A review of the genus Parapenaeon Richardson, 1904 (Crustacea: Isopoda: Bopyridae: Orbioninae), with description of three new species from China

Five species of the bopyrid genus Parapenaeon are reported from China, of which three are new to science, and one, Parapenaeon expansa Bourdon, 1979, is a new record. New species are Parapenaeon calculosa, sp. nov., Parapenaeon diatropa, sp. nov. and Parapenaeon sicyoniae, sp. nov., from the East and South China Seas. The female of each new species has six pleomeres, no lateral plates on the sixth pleomere, and biramous uropods, characters that place them in the genus Parapenaeon Richardson, 1904. Each can be distinguished from previously described species of the genus Parapenaeon in body shape, by the characters of oostegite 1, the barbula, brood pouch, pleopods and uropods of the females. A table including all of the currently recognized species of Parapenaeon with type localities, known geographical distribution and reported hosts, is given. A key to the recorded species of Parapenaeon Richardson, 1904 is provided, as is a new diagnosis of the genus. http://zoobank.org/urn:lsid:zoobank.org:pub:35CD12BB-D1F3-48DF-BABB-2EAA3030395B


Introduction
The genus Parapenaeon Richardson, 1904 contains 10 previously described species (Bourdon 1979a(Bourdon , 1981Boyko et al. 2014) (hosts, type locality, distribution and primary genus of all described species can be seen from Table 1). Richardson (1904) erected the genus with Parapenaeon consolidata its type species; the females of this genus are characterized by having six pleomeres, coxal plates on the first two pereomeres of the short side, no lateral plates on the sixth pleomere, uniramous uropods and tuberculate biramous pleopods. Thielemann (1910) described Epipenaeon japonica, which Nierstrasz and Brender à Brandis (1923) found again and recorded under the name Epipenaeon japonicum; and they also described Parapenaeon secundum. Bourdon (1979a) transferred E. japonicum to the genus Parapenaeon because its female has six pleomeres, not five pleomeres as is characteristic for Epipenaeon. Markham (1982) found this species in Hong Kong and discussed the gender of the generic name Parapenaeon, concluding that it is feminine and so using the name P. japonica. Bourdon (1979a) described another species, Parapenaeon expansus, from Madagascar. Markham (1994) again discussed the gender of the genus name and rendered Parapenaeon secundum, Parapenaeon brevicoxale and P. expansus as Parapenaeon secunda, Parapenaeon brevicoxalis and Parapenaeon expansa. Parapenaeon japonica is a very widespread species, has been described and re-described thoroughly (see synonym list). Examination of 12 species of Penaeidae collected in Chinese waters found five species of Parapenaeon infesting them. Of these, three are new species and one, P. expansa, is recorded for the first time from China. A table including all of the currently recognized species of Parapenaeon with type localities, known geographical distribution and reported hosts, is provided. A key to the 13 species of the genus Parapenaeon Richardson, 1904 now known is presented.

Material and methods
Materials for this study are from the China/Vietnam Comprehensive Oceanographic Survey of Beibu Gulf, Gulf of Tonkin (1959 and East China Sea (2000). All materials examined have been deposited in the Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China (IOCAS). The initials CIEPE as follows: Animals were examined and drawn using a Zeiss Stemi SV Apo. Males to be studied by scanning electron microscope were fixed in 2.5% glutaraldehyde in 0.2 M Millonig's phosphate buffer at pH 7.4 for 1.5 h and post-fixed in 1% osmium tetroxide in 0.2 M Millonig's buffer for 1 h. The specimens were then dehydrated through a graded series of ethanol, followed by critical-point drying. After sputter coating with colloidal gold, the specimens were examined with a KYKY2800B scanning electron microscope.
The host species M. toloensis, M. dura, M. mogiensis and M. novaeguineae have never before been reported to bear bopyrid parasites, whereas M. stridulans have been reported to bear Epipenaeon ingens Nobili, 1906 andOrbione thielemanni Nierstrasz andBrender à Brandis, 1931. With the addition of the new host records, P. japonica is now known to infest 21 different penaeoid host species, the most for any orbionine bopyrid species. It is also the most widespread geographically of any orbionine species.

Remarks
Parapenaeon expansa has been found across the Indian Ocean and on the Pacific side of Australia, but this is the first published record of its occurrence in China. It has previously been found infesting nine species of hosts; those reported here are both new records for any bopyrid parasite. The specimens from Pakistan recorded by Kazmi and Tirmizi (1994) as P. japonica we believe were misidentified specimens of P. expansa and are cited in our synonymies accordingly above. The present specimens (Figures 4,5) conform well to the descriptions of Bourdon (1979a) and Kazmi and Tirmizi (1994). Characters of some females that differ from previous records are the inner projection of the barbula ( Figure 4E) being much smaller than the outer one, and the maxilliped palp being slightly segmented. In one male specimen ( Figure 5H, I) the margin of the pleon is dentate and obscurely segmented in ventral view.  examined these specimens and recorded two Parapenaeon species (P. expansus and P. monolioncus sp. nov.) in her doctoral dissertation. Now we consider all these materials to represent P. expansa, with the name P. monolioncus being invalid because of its presentation in an unpublished dissertation (not a published work in the sense of the ICZN); it is introduced here in synonymy.
Head elliptical with curved posterior edge ( Figure 6K). Eyes absent. First antenna of three articles, with setae on distal article; second antenna of five articles, terminal two or three articles setose ( Figure 6M).

Variations
Paratype females differ little from the holotype. An immature female (CIEPE405101) has dentate coxal plates on first three pereomeres on long sides, those on short sides being smaller than those on long sides ( Figure 6N, O). Slender pleopods extend beyond the lateral plates, and are visible in dorsal view.

Etymology
The specific name, calculosa a Latin adjective meaning 'pebbly', refers to the surfaces of the pleopods of the holotype female, which are thickly tuberculated in a pattern reminiscent of small stones or pebbles.

Remarks
The female of P. calculosa, as in other species of the genus Parapenaeon, has six pleomeres, the first five bearing lateral plates. The male has a pleon fused and lacking appendages, as is typical for Parapenaeon. The new species is most similar to P. japonica (Thielemann 1910). The new species differs from P. japonica in the following. (1) The new species has a straight posterior edge of the first oostegite, but all specimens of P. japonica have curved posterior edge of the first oostegite. (2) Sixth pleomeres of the new species can be seen from dorsal view ( Figure 6A, J), but in P. japonica only five pleomeres can be seen, sixth pleomere usually hidden under the fifth pleomere ( Figures 1A, 2A, 3A). (3) The new species with tubercles on the surface of the lateral plates, and P. japonica with smooth lateral plates. (4) The new species barbula with one pairs of digitate projections, and the barbula of P. japonica with two pairs of digitate projections. (5) Male of the new species with smooth pleon, without anal cone or other tubercles, and P. japonica with distinct anal cone, some specimens with midventral tubercular on the pleon ( Figure 3J).
Parapenaeon diatropa sp. nov. (Figures 7, 8)  Description of holotype female (CIEPE001101-1) ( Figure 7A-I) Length 5.97 mm, maximal width 4.09 mm, head length 0.94 mm, head width 1.24 mm. Head oval, with deep bilobate anterior edge and curved posterior edge, welldeveloped frontal lamina extending beyond sides of the head ( Figure 7A). Eyes absent. First and second antennae of three and five articles, respectively, terminal setae not evident ( Figure 7C). Maxilliped triangular, with short curved stout palp ( Figure 7D). Barbula with two pairs of lateral projections on each side, outer pair with slightly digitate edge, but inner projections smooth. (Figure 7E).
Pereon broadest across fourth pereomere ( Figure 7A). Coxal plates welldeveloped on long side of all pereomeres, margins entire. Coxal plates on short side of first two pereomeres also well-developed, but those on other pereomeres rudimentary. Dorsolateral bosses on first five pereomeres. Brood pouch wide open ( Figure 7B). First oostegite ( Figure 7F, G) plates of nearly equal length, internal ridge bearing five to eight small tubercules, posterolateral point broadly triangular, pointing posteriorly, and with posterior edge curved. Pereopods larger posterior ( Figure 7H, I), surface of the carpi and meri smooth, bases of all pereopods produced into lobes.
Pleon of six pleomeres, first five bearing tubercular biramous pleopods and rudimentary lateral plates. Pleopods are slender and do not extend beyond edges of lateral plates, so they are not visible in dorsal view ( Figure 7B). Fifth pleomere widely median separated, and small sixth pleomeres can be seen from dorsal view ( Figure 7A). Biramous uropods tuberculate. Exopodites of uropods different endopodites, the former larger, sharp terminal, and slender, but the latter short, cylindrical. Uropods are visible dorsally ( Figure 7B).
Head ( Figure 7J) trapezoidal, its posterior edge straight. Black eyes near posterolateral corners of head ( Figure 7J). First and second antennae ( Figure 8A) of three and four articles respectively, setae not evident.
Pleon fused, median part with pigment. Anal cone visible in dorsal view ( Figure 7K).

Variations
Immature females have black eyes, flatter bodies and coxal plates on the short sides of all pereomeres; other characters agree with the holotype.

Etymology
The specific name, the Greek adjective diatropos, refers to uropods of holotype female with remarkable diverse rami.

Remarks
The new species, P. diatropa, is most similar to P. japonica (Thielemann 1910). The female of P. diatropa differs from that of P. japonica in longer body shape, uropods with remarkable different rami, cylindrical endopodite and longer and sharp exopodite; pleopods not extending beyond the margin of pleon, cannot be seen from the dorsal view; a simple barbula whose inner projections are almost smooth, oostegite 1 with almost smooth inner ridge bearing only small tubercules, whereas in P. japonica, almost round body shape, flake shape uropods with similar endopodite and exopodite; pleopods usually extending beyond the margin of pleon; heavy tubercular digitate projections on each side of the barbula; having long and thick tubercules on the inner ridge of oostegite 1.  Figure 9A). First antenna of three articles without evident setae, basal two articles stout, terminal article very narrow; second antenna of four articles, each much narrower than that proximal to it, terminal article with sparse setae ( Figure 9C). Palp of maxilliped broadly triangular, offset slightly from medial margin, non-setose, not articulating with maxilliped ( Figure 9D). Barbula with two pairs of digitate lateral projections on each side, more branches on outer projections than inner ones. Small tubercule medial to each inner projection ( Figure 9E).
Pereon broadest across third pereomere ( Figure 9A). Coxal plates well-developed on long side of all pereomeres. Coxal plates on short side of first two pereomeres also well-developed, but those on third and fourth pereomeres rudimentary, absent from other pereomeres. Round dorsolateral bosses on first four pereomeres. Brood pouch Pleon of six pleomeres, first five bearing smooth lateral plates ( Figure 9J) and biramous digitate pleopods ( Figure 9K-O). Sixth pleomeres visible in dorsal view, with digitate biramous uropods ( Figure 9J). Exopodites of uropods round, endopodites as slender triangles.  Figure 10A-D). Head fan-shaped ( Figure 9P). Eyes absent. First antenna of three articles, terminal one setose. Second antenna of four articles, terminal one setose ( Figure 10B). Pereomeres almost equally wide, lacking midventral projections ( Figures 9Q,  10A). All pereopods of similar size and structure, propodi, carpi and meri with clusters of setae near distal margins ( Figure 10B-D); those projections on propodi in two lines along sides of grooves receiving tip of dactyli ( Figure 10D).
Pleon subtriangular, fused, its anterior region indicating remnant of former first pleomeres much broader than rest of pleon. No pleopods or uropods ( Figure 9Q).

Variations
Other males and females do not differ significantly from the type specimen.

Etymology
The specific name, sicyoniae is the genitive form of the genus name of the host of the new species.

Remarks
The female of P. sicyoniae shows the reduced and surrounded sixth pleomere characteristic of the genus Parapenaeon. Parapenaeon sicyoniae is most similar to P. diatropa, but the former can be distinguished the from latter as follows: (1) the new species with round body, and P. diatropa with much long body; (2) pleopods of new species foliate and can be seen from the dorsal view, but P. diatropa with slender pleopods and cannot be seen from dorsal view; (3) brood pouch of the new species nearly closed, but P. diatropa with open brood pouch; (4) the male of the new species without eyes, but the allotype male of P. diatropa with dark eyes.  regarded these specimens as one species of the genus Minicopenaeon in her doctoral dissertation, but because they have coxal plates on the short side of pereomere 2, they belong to the genus Parapenaeon. A key to the species of genus Parapenaeon Richardson, 1904 is presented below.
The 12 host species identified to species recorded in this report include eight species in the genus Metapenaeopsis and one species of each of the genera Fenneropenaeus, Marsupenaeus, Sicyonia and Trachypalambria. Of these 12 species, five have not previously been reported as hosts of bopyrid parasites and are therefore new records here. They are Metapenaeopsis toloensis, M. dura, M. lamellata, M. novaeguineae and Sicyonia cristata.
Key to 13 species of the genus Parapenaeon Richardson, 1904 based on mature females