Caridina clandestina, Klotz & Rintelen & Annawaty & Wowor & Rintelen, 2023

Klotz, Werner, Rintelen, Thomas von, Annawaty, Annawaty, Wowor, Daisy & Rintelen, Kristina von, 2023, Caridina clandestina, new species, an unusual new freshwater shrimp (Crustacea: Decapoda: Atyidae) from the remote high elevation Napu Valley of Sulawesi, Indonesia, Raffles Bulletin of Zoology 71, pp. 12-25 : 14-22

Caridina clandestina , new species

( Figs. 2A–N , 3A–O , 4B, C )

Material examined. Chelae built for filter feeding. Holotype: male (CL 5.5 mm) ( MZB Cru 5362), Central Sulawesi, Poso Regency, Lore Peore District, Ds. Watutau, Dusun 1, Napu Valley , Lariang River , 1°33′34.2″S 120°20′19.0″E, 1089 m asl, coll. T. von Rintelen & W. Klotz, 6 May 2017 . Paratypes: 8 males (CL 4.0– 6.4 mm), 6 females (CL 3.5–6.0 mm), 2 juveniles (CL 2.7–3.5 mm) ( MZB Cru 5363) , 10 males (CL 5.0– 5.6 mm), 1 female (CL 6.2 mm), 1 juvenile (CL 2.8 mm) ( ZMB 30207 a), same data as holotype ; 4 males (CL 4.2–5.3 mm), 3 females (CL 3.7–5.0 mm) ( ZMB 29430 a), Central Sulawesi, Poso Regency, Lore Timur District , Ds. Maholo at Hambu bridge, Napu Valley , Lariang River , 1°29′22.6″S 120°23′10.7″E, 1119 m asl, coll. T. von Rintelen & A. Wessel, 7 October 2005 ; 1 female (CL 5.5 mm), 2 ov. females (CL 5.4 mm) ( MZB Cru 5364) ; 5 males (CL 4.8–5.4 mm), 1 female (CL 5.2 mm), 7 ov. females (CL 4.9–5.9 mm) ( ZMB 29431 ), Central Sulawesi, Poso Regency, Lore Peore District , Ds. Watutau , Dusun 1, Napu Valley , Lariang River , 1°33′34.2″S 120°20′19.0″E, 1089 m asl, coll. T. von Rintelen, 7 October 2005 ; 5 males (CL 5.0– 5.4 mm), 3 females (CL 5.4–6.1 mm), 6 juveniles (CL 2.2–3.8 mm) ( MZB Cru 5365) , 1 juvenile (CL 2.9 mm) ( ZMB 30203 a), Central Sulawesi, Poso Regency, Lore Peore District , Ds. Watutau , Dusun 1, Napu Valley , unnamed stream feeding to Lariang River , 1°32′07.4″S 120°22′47.6″E, 1125 m asl, coll. T. von Rintelen et al., 6 May 2017 .

Chelae built for scraping. 5 males (CL 4.5–5.3 mm), 3 females (CL 3.8–5.9 mm), 2 ov. females (CL 5.6–5.8 mm) ( MZB Cru 5366) (ex. ZMB 29430 b) ; 4 males (CL 4.6–5.3 mm), 1 female (CL 3.9 mm), 2 ov. females (CL 5.7–5.9 mm) ( ZMB 29430 b), Central Sulawesi, Poso Regency, Lore Timur District, Ds. Maholo, Napu Valley , Lariang River , 1°29′22.6″S 120°23′10.7″E, 1119 m asl, coll. T. von Rintelen & A. Wessel, 7 October 2005 ; 1 male (CL 5.6 mm), 2 females (CL 5.6–6.1 mm), 2 ov. females (CL 5.7–6.2 mm), 1 loose carapax (CL 5.4 mm) ( MZB Cru 5367), Central Sulawesi, Poso Regency, Lore Peore District , Ds. Watutau , Dusun 1, Napu Valley , Lariang River , 1°33′34.2″S 120°20′19.0″E, 1089 m asl, T. von Rintelen, 7 October 2005 ; 5 males (CL 4.7–6.1 mm), 5 females (CL 3.6–6.1 mm), 2 juveniles (CL 3.1–3.2 mm) ( MZB Cru 5368) , 2 males (CL 5.7–5.8 mm), 10 females (CL 3.6–6.3 mm), 3 juveniles (CL 2.7–3.2 mm) ( ZMB 30207 b), Central Sulawesi, Poso Regency, Lore Peore District , Ds. Watutau , Dusun 1, Napu Valley , Lariang River , 1°33′34.2″S 120°20′19.0″E, 1089 m asl, coll. T. von Rintelen & W. Klotz, 6 May 2017 ; 2 males (CL 4.4–5.0 mm), 2 females (CL 5.0– 6.1 mm), 1 ov. female (CL 6.4 mm) ( MZB Cru 5369) , 13 males (CL 4.5–5.5 mm), 25 females (CL 3.4–6.2 mm), 17 juveniles (CL 1.9–3.3 mm) ( ZMB 30203 b), Poso Regency, Lore Peore District, Ds. Watutau , Dusun 1, Napu Valley , unnamed stream feeding to Lariang River , 1°32′07.4″S 120°22′47.6″E, 1125 m asl, coll. T. von Rintelen et al., 6 May 2017 ; 6 males (CL 4.5–5.7 mm), 19 females (CL 3.2–6.0 mm), 22 juveniles (CL 1.7–3.3 mm) ( MZB Cru 5370), Central Sulawesi, Poso Regency, Lore Timur District , Ds. Maholo at Hambu bridge, Napu Valley , Lariang River , 1°29′22.6″S 120°23′10.7″E, 1119 m asl, coll. T. von Rintelen & W. Klotz, 6 May 2017 .

Description.

Cephalothorax and cephalic appendages. Postorbital carapace length 1.7–6.6 mm (median 4.5 mm, n = 212). Rostrum ( Fig. 2A, B ) sigmoidal, dorsal margin with teeth placed at the basal part of the rostrum, main part of dorsal margin unarmed, teeth on ventral margin placed at about mid length of rostrum, overreaching distal margin of the scaphocerite in adult specimens, shorter than scaphocerite in juveniles, 0.65–1.4 (median 1.04, n = 37) times as long as carapace, rostral formula based on 157 specimens 1–4 (2) + 3–10 (5–7) / 2–16. Antennal spine well separated from inferior orbital angle. Pterygostomial angle broadly rounded. Eyes well developed with globular cornea. Antennular peduncle ( Fig. 2A, B, G ), 0.74–0.87 (median 0.78, n = 10) times as long as carapace in females, 0.85–0.92 (median 0.88, n = 10) times as long as carapace in apparently adult males, first segment 1.36–1.82 (median 1.58, n = 20) times as long as second segment, second segment 1.73–2.83 (median 2.0, n = 20) times longer than third segment. Stylocerite reaching to 0.62–0.78 (median 0.73, n = 16) times of first segment of antennular peduncle. Scaphocerite ( Fig. 2H ) 3.40–4.44 (median 3.93, n = 17) times as long as wide.

Abdominal somites, telson, and uropods. Sixth abdominal somite 0.52–0.67 (median 0.59, n = 23) times carapace length, 1.48–2.18 (median 1.89, n = 23) times as long as fifth somite, 0.72–0.93 (median 0.85, n = 23) times as long as telson. Telson ( Fig. 2C, D ) 3.29–3.68 (median 3.52, n = 4) times as long as proximal wide, distal margin convex without a median projection, with two to five pairs of short spiniform setae dorsally and one pair of short spiniform setae dorsolateral; distal end with four to seven long spiniform setae, lateral pair longer than others. Preanal carina ( Fig. 2E ) rounded, without a spine. Uropodal diaeresis ( Fig. 2F ) with 10–14 stout movable spiniform setae, outermost ones slightly shorter than lateral angle.

Mouthparts and branchiae. Incisor process of mandible ( Fig. 2I ) ending in irregular teeth, molar process truncated. Lower lacinia of maxillula ( Fig. 2J ) subrectangular, upper lacinia elongate, with numerous distinct teeth on inner margin, palp slender with few pappose setae and one conical spiniform seta near tip. Upper endites of maxilla ( Fig. 2K ) subdivided, palp slender, scaphognathite tapering posteriorly, fringed with long, curved setae at posterior margin. End of palp of first maxilliped ( Fig. 2L, M ) truncated or ending blunt triangular. Podobranch on second maxilliped ( Fig. 2N ) slightly reduced to a lamina with few finger-like extensions distal. Third maxilliped ( Fig. 3A ) with two arthrobranches. First pereiopod with an arthrobranch. Pleurobranches present on all pereiopods. Epipods well developed on third maxilliped and first pereiopod, absent from pereiopods 2 to 5.

Pereiopods. Chelipeds of first and second pereiopods ( Fig. 3B–I ) dimorphic, either built for filter-feeding or for scraping. Chela of first pereiopod built for filter-feeding ( Fig. 3B, C ) 2.14–3.48 (median 3.09, n = 50) times as long as wide, 1.32–1.90 (median 1.5, n = 50) times length of carpus; tips of fingers ( Fig. 3C ) rounded, without hooks, with long hairs near tip (about as long as dactylus); dactylus 2.47–5.0 (median 3.03, n = 51) times as long as palm; carpus slender, hardly excavated distally, 1.76–2.75 (median 2.24, n = 51) times as long as wide, 0.78–1.14 (median 0.96, n = 40) times length of merus. Chela of first pereiopod built for scraping ( Fig. 3D, E ) 1.74–2.54 (median 2.11, n = 88) times as long as wide, 1.20–1.90 (median 1.57, n = 87) times length of carpus; tips of fingers ( Fig. 3E ) rounded, without hooks, with short hairs near tip (distinctly shorter than dactylus), dactylus 0.73–2.05 (median 1.24, n = 88) times as long as palm; carpus less slender, moderately excavated distally, 1.29–2.24 (median 1.64, n = 86) times as long as wide, 0.82–1.46 (median 1.0, n = 71) times length of merus. Merus similar in both cheliped types, 1.60–5.83 (median 2.59, n = 109) times as long as wide, 0.91–1.29 (median 1.0, n = 35) times as long as ischium.

Chela of second pereiopod built for filter-feeding ( Fig. 3F, G ) 3.25–6.57 (median 3.56, n = 11) times as long as wide, 0.89–1.15 (median 1.06, n = 11) times length of carpus; tips of fingers ( Fig. 3G ) rounded, without hooks, with long hairs near tip (about as long as dactylus); dactylus 1.96–4.19 (median 3.16, n = 11) times as long as palm; carpus slender, hardly excavated distally, 3.88–4.38 (median 4.24, n = 11) times as long as wide, 1.05–1.26 (median 1.13, n = 11) times length of merus. Chela of second pereiopod built for scraping ( Fig. 3H, I ) 2.58–3.17 (median 2.88, n = 14) times as long as wide, 0.80–0.97 (median 0.89, n = 14) times length of carpus; tips of fingers ( Fig. 3I ) rounded, without hooks, with short hairs near tip (distinctly shorter than dactylus), dactylus 1.31–2.33 (median 1.66, n = 14) times as long as palm; carpus slender, hardly excavated distally, 4.13–5.0 (median 4.63, n = 14) times as long as wide, 1.19–1.45 (median 1.31, n = 14) times length of merus. Merus similar in both cheliped types, 3.63–4.90 (median 4.06, n = 25) times as long as wide, 0.89–1.15 (median 1.0, n = 25) times as long as ischium.

Third pereiopod ( Fig. 3J, K ) stout, dactylus 2.42–4.55 (median 3.30, n = 23) times as long as wide (terminal claw and spiniform setae on flexor margin included), terminating in one large claw with 5–10 short spiniform setae on flexor margin; propodus stout, slightly curved in adult males, 6.92–11.0 (median 8.8, n = 23) times as long as wide, 1.9–3.39 (median 3.09, n = 23) times as long as dactylus; carpus 3.72–8.14 (median 4.46, n = 23) times as long as wide, 0.56–0.77 (median 0.63, n = 23) times as long as propodus; merus 5.0–8.89 (median 6.42, n = 23) times as long as wide, 1.60–2.21 (median 1.89, n = 23) times as long as carpus, bearing 2–4 strong spiniform setae on posterior margin of outer surface. Ischium without or with one spiniform seta.

Fifth pereiopod ( Fig. 3L, M ) slender, dactylus 2.2–4.0 (median 3.7, n = 19) times as long as wide (terminal claw and serrate setae on flexor margin included), terminating in one large claw with 25–57 serrate setae on flexor margin, first serrated seta more stronger than others; propodus 8.62–10.67 (median 9.66, n = 18) times as long as wide, 2.63–4.04 (median 2.77, n = 18) times length of dactylus, carpus 4.07–5.0 (median 4.44, n = 17) times as long as wide, 0.46–0.61 (median 0.54, n = 17) times as long as propodus; merus 4.62–9.11 (median 5.71, n = 17) times as long as wide, 1.27–1.79 (median 1.54, n = 17) times length of carpus, bearing two or three strong spiniform setae on posterior margin of outer surface. Ischium without a strong spiniform seta.

Pleopods. Endopod of first pleopod ( Fig. 3N ) in male specimens subrectangular, 2.5–3.4 (median 2.8, n = 13) times as long as wide, lacking an appendix interna, outer margin beset with pappose setae, distal margin beset with long simple setae, short simple setae arranged in two rows and patches on proximal part of inner margin.

Appendix masculina on male second pleopod ( Fig. 3O ) slender, rod-shaped, 7.25–13.0 (median 11.43, n = 12) times as long as wide, 0.47–0.87 (median 0.77, n = 12) with short strong spiniform setae on inner and distal margin, few long spiniform setae on basal part, appendix interna reaching to 0.57–1.06 (median 0.61, n = 12) of appendix masculina.

Colouration. Brownish to blueish with some weak white transversal bands on abdominal tergites, eggs brownish ( Fig. 4B, C ).

Reproductive biology and larval development. Ovigerous females with few eggs (n = 31 for one female). Size of undeveloped eggs (early-stage embryos without eyespot) 1.30 × 0.91 mm, size of developed eggs (late-stage embryos with eyes) 1.37 × 0.78 mm. Number and large size of eggs are indicative of completely suppressed larval development as defined by Lai & Shy (2009).

Ecology. Caridina clandestina , new species, is a highland species which is found around 1,100 m asl. So far, the new species is known to inhabit the upper part of Lariang catchment, the main Lariang River and the tributaries ( Fig. 1B ). The water current is moderately fast. During the 2017 sampling, the river water was murky and fast due to heavy rain the night before sampling day. Both sides of the river and the tributary banks were covered by tall grass and plants ( Fig. 4A ). The shrimps were hiding among the roots of the grass in the parts where water current was not strong.

No observation of the shrimps in their natural habitat was possible during the field trips. However, it was remarkable that both morphs were found in sympatry at most of the collection sites. During the 2017 fieldwork, the species was very abundant at all sites and was found together with the landlocked species Caridina sulawesi Cai & Ng, 2009 and Caridina parvidentata J. Roux, 1904 ( Figs. 1B , 7) as well as the amphidromous species Caridina villadolidi Blanco, 1939 . The new species is certainly landlocked given its large egg size and its rather restricted occurrence not extending to the lower reaches of the Lariang River in the Bada Valley ( Fig. 1B ).

Distribution. Endemic to Sulawesi, and only known from the upper reaches of the Lariang River watershed in the Napu Valley of Central Sulawesi ( Figs. 1 , 4A ).

Etymology. The new species name clandestina (Latin, nominative feminine singular for ‘clandestinus’, meaning secret, concealed) was proposed by Martin Rümmler, Berlin, Germany. His suggestion was picked as being most suitable for this unusual species, among almost 100 other suggestions given by radio listeners (see Introduction). The name refers to its previously well-hidden occurrence in a double sense – occurring only in a small remote area and thus not collected until 2005, and the two existing morphs of this species that were only recently discovered.

Common name. Secret Sulawesi Shrimp.

Remarks. Caridina clandestina , new species, is the first species of the genus Caridina showing a dimorphism of chelipeds. Among atyids, so far dimorphic chelipeds have only been described in two genera, i.e., Atyoida Randall, 1840 ( Chace, 1983) and Halocaridinides Fujino & Shokita, 1975 . In the genus Atyoida , the cheliped morphology might be either dimorphic such as in A. pilipes ( Newport, 1847) or polymorphic such as in A. bisulcata Randall, 1840 and A. serrata (C.S. Bate, 1888). This is due to their protandrous nature ( Chace, 1983).

Dimorphic chelae were also recently described in Halocaridinides socotraensis Fransen & Van Damme, 2018 . In contrast to the proposed new species, chela morphometry in H. socotraensis is continuous, and the two extreme ends of the morphometric spectrum are observed in the authors’ drawings ( Fransen & van Damme, 2018: figs. 6, 10, 11). In C. clandestina , new species, cheliped morphology is neither related to sex ( Fig. 5A ) nor size ( Fig. 5B ) and thus might be driven by microhabitat usage. Long versus short fingers and brushes of cheliped, and length to width ratio of carpus of first cheliped might also be considered as morphometric extremes in a single variable form. However, a scatterplot analysis clearly shows two distinct morphs without overlap ( Fig. 5A ).

With slender chelipeds adapted for filter-feeding, C. clandestina , new species, is similar to C. longidigita Cai & Wowor, 2007 from Lake Poso, and the two species also share a similar rostrum morphology. However, they can be easily differentiated by the sexual appendages: the endopod of first pleopod of males is subrectangular with conspicuous setae on all margins in C. clandestina ( Fig. 3N ), but triangular with a few setae in C. longidigita ( Cai & Wowor, 2007: fig. 5G). The appendix masculina on the second pleopod of males is much more slender, beset with strong short spiniform setae in the new species ( Fig. 3O ), but much less developed with few long spiniform setae distal in C. longidigita ( Cai & Wowor, 2007: fig. 5H). Specimens of both sexes can be differentiated by the preanal carina which is rounded in C. clandestina ( Fig. 2E ), but with a prominent spine in C. longidigita ( Cai & Wowor, 2007: fig. 4K). Dimorphic chelipeds have never been found in the latter species.

The male sexual appendages of C. clandestina , new species, resemble those of C. pareparensis species group, but can be distinguished from C. pareparensis De Man, 1892 , C. parvidentata J. Roux, 1904 , C. sulawesi Cai & Ng, 2009 , and C. leclerci Cai & Ng, 2009 , by the long, sigmoid rostrum unarmed in the distal half of dorsal margin (vs. short, either unarmed or with few dorsal teeth placed alongside the rostrum until close to the tip). Furthermore, C. clandestina can be distinguished from these species by lacking a prominent sexual dimorphism on the dactylus and propodus of the third pereiopod (vs. showing a remarkable dimorphism with numerous curved spiniform setae at the inner margin of the propodus in males). Although the general morphology of the proposed new species is closer to the lacustrine species from Lake Poso and the Malili lake system, the morphology of the sexual appendages places the species close to the C. pareparensis species group.

This finding is also supported by the molecular phylogenetic data. Caridina clandestina , new species, is recovered as a distinct and highly supported clade that is basal within the equally well-supported C. pareparensis species group ( Fig. 6 ). The new species differs from all other species in the C. pareparensis species group by a p-distance of at least 10.8% in COI and 3.8% in 16S. Caridina clandestina , new species, is subdivided into two moderately distinct subclades, of which only one has any support. The maximum p-distance is 2.8% in COI and 0.9% in 16S between the subclades, which match neither the two cheliped morphs nor geography.

Figures

Fig. 2. A, C–N, Caridina clandestina, new species, paratype male filter feeding morph (CL 5.6 mm) (ZMB 30207a), Lariang River, Central Sulawesi; B, Caridina clandestina, new species, paratype male short chelae morph (CL 4.7 mm) (ZMB 30203b), Napu Valley, stream, tributary of Lariang River, Central Sulawesi. A, cephalothorax and cephalic appendages; B, rostrum; C, telson; D, distal part of telson; E, preanal carina; F, uropodal diaeresis; G, antennular peduncle; H, scaphocerite; I, distal part of mandible; J, maxillula; K, maxilla; L, first maxilliped; M, palp of first maxilliped; N, second maxilliped. Scale bars: A–C, G–I, K–N = 1.0 mm; D, E, F, J = 0.5 mm.

Fig. 3. A–C, F, G, J–O, Caridina clandestina, new species, paratype male filter feeding morph (CL 5.6 mm) (ZMB 30207a), Lariang River, Central Sulawesi; D, E, H, I, Caridina clandestina, new species, paratype male short chelae morph (CL 4.7 mm) (ZMB 30203b), Napu Valley, stream, tributary of Lariang River, Central Sulawesi. A, third maxilliped; B, first pereiopod; C, fingers of first pereiopod; F, second pereiopod; G, fingers of second pereiopod; J, third pereiopod; K, dactylus of third pereiopod; L, fifth pereiopod; M, dactylus of fifth pereiopod; N, endopod of male’s first pleopod; O, endopod and appendix masculina on second pleopod. Scale bars: A–F, H–J, L, N, O = 1.0 mm; G, K, M = 0.5 mm.

Fig. 4. A, Lariang River, natural habitat of Caridina clandestina, new species; B, colouration of living specimen; C, specimen with chelae adapted for filter feeding.

Fig. 1. A, map of Sulawesi with the study area framed in red as shown on the detail map (B) of the Napu and Bada Valleys; B, the symbols show the sampling locations of Caridina clandestina, new species (black circles), C. sulawesi Cai & Ng, 2009 (white circles), C. parvidentata J. Roux, 1904 (square), and C. villadolidi Blanco, 1939 (diamond).

Fig. 5. A, scatterplot analysis of chelae morphology in both forms of Caridina clandestina, new species; B, chelae morphology in both forms of Caridina clandestina is not related to size of specimens.

Fig. 6. Molecular phylogeny of all described endemic species of Caridina from Sulawesi. Topology based on BI analysis of concatenated dataset of two mitochondrial gene fragments (16S and COI). Numbers on branches are, from the top, Bayesian posterior probabilities (>0.9) and ML/MP bootstrap values (>70). An asterisk indicates nodes with full support (1/100/100). The scale bar indicates the substitution rate.