Description of Barathricolathermophilus, a new species from a deep-sea hydrothermal vent field in the Indian Ocean with redescription of the Barathricola type species (Crustacea, Copepoda, Cyclopoida)

Abstract Re-study of the type species of the genus Barathricola Humes, 1999 (Copepoda, Cyclopoida, Schminkepinellidae) described from the Pacific Ocean (Juan de Fuca Ridge), and study of the species Barathricolathermophilussp. nov. from a deep-sea hydrothermal vent field on the Central Ridge in the Indian Ocean revealed a derived feature and widespread geographic distribution of this deep-sea genus of cyclopoids. The derived feature of Barathricola is the sexually dimorphic third endopodal segment of leg 3 possessing a small outer terminal spine together with spine-like outgrowths on this segment. The new species differs from Barathricolarimensis Humes, 1999 in not expressing sexual dimorphism in leg 5, having three spines and one seta on its exopod in both sexes (B.rimensis has three spines and one seta on the female exopod but three spines and two setae on the male exopod) and in having broader caudal rami which are 8.9 times longer than wide in the female (this ratio for B.rimensis is 11). An amended diagnosis of the genus Barathricola, a key and a table of morphological differences for all species of Schminkepinellidae are given.


Introduction
Cyclopoids of the family Schminkepinellidae were discovered in the deep-sea and in marine caves (Martínez Arbizu 2006). The genera initially allocated to Schminkepinellidae were the monotypic genera Cyclopinella G.O. Sars, 1913Barathricola Humes, 1999, Einslepinella Martínez Arbizu, 2006, Muceddina Jaume & Boxshall, 1996, and Schminkepinella Martínez Arbizu, 2006. The type species Cyclopinella tumidula Sars, 1913 was collected from benthic muds off the Norwegian coast (Sars 1913). Muceddina multispinosa Jaume & Boxshall, 1996, the only species of this genus, was collected from anchialine caves on Mediterranean and eastern Atlantic islands (Jaume and Boxshall 1996). Humes (1999) recorded Barathricola rimensis Humes, 1999 from a depth of 2254 m at a hydrothermal vent area in the northeastern Pacific. Martínez Arbizu (2006) described Schminkepinella plumifera from a depth of 3211 m and Einslepinella ulrichi from a depth of 529 m in the Arctic Ocean, both as new genera and species. The family was considered as the sister group of Poecilostomatoida allocated to the order Cyclopoida (Martínez Arbizu 2000). A molecular analysis conducted by Khodami et al. (2017) placed Schminkepinellidae as the sister group of Poecilostomatoida but was not verified by the analysis of Mikhailov and Ivanenko (2019) based on data provided by the authors. Karanovic (2008) described shallow water Cyclopinella tincanbayensis Karanovic, 2008 from Queensland in Australia, synonymised Barathricola and Muceddina with Cyclopinella based on characters shared by these two genera and Cyclopinella.
In June 2018 the Korea Institute of Ocean Science and Technology (KIOST) made an expedition to deep-sea hydrothermal vent fields on the Central Indian Ridge in the Indian Ocean and sampled benthic habitats, using the research vessel ISABU. Several species of copepods were discovered from this expedition. A new species of the genus Barathricola, which is described herein, is among these copepods. In addition, to verify diagnostic characters and the validity of the genus Barathricola we restudied the type specimens of the genera Barathricola and Muceddina.

Materials and methods
Samples of the meiobenthos around the hydrothermal vents of the Onnuri Vent Field (OVF), Central Indian Ridge, Indian Ocean, were made using a TV-grab (Video-Guided Hydraulic Grab, Octopus, Germany) during the deep-sea expedition of the research vessel RV ISABU of the KIOST in June 2018. Sampled sediments were fixed and preserved in 10% formalin for a couple of months. Copepods were sorted out from the sediments and stored in 80% ethanol.
Prior to description of the species, selected copepod specimens were soaked in lactic acid. Dissections were performed using the reversed slide method of Humes and Gooding (1964). The specimens of Barathricola and Muceddina were studied with a Leica DMR compound microscope using bright-field and differential interference contrast optics. Drawings were made with a camera lucida mounted on the microscope. In the description, the body lengths of the specimens were measured from the anterior margin of the cephalothorax to the end of caudal rami, excluding setae. Type specimens of the new species have been deposited in the Marine Biodiversity Institute of Korea (MABIK), Seocheon, Korea.
Labrum weak, easily destroyed. Mandible (Fig. 1H) consisting of coxa, basis, exopod, and endopod. Coxa with setules on outer margin; cutting margin of gnathobase with six acutely pointed teeth, two thin proximal setae, three setules between distal second and third teeth, and one small, transparent digitiform process bearing fine spinules distally between distal first and second teeth. Basis elongate, 42 × 9 μm, bearing five or six setules subdistally. Exopod small, indistinctly 3-segmented, armed only with two setae on third segment, outer one of these setae sparsely pinnate and slightly longer than inner one. Endopod 2-segmented, armed with two and four setae on first and second segments, respectively, all six setae sparsely pinnate; first segment with several setules on medial margin. Maxillule ( Fig. 1I) with eight setae on praecoxal arthrite; second distal seta spiniform. Coxal endite absent. Epipodite with two unequal setae. Basis with four setae, three proximal and one distal. Exopod with four large setae distally; setae becoming longer from outer to inner margin. Endopod shorter than exopod, armed with five setae, one on medial margin, and four distally. Maxilla ( Fig. 2A) stout, 5-segmented, consisting of syncoxa, basis, and 3-segmented endopod. Syncoxa armed with 11 setae, grouped as four, one, three, and three on first to fourth endites, respectively; third and fourth endites ornamented with two spinules at distal region. Basis armed with three unequal setae (one large, proximally unarticulated, spiniform, one long, and one small setae) and ornamented with one spinule. First endopodal segment with four setae (two proximal and two distal). Second endopodal segment with two long setae; third endopodal segment small, with four setae (one long and three shorter).
Maxilliped (Fig. 2B) slender, 7-segmented, consisting of syncoxa, basis, and 5-segmented endopod. Syncoxa with several scattered rows of minute setules, and armed with three setae, proximal one small and naked. Basis with two setae and rather long setules on medial margin. Endopod armed with one, one, one, one, and three setae on first to fifth segments, respectively; middle seta on terminal segment naked, much longer than other setae, longer than basis and endopod combined. Articulation incomplete between third and fourth endopodal segments.
Legs 1-4 (Figs 2C-E; 3A) with 3-segmented exopod and endopod, lacking inner seta on first exopodal segment; third exopodal segment distinctly broader than proximal segments. All intercoxal sclerites smooth without spinule/setule array along distal margin and on both anterior and posterior surfaces. Endopods of legs 1-3 shorter than exopod, but that of leg 4 distinctly longer than exopod. Leg 1 (Fig. 2C) basis with seven thick setules on inner margin; inner distal spine large, 48 μm long, extending to middle of third endopodal segment, spinulose along both margins. Leg 2 ( Fig. 2D) with inner coxal seta characteristically bent at proximal quarter; outer seta on basis shorter than those of legs 1, 3 and 4. Inner distal corner of basis of legs 2-4 with pointed dentiform process. Leg 3 (Fig. 2E) with two distal spines on third endopodal segment (outer spine ca. half as long as inner spine). Leg 4 (Fig. 3A), third endopodal segment elongate, 3.6 times as long as wide; inner distal seta on second endopodal segment and two inner and one outer setae on third endopodal segment transformed to spines. Armature formula for legs 1-4 as in Table 1.  Leg 5 (Fig. 3B) 3-segmented, consisting of coxa, basis and exopod; intercoxal sclerite small, narrow, with pointed outer distal corners and slightly concave distal margin. Coxa quadrate, unarmed, not articulated from somite. Basis also quadrate, armed with one pinnate seta outer distally. Exopod 54 × 24 μm, 2.25 times as long as wide, armed with three spines (two distal and one outer) and one pinnate seta; medial margin spinulose and outer margin setulose.
Mandible and other mouth appendages as in female. Legs 1, 2, and 4 also as in female. Leg 3 sexually dimorphic; third endopodal segment (Fig. 3G) bearing two spines, three setae, and distally two small specialized elements, one curved, non-articulating, spinule-like element and one straight, distally bifurcate articulating element.
Leg 5 as in female. Leg 6 ( Fig. 3E) represented by three naked setae on genital operculum, medial one smaller than other two.
Etymology. The specific name thermophilus is a combination of Greek words therm (=heat) and phil (=loving), referring to the finding of the new species in a hydrothermal vent field. Humes, 1999 Figs 4-7 Material. Females and males from the type locality dissected by A.G. Humes and marked as Barathricola rimensis in the Zoological Museum of Lomonosov Moscow State University (collection numbers: w.cyc.sch.1.1-1.5). The hydrothermal vent field is at Juan de Fuca Ridge (44°08.6'N, 129°42'W) in the northeastern Pacific, 26 August 1996 at 2254 m depth.

Barathricola rimensis
Redescription of female. Body as in original description. Differs from Barathricola thermophilus sp. nov. in following features.
Mandible (Fig. 5B, C) with coxa having medially directed gnathobase armed distally with row of seven or eight slender teeth. Palp biramous. Basis elongate, with minute exopodal process carrying two long setae, and two prominent setae distally on margin of basis; endopod two-segmented, first segment small, trapezoidal, bearing two setae and row of minute spinules, second segment small with four distal setae and row of minute spinules along anterior edge.
Maxillule ( Fig. 6A) with large praecoxa bearing arthrite with eight setae; coxa-basis with 3+1 setae; exopod with two short stout setae and two long slender setae; endopod with five setae. Maxilla (Fig. 6B) with praecoxa having two endites, proximal endite bearing four setae, distal endite represented by single seta. Coxa with two endites, both with three setae. Basis with endite bearing three setae, one short, one long and slender, and one stout and claw-like, and having few minute subterminal spinules. Endopod three-segmented, with first segment having two endites with two setae each, small second segment bearing two setae, and minute third segment with four setae. Maxilliped (Fig. 6C) with both coxa and basis swollen medially and bearing three and two setae, respectively; endopod slender, consisting of five segments armed with 1, 1, 1, 1, and 3 setae. Coxae of maxillipeds joined ventrally by one sclerotized line.
Leg 5 (Fig. 7F). Both legs connected by small quadrangular intercoxal sclerite and consisting of coxa, basis, and one-segmented exopod. Coxa and basis with setules along both sides. Basis with outer seta 44 mm long. Exopod 21 mm in greatest dimensions (15.5 mm wide distally) bearing three spines and one seta. Outer marginal barbed spine 57 mm, two terminal spines 58 mm (outer) and 41 mm (inner), both with minute outer spinules and longer inner fringelike setules. Seta between these two spines smooth, 55 mm. Outer margin of segment proximal to spine with setules; distal to spine and along inner side of segment with shorter setules, inner margin with minute spinules.
Remarks. Martínez Arbizu (2006) established the family Schminkepinellidae into which he incorporated five genera, Cyclopinella, Muceddina, Barathricola, and his two new genera Einslepinella and Schminkepinella. The family is a monophyletic group of genera distinguished from other cyclopoid families by the reduction of a maxillulary coxal endite and the transformation of the distal inner seta on the middle endopodal segment of leg 3 into a spine (Martínez Arbizu 2006). None of the synapomorphies for the order Cyclopoida (a brush-like seta on the exopod of mandible, a brush-like seta on the exopod of maxillule, one or more flange-like setae on the endopod of swimming leg 4, pores with sensory dendrites laterally on the male cephalosome) proposed by Abiahy et al. (2006) are found in Schminkepinellidae. Karanovic (2008) described Cyclopinella tincanbayensis as a new species and synonymized two monotypic genera Muceddina and Barathricola with Cyclopinella and included these genera within Cyclopinidae based on the two major characters as synapomorphic shared by these nominal genera and Cyclopinella: the third endopodal segment of leg 4 with all armature elements transformed into spines and the three-segmented female leg 5 with an uniform armature and the elongate exopod. Karanovic (2008) recognized the mandibular palp as the most important morphological character differentiating species of Cyclopinella and its reduced segmentation and setation is consistent with reductions in other cephalic appendages and in the maxilliped. Our re-examination of the type species of the genus Muceddina, confirmed the original description and did not reveal the presence of a sexually dimorphic leg 3. This as well as our re-examination of the type specimens of Barathricola rimensis does not provide sufficient support for inclusion of Muceddina multispinosa and Barathricola rimensis in Cyclopinella. Additional data are needed to provide for the proposed taxonomic changes; here Barathricola and Muceddina are considered valid genera with clear distinctive characters separating them from other genera (see Key and Table 2). Cyclopinella tincanbayensis should remain in Cyclopinella although its distinctive characters may be significant enough to consider moving it to a new genus after revision. Barathricola, Cyclopinella, and Muceddina should remain in the Schminkepinellidae as was proposed by Martínez Arbizu (2006) until more data are available.
Data here show that the sexual dimorphism in leg 3 occurs in B. thermophilus and B. rimensis. Thus, the sexually dimorphic leg 3 known from the two species living in the hydrothermal vent environment is clearly the derived character of the genus Barathricola as mentioned by Martínez Arbizu (2006). Barathricola thermophilus sp.   nov. shares with B. rimensis the shape of the mandibular palp and a number of other characters, e.g., Humes (1999) described the mandibular exopod of B. rimensis as "a minute process carrying two long setae", but his illustrations and those here for this appendage show that the exopod is indistinctly 3-segmented, with two setae on the third segment, as in B. thermophilus sp. nov. In addition, the two species share the identical armature formula for the antenna (0-1-5-7), the loss of an inner seta on the basis of the mandible, a two-segmented mandibular endopod bearing two and four setae on the first and second segments, respectively, and elongate caudal rami. Although the two species of Barathricola are very similar to each other, they cannot be treated as conspecific due to a significant difference in leg 5 of the male. The exopod (terminal segment) of leg 5 is armed with three spines and two setae (formula I, I+1+I, 1) in B. rimensis, in contrast to three spines and one seta (formula I, I+1+I) in B. thermophilus sp. nov. lacking a seta on the inner margin of the exopod. Within the Schminkepinellidae males of six species are known, including B. rimensis and B. thermophilus sp. nov. In these species a sexual dimorphic leg 5, as in B. rimensis, is known in Muceddina multispinosa, Schminkepinella plumifera, and Einslepinella ulrichi. However, Sars (1913) recorded that leg 5 of male Cyclopinella tumidula is of exactly the same appearance as in the female. Thus, the sexual dimorphism in leg 5 appears to be a character differentiating species, but not genera, in the Schminkepinellidae. An additional morphological difference between the two species of Barathricola is the ratio of the length to the width of the caudal ramus is 11.0:1 in the female and 8.5:1 in the male of B. rimensis, which is 8.9:1 in the female and 6.1:1 in the male of B. thermophilus sp. nov. Leg 5 sexually dimorphic, with exopod bearing 3 spines + 1 seta in female and 3 spines + 2 setae in male; length/width ratio of caudal ramus 11:1 in female and 8