Parastenocaris biwae Miura, 1969

Karanovic, Tomislav & Lee, Wonchoel, 2012, A new species of Parastenocaris from Korea, with a redescription of the closely related P. biwae from Japan (Copepoda: Harpacticoida: Parastenocarididae), Journal of Species Research 1 (1), pp. 4-34 : 8-16

Parastenocaris biwae Miura, 1969

( Figs. 1-3 )

Synonymy. Parastenocaris biwae Miura, 1969, p. 40 , fig. 1-15; Dussart and Defaye, 1990, p. 254.

Parastenocaris brevipes Kessler, 1913 : Reid, 1995, p. 177, fig. 2i.

Type locality. Japan, Shiga Prefecture, Lake Biwa, western shore, Shirahige , sandy beach .

Specimens examined. Two males (NIBRIV0000232643 and NIBRIV0000232644) and one female (NIBRIV0000 232645), each dissected on one slide; Japan, Shiga Prefecture, Lake Biwa drainage area, confluence of Seto and Daido rivers, sandy/gravely beach, 27 September 2009, leg. T. Karanovic .

Redescription. Male (based on two newly collected specimens): Total body length, measured from tip of rostrum to posterior margin of caudal rami (excluding caudal setae), from 600 to 612 µm. Preserved specimen colourless. Nauplius eye absent. Body composed of prosome (consisting of cephalothorax and three free pedigerous somites (first pedigerous fused to cephalothorax)), and urosome (consisting of fifth pedigerous somite, genital somite, four abdominal somites, and caudal rami). Podoplean boundary between prosome and urosome inconspicuous. Habitus ( Fig. 1A ) cylindrical and very slender, without any demarcation between prosome and urosome; prosome/urosome ratio about 0.8 in dorsal view; greatest width in dorsal view at posterior end of cephalothorax but hard to establish (fourth pedigerous somites only slightly narrower); free prosomal somites in lateral view as wide as cephalothorax or urosome. Body length/width ratio about 9.1; cephalothorax 1.1 times as wide as genital somite. Free pedigerous somites without any lateral or dorsal expansions, all connected by well developed arthrodial membranes. Hyaline fringes of all somites smooth, very narrow and hard to distinguish from arthroidal membranes, especially dorsally, except in preanal somite, where hyaline fringe well developed ( Fig. 1A ). Integument weakly sclerotized, smooth but covered with shallow pits on all somites and caudal rami, ornamented only with sensilla and pores (no spinules, except on posterior margin of caudal rami ventrally), with round dorsal double cuticular window on cephalothorax, trapezoidal simple dorsal cuticular window on genital, and elongated simple dorsal windows on three postgenital somites ( Fig. 1A ). Pleural areas of cephalothorax and free pedigerous somites not well developed, cephalic appendages and coxae of swimming legs clearly exposed in lateral view.

Rostrum ( Fig. 1A ) small, membranous, not demarcated at base, ornamented with two large dorsal sensilla (No. 1), linguiform but with pointed tip, hardly reaching distal margin of first antennular segment, about as long as wide.

Cephalothorax ( Fig. 1A, C ) about 1.8 times as long as wide in dorsal view; representing 20% of total body length. Surface of cephalic shield ornamented with 16 pairs of large sensilla; with a dense pattern of cuticular pits of different sizes; five pairs of sensilla surround double cuticular window, but its surface completely smooth; pairs of sensilla Nos. 12-16 belong to first pedigerous somite incorporated into cephalothorax. Athroidal membrane between cephalothorax and second pedigerous somite (first free) wider than between any other somites.

Second pedigerous somite ( Fig. 1A ) slightly narrower than posterior half of cephalothorax in dorsal view, with four pairs of large sensilla (three dorsal and one lateral; Nos. 17-20; note lateral pair of sensilla No. 20 not visible in Fig. 1A ), and with unpaired dorsal pore in anterior half. Postero-dorsal pair of sensilla (No. 18) serially homologous to pair No. 13 on first pedigerous somite, but for other pairs serial homology not that obvious.

Third pedigerous somite ( Fig. 1A ) slightly wider and shorter than second pedigerous, with four pairs of large sensilla (Nos. 21-24), also with unpaired dorsal pore; all sensilla serially homologous to those on second pedigerous somite (i.e. pairs Nos. 17 and 21, Nos. 18 and 22, Nos. 19 and 23, and Nos. 20 and 24); serial homology of dorsal cuticular pores between these two somites not that clear.

Fourth pedigerous somite ( Fig. 1A ) widest and longest free prosomal somite in dorsal view, with only three pairs of large posterior sensilla (two dorsal and one lateral; Nos. 25-27), with arched sutures in anterior part dorsally and unpaired cuticular pore in between them. Serial homology of sensilla between third and fourth pedigerous somites not that clear, except for lateral pairs (Nos. 24 and 27).

First urosomite (=fifth pedigerous somite) ( Fig. 1A ) slightly narrower and shorter than fourth pedigerous somite, also with three pairs of large posterior sensilla (Nos. 28-30), without arched dorsal sutures or cuticular pores. All three pairs of sensilla serially homologous to those on fourth pedigerous somite (i.e. Nos. 25 and 28, Nos. 26 and 29, and Nos. 27 and 30; note: lateral pair of sensilla No. 30 not visible in dorsal view in Fig. 1A ).

Second urosomite (=genital somite) ( Fig. 1A, D ) slightly narrower and longer than first urosomite, about 1.2 times as wide as long in ventral view, with trapezoidal small cuticular window in anterior half, also with three pairs of posterior sensilla (Nos. 31-33), but dorsal pair (No. 31) closer to each other than in first urosomite; single longitudinally placed spermatophore inside longer than somite. Dorsal pair of sensilla (No. 31) probably serially homologous to that on first urosomite (No. 28), but other two pairs probably not serially homologous.

Third urosomite ( Figs. 1A ) about as long as second urosomite but slightly narrower, with shorter but much wider dorsal cuticular window, and with three pairs of large posterior sensilla (Nos. 34-36). All sensilla probably serially homologous to those on second urosomite, but dorsal pair (No. 34) more widely spaced.

Fourth urosomite ( Fig. 1A ) with slightly larger dorsal cuticular window, but similar size and same ornamentation, consisting of also three pairs of large posterior sensilla (Nos. 37-39). All sensilla serially homologous to those on third usoromite, but dorsal pair (No. 37) slightly closer to each other.

Fifth urosomite (=preanal somite) ( Fig. 1A ) slightly narrower and longer than fourth urosomite, with largest dorsal cuticular window of all urosomites, and without any surface ornamentation; hyaline fringe well defined on all sides.

Sixth urosomite (=anal somite) ( Figs. 1A, B ) about 1.5 times as long as and 0.9 times as wide as preanal somite, ornamented with pair of large dorsal sensilla at base of anal operculum (No. 40), pair of large lateral cuticular pores in anterior half, and pair of ventral pores at base of caudal rami (no spinules on ventral surface), in addition to numerous shallow cuticular pits. Anal operculum well developed, unornamented on outer surface, with smooth and convex distal margin, not reaching posterior end of anal somite, representing 53% of somite’s width. Anal sinus wide opened, ornamented with two long diagonal rows of slender spinules on ventral side, and one additional row on dorsal side (inner side of anal operculum).

Spermatophore ( Figs. 1D , 2 ) about 2.3 times as long as wide, kidney-shaped, with long and narrow, curved neck.

Caudal rami ( Fig. 1A, B ) slender, about 3.2 times as long as greatest width (ventral view) and about 0.7 times as long as anal somite, cylindrical but tapering towards posterior end, slightly divergent, with space between them about 1.5 times of one ramus width; armed with seven elements (three lateral, one dorsal, and three apical). Ornamentation consists of large lateral cuticular pore at about 2/3 of ramus length, and posterior ventral row of several spinules along posterior margin. Dorsal seta slender and smooth, inserted closer to inner margin at midlength, about 0.8 times as long as caudal ramus, triarticulate basally (inserted on two pseudo-joints). Lateral setae slender and smooth, inserted very close to each other also at midlength, two larger ones more anteriorly and minute one in between and more posteriorly. Anterior lateral seta which inserted more dorsally longest, half as long as ramus, 2.3 times as long as ventral anterior seta, and about five times as long as minute (distal) seta. Inner apical seta smooth, inserted close to ventral margin, about 0.8 times as long as ramus. Middle apical seta strongest, without breaking plane, smooth, about 4.7 times as long as ramus, pointing posteriorly, with slightly curled tip inwardly. Outer apical seta also without breaking plane and smooth, relatively strong basally but much shorter, about 0.9 times as long as ramus, inserted close to dorsal surface and pointing latero-posteriorly.

Antennula ( Fig. 1E ) shorter than cephalothorax, slender, eight-segmented, prehensile and strongly digeniculate, ornamented with six ventral spinules on first segment distally, and with ribbed elongated chitinous plate on anterior surface of sixth segment. First segment very short, while second longest. Geniculation between third and fourth and between sixth and seventh segments; last two segments at 90̊angle. Distal anterior corner of seventh segment produced into very small spiniform process, but larger proximal spiniform process present on fifth segment on anterior surface. Long aesthetasc on fifth segment reaching beyond tip of appendage for length of last segment, fused basally to slightly longer seta, relatively slender and blunt distally; much shorter and more slender apical aesthetasc on seventh segment, fused basally to two setae (acrotheck). Setal formula: 0.6.4.2.4.0.1.9. All setae slender and all, except largest seta on second segment, smooth; most setae with pore on tip; proximalmost seta on second segment unipinnate with several long spinules along anterior surface, much shorter than two large setae on fifth segment or longest apical seta on eighth segment (latter probably longest); only seta on eighth segment minute.

Antenna ( Fig. 1F ) relatively stout and short, composed of coxa, allobasis, one-segmented endopod, and one-segmented exopod. Coxa very short, unarmed, ornamented with three short spinules. Allobasis about three times as long as wide, unarmed but ornamented with two rows of large spinules on anterior surface. Endopod 0.8 times as long as allobasis and nearly three times as long as wide, with two parallel surface frills subdistally, ornamented with large spinules along anterior surface, armed laterally with two short spines (proximal one shorter) and apically with five strong elements (two geniculate). Exopod minute, cylindrical, about twice as long as wide, unornamented but armed with single apical seta, which three times as long as segment. All antennal armature unipinnate.

Labrum large and triangular in lateral view, with narrow and straight cutting edge, without any ornamentation on anterior surface, with several parallel rows of spinules along cutting edge (those on outer distal corners strongest).

Paragnaths strongly fused into trilobite structure, with numerous distal rows of slender short spinules on lateral lobes, one distal row of minute spinules on central lobe, and another transverse row of 10 very long spinules on posterior surface of central lobe at about 2/3 of its length.

Mandibula with narrow cutting edge on elongated coxa, armed with one complex tooth ventrally, one unipinnate seta dorsally, and several smaller teeth and/or spinules in between. Palp one-segmented, cylindrical, about 2.5 times as long as wide, unornamented, and armed apically with two smooth and subequal setae, each with pore on tip.

Maxillula with relatively large praecoxa, arthrite rectangular, about 1.5 times as long as wide from lateral view, ornamented with single spinule on posterior surface near dorsal margin, armed with lateral strong seta and four apical elements (probably three spines and one strong seta; apical spines with crown of spinules on tip, resembling small hands). Coxal endite armed with one smooth seta apically. Basis slightly longer than coxal endite, armed with three apical setae (two smooth and slender, one curved and unipinnate), and single minute lateral seta. Endopod and exopod absent (fused to basis without trace), minute seta on basis probably representing remnants of exopodal armature. All coxal and basal setae, as well as smooth lateral seta on praecoxa, with pore on tip.

Maxilla composed of syncoxa, basis, and one-segmented endopod, ornamented with row of five spinules on inner side of syncoxa proximally, and with arched row of six spinules on posterior side of syncoxa close to outer margin. Syncoxa with two endites, basal armed with single smooth seta apically, distal armed with two smooth and one pinnate seta apically. Basis drawn out into strong and unipinnate claw, without seta at base, with cuticular pore on convex margin near distal tip. Endopod represented by minute segment, armed with two smooth subequal apical setae. All setae on maxilla with pore on tip.

Maxilliped with short and relatively strong syncoxa, unarmed and unornamented; basis slender, almost five times as long as wide and three times as long as syncoxa, unornamented and unarmed; endopod represented by short curved claw, swollen at base as indication of ancestral one-segmented endopod, ornamented with several strong spinules along concave margin distally, about 0.7 times as long as basis.

First swimming leg ( Fig. 2A ) with unarmed praecoxa, coxa, and intercoxal sclerite. Intercoxal sclerite very small, with narrow and concave distal margin and smooth. Praecoxa ornamented with several rows of minute spinules on anterior surface. Coxa with posterior row of large spinules on posterior surface and close to outer margin. Basis somewhat shorter than coxa, pentagonal, ornamented with bunch of large spinules on outer margin, another bunch along distal margin at base of endopod, and several long spinules on inner margin proximally; armed with single short seta on outer margin. Exopod three-segmented, armed with one outer spine on first segment and four elements on third segment (two outer spines and two apical geniculate setae); ornamented with few large spinules along outer margin and distally on all segments. Endopod two-segmented, about as long as exopod; first segment reaching slightly beyond distal margin of second exopodal segment, about four times as long as wide, unarmed, ornamented with two short rows of large spinules on outer margin, one longer row of even longer spinules on inner margin, and three spinules on anterior surface along distal margin; second segment armed apically with long geniculate seta and much shorter spine; endopodal geniculate seta 1.5 times as long as entire endopod, 1.2 times as long as larger geniculate exopodal seta, and almost 2.4 times as long as outer spine on endopod. All exopodal and endopodal armature unipinate along outer margin. Endopod on one leg in one male deformed ( Fig. 2A ), all others normal.

Second swimming leg ( Fig. 2B ) with smooth praecoxa and intercoxal sclerite. Intercoxal sclerite large, trapezoidal, with deeply concave distal margin. Praecoxa triangular and large. Coxa short, rhomboidal, with diagonal row of small spinules on anterior surface and two shorter rows of spinules along distal margin on posterior surface. Basis larger than coxa, semicircular, unarmed, ornamented with row of spinules on outer margin and another arched row of spinules at base of endopod. Exopod three -segmented, ornamented with large spinules along outer margin, and with distal hyaline frills on each segment on inner side; first segment armed with single outer spine; second segment unarmed; third segment armed with three long elements (probably outer spine and two apical setae), innermost one 1.55 times as longer as entire exopod; all exopodal armature bipinnate. Endopod one-segmented, cylindrical and slender, 5.3 times as long as wide, reaching 3/4 of first exopodal segment in length, ornamented with four large spinules along apical margin; armed apically with single smooth seta, which about 0.9 times as long as segment and pointing inwards.

Third swimming leg ( Fig. 2 C-E) with smooth intercoxal sclerite, which largest of all legs, trapezoidal, and with short and concave distal margin. Praecoxa not well defined on anterior surface, triangular on posterior surface, about as large as in second leg, unarmed, and unornamented. Coxa rectangular, with arched row of large spinules on anterior surface, and two rows of spinules along posterior margin on posterior surface (outer minute). Basis robust, ornamented with long row of large spinules and one pore on anterior surface, armed with outer long and slender seta; distal inner corner of basis produced distally as bulbous soft semicircular lobe, partly shielding endopod. Endopod represented with single smooth and minute armature element, inserted on inner margin at 3/4 of basis length, shorter but stronger than spinules on anterior surface. Exopod with both segments fused; ancestral proximal segment 2.5 times as long as wide, curved inwards and with thin hyaline lamella along inner margin, and three strong and short chitinous beaks on posterior surface, ornamented with two or three minute spinules on distal outer corner; armed subapically with simple, strong, smooth and inwardly curved spine, which about as long as apophysis and more or less flat distally; ancestral distal segment (apophysis) cylindrical, oriented slightly inwards, ornamented with single pore on anterior surface; armed with single short element on top, which leaf-like, with very thin cuticulum, more or less ovoid.

Fourth swimming leg ( Fig. 2F ) with smooth praecoxa and intercoxal sclerite. Intercoxal sclerite shorter and smaller than in third, with equally long and concave distal margin. Praecoxa small and triangular. Coxa rhomboidal, slightly larger than in second leg, unarmed, ornamented with short distal row of minute spinules on posterior surface. Basis large and more or less rectangular, armed with single smooth outer seta, ornamented with two minute spinules on outer margin at base of outer seta, and with three huge chitinous spiniform process on inner distal corner; anterior process bilobate distally and very wide; inner process spiniform and curved outward, longest; posterior process shortest but most strongly chitinized. Exopod three-segmented, ornamented with few large spinules along outer margin on all segments, and with hyaline frills distally on inner side; first segment with strongly concave and smooth inner margin, armed with single outer spine; second segment unarmed; third segment armed with outer spine and long and strong apical seta; apical seta 1.2 times as long as entire exopod, and more than twice as long as outer spine. Endopod one-segmented, about as strong but longer than first exopodal segment, cylindrical proximally and bilobate distally, with inner lobe longer and stronger, ornamented with several rows of very long spinules; inner lobe smooth and with thin cuticulum.

Fifth leg ( Fig. 2G ) simple short cuticular plate, almost rectangular in shape, ornamented with single pore on anterior surface and single spinule at base of outermost seta, armed with three smooth setae; outermost seta (ancestral basal one) longest, almost three times as long as entire leg; middle seta (probably ancestral outer endopodal) much shorter, 1.7 times as long as leg, and 1.4 times as long as innermost seta (inner endopodal). Fifth legs distinct at base, with small space between them, pointing caudally, not reaching distal margin of fifth pedigerous somite.

Sixth legs ( Fig. 1D ) smooth, unarmed and unornamented, forming simple large operculum covering gonopore, probably both fused together or right one reduced and left one enlarged, representing 55% of somite’s width.

Female (based on single newly collected specimen): Body length, excluding caudal setae, 584 µm. Habitus, ornamentation of prosomites, colour and nauplius eye similar to male, except genital and first abdominal somite fused into double somite and habitus slightly less slender.

Genital double somite ( Fig. 3 A-C) about as wide as long (ventral view), without any trace of subdivision, with oval dorsal cuticular window in anterior half, which much larger than that in male (originating from fused windows of two ancestral somites). Genital complex ( Fig. 3B ) occupying anterior ventral half of genital double somite; genital apertures covered by vestigial sixth legs; median copulatory pores also covered by fused sixth legs; seminal receptacles small, bell-shaped, with strongly sclerotized lateral walls; copulatory duct very short and weakly sclerotized. All posterior sensilla homologous to those on male third urosomite, while all sensilla from male second urosomite missing except lateral pair (No. 32).

Third, fourth (preanal), and fifth (anal) urosomites very similar to male ( Fig. 3A, B ).

Caudal rami ( Fig. 3A, B ) slightly shorter in proportion to anal somite than in male, about 3.7 times as long as wide in ventral (or dorsal) view, and slightly less divergent, but also cylindrical and armed and ornamented as in male.

Antennula seven-segmented, ornamented on first segment with few minute spinules on ventral surface, not geniculate, with slender aesthetasc on fourth segment, not reaching beyond tip of appendage, and more slender apical aesthetasc on seventh segment, which fused basally to two apical setae; proximal aesthetasc much more slender than in male; setal formula: 0.4.5.2.1.0.9. All setae, except proximalmost one on second segment, smooth, and most setae with pore on tip.

Antenna, labrum, paragnaths, mandibula, maxillula, maxilla, maxilliped, first swimming leg ( Fig. 2I ), and second swimming leg ( Fig. 2J ) same as in male.

Third swimming leg ( Fig. 3C ) with smooth praecoxa and intercoxal sclerite. Coxa with three large spinules on anterior surface, and two rows of spinules along distal margin on posterior surface, unarmed. Basis ornamented with several large spinules on outer margin distally and another row of smaller spinules at base of endopod, armed with very long and smooth outer seta, which 0.8 times as long as entire exopod. Exopod two-segmented, ornamented with large spinules along outer margin, both segments with hyaline frills distally on inner side; first segment armed with single outer spine; second with outer spine and apical strong seta; all elements bipinnate; apical seta 1.5 times as long as entire exopod. Endopod one-segmented, small, cylindrical and unornamented, armed with apical spiniform bipinnate element on tip, which basally fused to segment, reaching 4/5 of first exopodal segment in length.

Fourth swimming leg ( Fig. 3D ) without spiniform processes on basis. Endopod one-segmented, slender and long, cylindrical, curved inwards, ornamented with apical row of five large spinules at base of apical spine (no lateral spinules on inner margin); apical spine not distinct at base, bipinnate and robust, and about 0.7 times as long as endopod; endopod with apical spine almost reaching posterior margin of third exopodal segment in length. Exopod similar to male, but inner margin of first exopodal segment not as much concave; apical seta nearly 1.2 times as long as entire exopod.

Fifth leg ( Figs. 2K , 3B ) also simple cuticular plate, but with inner distal corner produced into strong and blunt spiniform process, which about 1.4 times as long as rest of leg, reaching in length tips of innermost seta; armature and ornamentation same as in male, except spinule at base of outermost seta (or very reduced setae) somewhat longer.

Sixth legs vestigial ( Fig. 3B ), narrowly fused into simple cuticular flap, covering gonopore, unornamented and unarmed; distal margin thin, medial part very short, lateral part longer and bilobate, each lobe terminating into more or less sharp tip.

Remarks. This species is only known from the Lake Biwa drainage area in Japan, but it is rare there these days. Our repeated efforts to collect it from the lake’s shore (including the type locality) failed, despite more than 30 samples taken in 2009 and 2010. As a part of the survey of subterranean biodiversity in the Lake Biwa drainage area, more than 100 samples were taken from 2008 to 2011, from caves, wells, river interstitial and lake interstitial, and the species was found in a single sample represented by three individuals. Specimens were obtained from the interstitial on the river banks, at the confluence of Daido and Seta rivers, from a mixture of medium size sand, gravel and large rocks. Relatively large size of this species suggests that it may prefer gravelly rather than sandy sediments.

Figures

Fig. 1. Parastenocaris biwae Miura, 1969, male: A. habitus, dorsal view. B. anal somite and caudal rami, ventral view. C. cephalothoracic shield, lateral view (dissected). D. anal somite with spermatophore inside, ventral view. E. antennule, ventral view. F. antenna, dorsal view. Arabic numerals indicating pairs of sensilla numbered consecutively from anterior to posterior part of the body and from dorsal to ventral side. Scale bars 100 µm for all.

Fig. 2. Parastenocaris biwae Miura, 1969, A-G. male, H-K. female: A. first swimming leg with abnormal endopod (undissected). B. endopod of second swimming leg. C. third swimming leg, anterior view (undissected). D. third swimming leg, posterior view (dissected and mounted). E. tip of third leg, posterior view. F. fourth swimming leg without last two exopodal segments, posterior view. G. fifth leg, anterior view. H. spermatophore. I. first endopodal segment of first swimming leg, anterior view. J. second swimming leg, anterior view. K. fifth legs, anterior view. Scale bar 100 µm for all.

Fig. 3. Parastenocaris biwae Miura, 1969, female: A. urosome, lateral view. B. urosome, ventral view. C. third swimming leg, anterior view. D. fourth swimming leg, anterior view. Arabic numerals indicating pairs of sensilla homologous to those in male specimens. Scale bars 100 µm for all.