Vol. 40(1):23−35 Ocean and Polar Research March 2018 http://dx.doi.org/10.4217/OPR.2018.40.1.023

Article

The First Record of Monothula subtilis (Giesbrecht, 1893 [“1892”]) (Cyclopoida, ) in the Equatorial Pacific Ocean

Kyuhee Cho1* and Woong-Seo Kim2 1Envient Inc., Daejeon 34052, Korea 2Deep-Sea and Seabed Mineral Resources Research Center, KIOST Busan 49111, Korea

Abstract : A small cyclopoid M. subtilis (Giesbrecht, 1893 [“1892”]) belonging to the genus Monothula Böttger-Schnack and Huys, 2001 was collected by using 60 µm mesh net and firstly recorded in the epipelagic layer of the equatorial Pacific Ocean. We redescribed its morphological characteristics for both female and male, comparing with those of previous studies. Specimens of M. subtilis from the equatorial Pacific Ocean differ from those previously reported by others in terms of the length of the seta G on antenna, being much shorter than setae E and F; in the distal spine on the swimming leg 4, being longer than the length of the third segment on P4. The outer spine of the P3 enp-3 in male is slightly over the tip of conical process. The spine lengths of the distal endopods of P2−P4 for both sexes showed variations among individuals, and the proportions of spine lengths in female are higher than those in male. Key words : , copepod, tropical Pacific, , Monothula subtilis

1. Introduction southern Korean waters, the East China Sea, and adjacent waters of Japan (Chen et al. 1974; Itoh 1997; Wi et al. The family Oncaeidae Giesbrecht, 1893 [“1892”] is 2009, 2011, 2012). Compared to the area above mentioned, definitely appreciated as important zooplankton in terms there have been minimal studies on taxonomy in the open of both numerical abundance and diversity in tropical Pacific Ocean. marine ecosystem emerged during the past 2−3 decades, The characteristics of the genus Monothula belonging especially in the case of small species (< 0.1 mm) to the family Oncaeidae, are as follows: absence of the (Böttger-Schnack 1994; Roman et al. 1995; Mckinnon et outer spine on P2−P4 enp-3 and the presence of a single al. 2013). They are one of marine zooplankton groups, dorsal egg-sac. Monothula subtilis is the only species occurring in all water columns of the world’s oceans. In belonging to this genus (Böttger-Schnack and Huys 2001). recent years, numerous field and taxonomic studies have Giesbrecht (1893) firstly described female of the species attempted to find and explore small species, using a fine- as subtilis from the Gulf of Naples, Mediterranean mesh (< 0.1 mm) net. As a result, they have been Sea with the figures of the female habitus, urosome, examined in various areas of the world oceans and seas, antenna, maxilliped and swimming leg 4. Razouls (1972) such as the Red Sea (Böttger-Schnack 1999, 2002, 2005, gave partial figures (urosome, antennule, antenna, maxilliped, 2009), the Mediterranean Sea (Kršinić and Malt 1985; and swimming leg 4) of female M. subtilis from the region Böttger-Schnack 2003), the Arabian Sea, the Antarctic of Banyuls (Gulf of Lion), but morphological details and and the Pacific Ocean (Heron 1977; Heron et al. 1984; several armature elements on appendages were absent. Heron and Frost 2000; Böttger-Schnack 2004), the Gallo (1976) illustrated urosome, P1−P4, antennule, antenna, maxilla, and maxilliped of male from La Pallice *Corresponding author. E-mail : [email protected] Harbor, the northeast Atlantic Ocean, however, Gallo 24 Cho, K. and Kim, W.-S. missed figures of several armature elements and portrayed Morphological terminology followed Huys et al. inaccurately. The figures of Razouls (1972) and Gallo (1996). Abbreviations used in the text and figures are as (1976) could be referred to the web site (Razouls et al. follows: Al, antennule; A2, antenna; ae, aesthetasc; P1− 2005−2017). Malt (1982) described the developmental P6, first to sixth thoracopod; exp, exopod; enp, endopod; stages of M. subtilis from the mouth of English Channel exp (enp)-1 (2, 3) to denote the proximal (middle, distal) near the Atlantic Ocean. Subsequently Böttger-Schnack segment of a three-segmented ramus. The observable and Huys (2001) rearranged this species as a new genus pores and other integumental structures (e.g., pits, scales) Monothula, and redescribed both sexes of M. subtilis from on the body surface under the light microscope were only the Red Sea, the east Mediterranean Sea, the Arabian Sea figured. and the eastern Indian Ocean in more detail. All materials were deposited in the National Institute of During the investigation on the zooplankton community Biological Resources (NIBR), Korea. at the Korean long-term environmental monitoring station in the equatorial Pacific Ocean (MOMAF 2009), taxonomic 3. Descriptions study of oncaeid was carried out. Many small species of the family Oncaeidae were sampled, including Family Oncaeidae Giesbrecht, 1893 [“1892”] genus Monothula, which is first recorded in the equatorial Genus Monothula Böttger-Schnack and Huys, 2001 Pacific Ocean. In this study, we redescribe both sexes of M. subtilis, Monothula subtilis (Giesbrecht, 1893 [“1892”]) based on the specimens from the equatorial Pacific Ocean (Figs. 1−5) and compare with previous descriptions from other Oncaea subtilis Giesbrecht, 1893 [“1892”], 593−599, localities, and discuss zoogeography of the species. We 603−604, 756, 774, plate 47, Figs. 14, 18, 25, 43 and 60 also provide information on the variation in endopodal (female); Malt, 1982, 129−130, 134−141, Figs. 6a−g, 7a− spine length of swimming legs 2 to 4 for both sexes. n, 8a−z and 9a−p; Heron and Frost, 2000, 1054−1055, Figs. 21F−K, 22A−J. 2. Materials and Methods Monothula subtilis Böttger-Schnack and Huys, 2001, 467−481, Figs. 1−5. Monothula subtilis was collected at KOMO (KODOS Long-term Monitoring Station; 10o30'N, 131o20'W) in the Material examined: Six females (NIBRIV0000812653− central part of the Clarion-Clipperton Fracture Zone of the 812658), each dissected and mounted on 7, 9, or 10 slides. northeast equatorial Pacific Ocean on 21 August 2009. Three males (NIBRIV0000812659−812661), each dissected Sampling was made by using a conical net with 60 µm and mounted on 6 or 9 slides. mesh (60 cm mouth diameter) by hauling vertically from All specimens collected from the northeast Pacific the depth of 100 m to the surface. Samples were initially Ocean (10o30'N, 131o20'W) on 21 August 2009. fixed in 99.9% ethyl alcohol on board. The specimens of At sampling station, surface temperature and salinities M. subtilis were sorted out from the collected zooplankton were 28.5oC and 33.5, respectively. Temperature decreased samples under a stereomicroscope (Stemi 2000-C, Zeiss) to 13.6oC at 100 m depth, while salinity remained at 34.6− in the laboratory. Specimens were dissected with tungsten 34.7. needles and mounted in lactophenol, and sealed with transparent nail-varnish. All drawings and measurements Female. Body length 558−613 μm (illustrated indiv.: were performed with the aid of a drawing tube attached to 593 μm, n = 6). a differential interference contrast microscope (BX51, Prosome length about 1.7 times to that of urosome; 1.5 Olympus). Scale bars were given in micrometers (μm). times to that including caudal rami. Second pedigerous Body length was measured from the anterior tip of somite without conspicuous dorso-posterior projection in prosome to the posterior end of caudal ramus in lateral lateral aspect (Fig. 1B). Integumental pores on prosome as view. Ratio of prosome to urosome (including caudal indicated in Fig. 1A, B. Fourth pedigerous somite with ramus) length was also calculated. Telescoping of somites rounded and prominent posterolateral corners (arrowed in was not considered in length measurements. The antenna, Fig. 1A). One pair of secretory pores discernible on lateral labrum, and maxilliped of female were examined with view of first and second postgenital somites, respectively scanning electron microscopy (S2380N, Hitachi). (Fig. 1B). Monothula subtilis in Equatorial Pacific 25

Fig. 1. Monothula subtilis (Giesbrecht, 1893 [“1892”]). Female (A) Habitus, dorsal; (B) Habitus, lateral; (C) P5-bear- ing somite and genital double-somite, ventral; (D) Caudal rami, left, ventral; (E) P6; (F) Antennule 26 Cho, K. and Kim, W.-S.

Fig. 2. Monothula subtilis (Giesbrecht, 1893 [“1892”]). Female (A) Antenna, anterior; (A') Endopod segments of antenna, posterior; (B) Oral area showing position of labrum, mandible, and maxillule, arrow indicating teeth on posterior part; (C) Mandible; (D) Maxillule; (E) Maxilla; (E') Maxilla, detail of allobasis; (F') Maxilliped, posterior; (G) Maxilliped, anterior Monothula subtilis in Equatorial Pacific 27

Genital double-somite about 1.4 times as long as Anterior surface (Fig. 2B) with paired rows of long maximum width in dorsal aspect and 4/5 length of setules either side of median swelling and paired slitlike postgenital somites combined; lateral margins rounded forms latero-posteriorly. Posterior part of medial incision (pot shaped), largest width measured at anterior one third, ornamented with 2 spinous teeth (arrowed in Fig. 2B). posterior part tapering gradually; paired genital apertures Posterior face with 3 secretory pores located distally on located at about 2/5 the distance from anterior margin of each lobe (dotted line as in Fig. 2B). genital double-somite (Fig. 1A). Pore pattern on dorsal Mandible (Fig. 2C) represented by flattened gnathobase surface as in Fig. 1A; ventral surface with several rows of with 5 elements. Outer stout seta (a) with long, fine minute spinules medially and laterally (Fig. 1C). setules along dorsal side: ventral blade (b) strong and Anal somite as long as wide and about as long as spiniform, with row of setules on posterior side; dorsal caudal rami (Fig. 1A). Anterior margin of anal opening blade (c) strong and broad, spinulose along entire dorsal (vestigial anal operculum) with line of minute spinules. margin and with few setules near ventral margin; 2 Posterior margin of somite finely serrate ventrally and posterior spinulose setae setiform, the shorter (d) unipinnate, laterally (Fig. 1B, D). longer (e) multipinnate. Caudal ramus (Fig. 1A) about 3 times longer than wide; Maxillule (Fig. 2D) faintly bilobed, surface ornamen- seta VI shorter than half length of seta IV; seta VII shorter tation not discernible. Inner lobe (praecoxal arthrite) with than seta IV, bare. Ornamentation on inner margin of 3 elements: outermost element spiniform and naked, tip somite not discernible. Dorsolateral surface (Fig. 1D) with with tubular extension; middle element setiform and secretory pore and minute spinules near insertion of seta unipinnate; innermost element smallest, located along II. concave inner margin close to other elements, unornamented Antennule 6-segmented (Fig. 1F). Armature formula: and with rounded tip. Outer lobe with 4 setiform elements; 1-[3], 2-[8], 3-[5], 4-[3+ae], 5-[2+ae], 6-[6+(l+ae)]. outermost element naked, shorter than the following; Antenna 3-segmented, distinctly reflexed (Fig. 2A). element next outermost longest, unipinnate, and with 2 Coxobasis with row of spinules along outer margin and long setules along inner margin; element next innermost few spinules on inner margin, minute denticle on proximal swollen at base, with long setules bilaterally; innermost part of outer (exopodal) margin; with long seta at inner seta naked. distal corner, ornamented with strong spinules bilaterally. Maxilla (Fig. 2E) 2-segmented. Syncoxa unarmed, with Endopod segments unequal in length. Proximal endopod one large secretory pore. Allobasis produced distally into segment elongate-oval, expanded outer margin bearing slightly curved claw bearing 2 rows of very strong spinular row; posterior surface with row of short, strong spinules along medial margin: spinules of inner row denticles along inner margin (Fig. 2A'). Distal endopod shorter, proximal group of 4 spinules on outer row longer segment over 4 times longer than wide, slightly longer (Fig. 2E'); outer margin with strong seta shorter than than proximal endopod segment, with narrow cylindrical allobasal claw, ornamented with long setules bilaterally; base articulating with proximal endopod segment; posterior inner margin with slender pinnate seta and strong basally surface with 2 rows of spinules of different length along swollen spine with 2 rows of long spinules along medial outer margin (Fig. 2A') and additional patch of setules margin, and 1 row of shorter spinules along outer margin. distally; lateral armature consisting of one long spiniform Maxilliped (Figs. 2F, G and 5C, D) 4-segmented. seta III with strong spinules bilaterally and 3 naked setae, Syncoxa unarmed, anterior surface ornamented with row with seta IV shortest; distal armature consisting of four of long spinules. Basis elongate, palmar margin with 2 spiniform setae A−D, ornamented with strong spinules long spiniform elements equal in length, proximal bilaterally, and 3 short naked setae E−G; seta E longer element ornamented with strong spinules bilaterally, distal than seta F (Fig. 2A), seta G shortest (Figs. 2A' and 5A). element bipinnate along inner margin; anterior surface Labrum (Figs. 2B and 5B) distinctly divided into 2 with 2 rows of strong spinules of varying length along rounded lobes with row of minute denticles or spinules palmar margin, few additional spinules on outer margin processes along inner margin and row of fine spinules at (Fig. 2G). Proximal endopod segment unarmed. Distal laterodistal margin. Distal (ventral) margin of each lobe endopod segment drawn out into long curved claw, with with 3 marginal teeth of different size medially (usually 1 pinnules along proximal 4/5 of concave margin, and row large and 2 small) (arrowed in Fig. 5B). Median concavity of denticle-like structure on posterior outer margin (Figs. covered anteriorly by overlapping rows of long spinules. 2F and 5D); accessory armature consisting of minute, 28 Cho, K. and Kim, W.-S.

Fig. 3. Monothula subtilis (Giesbrecht, 1893 [“1892”]). Female (A) P1, anterior; (B) P2, anterior; (C) P3, anterior; (D) P4, posterior. Male (E) P1, endopod-3, anterior; (F) P2, endopod-3, posterior; (G) P3, endopod-3, anterior; [arrows in (B)−(G) indicating pore on inner margin of endopod-3] Monothula subtilis in Equatorial Pacific 29 naked seta on outer proximal margin and unipectinate Male. Body length 405−518 μm (illustrated indiv.: 405 spine fused basally to inner proximal corner of claw. μm, n = 3). General features as in female (Fig. 4A, B). Swimming legs 1−4 biramous (Fig. 3A−D), with 3- Sexual dimorphism in antennule, maxilliped, P5, P6, segmented exopods and endopods, respectively, and with endopods of P1−P3, caudal ramus, and genital segmen- serrate, hyaline flanges on spines; intercoxal sclerites well tation. developed without ornamentation. Coxae and bases with Posterior margin of P5-bearing somite with paired row sparse surface ornamentation as figured. Bases with of denticles ventrally (arrowed in Fig. 4B). plumose (P1 and P4) or short naked (P2, P3) outer seta; Caudal rami about 1.9 times longer than wide, shorter inner margin in P1 and P2 with short spinule(s) (Fig. 3A, than in female. Caudal seta VII relatively longer than in B). Inner basal seta on P1 spiniform and minutely pinnate female: seta VII longer than seta IV (Fig. 4A'). Seta III (Fig. 3A). with weak transverse constriction at about midlength (Fig. Swimming leg armature formula (Roman numerals 4A'). Dorsal surface lacking spinular row near insertion of indicate spines, Arabic numeral indicate setae): seta II (Fig. 4A'). Dorsal surface of genital somite with pore pattern as in Leg Coxa Basis Exopod Endopod Fig. 4A. Surface of genital flaps ornamented with several PI 0-0 1-I I-0; I-1; III,I,4 0-1; 0-1; 0,I,5 rows of small spinules (Fig. 4D). P2 0-0 1-0 I-0; I-1; III,I,5 0-1; 0-2; 0,II,3 Antennule (Fig. 4C, C') 4-segmented; distal segment P3 0-0 1-0 I-0; I-1; II,I,5 0-1; 0-2; 0,II,2 corresponding to fused segments 4−6 of female. Armature P4 0-0 1-0 I-0; I-1; II,I,5 0-1; 0-2; 0,II,1 formula: 1-[3], 2-[8], 3-[4], 4-[1l+2ae+(l+ae)]. Maxilliped (Fig. 4E, F) 3-segmented, lacking small Exopods. Distal spine about equal in length to P2 or segment compared with that of female. Syncoxa with slightly longer than P1, P3, and P4 distal exopod segment. several rows of spinules on posterior surface, unarmed. Inner margin of proximal exopod segments with long Basis robust, moderately inflated in proximal half; setules. Secretory pore present on posterior surface of anterior surface with row of short spinules along palmar distal segments and small denticles on P1 and P2 exp-2 margin, developed into small distal flap, in addition to 2− (Fig. 3A, B). 3 transverse spinular rows (Fig. 4E); posterior surface Endopods. Posterior surface of distal endopod segments with 3 rows of short spinules of increasing length along with large secretory pore, located distally on P1 and palmar margin; with 2 minutely pinnate setae within subdistally at position of absent outer subdistal spine in longitudinal cleft, proximal seta almost 2 times longer P2−P4 (arrowed in Fig. 3B−D). Inner margin of P1 enp-2 than distal seta (Fig. 4F). Endopod drawn out into long ornamented with long spinules (Fig. 3A). P1 enp-3 curved claw, concave margin unornamented, showing ornamented with longitudinal row of denticles on anterior notch on inner margin; with short, unipectinate spine surface; outer margin terminating in long process obscuring fused to inner base of claw and small lamella at the end. insertion of distalmost inner seta. Distal margin of P2 and P1−P4 with armature as in female. Distal endopod P3 produced into conical process ornamented with apical spine of P1 (Fig. 3E) shorter than in female; outer pore. Inner setae of distal endopod segments in P1−P4 subdistal spines on distal endopod segment in P2−P3 (Fig. with spinule comb along proximal inner margin. Distal 3F, G) shorter than in female. Length ranges of outer spine on P4 slightly longer than distal segment. Length distal spine (ODS) relative to distal spine (DS) of three ranges of outer distal spine (ODS) relative to distal spine males are as follows: P2 enp-3 ODS: 48−57%; P3 enp-3 (DS) of six females are as follows: P2 enp-3 ODS: 40− ODS: 40−42%; P4 enp-3 ODS: 28−37%. 45%; P3 enp-3 ODS: 32−38%; P4 enp-3 ODS: 31−33%. P5 (Fig. 4G) exopod with general shape and armature P5 (Fig. 1C) with fused small segment, representing as in female, except for outer slender setae slightly longer exopod, and long unipinnate seta on somite. Exopod than spiniform inner seta; long seta arising from lateral about as long as wide, armed with stout spiniform seta, surface of somite ornamented with one denticle on distal and slender seta similar in length; posterior margin margin ornamented with minute spinules laterally (Fig. 1C). P6 (Fig. 4D) represented by posterolateral flap closing P6 (Fig. 1E) represented by operculum closing off each off genital aperture on either side; covered by pattern of genital aperture; armed with long spine and short spinule. denticles as in Fig. 4D; posterolateral corners protruding 30 Cho, K. and Kim, W.-S.

Fig. 4. Monothula subtilis (Giesbrecht, 1893 [“1892”]). Male (A) Habitus, dorsal; (A') Anal somite and caudal ramus; (B) Habitus, lateral, arrow indicating denticles; (C) Antennule; (C') Distal segment of antennule; (D) Urosome excepted P5-bearing somite, ventral; (E) Maxilliped, anterior; (F) Maxilliped, posterior; (G) P5 Monothula subtilis in Equatorial Pacific 31 laterally so that they are discernible in dorsal aspect (Fig. described “… distal armature comprising 5 curved, and a 4A). spine”. The distal spine on P4 enp-3 is slightly longer than the last segment on P4 and it is similar to the figures of Remarks Giesbrecht (1893, fig. 60), Malt (1982, fig. 7m) and Females of M. subtilis from the equatorial Pacific Heron and Frost (2000, fig. 22F), whereas it is almost the Ocean are similar to specimens described by Böttger- same as the last segment described by Böttger-Schnack Schnack and Huys (2001), except for the following and Huys (2001) in Red Sea specimens. characteristics: the setae E−G of distal armature on The proportional lengths of outer distal spine relative to antenna and the distal spine length on P4 enp-3. The seta the distal spine on P2−P4 enp-3 for female M. subtilis E on antenna is longer than seta F in the Pacific from the northeast Pacific Ocean (Heron and Frost 2000, specimens, whereas Böttger-Schnack and Huys (2001) fig. 22D−F) are in the range of variation determined in drawn them almost equally in length in Red Sea specimens. our specimens from the equatorial Pacific Ocean (Table In the figures of Giesbrecht (1893, fig. 18) and Heron and 1), except for the outer distal spine on P2 enp-3 (ODS:DS Frost (2002, fig. 21H), the seta E or F is almost as long as = 0.36:1), which is slightly lower than those of our setae A−D. The seta G of antenna in the Pacific specimens specimens (P2, ODS:DS = 0.40−0.45:1). Also, the values is much shorter than that described by Böttger-Schnack of ODS/DS ratios on P2 (ODS:DS = 0.36:1) and P4 and Huys (2001) (Fig. 5A). The length of seta G is similar (ODS:DS = 0.25:1) in illustrations provided by Malt to that of the seta IV on antenna. In general, the seta G (1982, fig. 7k, m) are lower than those reported for overlaps with setae A−D, thus it is difficult to be specimens from the equatorial Pacific Ocean (P4, recognized. Because of these, Malt (1892, p136) seemed ODS:DS = 0.31−0.33:1). In the case of male from the to miss one of the setae in the figure of antenna and equatorial Pacific Ocean, the values of the spine length

Fig. 5. Monothula subtilis (Giesbrecht, 1893 [“1892”]). Female (A) Distal part of Antenna, posterior, arrow indicating seta G; (B) Labrum, arrows indication teeth; (C) Maxilliped, arrow indicating ornamentation on claw; (D) Claw of Maxilliped, posterior, showing ornamentation along outer margin 32 Cho, K. and Kim, W.-S. ratios on P2−P4 enp-3 are slightly higher than those of almost as long as conical process, showed a striking female (Table 1). By contrast, the range of males from the difference from female’s. The Pacific specimens evidently Red Sea is lower than that of females (calculated by manifested in the outer distal spine on P3 enp-3, being Böttger-Schnack and Huys 2001, figs. 3B−D and 5C, D). slightly beyond the tip of the conical process. Gallo The spine length ratios on P2−P4 of females in Oncaeidae (1976) portrayed the male of Monothula including P1−P4 show that the range of females is wide and the value is (Razouls et al. 2005−2017). In Gallo’s illustration, conical high, as compared with males (Cho et al. 2017a, 2017b). processes on P2−P3 enp-3 are much shorter than the In the case of males of M. subtilis, the range and value of lengths of outer distal spine. To ensure accuracy of the ratios are higher than those of females (Table 1). length ratio of the spine to conical process in male, The body sizes of our specimens (females 558−613 μm, observations with specimens from various areas are still males 405−518 μm) are larger than those of the Red Sea necessary. specimens (Böttger-Schnack and Huys 2001, females 440−520 μm, males 340−380 μm). The body sizes of M. 4. Discussion subtilis reported in other areas are as follows: 460−690 μm in females and 380−440 μm in males from north The coarse nets of mesh size over 200 μm were widely Atlantic Ocean (the mouth of the English Channel) by used for zooplankton collection in most marine field Malt (1982); 450−660 μm in females and 450−600 μm in surveys. But recent studies suggested that the abundance males from the Mediterranean and the Adriatic Seas by and species composition of zooplankton were affected by Malt et al. (1989, Table IV); 520−630 μm in females and plankton nets of different mesh sizes (Hopcroft et al. 390−460 μm in males from the northeast Pacific Ocean by 2001; Hwang et al. 2007; Wu et al. 2011; Makabe et al. Heron and Frost (2000). It is well known that the size 2012). According to Hopcroft et al. (2001), small copepods variation according to regions is common in oncaeid with prosome lengths less than 450 μm were collected species. successfully by fine mesh nets (64 μm), and those with Sexual dimorphism of male was observed in the 450−1400 μm prosome lengths by coarse mesh nets endopodal spine length, as well as in body size. In males (200 μm). Miyashita et al. (2009) reported the efficiency of the Pacific specimens, the distal spine on P1 enp-3 and of the mesh size (64 or 300 μm). The 64 μm net captured the outer distal spines of P2 and P3 enp-3 are shorter than small-sized oncaeid copepods such as M. subtilis and those in female of the Red Sea specimens. But in male Oncaea waldemari which were absent or under-represented from the Red Sea, the length of outer distal spines, being in the 300 μm net samples.

Table 1. Comparison of morphological characters for both sexes of Monothula subtilis (Giesbrecht, 1893 [“1892”]) from the equatorial Pacific Ocean with specimens from other regions. Abbreviations: A2 = antenna; CR = caudal ramus; DS = distal spine; L = length; ODS = outer distal spine Gulf of Northeast Equatorial Pacific Red sea Atlantic Northeast Pacific Naples Atlantic Böttger-Schnack and Giesbrecht Gallo Heron and Frost This present study Malt 1982 Huys 2001 1893 1976 2000 Female Male Female Male Female Male Female Male Female Male Size range (mm) 558-613 405-518 450-520 340-380 480-500 460-690 380-440 520-630 390-460 L ratio spines ODS:DS 0.40-0.45 0.48-0.57 0.48* 0.40* 0.28* 0.36* 0.36* P2 enp-3 L ratio spines ODS:DS 0.32-0.36 0.40-0.42 0.42* 0.33* 0.26* 0.36* 0.39* P3 enp-3 L ratio spines ODS:DS 0.31-0.33 0.28-0.37 0.33* 0.30* 0.27* 0.25* 0.32* P4 enp-3 L ratio P4 DS:enp-3 longer longer equal longer shorter longer longer A2 L of setae E: F longer about equal unequal† longer unequal† L of setae G: IV about equal longer about equal - longer CR L of IV:VII longer slightly slightly longer longer longer shorter *calculated from reference papers’ figures †one of setae E and F is much longer and almost reached setae A−D lengths Monothula subtilis in Equatorial Pacific 33

Kang et al. (2004, 2007, 2008) collected zooplankton for ecological research purposes with regard to species by the 300 μm mesh net in the equatorial Pacific Ocean diversity, variation of characteristics, and indicator species and they classified oncaeid copepods at the genus level of various environments. such as “Oncaea spp.” due to lack of taxonomical Monothula subtilis is predominant in the epipelagic information. Through further taxonomic analysis of zone (Böttger-Schnack 1995; Kršinić and Grbec 2002). species composition, however, four species such as Thus it is generally regarded as an epipelagic species Oncaea media, Oncaea mediterranea, , (Malt 1983). We have no data of its vertical distribution and Triconia conifera (noted as Oncaea conifera) were pattern through whole water column, because vertical identified in this area (MOMAF 2008). Then the oncaeid towing of the net from the depth of 100 m to the surface species of various sizes (body length > 300 μm) were was used to collect the zooplankton sample. This species, sampled by using a 60 μm mesh net and identified many however, was found at the 450−1050 m depth in the undescribed species and unrecorded species in four genera central Arabian Sea and much deeper bathypelagic zone of oncaeid copepods such as Monothula, Oncaea, (1050−1850 m) in the Arabian Sea off Oman (Böttger- Spinoncaea, and Triconia (Cho 2011). During the Schnack 1996). Accordingly, the spatial distribution of the taxonomic study, both sexes of two large species of the species is not confined in the epipelagic zone, but can be conifera-subgroup, Triconia derivata and Triconia hirsuta, widespread in the whole water column. Moreover the were found. Particularly, T. hirsuta was described in this relative importance of Oncaeidae, the Family which area for the first time together with its hitherto unknown Monothula belongs to, comparing with other copepods male of the species (Cho et al. 2017b). Also, in the has been found to increase strongly with increasing depth, dentipes-subgroup, new species Triconia pacifica, and especially in meso- and bathypelagic zones (Böttger- new variant forms of Triconia giesbrechti and Triconia Schnack 1994). The structure of the midwater zooplankton elongata were reported (Cho et al. 2013). Even though communities in the equatorial Pacific Ocean has so far many species of oncaeid copepod have been found in the remained unknown. Therefore, further studies of the equatorial Pacific Ocean, there is still unknown species of oncaeid community in deep water layer of the equatorial atlantica-vodjanitskii-group and tregoubovi-group (Cho Pacific Ocean need to be conducted. 2011). Malt (1983) reported the wide distribution of M. subtilis Acknowledgement between 65oN and 40oS (see 1983: p9 for distribution). This species has been reported from a wide range of We thank two anonymous referees for the constructive localities such as the Red Sea, the east Mediterranean Sea, comments that improved the quality of this manuscript. the Arabian Sea, and the east Indian Ocean (Giesbrecht This research was supported by the Ministry of Oceans 1893; Böttger-Schnack 1994, 1995, 1996; Böttger-Schnack and Fisheries of Korea (PM59941). and Huys 2001; Kršinić and Grbec 2002; Kršinić et al. 2007), the Black Sea (Gubanova et al. 2014), near the References Atlantic coast (Malt 1982; Rawlison et al. 2005; Miyashota et al. 2009), and the northeast Pacific coast (Heron and Böttger-Schnack R (1994) The microcopepod fauna in the Frost 2000). The occurrence of M. subtilis was well Eastern Mediterranean and Arabian Seas: a comparison summarized in the world ocean map in the web site with the Red Sea fauna. Hydrobiologia 292/293:271−282 (Razouls et al. 2005−2017, for details see “Location” on Böttger-Schnack R (1995) Summer distribution of micro- Monothula subtilis in Diversity and Geographic Distribution and small meso-zooplankton in the Red Sea and Gulf of of Marine Planktonic Copepods on the web site http:// Aden, with special reference to non-calanoid copepods. copepodes.obs-banyuls.fr/en) including above mentioned Mar Eco-Prog Ser 118:81−102 records and those from various other studies. Although Böttger-Schnack R (1996) Vertical structure of small Böttger-Schnack and Huys pointed out, M. subtilis tends metazoan plankton, especially non-calanoid copepods. I. to occur in tropical and subtemperate regions (Böttger- Deep Arabian Sea. J Plankton Res 18:1073−1101 Schnack and Huys 2001), it did not occur in the equatorial Böttger-Schnack R (1999) Taxonomy of Oncaeidae (Copepoda, Pacific Ocean of the map. In present study, we first report ) from the Red Sea. - I. 11 species of the occurrence of M. subtilis in the equatorial Pacific Triconia gen. nov. and a redescription of T. similis (Sars) Ocean. The results can be used as more reliable information from Norwegian waters. Mitt hamb zool Mus Inst 34 Cho, K. and Kim, W.-S.

96:37−128 based on their first records in the tropical Pacific. Böttger-Schnack R (2002) Taxonomy of Oncaeidae (Copepoda, Korean J Environ Biol 35:64−82 Poecilostomatoida) from the Red Sea. VI. Morphology Giesbrecht W (1893) Systematik und Faunistik der pelagischen and zoogeography of Oncaea bispinosa sp. nov., a sister Copepoden des Golfes von Neapel und der angrenzenden taxon of O. zernovi Shmeleva. J Plankton Res 24:1107− Meeres-Abschnitte. Fauna Flora Golf. Neapel, 19:1−831 1129 Gubanova A, Altukhov D, Stefanova F, Arashkevich E, Böttger-Schnack R (2003) Taxonomy of Oncaeidae (Copepoda, Kamburska L, Prusova I, Svetlichny L, Timofte F, Uysal Poecilostomatoida) from the Red Sea. V. Three species Z (2014) Species composition of Black Sea marine of Spinoncaea gen. nov. (ivlevi-group), with notes on planktonic copepods. J Mar Sys 135:44−52 zoogeographical distribution. Zoological J Linnean Heron GA (1977) Twenty-six species of Oncaeidae (Copepoda: Society 137:187−226 Cyclopoida) from the southwest Pacific-Antarctic area Böttger-Schnack R (2004) Triconia parasimilis Böttger- (Biology of the Antarctic Seas VI). Antarct Res Ser Schnack,1999 (Copepoda, Oncaeidae), first record from 26:37−96 the NW Pacific (Oyashio), with the description of the Heron GA, English TS, Damkaer DM (1984) Arctic Ocean male. Mitt Hamb zool mus Inst 101:213−223 Copepoda of the genera Lubbockia, Oncaea, and Böttger-Schnack R (2005) Taxonomy of Oncaeidae (Copepoda: Epicalymma (Poecilostomatoida: Oncaeidae), with remarks Cyclopoida) from the Red Sea. VII. Oncaea cristata, a on distributions. J Crust Biol 4:448−490 new species related to the ovalis-complex, and a revision Heron GA, Frost BW (2000) Copepods of the family of O. ovalis Shmeleva and O. bathyalis Shmeleva from Oncaeidae (Crustacea: Poecilostomatoida) in the northeast the Mediterranean. Cah Biol Mar 46:161−209 Pacific Ocean and inland coastal waters of Washington Böttger-Schnack R (2009) Taxonomy of Oncaeidae (Copepoda, State. Proc Biol Soc Wash 113:1015−1063 Cyclopoida s.l.) from the Red Sea. IX. Epicalymma Hopcroft RR, Roff JC, Chavez FP (2001) Size paradigms in bulbosa sp. nov., first record of the genus in the Red copepod communities: a re-examination. Hydrobiologia Sea. J Plankton Res 31:1027−1043 453/454:133−141 Böttger-Schnack R, Huys R (2001) Taxonomy of Oncaeidae Huys R, Gee JM, Moore CG, Hamond R (1996) Marine and (Copepoda, Poecilostomatoida) from the Red Sea. III. brackish water harpacticoid copepods, Part 1. Field Morphological and phylogenetic position of Oncaea Studies Council, Shropshire, 352 p subtilis Gesbrecht, 1892. Hydrobiologia 453/454:467− Hwang JS, Kumar R, Dahms HU, Tseng LC, Chen QC 481 (2007) Mesh size affects abundance estimates of Oithona Chen QC, Zhang SZ, Zhu CS (1974) On planktonic spp. (Copepoda, Cyclopoida). Crustaceana 80:827−837 copepods of the Yellow Sea and the East China Sea. 2. Itoh H (1997) Family Oncaeidae. In M Chihara, M Murano, Cyclopoida and Harpacticoida. Stud Mar Sinica 9:27− editors. An illustrated guide to marine plankton in Japan. 100 (in Chinese) Tokai University Press, Tokyo, pp 978−988 (in Japanese) Cho K (2011) Study on the taxonomy of family Oncaeidae Kang JH, Cho KH, Son JW, Kim WS (2007) Longitudinal (Copepoda, Cyclopoida) from the CCFZ (Clarion-Clipperton distribution of zooplankton at 10.5oN in the Northeastern Fracture Zone; C-C zone) in the Northeast Equatorial Pacific. Ocean Polar Res 29:283−295 Pacific. Ph.D. Thesis, Hanyang University, Seoul, 274 p Kang JH, Kim WS, Chang KI (2008) Latitudinal distribution Cho KH, Böttger-Schnack R, Kim WS, Lee WC (2017b) of mesozooplankton in the off-equatorial northeastern Two species of the conifera-subgroup of Triconia Pacific before and after the 1998/99 La Niña event. Mar (Copepoda, Oncaeidae) from the northeastern equatorial Environ Res 65:218−234 Pacific, with a description of the unknown male of T. Kang JH, Kim WS, Son SK (2004) Latitudinal differences hirsuta. Zootaxa 4286:347−369 in the distribution of mesozooplankton in the Northeastern Cho KH, Kim WS, Böttger-Schnack R, Lee WC (2013) A Equatorial Pacific. Ocean Polar Res 26:351−360 new species of the dentipes-subgroup of Triconia and a Kršinić F, Bojanić D, Precali R, Kraus R (2007) Quantitative redescription of T. giesbrechti and T. elongata (Copepoda: variability of the copepod assemblages in the northern Cyclopoida: Oncaeidae) from the tropical Pacific and the Adriatic Sea from 1993 to 1997. Estuar Coast Shelf S Korea Strait. J Nat Hist 47:1707−1743 74:528−538 Cho KH, Kim WS, Lee WC (2017a) Redescription of two Kršinić F, Grbec B (2002) Some distributional characteristics species of Triconia (Copepoda, Cyclopoida, Oncaeidae) of small zooplankton at two stations in the Otranto Strait Monothula subtilis in Equatorial Pacific 35

(Eastern Mediterranean). Hydrobiologia 482:119−136 adjacent coast. Estuar Coast Shelf S 62:205−215 Kršinić F, Malt SJ (1985) Little known species of small Razouls C, de Bovée F, Kouwenberg J, Desreumaux N Oncaeidae (Cyclopoida) from the South Adriatic. J (2005−2017) Diversity and geographic distribution of Plankton Res 7:189−199 marine planktonic copepods. Monothula subtilis (Giesbrecht, Makabe R, Tanimura A, Fukuchi M (2012) Comparison of (1893 [“1892”]). http://copepodes.obs-banyuls.fr/en/fichesp. mesh size effects on mesozooplankton collection efficiency php?sp=2108 Accessed 18 Aus 2017 in the Southern Ocean. J Plankton Res 34:432−436 Roman MR, Dam HG, Gauzens AL, Urban-Rich J, Foley Malt SJ (1982) New and little known species of Oncaeidae DG, Dickey TD (1995) Zooplankton variability on the o (Cyclopoida) from the Northeastern Atlantic. Bull Br equator at 140 W during the JGOFS EqPac study. Deep- Mus Nat Hist (Zool) 42:185−205 Sea Res II 42:673−693 Malt SJ (1983) Copepoda, Oncaea. Fich Ident Zooplnakton Wi JH, Böttger-Schnack R, Soh HY (2012) Two new 169/170/171:1−11 species belong to the dentipes- and conifera-subgroups Malt SJ, Lakkis S, Ziedane R (1989) The copepod genus of Triconia (Copepoda: Cyclopoida: Oncaeidae) from the Oncaea (Poecilostomatoidea) from the Labanon: taxonomic East China Sea. J. Crust Biol 32:843−859 and ecological observations. J Plankton Res 11:949−969 Wi JH, Shin KS, Soh HY (2011) The similis-subgroup McKinnon AD, Duggan S, Böttger-Schnack R, Gusmāo within Triconia (Copepoda: Cyclopoida: Oncaeidae) from LFM, O’Leary RA (2013) Depth structuring of pelagic Korean waters. Zool Stud 50:588−604 copepod biodiversity in waters adjacent to an Eastern Wi JH, Yoon YH, Soh HY (2009) Five Oncaea species Indian Ocean coral reef. J Nat Hist 47:639−665 (Copepoda, Poecilostomatoida, Oncaeidae) from the Miyashita LA, Melo Júnior M, Lopes RM (2009) Estuarine Korean waters, with notes on the spation-temporal dis- and oceanic influences on copepod abundance and tribution of Korean oncaeid species. Ocean Sci J 44:95− production of a subtropical coastal area. J Plankton Res 115 31:815−826 Wu CJ, Shin CM, Chiang KP (2011) Does the mesh size of MOMAF (2008) A report on 2007 Deep sea bed mineral the plankton net affect the result of statistical analyses of resources exploration. CRPM 44000-1936-5. Ministry of the relationship between the copepod community and Maritime Affairs and Fisheres, Seoul, 755 p water masses? Crustaceana 84:1069−1083 MOMAF (2009) A report on 2008 Deep sea bed mineral resources exploration. CRPM 51101-2042-5. Ministry of Received Sep. 26, 2017 Maritime Affairs and Fisheres, Seoul, 596 p Revised Dec. 8, 2017 Rawlinsona KA, Davenporta J, Barnes DKA (2005) Tidal Accepted Jan. 9, 2018 exchange of zooplankton between Lough Hyne and the