Paraprotella teluksuang, Lim & Othman & Takeuchi, 2015

Lim, Jacqueline Hui Chern, Othman, Bin Haji Ross & Takeuchi, Ichiro, 2015, Description of Orthoprotella bicornis, new species, and Paraprotella teluksuang, new species (Crustacea: Amphipoda) from Johor, Malaysia with special reference to unusual sexual bias towards females in Paraprotella, Raffles Bulletin of Zoology 63, pp. 33-48 : 41-46

Paraprotella teluksuang , new species

( Figs. 6–8 )

Material examined. Holotype: female, 7. 9 mm, UKMMZ-1511, Mahkota artificial reef, Teluk Suang, Pulau Tinggi, 02°17.637ʹN, 104°05.817ʹE, hydroids, SCUBA diving, 10.7 m, Azman, B.A. R., Lim, J.H.C., Melvin, C.W.H., Gan, S.Y. & Shamsul, B., 9 June 2009 . Paratypes: 14 mature females, 8 premature females and 103 immature females, UKMMZ-1513, Mahkota artificial reef, Teluk Suang, Pulau Tinggi, 02°17.637ʹN, 104°05.817ʹE, SCUBA diving, 10.7 m, Azman, B.A. R., Lim, J.H.C., Melvin, C.W.H., Gan, S.Y. & Shamsul, B., 9 June 2009 ; 15 mature females, 8 premature females and 104 immature females, UKMMZ-1514, same station data; 1 mature female, 4 premature females and 101 immature females, UKMMZ-1515, Pulau Mentinggi, 02°16.408ʹN, 104°06.958ʹE, SCUBA diving, 6.6 m, Azman, B.A. R., Lim, J.H.C., Melvin, C.W.H., Gan, S.Y. & Shamsul, B., 10 June 2009 , 1 immature female, UKMMZ-1516, Pulau Pemanggil, 02°35.847ʹN, 104°18.971ʹE, SCUBA diving, 16.3 m, Azman, B.A. R., Lim, J.H.C., Melvin, C.W.H., Gan, S.Y., Khoo, M.L. & Shamsul, B., 5 August 2009 .

Type locality. Mahkota artificial reef, Teluk Suang, Pulau Tinggi, TLSI, Johor, Malaysia .

Description. Female: Holotype, 7.9 mm. UKMMZ-1512 ( Fig. 6 ). Head length 0.80 mm, and pereonite 1 length 0.70 mm; Head and pereonite 1 completely fused, suture absent; Head with an unpaired anterodorsally curved projection. Pereonite 1 with an unpaired dorsodistal projection. Pereonite 2 length 1.23 mm, with a pair of mid-dorsal projections. Pereonite 3 length 1.4 mm, with an anterolateral projection provided with a few small setae, distolaterally with a platelike projection and an obtuse mid-dorsal hump. Pereonite 4 subequal with pereonite 2, 1.2 mm, with a weak mid-dorsal hump. Pereonite 5 longest, length 1.57 mm. Pereonite 6 length 0.6 mm. Pereonite 7 shortest, length 0.4 mm. Antenna 1 incomplete, at least 0.6 × body length, peduncular article 1 with 2 plumose setae and tuft of fine setae at distal margin; article 2 longest, about 2.2 × longer than article 1; article 3 longer than article 1, about 0.5 × the length of article 2; flagellum about 1.1 × peduncular length with more than 14 articles, proximal article composed of 2 articles ( Fig. 6 : A1). Antenna 2 about 0.4 × antenna 1; flagellum 0.1 × peduncular length, with 2 articles; proximal article 2.3 × distal article ( Fig. 6 : A2).

Mouthparts. Upper lip symmetrical, slightly depressed medially, smooth, with no fine setae at apical margin ( Fig. 7 : UL). Lower lip well developed, inner lobes separated into 4 lobes, without fine setae ( Fig. 7 : LL). Mandible left incisor with 5 teeth; lacinia mobilis with 5 teeth, followed by 3 bundled setae; molar well developed [ Fig. 7 : MD (R)]. Mandible right incisor with 5 teeth; lacinia mobilis serrated, with many small teeth, followed by 2 bundled setae; molar well developed; palp for left and right similar, 3-articulate; article 2 with marginal and facial setae; article 3 with setal formula 2-6-1 [ Fig. 7 : MD (L)]. Maxilla 1 outer lobe with 6 stout apical setal-teeth, two of which are pectinate; palp biarticulate; distal article 3 × longer than proximal article, provided with 4 apical setae and 1 facial seta ( Fig. 7 : MX 1). Maxilla 2 inner plate medially expanded with 5 slender setae apically; outer plate subrectangular, more slender than inner plate, with 6 apical setae ( Fig. 7 : MX 2). Maxilliped basal endite (inner plate) subrectangular, with 2 simple setae and 2 plumose setae at distal margin; ischial endite (outer plate) 3 × the length of inner plate, not extending beyond article 2 of palp, with 2 simple setae distally and 3 facial setae; palp 4-articulate, article 2 longest with 6 setae on inner margin; article 3 subequal in length with article 1, provided with 8 setae on inner distal corner and 1 seta on outer corner; palp article 4 (dactylus) falcate with row of setules along inner margin and 2 small setae at tip ( Fig. 7 : MXP).

Pereon. Gnathopod 1 basis, shorter than ischium, merus and carpus combined, with 4 setae on posterodistal corner and 1 seta on anterodistal corner; ischium shortest; merus and carpus subtriangular; carpus 0.6 × shorter than basis, anterior margin setaceous; propodus short and mitten-like, 1.2 × longer than carpus, convex on dorsal margin, with 2 rows of facial setae, palm begins 1/4 along posterior margin with 1 pair of proximal robust setae; dactylus slightly curved, pectinate along inner margin with a few fine setae at tip ( Fig. 6 : G1). Gnathopod 2 begins 1/5 along anterior margin of pereonite 2, basis subequal with length of pereonite 2, anterodistal corner with acute triangular projection; ischium as long as wide with posterodistal setae; merus subovate, very scarcely setose; carpus subtriangular; propodus longest, 1.1 × the length of basis, oblique, palm sinuous, with proximal grasping spine, mid palmar projection with 1 seta followed by a deep sinus and two small triangular projections; palm with serriformed teeth between proximal projection and mid palmar projection; dactylus length subequal with basis, falcate, with fine setae along entire outer margin ( Fig. 6 : G2). Gill 3 length 0.5 × pereonite 3, oval. Pereopod 3 about 0.4 × the length of its gill, 3 articulate, article 2 subovate, covered in short and long setae, article 3 vestigial, with 1 terminal plumose seta ( Fig. 8 P 3 ). Gill 4 length 0.5 × pereonite 4, oval, shorter than gill 3 (0.9 × shorter). Pereopod 4 about 0.4 × the length of its gill, slightly shorter than pereopod 3 (0.9 × shorter), 3 articulate, article one subrectangular, article 2 subovate covered in short and long setae, article 3 vestigial with 1 terminal seta ( Fig. 8 : P4). Pereopods 5–7 well developed, progressively robust, carpus decreasing in length from pereopods 5–7, length of propodus increases significantly from pereopods 5–7. Pereopod 5 slender, equipped with long setae, basis longest, rectolinear; carpus length 4.7 × width, subequal in length with ischium and merus combined, 0.9 × length of basis; propodus shorter than carpus (0.9 × shorter), palm with a pair of proximal grasping spines followed by several marginal setae, outer margin with several long and short setae; dactylus falcate, scarcely setose, proximally with 1 plumose seta ( Fig. 8 : P5). Pereopod 6 basis wider but subequal in length with pereopod 5 basis; merus slightly pronounced posterodistally; carpus length 2.5 × width, 0.7 × the length of basis, 0.8 × shorter and 1.5 × wider than pereopod 5 carpus, more setose on inner margin; propodus longest, longer than carpus (1.4 × longer), palm with a pair of proximal grasping spines followed by several short marginal setae, outer margin with several long and short setae; dactylus falcate, fitting onto palm, with 1 plumose proximal seta ( Fig. 8 : P6). Pereopod 7 equipped with finer and shorter marginal setae throughout articles, basis length about 2 × width; merus pronounced posterodistally; carpus length 1.8 × width, 0.7 × the length of basis, subequal in length with merus, subequal in length and 1.3 × wider than pereopod 5 carpus; propodus longest, subequal in length with merus and carpus combined, 2 × longer than carpus, palm with a pair of proximal grasping spines followed by several short marginal setae, outer margin with several long and short setae; dactylus falcate ( Fig. 8 : P7).

Pleon. Uropod 2 vestigial. Telson with a pair of normal setae and a pair of plumose setae [ Fig. 8 : ABD (V) and ABD (L)].

Remarks. The genus Paraprotella is unique in having 3-articulate pereopods 3 and 4. This genus was established by Mayer in 1903 based on P. prima Mayer, 1903 (from Japan, Thailand and Singapore) and P. secunda Mayer, 1903 (from Japan) ( Mayer, 1903; Arimoto, 1976). Takeuchi & Guerra-García (2002) later added another species, P. saltatrix , from Phuket, Thailand, bringing the total to three species. No male specimens were collected in the present material; this phenomenon is also observed in P. saltatrix ( Takeuchi & Guerra-García, 2002) .

Paraprotella teluksuang , new species, shares several similar characteristics with P. saltatrix such as head and pereonites 1–4 lacking lateral projections, mandibular palp article 3 with setal formula of 2 (long setae near proximal end)–x (number of short setae)-1 (long seta near apical end) and the more robust structure of pereopods 3 and 4, with article 2 longer than article 1 and article 3 minute.

Paraprotella teluksuang , new species, differs from P. saltatrix based on the following characteristics: 1) lack of a distinct suture between head and pereonite 1 (present in P. saltatrix ); 2) lack of a dorsodistal projection on pereonite 2 (present in P. saltatrix ); 3) pereonites 3 and 4 with very slight middorsal round projections, almost unnoticeable on pereonite 4 (with shallow mid-dorsal projections in P. saltatrix ); 4) specimens of the present material are more robust in body somites; 5) P. teluksuang , new species, having 2 rows of facial setae on gnathopod 1; and 6) vestigial uropod and telson with 1 normal seta and 1 plumose seta (uropod in P. saltatrix with 1 seta; uropod in P. prima 1-articulate and uniramous; unknown for P. secunda ).

Paraprotella prima and P. secunda described in Mayer (1903) are equipped with more projections on the pereonites particularly the female specimens; compared with P. teluksuang , new species, and P. saltatrix . Paraprotella prima Mayer, 1903 has distinct lateral triangular projections on pereonites 1 to 4 which are absent in P. teluksuang , new species, P. secunda and P. saltatrix . The large lateral projections are present on pereonite 6 of P. secunda , small tubercles in P. prima but absent in P. teluksuang , new species, and P. saltatrix . P. prima is armed with 1 projection on dorsal margin of pereonite 1, 1 dorsodistal projection and 1 pair of acute spines mid-dorsally on pereonite 2 while P. secunda is armed with only 1 projection/spine on pereonites 1 and 2. The latter 4 species, have long antenna 1, usually more than half of total body length.

In P. secunda Mayer, 1903 , identification was based on 2 premature individuals (1 premature male and female). Pereopods 5 to 7 of both individuals were also detached. No illustrations were provided and only description of whole body, antenna 1 and gnathopod 2 were included. Based on these 2 individuals, the male individual of P. secunda shows similar characteristics with the female of P. prima in pereonites 3 with a pair of mid-dorsal spines. P. secunda also has a tooth at distal end of pereonite 3 (absent in P. teluksuang , new species, P. prima and P. saltatrix ). Following descriptions of Mayer (1903) and Arimoto (1976), it is clear that P. teluksuang , new species, differs from P. prima Mayer, 1903 and P. secunda Mayer, 1903 in terms of dorsal and lateral projections, setal formula of the mandibular palp (2-x-1) instead of 1-x-y-1, and the abdomen.

1.49 mm to 9.14 mm ( Fig. 9 ). The growth of females in caprellidean amphipods is divided into three stages, ‘immature’, ‘premature’ and ‘mature’. In the immature stage, oostegites are smaller in size compared to the corresponding gills while in the premature stage its oostegites are larger than the gills and leaf-like in shape. The final mature stage can be identified from the large oostegites or brood pouch expanding downwards and marginally lined with long setae to circulate water into and out of the brood pouch containing eggs ( Takeuchi & Hirano, 1991). Individuals in the range of 6.11–7.25 mm (n= 20) in body length are premature females, and those larger than 7.25 mm (n= 31) are all mature females ( Fig. 9 ). This is the second report of female biased population. The first report was by Takeuchi & Guerra-Garcia (2002) on Paraprotella saltatrix from Phuket Island, Thailand, where specimens collected from two localities contained only female individuals.

Parthenogenesis is uncommon in macrobenthic Amphipoda with only a few subjective reports from several species; Corophium bonelli Milne Edwards, 1830 (see Crawford 1937; Moore 1981; Myers et al., 1989) and the cavernicolous amphipod Stygobromus such as S. spinatus ( Holsinger, 1967) , S. pseudospinosus Holsinger, 1978 and S. albapinus Taylor & Holsinger, 2010 to mention a few (see Culver & Holsinger, 1969; Holsinger, 1978; Taylor & Holsinger, 2010). Parthenogenesis is considered a means of sustaining lineage and population expansion. Asexual reproduction such as this is also known to occur in certain favorable food and environmental circumstances ( Sch ӧn et al., 2009).

Etymology. This species was named after the type locality, Teluk Suang. The name is treated as a Latin noun in apposition.

Distribution. Currently only known from TLSI, Johor, Malaysia.

Figures

Fig. 6. Paraprotella teluksuang, new species, female holotype, 7.90 mm, UKMMZ-1511, Mahkota artificial reef, Teluk Suang, Pulau Tinggi, TLSI. Scale bars A1 = 0.3 mm; A2 and G2 = 0.2 mm; G1 = 0.1 mm; whole body = 0.5 mm

Fig. 7. Paraprotella teluksuang, new species, female holotype, 7.90 mm, UKMMZ-1511, Mahkota artificial reef, Teluk Suang, Pulau Tinggi, TLSI. Scale bars = 0.025 mm

Fig. 8. Paraprotella teluksuang, new species, female holotype, 7.90 mm, UKMMZ-1511, Mahkota artificial reef, Teluk Suang, Pulau Tinggi, TLSI. Scale bars ABD (L), ABD (V), P3 magnified and P4 magnified = 0.1 mm; P3, P4, P5, P6 and P7 = 0.2 mm

Fig. 3. Orthoprotella bicornis, new species, male holotype, 8.37 mm, UKMMZ-1502, Kampung Sebirah, Pulau Tinggi, TLSI. Scale bars ABD (L), ABD (V) = 0.1 mm; P3, P4, P5, P6 and P7 = 0.2 mm.

Fig. 9. Size distribution of body length (mm) in Paraprotella teluksuang, new species, collected from three stations, Mahkota artificial reef, Teluk Suang, Pulau Tinggi; Pulau Mentinggi and Pulau Pemanggil, TLSI, Malaysia.