Caridina holthuisi, Rintelen & Cai, 2009

Rintelen, Kristina von & Cai, Yixiong, 2009, Radiation Of Endemic Species Flocks In Ancient Lakes: Systematic Revision Of The Freshwater Shrimp Caridina H. Milne Edwards, 1837 (Crustacea: Decapoda: Atyidae) From The Ancient Lakes Of Sulawesi, Indonesia, With The Description Of Eight New Species, Raffles Bulletin of Zoology 57 (2), pp. 343-452 : 364-369

Caridina holthuisi , new species

( Figs. 10-12 , Table 5)

Caridina opaensis – Woltereck, 1937a: 222, fig. I.4, pls. 3,6 (locality: Matanno [Matano], Soroako).

Cardina opaensis – Brooks, 1950: 168 (erroneous spelling).

Material examined. – Holotype – ovigerous female (cl 3.2 mm)( MZB Cru 2125), Lake Matano , south shore, canal between island and mainland, 02°28.46'S, 121°15.83'E, loc. 62-03, on leaf litter, coll. K. & T. von Rintelen, 1 Oct.2003.

Paratypes ( Lake Matano ) – 7 ex. ( ZMB 29272), south shore, 02°27.85'S, 121°13.87'E, loc. 125-04, on leaf litter, coll. K . & T. von Rintelen , 1 Aug.2004 ; 5 ex. ( ZMB 29065, some SEM material), south shore, 02°27.84'S, 121°13.88'E, loc. 63-03, on leaf litter, coll. K . & T. von Rintelen , 24 Sep.2003 ; 4 ex. ( ZMB 29073), south shore, at small islands, 02°28.461'S, 121°15.591'E, loc. 137-04, on macrophytes, coll. K . & T. von Rintelen , 24 Jul.2004 ; 44 ex. ( MZB Cru 1790, n=22; ZMB 29075, n=22, some SEM material), south shore, canal between island and mainland, 02°28.46'S, 121°15.83'E, loc. 62-03, on leaf litter, coll. K . & T. von Rintelen , 1 Oct.2003 ; 24 ex. ( MZB Cru 1791, n=11; ZMB 29105, n=13, some SEM material), north shore, 02°26.36'S, 121°19.03'E, loc. 84-03, on leaf litter, coll. K . & T. von Rintelen , 1 Oct.2003 ; 6 ex. ( ZMB 29107, some SEM material), south shore, Soroako , Salonsa, Pantai Ide, 02°30.89'S, 121°20.53'E, loc. 40-03, on mixed substrate, coll. K . & T. von Rintelen , 17 Sep.2003 ; 1 ex. ( ZMB 29139), north shore, 02°29.75'S, 121°25.81'E, loc. 42-03, on rocks, coll. K . & T. von Rintelen , 17 Sept. 2003 ; 4 ex. ( ZMB 29140), south shore, 02°28.5'S, 121°15.55'E, loc. 139-04, on mixed substrate, coll. K . & T. von Rintelen , 24 Jul.2004 ; 16 ex. ( MZB Cru 1792, n=8; ZMB 29189, n=8), at small islands, 02°28.458'S, 121°15.57'E, loc. F4-02, on mixed substrate, coll. F. Herder, 2 Nov.2002 ; 1 ex. ( ZMB 29225), north shore, 02°27.28'S, 121°21.21'E, loc. 98-03, on leaf litter, coll. K . & T. von Rintelen , 5 Oct.2003 ; 4 ex. ( ZMB 29227), south shore, 02°27.84'S, 121°13.88'E, loc. 01-05, on macrophytes, coll. K . & T. von Rintelen , 1 Jan.2005 ; 1 ex. ( ZMB 29231), south shore, Soroako, Salonsa , INCO boat house, 02°30.71'S, 121°20.45'E, loc. 19-03, on rocks, coll. K . & T. von Rintelen , 19 Sep.2003 ; 6 ex. ( ZMB 29232, n=6 and some juveniles), north shore, 02°28.42'S, 121°24.21'E, loc. 41-03, on leaf litter, coll. K . & T. von Rintelen , 17 Sep.2003 ; 9 ex. ( MZB Cru 1793, n=4; ZMB 29286, n=5, some SEM material), northwest shore, 02°25.742'S, 121°13.797'E, loc. 134-04, on leaf litter, coll. K . & T. von Rintelen , 23 Jul.2004 ; 11 ex. ( MZB Cru 1794, n=5; ZMB 29185, n=6), Matano catchment, river, near mouth at northwest corner of Lake Matano, 02°25.88'S, 121°13.08'E, loc. 24-03, on leaf litter, coll. K . & T. von Rintelen , 13 Sep.2003 .

Paratypes ( Lake Mahalona ) – 12 ex. ( MZB Cru 1795, n=6; ZMB 29059, n=6), Lake Mahalona (no further details given), loc. F3-02, substrate unknown, coll. J. Frommen, 1 Nov.2002 ; 9 ex. ( ZMB 29063, n=9 and some juveniles, some SEM material), east shore, at mouth of Petea River , 02°34.54'S, 121°30.48'E, loc. 55-03, on leaf litter, coll. K . & T. von Rintelen, 23 Sep.2003 ; 11 ex. ( MZB Cru 1796, n=5; ZMB 29324, n=6), east shore, estuary of Ponsoa River, 02°35.101'S, 121°30.681'E, loc. 146-04, on Ottelia , coll. P. Koller, K . & T. von Rintelen, 3 Aug.2004 .

Paratypes ( Lake Towuti ) – 33 ex. ( MZB Cru 1797, n=15; ZMB 29036, n=18), southwest shore, west of Cape Tetetu, 02°54.13'S, 121°23.78'E, loc. 76-03, on leaf litter, coll. K . & T. von Rintelen , 28 Sep.2003 ; 3 ex. ( ZMB 29078, some SEM material), west shore, at entrance to outlet bay, Cape Larona, 02°48.43'S, 121°24.75'E, loc. 73-03, on leaf litter, coll. K . & T. von Rintelen , 27 Sep.2003 ; 21 ex. ( MZB Cru 1798, n=11; ZMB 29228, n=10 and some juveniles), east shore, 02°40.84'S, 121°41.32'E, loc. 87-03, on leaf litter, coll. K . & T. von Rintelen , 2 Oct.2003 ; 4 ex. ( ZMB 29303, some SEM material), northeast shore, at Lengkona, 02°40.483'S, 121°41.382'E, loc. 116-04, on leaf litter, coll. K . & T. von Rintelen , 28 Jul.2004 ; 3 ex. ( MZB Cru 1799), west shore, west of Cape Timbalo , 02°42.631'S, 121°26.389'E, loc. 145-04, on mixed substrate, coll. K . & T. von Rintelen , 26 Jul.2004 ; 2 ex. ( MZB Cru 1800), northwest shore, south of Timampu , 02°39.466'S, 121°25.859'E, loc. 140-04, on macrophytes, coll. K . & T. von Rintelen , 25 Jul.2004 .

Comparative material examined. – Caridina opaensis Roux, 1904: 547 , pl. 9, Figs. 8-10 (type locality: Southeast Sulawesi, Lake Opa , 30 m above sealevel).

Syntypes – 2 females (cl 2.9-3.3 mm) ( NHMB 9 a), Southeast Sulawesi, Opa, Sulawesi, Indonesia, coll. Sarasin , 1904.

Others (all Southeast Sulawesi): 1 ex. ( ZMB 29008), Benua River , northern arm, 04°13.388'S, 122°6.397'E, loc. 85-05, coll. M. Glaubrecht, K . & T. von Rintelen , 31 May 2005 ; 1 ex. ( ZMB 29010), stream at road Kendari – Lapuko , near Mulyasari, 04°7.34'S, 122°36.82'E, loc. 103-05, coll. K . & T. von Rintelen , 1 Jun.2005 ; 1 ex. ( ZMB 29018), stream at Labeala , east of Pundihaha, road Kendari – Kolaka, 03°57.987'S, 122°20.739'E, loc. 77-05, coll. M. Glaubrecht, K . & T. von Rintelen , 30 May 2005 ; 1 ex. ( ZMB 29338), stream in Pruiala , north of Aopa area, 04°3.67'S, 122°6.845'E, loc. 83-05, coll. M. Glaubrecht, K . & T. von Rintelen , 31 May 2005 ; 1 ex. ( ZMB 29339), Simbune River , approx. 1 km northeast of Raterate, road Kendari – Kolaka, 04°2.326'S, 121°54.204'E, loc. 79-05, coll. M. Glaubrecht, K . & T. von Rintelen , 30 May 2005 ; 1 ex. ( ZMB 29340), Humbuti River , northwest of Abuki, 03°38.91'S, 121°52.38'E, loc. 78-05, coll. M. Glaubrecht, K . & T. von Rintelen , 30 May 2005 .

Description. – Carapace length 2.3-3.8 mm (n=29). Rostrum ( Fig. 11 A-E; Table 5) usually broad, reaching near or slightly beyond end of scaphocerite, 0.6-1.2 times as long as carapace (n=32), armed dorsally with 14-28 teeth (including 4-8 teeth posterior to orbital margin), armed ventrally with 3-7 teeth. Antennal spine situated below inferior orbital angle. Pterygostomial angle broadly rounded. Eyes well developed, anterior end 0.5-0.6 times length of basal segment of antennular peduncle (n=6). Antennular peduncle 0.8-1.0 times as long as carapace (n=6), second segment 1.6-2.1 times length of third segment, third segment 0.3-0.4 times length of basal segment. Stylocerite reaching 0.9-1.0 times length of basal segment of antennular peduncle (n=6). Scaphocerite ( Fig. 11H ) 3.8-4.8 times as long as wide (n=5).

Sixth abdominal somite 0.5-0.7 times length of carapace (n=15), 1.4-1.8 times as long as fifth somite (n=15), 0.9-1.0 times length of telson (n=10). Telson ( Fig. 11 J-K) 2.9-3.5 times as long as wide (n=6), distal margin rounded, without projection, with 3-4 pairs of spinules and 1 pair of dorsolateral spinules; distal end with 3-4 pairs of spines, lateral pair longer than intermediate pairs, median pair shortest. Preanal carina ( Fig. 11I ) with a spine. Uropodal diaeresis ( Fig. 11L ) with 12-13 movable spinules (n=5).

5 pairs of pleurobranchs well developed; 3 pairs of arthrobranchs, 2 on third maxillipeds, with second pair strongly reduced in size, 1 pair on first pereiopod; 1 pair of podobranchs on second maxilliped reduced strongly to a laminate form. Epipod present on first two pereiopods. Incisor process of mandible ( Fig. 12A ) ending in a row of 3-4 small teeth, molar process truncated. Lower lacinia of maxillula ( Fig. 12B ) broadly rounded, upper lacinia elongate, with numerous distinct teeth and setae on inner margin, palp slender. Upper endites of maxilla ( Fig. 12C ) subdivided, palp short, scaphognathite tapering posteriorly with numerous long, curved setae at posterior end. Distal end of palp of first maxilliped ( Fig. 12F ) triangular, with a finger-like projection; flagellum of the exopod very elongated, endopod high, not exceeding the flagellum of exopod in length. Second maxilliped ( Fig. 12E ) typical. Third maxilliped ( Fig. 12D ) with ultimate segment distinctly shorter than penultimate segment.

cl (mm) 2.3-3.8 2.8 ± 0.4 2.7 29 rl / cl 0.6-1.2 0.9 ± 0.1 0.9 32 n dorsal rostral teeth 14-28 20 ± 3 20 32 n ventral rostral teeth 3-7 5 ± 1 5 32 abds6 / cl 0.5-0.7 0.6 ± 0.1 0.6 15 abds6 / abds5 1.4-1.8 1.6 ± 0.1 1.6 15 abds6 / h tel 0.9-1.0 0.9 ± 0.0 0.9 10 h tel / w tel 2.9-3.5 3.3 ± 0.2 3.4 6 n spines uropodal diaeresis 12-13 13 ± 1 13 5 h ch1 / w ch1 1.8-2.3 2.1 ± 0.2 2.1 18 h ch1 / h ca1 1.1-1.4 1.2 ± 0.1 1.2 17 h ca1 / w ca1 2.0-3.1 2.7 ± 0.3 2.7 13 h ch2 / w ch2 2.3-3.5 2.8 ± 0.3 2.8 18 h ch2 / h ca2 0.7-0.9 0.8 ± 0.1 0.7 22 h ca2 / w ca2 4.3-7.0 5.7 ± 0.9 5.7 18 n spines p3 3-6 4 ± 1 4 5 n spines p5 27-39 34 ± 5 33 5

Chela and carpus of first pereiopod distinctly stouter and broader than chela and carpus of second pereiopod ( Fig. 11 S-T); chela of first pereiopod 1.8-2.3 times as long as wide (n=18), 1.1-1.4 times length of carpus (n=17); tips of fingers rounded, without hooks; dactylus 0.9-1.3 times as long as palm (n=9); carpus 2.0-3.1 times as long as wide (n=13), 1.1-1.3 times length of merus (n=9). Chela of second pereiopod 2.3-3.5 times as long as wide (n=18), 0.7-0.9 times length of carpus (n=22); tips of fingers rounded, without hooks, dactylus 1.0-1.4 times as long as palm (n=9); carpus 4.3-7.0 times as long as wide (n=18), 1.2-1.5 times as long as merus (n=10).

Third pereiopod ( Fig. 11M,O ) slender, dactylus 4.2-5.0 times as long as wide (terminal spine included, without spines of flexor margin; n=5), terminating in one large claw with 3-6 accessory spines on flexor margin; propodus 8.8-13.5 times as long as wide, 2.8-3.8 times as long as dactylus; carpus 4.8-5.6 times as long as wide, 0.6-0.7 times as long as propodus, 0.5-0.6 times as long as merus; merus 7.2-8.8 times as long as wide, bearing 3-4 strong, movable spines on posterior margin of outer surface.

Fifth pereiopod slender ( Fig. 11N,P ), dactylus 3.7-6.3 times as long as wide (terminal spine included, without spines of flexor margin; n=5), terminating in one large claw with 27- 39 accessory spines on flexor margin; propodus 11.0-15.0 times as long as wide, 2.7-3.1 times as long as dactylus; carpus 4.6-5.5 times as long as wide, 0.5 times as long as propodus, 0.6-0.7 times as long as merus; merus 6.5-8.5 times as long as wide, bearing 2-3 strong, movable spines on posterior margin of outer surface.

Endopod of male first pleopod ( Fig. 11Q ) elongated triangular, 1.8-2.5 times as long as proximally wide (n=5), without appendix interna. Appendix interna of male second pleopod ( Fig. 11R ) 0.8-0.9 times length of appendix masculina (n=5).

Ovigerous females with 19- 25 eggs (n= 2 females); egg size 0.8-1.0 x 0.5-0.6 mm (n=38, eggs with and without eyes).

Distribution. – Endemic to the Malili lake system; occurring in all three major lakes and in Petea River, widely distributed within each lake ( Fig. 10B ).

Biology and ecology. – C. holthuisi is a soft substrate dweller, mainly found under dead leaves (leaf litter), but also sporadically on macrophytes. Its colour pattern is similar to its substrate, the usually dark brown leaves that can be found covering the shallow bottom in various shore areas. When disturbed, C. holthuisi rather tries to escape downwards than in other directions to hide under its substrate. When a pile of dead leaves is sampled with a dip net, specimens usually accumulate at the bottom of the net.

Colour pattern. – The body, and often also the appendages too, show a vivid dark brown colour similarly to the brown colour of the species’ leaf substrate ( Fig. 10A ). Various white-beige markings (usually transversal stripes or a dorsal longitudinal stripe) are possible. Eggs are also dark brown.

Etymology. – Caridina holthuisi , new species, is named in honour of L.B. Holthuis as one of the well-known carcinologist of our time, who also contributed greatly to our knowledge of the shrimp genus Caridina .

Taxonomic remarks. – Woltereck (1937a, b) described some specimens from Lake Matano as Caridina opaensis Roux, 1904 , and thus mentioned it as the only non-endemic species in the Malili lake system. Brooks (1950: 169) even discussed the origin of Lake Matano’s fauna based on the presumed non-endemism of this species. However, albeit some first glance similarities between the true C. opaensis Roux, 1904 from Southeast Sulawesi and Woltereck’s C. opaensis , i.e. C. holthuisi , new species ( Fig. 29 F-G), both are morphologically distinct species and Woltereck’s ‘ C. opaensis’ is here considered as to be C. holthuisi , new species. C. holthuisi can be distinguished from C. opaensis by its generally smaller size (cl 2.3-3.8, mean 2.8 vs. 2.9-4.9, mean 4.0, n= 23 in C. opaensis ), a generally longer rostrum compared to the carapace length (0.6-1.2, mean 0.9, vs. 0.40.8, mean 0.7, n= 25 in C. opaensis ), a lower number of movable spinules on the uropodal diaeresis (12-13 vs. 14-19, n=6, in C. opaensis ), and a lower number of accessory spines on flexor margin of dactylus of the third and fifth pereiopod (3-6 and 31-39 vs. 6 and 54-64, n= 3 in C. opaensis ).

C. holthuisi slightly resembles C. dennerli , but differs not only in its substrate preference (leaf litter vs. rocks in C. dennerli ), or colour pattern (compare respective description), but also by a broader rostrum, a different number of ventral teeth on the rostrum (5-11, median 9 vs. 3-7, median 5), and distinctly stouter pereiopods in C. holthuisi (for example chela of first pereiopod 1.8-2.3, median 2.1 vs. 2.4-3.8, median 2.7 in C. dennerli ).

C. holthuisi can resemble C. masapi , but the rostrum in C. masapi usually differs by a more or less dense denticulation on the dorsal margin, and a straighter and broader shape (vs. usually with a conspicuous unarmed gap on the dorsal margin and a more slender and cambered shape in C. masapi ).

Besides the morphological differences, C. holthuisi is genetically distinct from C. opaensis ( Fig. 63 ). All sequenced specimens of C. opaensis from and around the type locality are not closely related to any of the ancient lake species (compare von Rintelen et al., in review). On the other hand, all specimens of C. holthuisi appear within the Malili clade. Therefore, they must be regarded as truly endemic to the lakes. However, within the Malili clade, C. holthuisi is not monophyletic, but appears in two allopatric clades ( Figs. 10B , 63-64 ). The existence of two cryptic species is therefore possible despite the fact that morphological differences have not been observed so far.

Figures

Fig. 10. Caridina holthuisi from the Malili lake system. A. Distribution (the equal sign roughly marks the geographic boundary between the two genetic clades; compare taxonomic remarks). B. Colour pattern of living animal (not to scale). Pictures courtesy of Chris Lukhaup.

Fig. 11. Caridina holthuisi from the Malili lake system and C. opaensis from SE Sulawesi. Cephalothorax and cephalic appendages from: A. Female, MT (ZMB 29286); B. Male, MT (ZMB 29286); C. Woltereck’s drawing of the rostrum (modified from 1937a); D. Female, MT (ZMB 29107); E. Female, TW (ZMB 29303); F. Female, SE Sul (ZMB 29338); G. Female, SE Sul (ZMB 29339). H. Scaphocerite, male, MT (ZMB 29232); I. Preanal carina; J. Telson, female, MT (ZMB 29105); K. Distal end of telson; L. Uropodal diaeresis; M. Third pereiopod, female MT (ZMB 29075); N. Fifth pereiopod; O. Dactylus of third pereiopod; P. Dactylus of fifth pereiopod; Q. Endopod of male first pleopod, MT (ZMB 29232); R. Appendix masculina of male second pleopod; S. SEM image of chela and carpus of first and second pereiopods, female, MT (ZMB 29286); T. First pereiopod, female (ZMB 29075); U. Second pereiopod. Scale bars: A-B, D-H = 1.0 mm; I-J, M-N, Q-U= 0.5 mm; K-L, O-P = 0.1 mm; C = no scale available.

Fig. 12. Caridina holthuisi from the Malili lake system. A. Mandible (ZMB 29286); B. Maxillula; C. Maxilla; D. third maxilliped; E. second maxilliped; F. first maxilliped. Scale bars: A-F = 1mm.

Fig. 8. Caridina glaubrechti from the Malili lake system. A. Cephalothorax and cephalic appendages, female (ZMB 29053); B. Preanal carina, male (ZMB 29109); C. Uropodal diaeresis, female (ZMB 29053); D. Scaphocerite, male (ZMB 29109); E. Dactylus of third pereiopod, female (ZMB 29074), F. Telson, female (ZMB 29053); G. Telson, another female (ZMB 29053); H. Third pereiopod, female (ZMB 29074); I. Dactylus of fifth pereiopod; J. Fifth pereiopod; K. Endopod of male first pleopod (ZMB 29109); L. Appendix masculina of male second pleopod; M. Distal end of telson, female (ZMB 29053); N. Distal end of telson, another female (ZMB 29053); O. First pereiopod, female (ZMB 29053); P. Second pereiopod; Q. SEM image of chela and carpus of first and second pereiopods, female (ZMB 29053). Scale bars: A, D = 1.0 mm; B, F-H, J-L, O-Q = 0.5 mm; C, E, I, M-N = 0.1 mm.

Fig. 9. Caridina glaubrechti from the Malili lake system. A. Mandible (ZMB 29053); B. Maxillula; C. Maxilla; D. second maxilliped; E. third maxilliped; F. first maxilliped. Scale bars: A-F = 1mm.

Fig. 29. Caridina parvula from the Malili lake system. A. Mandible (ZMB 29064); B. Maxillula; C. Maxilla; D. third maxilliped; E. second maxilliped; F. first maxilliped. Scale bars: A-F = 1mm.

Fig. 63. Bayesian Inference phylogram (mtDNA, 16S and COI) of Caridina from the ancient lakes of Sulawesi (for other taxa compare von Rintelen et al., in review). Numbers on branches are, from top, Bayesian posterior probabilities, ML and MP bootstrap values. The scale bar indicates the number of substitutions per site. For each sequenced specimen museum accession numbers are provided. Locality abbreviations (compare Fig. 1): Lam (Lampesue River catchment), LT (Lake Lontoa), MHL (Lake Mahalona), MS (Lake Masapi), MT (Lake Matano), MTca (Lake Matano catchment), Pat (Patingko River), Pon (Ponsoa River), TW (Lake Towuti), TWca (Lake Towuti catchment), PS (Lake Poso), PSca (Lake Poso catchment), SSul (South Sulawesi), SESul (Southeast Sulawesi).