: 355-375. https://doi.org/10.3897/zookeys.1203.121411
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A new family of antipatharian corals, Ameripathidae (Cnidaria: Anthozoa: Antipatharia), is established for Ameripathes pseudomyriophylla Opresko & Horowitz, gen. et sp. nov. The new family resembles Myriopathidae and Stylopathidae in terms of the morphology of the polyps and tentacles and the pinnulate branching of the corallum. Phylogenetic analysis using a genomic data set of 741 conserved element loci indicates that the new family is sister to a clade containing the Myriopathidae, Stylopathidae, Antipathidae, and Aphanipathidae.
Deep sea, fauna of Puerto Rico, genome skimming, mesophotic, molecular phylogenetics, new genus, new species, taxonomy, ultraconserved elements
Recently two samples were collected during an exploratory research cruise to the waters surrounding Puerto Rico conducted onboard the R/V Falkor (too) of the Schmidt Ocean Institute. These specimens matched the morphological characters of the specimens examined by
The specimen was collected 7 km east of Desecheo Island, Puerto Rico, in the Mona Passage, which connects the Atlantic Ocean to the Caribbean Sea, at a depth of 165 m during the Schmidt Ocean Institute expedition FKt230417 entitled: ‘Health diagnostics of deep-sea coral’ (Fig.
The syntype of Antipathes picea was collected by the U.S. Coast Survey Steamer Blake in 1879 and is deposited in the collections of the Museum of Comparative Zoology at Harvard University (specimen registration prefix “
The skeletal elements of the specimens “new to science” were examined using a Zeiss EVO MA 15 scanning electron microscope (SEM). Before scanning, the specimens were coated with a 30–40 nm thick layer of 60% gold: 40% palladium. SEM stubs are deposited at the
DNA extractions of the holotype and one paratype were performed using the DNeasy Blood and Tissue Kit (Qiagen, Germany) following the manufacturer’s protocol. The DNA was cleaned with a Qiagen Power Clean Pro kit, and concentrations were estimated using a High Sensitivity Qubit 4 Fluorometer (Invitrogen, US). For the new species, DNA was sheared using a QSonica Inc Sonicator Q800R to a target size range of 400–800 bp and then checked via gel electrophoresis on a 1.5% agarose gel. Following shearing, DNA libraries were prepared with the Kappa Hyper Prep protocol using a ½ reaction with iTruSeq adapters and dual indexes following
The conserved loci were bioinformatically obtained from the high-throughput sequencing data. First, raw reads were trimmed using Trimmomatic v. 0.35 (
Corallum branched and pinnulate; flabellate. Primary pinnules arranged bilaterally and alternately, secondary pinnules arranged uniserially. Spines up to 0.06 mm tall, conical, slightly compressed laterally with rounded apex, smooth or with knob-like protuberances. Polyps slightly transversely elongate up to 1.2 mm in transverse diameter, subequal tentacles, sagittals positioned lower than laterals, and a raised oral cone.
Examination of SEM images of the spines of the new family revealed that most spines are triangular and smooth with un-ornamented surfaces with a small number of polypar spines possessing a few small, rounded, low-relief, knob-like protuberances (Fig.
Examination of in situ images of the polyps of the new family revealed a slightly transversely elongated external morphology (Fig.
Skeletal spines of antipatharian families A Ameripathidae (Ameripathes pseudomyriophylla gen. et sp. nov.) B Antipathidae (Antipathes furcata Gray, 1857) C Antipathidae (Antipathes falkorae Horowitz, 2022) D Aphanipathidae (Aphanipathes sarothamnoides Brook, 1889) E Stylopathidae (Stylopathes litocrada Opresko, 2006) F Myriopathidae (Myriopathes cf. japonica (Brook, 1889)) G Cladopathidae (Cladopathes plumosa Brook, 1889) H Schizopathidae (Schizopathes affinis Brook, 1889) I Leiopathidae (Leiopathes sp. of Hamie 1849).
Polyps of live corals representing different antipatharian families A Ameripathidae (Ameripathes pseudomyriophylla gen. et sp. nov.) B Myriopathidae (Myriopathes sp.) C Stylopathidae (Stylopathes sp.) D Stylopathidae (Stylopathes sp.) E Antipathidae (Antipathes atlantica Gray, 1857) F Aphanipathidae (Anozopathes sp. Opresko & Bo, 2021) G Schizopathidae (Bathypathes sp.) H Cladopathidae (Heteropathes sp.) I Leiopathidae (Leiopathes sp.). Photo credits: A, C, D (Schmidt Ocean Institute); B (M. Bo); E (S. Weinberg); F, G, H (NOAA/OER; I (P. Etnoyer).
Antipathidae differs in corallum pattern with an unpinnulated corallum compared to the pinnulated corallum in the new family. Cladopathidae differs in polyp size and spine ornamentation, with polyps measuring at least 1.8–2.0 mm compared to up to 1.2 mm in transverse diameter in the new family and possessing smooth spines rather than ones with knob-like protuberances. Leiopathidae differs in corallum pattern, possessing an unpinnulated corallum compared to a pinnulated corallum in the new family. Aphanipathidae differs in spine height, spine ornamentation type, and polyp characteristics, possessing spines up to 0.5 mm tall, distinct tubercles on the surfaces of skeletal spines, and polyps that are as long as they are wide or can be transversely compressed, respectively, compared to spine heights 0.06 mm tall, low-relief, knob-like protuberances on the surfaces of skeletal spines, and slightly transversely elongate polyps with short, subequal tentacles with blunt, rounded tips in the new family. Myriopathidae differs in spine ornamentation type with striations on the surfaces of skeletal spines compared to the spines with a few small, rounded, low-relief, knob-like protuberances in the new family. Stylopathidae differs in subpinnule arrangement and spine surface ornamentation, presenting verticils or irregularly bilateral and smooth spines, respectively, compared to uniserially arranged subpinnules and spines with low-relief, knob-like protuberances spines in the new family. Schizopathidae differs in polyp size and spine ornamentation, having larger polyps (2–12 mm in transverse diameter) and smooth spines, respectively, compared to smaller polyps (up to 1.2 mm in transverse diameter) and spines with knob-like protuberances in the new family.
The recognition of the new family is further supported by the phylogenetic analysis (see further below) conducted on the holotype and one paratype showing that Ameripathidae is a distinct lineage sister to the Antipathidae + Aphanipathidae + Myriopathidae + Stylopathidae, representing a novel deep divergence in the order Antipatharia (Fig.
Maximum likelihood phylogeny of all black coral families and the new family based on a 50% complete matrix containing 741 loci. Boxed taxa (blue outline) represent the new species. Ultrafast bootstrap support is 100% at all nodes except for two nodes, which are noted in the phylogeny. The phylogeny was rooted to the Leiopathidae clade based on results from
Ameripathes pseudomyriophylla sp. nov. (see below).
Corallum sparsely branched, generally in one plane to the seventh order or more. Stem and branches consistently pinnulated to the second order and very rarely to the third order on older sections of the corallum, in some specimens. Primary pinnules 1–2 cm in length, thin; < 0.1 mm in diameter at their midsection. Primary pinnules arranged bilaterally and alternating in two rows. Secondary pinnules 0.5–2 cm in length; arranged uniserially at intervals starting near the base of primary pinnules, projecting anteriorly. Rarely, one or two tertiary pinnules occurring on a very small number of secondary pinnules and usually on the most basal secondary pinnules on the older portions of the corallum. Spines conical, slightly compressed laterally; ≤ 0.06 mm tall on the pinnules; mostly smooth, but some polypar spines possessing small, rounded, low-relief, knob-like protuberances. Spines taller, ≥ 0.14 mm, and needle-like on the thicker branches and stem. Number of spine rows per view and the density of spines in each row do not differ substantially from that on the pinnules. Polyps up to 1.25 mm in transverse diameter, appearing elongated transversely, arranged in a single row, with mostly seven or eight polyps per centimeter. Tentacles cylindrical, subequal in size; and when fully extended not much longer than the transverse diameter of the polyps. Tip of expanded tentacles rounded. Oral cone raised.
Although the family at present contains only a single genus, a comparison with genera of other families suggests that the major generic morphological feature of Ameripathes is the pinnulate nature of the corallum, with two bilateral rows of primary pinnules and one to two orders of subpinnules. This same pinnulation pattern occurs in the genus Myriopathes in the family Myriopathidae and in the deep-sea genus Dendrobathypathes Opresko, 2002 in the family Schizopathidae. The occurrence of similar branching or pinnulation patterns across families is common among antipatharians.
Another feature that occurs in both Ameripathes and Myriopathes is an increase in the size of the spines on the branches and stem where they are more cylindrical and needle-like. However, in Ameripathes the spines on the stem do not increase in density (number of rows and number per row) and do not become forked or antler-shaped, which is often the case in the Myriopathes.
Ameripathes pseudomyriophylla sp. nov. is the only species assigned to the newly described genus.
In accordance with Article 11.3 of the International Code for Zoological Nomenclature the name of the genus Ameripathes can be considered an arbitrary combination of letters; however, it is loosely derived from “americana” in reference to the early association of this taxon with Antipathes americana Duchassaing and Michellotti, and the commonly used suffix -pathes.
The single species assigned to this genus is known only from the Western Central Atlantic, in the Caribbean Sea and the Gulf of Mexico (Fig.
Antipathes americana Opresko, 1972: 975–979.
Antipathes picea Pourtalès, 1880: 115 (in part).
not Antipathes americana Duchassaing & Michelotti, 1860: 56.
Holotype
: USNM 1689129, 7 km east of Desecheo Island, Puerto Rico, 18.387°N, 67.408°W, 165 m depth, seawater temperature 22 °C. Schmidt Ocean Institute R/V Falkor (too), FKt230417, Health diagnostic of deep-sea coral, ROV SuBastian dive 506, April 19, 2023 (SEM stub No. 586–590). Paratypes: USNM 1689101, 6 km east of Desecheo Island, Puerto Rico, 18.389°N, 67.417°W, 183 m depth, seawater temperature 21 °C. Schmidt Ocean Institute R/V Falkor (too), FKt230417, Health diagnostic of deep-sea coral, ROV SuBastian dive 504 April 18, 2023 (SEM stub No. 581–585);
7 km east of Desecheo Island, Mona Passage, Puerto Rico, 165 m depth
As for the genus.
The holotype (USNM 1689129) is a 19-cm section of branch (Fig.
Spines (Fig.
Polyps occur in a single row. On the primary pinnules they are confined on or near the side on which the subpinnules occur. The polyps are 1.0–1.25 mm in the transverse diameter (Fig.
The colony from which the holotype was collected was imaged in situ (Fig.
Specimen USNM 11689101 is a 12-cm section of branch from a colony estimated to be ~ 0.3 m tall based on in situ imagery (Fig.
Spines on the pinnules are conical, slightly compressed laterally (especially those nearer the tips of the pinnules), with a rounded apex, and smooth or with one to two small, rounded, low-relief, knob-like protuberances 0.003–0.006 mm tall on polypar spines visible in lateral view (Fig.
Polyps occur in a single row. On the primary pinnules they are confined on or near the side on which the subpinnules occur. The polyps are 1.0–1.25 mm in the transverse diameter (Fig.
The specimen from R/V Pillsbury sta. 857 (
Spines (Fig.
Polyps occur in a single row. On the primary pinnules they are confined on or near the side on which the subpinnules occur. The polyps are 0.6 mm in transverse diameter near the tips of the pinnules, increasing to ~ 1.1 mm near the base. They appear elongated due to the small axial diameter of the pinnules. The interpolypar distance (between lateral tentacles of adjacent polyps) is 0.1–0.2 mm, and there are usually eight or nine polyps per centimeter, rarely as many as ten per centimeter. The tentacles (in preserved state) are subequal in size, ~ 0.4 mm long, with the sagittals placed lower than the laterals. The oral cone is ~ 0.25 mm high.
The MCZ specimen from Blake Sta. 260 is a 6.5-cm long branch or the stem of a small colony (with the basal plate missing). The primary pinnules are 1–2 cm long, ~ 0.17 mm in diameter at their base, and spaced ~ 3.0 mm apart in each row. Primary pinnules longer than ~ 2 cm develop into pinnulated branches with the primary pinnules 3 mm apart in each lateral row. The interior angle formed by the two rows of primary pinnules is 160–1750, but the pinnules are curved backwards so that they appear in the plane of the stem/branch. The distal angle of the pinnules is ~ 750. There are ≤ 4 secondary pinnules on each primary; the first is 0.05 mm from the base of the primary, the second 1.5–1.8 mm from the first, the third 2.0–2.5 mm from the second; and the fourth 3 mm from the third. The secondary pinnules are 0.2–0.7 cm long. They extend outward on the convex side of the primaries and are also angled distally ~ 600 to the primary. Tertiary pinnules are present on a few of the basal-most secondaries and are in the same plane as the secondary or extend upward to be parallel to the branch. The spines are 0.06 mm tall on the pinnules and 2–3× taller on the lower part of the stem/branch (≤ 0.17 mm). They are less regularly arranged near the base of the stem and extend out in various directions. In places, they are completely absent. Polyps are not present.
The specimen from Silver Bay sta. 190 (
The five specimens in the type series are fairly consistent in morphological features. They all form a branched pinnulate corallum with at least two orders of pinnules. The colonies tend to be planar. The occurrence and number of secondary and tertiary pinnules is, however, variable, both within a colony and between colonies, explainable perhaps by the size and age of the colony or the section of the colony sampled. The primary pinnules are always arranged bilaterally and alternately in two rows. The distance between primary pinnules in each row ranges from 2 to 3 mm; the total density for both rows is fairly consistent at eight or nine per centimeter. On the largest specimens, the maximum length of the primary pinnules is 2 cm or slightly longer. Pinnules longer than 2 cm usually develop into pinnulated branches. The pinnules are always very thin, the axial diameter is usually < 0.2 mm near their insertion on a branch and only 0.05–0.06 mm at their midpoint. The number of secondary pinnules per primary pinnule is usually one or two; however, rarely, there are as many as four per primary. Secondary pinnules are variable in length within and between colonies and can be as long as the primary pinnules. Tertiary pinnules are very rare and appear to occur mainly on older sections of the corallum. The fact that tertiary pinnules could not be found on the holotype is most likely due to its being a section taken from the upper, younger part of the colony. When present, tertiary pinnules are very short and are mostly confined to the lowermost secondary pinnules; however, they occasionally can also be found on a more distal secondary pinnule. There are usually only one, and rarely two tertiary pinnules on a secondary. On the pinnules, the maximum size of the polypar spines is consistently 0.06 mm from colony to colony. The spines always increase in size and become more cylindrical and needle-like on the larger branches, and depending on the axial diameter, can be as tall as 0.17 mm. The number of rows of spines varies slightly from colony to colony ranging between three or four to four or five visible in one aspect.
The number of rows, however, does not increase on the larger branches, and the density of the spines is mostly five or six per mm, even on the thickest branches. The maximum size of the polyps varies only slightly between colonies in that the transverse diameter ranges from ~ 1–1.25 mm, and the density is typically 7–9 per cm. The interpolypar distance ranges from 0.1 to 0.6 mm.
A total of 60–986 conserved element loci were obtained per specimen. Total number of contigs ranged from 16,819 to 1,444,028 base pairs (bp) (average lengths (bp) ranged from 280 to 1,695). The 50% taxon occupancy matrix included 741 loci that were concatenated into an alignment with a total length of 391,648 bp. Read and locus summary statistics are detailed in Suppl. material
The species name is derived from pseudo (false) and myriophylla, in reference to the very similar appearance to species in the genus Myriopathes with M. myriophylla being the type species of the genus.
The species is only known only from the Caribbean and the Gulf of Mexico between 54 and 532 m depth.
Ameripathes pseudomyriophylla , holotype (USNM 1689129) A section of the collected specimen B colony from which the holotype specimen was collected C section of pinnulated branch showing two rows of alternating primary pinnules and uniserial secondary pinnules D dorsal view of pinnulation pattern (second-order uniserial pinnules indicated by the arrows) E section of pinnule showing preserved polyps with contracted tentacles.
Ameripathes pseudomyriophylla , paratype (USNM 1689101) A colony from which the paratype was collected B section of the collected specimen C lateral view of a polypar spine showing two knobs D dorsal view of single spine showing two knobs E lateral view of a pinnulated branch showing the arrangement of the pinnules and subpinnules F lateral view of a branch showing the arrangement of the pinnules and subpinnules.
This study describes the first new black coral family discovered in 18 years, underscoring the untapped potential for groundbreaking discoveries even in seemingly well-surveyed areas, such as the Gulf of Mexico. Furthermore, the identification of this new species, alongside another recent species described from the Caribbean Sea off Puerto Rico (
Traditionally, the taxonomic classification of black corals has relied heavily on morphological characters, which can be prone to issues of convergence and homoplasy (
The authors wish to thank W. Keel, W. Moser, and K. Reed for their assistance during visits to the Museum Support Center at the
The authors have declared that no competing interests exist.
No ethical statement was reported.
Funding for this project was provided by the Smithsonian Peter Buck Fellowship, Smithsonian Institution Barcode Network Award, and by a grant from the Department of Justice to the Smithsonian Institution. SH was supported by NOAA award NA18OAR0110289 and the National Academies of Sciences, Engineering, and Medicine Gulf Research Program Early-Career Fellowship under award 2000013668.
J.H. and D.M.O conceived the original idea and designed the study. J.H., D.M.O., S.H., C.M.H., and A.M.Q contributed to the overall research direction and planning. C.M.H. conducted the specimen collection. J.H., A.M.Q, and D.M.O developed the methodology and experimental protocols. J.H., D.M.O., S.H., C.M.H., and A.M.Q performed the data analysis and interpretation. J.H. and D.M.O wrote the first draft of the manuscript. J.H., D.M.O., S.H., C.M.H., and A.M.Q provided feedback and suggestions on the draft and edited the manuscript multiple times.
Jeremy Horowitz https://orcid.org/0000-0002-2643-5200
Dennis M. Opresko https://orcid.org/0000-0001-9946-1533
Santiago Herrera https://orcid.org/0000-0001-7204-9434
Colleen M. Hansel https://orcid.org/0000-0002-3506-7710
Andrea M. Quattrini https://orcid.org/0000-0002-4247-3055
Raw sequence reads were submitted to GenBank under BioProject # PRJNA1078781. 4K video can be found on https://tinyurl.com/SupplMat2.
Table of read and locus summary statistics for specimens
Data type: xlsx
Explanation note: Metadata for molecular data including the number of raw reads, assembly statistics, and NCBI details.