Alpheus cyanoteles Yeo & Ng, 1996

Anker, Arthur, 2023, Revision of Alpheus euphrosyne De Man, 1897 and A. microrhynchus De Man, 1897, with description of three new species and taxonomic remarks on several other morphologically and ecologically similar snapping shrimps (Malacostraca: Decapoda: Alpheidae), Zootaxa 5282 (1), pp. 1-115 : 46-50

Alpheus cyanoteles Yeo & Ng, 1996

( Figs. 23 , 24A–D , 51E )

Alpheus cyanoteles Yeo & Ng 1996: 46 , figs. 4–7; Hurt et al. 2021: 7.

Alpheus paludosus (lap. cal.).— Johnson 1965: 9 (part.?); Johnson 1966: 430; Lovett 1981: 67 (not A. paludicola Kemp, 1915 ).

Alpheus paludicola . — Banner & Banner 1966: 135 (part.?) (not A. paludicola Kemp, 1915 ).

Type material. Holotype, male (cl 13.7 mm, tl 35.7 mm, chl 14.0 mm), ZRC 1996.1 , Malaysia, Johor, Kota Tinggi, Sungei Tementang , 01°52’0.81 N, 103°55’49.2 E, freshwater stream, leg. P.K.L. Ng et al., 05.06.1995.

Additional material. Malaysia: 1 male (cl 10.2 mm), 1 female (cl 15.6 mm, tl 42.5 mm, chl 22.0 mm), MNHN-IU-2018-5734, Johor, Sungei Tementang, leg. H.H. Tan et al., 23.10.2009; 1 male (cl 12.8 mm), OUMNH. ZC. 2013.05.5, Johor, Mawai, Sungei Tementang, Kota Tinggi —Kuantan road, km 268.5 Kuantan / km 60.5 Johor Bahru , 01°52.846’N, 103°55.799’E, 19 m above sea level, leg. H.H. Tan, S. De Grave & A. Anker, 29.05.2013; 1 male (cl 9.5 mm), 2 females (cl 9.5, 9.8 mm), OUMNH. ZC. 2013.05.6 –8, Johor, Mawai, Sungei Kayu, Kota Tinggi —Kuantan road, km 262 Kuantan / km 67 Johor Bahru, 0155.557’N, 10354.400’E, 26 m above sea level, leg. H.H. Tan, S. De Grave & A. Anker, 29.05.2013; 2 males (cl 7.8, 8.3 mm), 1 female (cl 8.2 mm), ZRC 2014.0686 , Johor, Sedili, Sungei Kayu, swamp forest, 02.1937; 1 male (cl 9.5 mm), 1 female (cl 10.3 mm), ZRC 1996.46 , Johor, no further data; 1 male (cl 7.5 mm), ZRC 1996.5 , Johor, Kota Tinggi, Sungei Selangi, stream banks, leg. P.K.L. Ng et al., 1994; 1 male (cl 14.2 mm, tl 36.0 mm, chl 19.5 mm), ZRC 2000.2131 , Sarawak, Serian, fish market, O. Chia, 23.06.1998; > 40 specimens of both sexes, (cl indet., no ov. females, small vial with detached eggs present), ZRC 2000.2185 , Sarawak, Serian, fish market, H.H. Tan, 29– 31.10.1997; 2 males (cl 11.5, 12.5 mm), 1 female (cl 12.2 mm), MNHN-IU-2018-5591, same collection data as for previous specimens.

Description. See Yeo & Ng (1996) for original description and illustrations; a complementary, revised diagnosis is provided below.

Diagnosis. Medium-sized species of Alpheus (maximal cl 16.7 mm, tl ~43.0 mm). Carapace and pleon smooth, without pubescence. Rostrum short, subtriangular, wider than long, reaching 0.3 length of first article of antennular peduncle, sometimes obliquely ascendant; rostral carina low, short, gently sloping into very shallow rostro-orbital furrows, flattening between orbital hoods. Orbital hoods somewhat angular in dorsal view. Pterygostomial angle broadly rounded. Telson ovate-rectangular, gently tapering towards posterior margin, about 1.3 times as long as maximal width; dorsal surface with faint, longitudinal median depression, latter without setae, and two pairs of small spiniform setae inserted at some distance from margin; posterior margin broadly rounded; posterolateral angle with two very small spiniform setae. Antennular peduncle with stylocerite slightly convex laterally, with tip acute, not overreaching distal margin of first article; ventromesial carina with reduced tooth, latter without acute point; second article about 2.1 times as long as wide. Antennal basicerite armed with sharp distoventral tooth; scaphocerite with lateral margin nearly straight; blade broad, separated from strong distolateral tooth by deep cleft; anterior margin of blade rounded, reaching well beyond distolateral tooth. Third maxilliped with antepenultimate article not broadened; penultimate article about four times as long as wide. Chelipeds with ventromesial margin of meri unarmed distally. Major chela of A. edwardsii - type, with fingers about 0.6–0.7 length of palm; mesial face of palm smooth, with low mesial transverse ridge and very shallow and narrow mesial longitudinal groove; lateral face of palm with subrectangular lateral longitudinal groove; dorsal shoulder rounded, sloping gently with angle inferior to 45° into dorsal transverse groove, not overhanging; ventral shoulder pronounced, slightly protruding in lateral view, broadly rounded; mesial and lateral surfaces of both fingers smooth, without granules; mesial face of pollex with well-developed mesial subdistal ridge extending from low proximal protuberance and bordered by two shallow depressions; dactylus with dorsal ridge slightly curved mesially, not protruding; dactylar plunger large, stout, distinct from dactylar ventral margin; distal portion of plunger with obliquely flattened ventromesial area; adhesive discs small. Male minor chela moderately stout, strongly balaeniceps, with fingers about 0.9 length of palm; all surfaces smooth, without granulation; mesial face of palm with poorly developed mesial longitudinal groove; lateral face of palm with narrow lateral longitudinal groove; dorsal transverse groove and shoulder not distinct; ventral transverse groove and shoulder at most indicated by shallow sinus; dactylus with proximal balaeniceps expansion about 2.2 times as long as maximal dactylar width, with rows of balaeniceps setae. Female minor chela not balaeniceps; palm smooth, without sculpture; fingers subequal to palm, simple, with sharp cutting edges, not gaping. Second pereiopod with ratio of carpal subarticles approximately equal to 5: 2: 1: 1: 1.5. Third pereiopod with ischium unarmed; merus more than six times as long as maximal width, unarmed; propodus with about eight stout spiniform setae on ventral margin and one pair of spiniform setae on distoventral margin adjacent to dactylus; dactylus about 0.3 length of propodus, trigonal-conical, tapering. Fifth pereiopod with ischium unarmed. Male second pleopod with appendix masculina about same length as appendix interna or up to 1.3 times longer. Uropod with both protopod lobes ending in sharp tooth distally. Eggs not numerous (usually less than 30), very large; egg diameter about 1.5 mm.

Colour pattern. Carapace pale brownish orange, with darker grey-brown saddle and some orange mottling, posterior margin with narrow, transverse, dark blue band; pleon with whitish or pale yellow ground colour; each pleonite with one broad, transverse, dark greyish blue band on posterior half; middle section of each pleonite occupied by diffuse, transverse, pale orange band; antennular peduncles and scaphocerite yellowish, marbled with orange brown; antennular and antennal flagella pale bluish green; mesial face of major chela orange-brown or olive-brown, with paler orange or yellowish areas, especially on dorsal and ventral transverse grooves; dorsal margin of pollex and distomesial ridge area conspicuous blue; dactylus orange-brown with olive tinge and with bright blue markings on margins; distal portion of both fingers pink; minor chela brown- or olive-orange, fingers darker; second to fifth pereiopods reddish; telson pale yellow-orange proximally, turning bluish distally; uropodal exopod whitishyellow proximally, conspicuously deep blue posterior to transverse suture; uropodal endopod pale orange with some blue distally ( Figs. 23 , 24A–D ).

Type locality. Sungei Tementang , Kota Tinggi, Johor, Malaysia .

Distribution. Restricted to Sunda area ( Fig. 51E ): southern Johor in peninsular Malaysia (Sedili basin, e.g., Sungei Tementang, Sungei Kayu); Sarawak, Malaysian part of Borneo (vicinity of Serian); southern Thailand (Pattalung Province: Tapi River, see remarks below).

Common name proposed. Freshwater snapping shrimp.

Ecology and biology. Alpheus cyanoteles is a true freshwater snapping shrimp living in small rivers and streams above tidal influence (pH 4.7–5.8), shaded by healthy or degraded rainforests ( Fig. 23E ). The syntopic fauna consists of primary and secondary freshwater fishes (e.g., Cyprinidae , Balitoridae , Cobitidae , Siluridae , Phallostethidae , Synbranchidae , Nandidae , Channidae ) as well as palaemonid ( Macrobrachium spp. ) and atyid ( Caridina spp. ) shrimps, and freshwater crabs ( Parathelphusa sp. ) (see Yeo & Ng 1996 for extensive description of the type locality). The low number of eggs and their large size suggest that the larval development of A. cyanoteles is highly abbreviated. Abbreviated, semi-direct and direct larval development is part of a series of physiological and reproductive adaptations of various decapod crustaceans to life in freshwater environments. However, the material from Serian ( Sarawak) may have been collected in slightly brackish conditions (see comments below).

Alpheus cyanoteles becomes increasingly popular in aquarium trade as the world’s only true freshwater snapping shrimp and is occasionally sold in pet shops in Malaysia and Singapore. In Borneo, A. cyanoteles is apparently also sold as food on some traditional markets (see below).

Taxonomic remarks. Alpheus cyanoteles appears to be most closely related to A. microrhynchus . These two species share a great number of morphological features and have abbreviated larval development.The only consistent morphological difference between them is the presence of a moderately large, sharp tooth on the distolateral margin of the antennal basicerite in A. cyanoteles ( Yeo & Ng 1996: fig. 5b); this tooth is either absent or minute in A. microrhynchus ( De Man 1897) . In life, however, A. cyanoteles and A. microrhynchus can be easily distinguished from each other by their colour patterns, especially by the pleon decorated with broad, dark blue bands, alternating with diffuse orange bands, in A. cyanoteles ( Figs. 23 , 24 ) vs. with less conspicuous, narrower dusky grey-blue bands, without intercalated orange bands, in A. microrhynchus ( Figs. 21 , 22 ). Yeo & Ng (1996: fig. 5e) did not illustrate or mention the rather conspicuous, sharp, mesial subdistal ridge on the pollex of the major chela in A. cyanoteles (well visible in Figs. 23B , 24A, D ). This ridge is also present in A. microrhynchus ( Figs. 19D , 21E ), A. euphrosyne (abbreviated as “msr in Fig. 4 ; see also Figs. 5C , 9B ), A. eurydactylus ( Figs. 11C, D , 16C ), and several other species of this group, including herein described new taxa (see below and refer to Table 1 ).

Alpheus cyanoteles can be easily separated from A. euphrosyne , A. eurydactylus and A. richardsoni by the non-expanded, more trigonal-conical dactyli on the third to fifth pereiopods; and the absence of a spiniform seta on the ischium of the third and fourth pereiopods (although it may be obsolete or absent in large specimens of these three species); from A. euphrosyne and A. eurydactylus by the mesially non-granulated major chela; the much less sculptured male minor chela; and the presence of a distolateral tooth on the antennal basicerite (absent in A. eurydactylus , absent or minute in A. euphrosyne ); from A. eurydactylus and A. richardsoni and by the shorter rostrum; from A. euphrosyne by the non-overhanging dorsal shoulder and the much stouter dactylar plunger of the major chela; and from A. richardsoni by the much stronger distomesial ridge on the major chela and the noticeably slenderer male minor chela ( Yeo & Ng 1996: figs. 5–7; cf. Figs. 6 , 7 , 14 , 15 in the present study; Banner & Banner 1982: fig. 74). In life, A. cyanoteles is easily distinguishable from A. euphrosyne , A. eurydactylus and A. richardsoni by several marked differences in the colour pattern (cf. Figs. 8 , 9 , 16–18 , 23 , 24 ). For separation of A. cyanoteles from other species see below or refer to Table 1 .

The record of A. cyanoteles from Tapi River in Thailand is based on colour photographs supplied by Jens Ķhne in 2013 (A. Anker, pers. obs.). This interesting photographic record extends the previously known range of A. cyanoteles from Johor to southern Thailand and suggests that the species may also occurs in other river systems along the eastern coast of Malay Peninsula.

The material from the Serian fish market in Sarawak (Malaysian Borneo) was identified as A. cyanoteles based on the combination of morphological characters, including the presence of a stout, sharp tooth on the antennal basicerite, which seems to be the only morphological feature reliably separating A. cyanoteles from the closely related A. microrhynchus , its presumed oligohaline sister species. Serian is situated approximately 45 km south of Kuching and most likely these specimens were collected in one of the tributaries of Sungai Sabang or Batang Sadong. Taking into account the marine / brackish origin of both A. cyanoteles and A. microrhynchus and the presumably relatively recent invasion of freshwater habitats, it is possible that A. cyanoteles is able to tolerate slightly brackish conditions. However, this assumption needs to be confirmed by collection of fresh material from Serian and other localities in Borneo, with colour photographs and more reliable ecological data (salinity, pH). A molecular comparison between the Johor and Sarawak material of A. cyanoteles is highly desirable as these populations may well be genetically isolated, possibly as a result of independent freshwater invasion events. This hypothesis is supported by the possibly semi-direct or at least highly abbreviated larval development in A. cyanoteles , which presumably has some limiting effects on the circulation of larvae in both fresh and brackish waters.

Hurt et al. (2021) recovered A. cyanoteles very distant from the remaining members of the A. edwardsii group. This rather unexpected result can be explained by the generally unsatisfactory sampling of the large and heterogeneous A. edwardsii group, which was confirmed to be non-monophyletic. The fact that several important taxa, such as A. euphrosyne , A. microrhynchus , A. richardsoni and other species of the A. edwardsii group associated with estuaries, mangroves, mudflats and brackish lagoons, were not included in the molecular analysis of Hurt et al. (2021), certainly created strong biases for other groups, and may have resulted in a long branch attraction artifact for A. cyanoteles .

Figures

FIGURE 4. Alpheus euphrosyne De Man, 1897: chelipeds of male (cl indet.) from Sumatra, Indonesia (ZMA Crus.D.202726) showing main features and terminology used in the present study; A—major (right) cheliped, lateral view; B—same, mesial view; C—minor (left) cheliped, mesial view; D—same, lateral view. Abbreviations (in alphabetical order): ad—adhesive disks (plaques) on dactylus and palm (small on major chela, highly reduced in minor chela); be—balaeniceps expansion of minor chela dactylus; ddr—dorsal ridge of major chela dactylus (dactylar dorsal ridge); dla—dorsolateral angle of major chela pollex; dlt—dorsolateral tooth of major / minor chela palm; dma—dorsomesial angle of major chela pollex; dmt—distomesial tooth of major / minor chela palm; dp—plunger of major chela dactylus (dactylar plunger); ds—dorsal shoulder of major / minor chela palm; dtg—dorsal transverse groove of major / minor chela palm (also known as dorsal notch); lbd—lateral balaeniceps ridge of minor chela dactylus; lbp—lateral balaeniceps ridge of minor chela pollex; li—linea impressa of major / minor chela palm; lld—lateral longitudinal depression (groove) of major / minor chela palm; ltr—smooth lateral transverse ridge of major chela palm (often poorly developed); mbd—mesial balaeniceps ridge of minor chela dactylus; mbp—mesial balaeniceps ridge of minor chela pollex; mld—mesial longitudinal depression (groove) of major / minor chela palm; msr—mesial subdistal ridge on major chela pollex; mtr—smooth mesial transverse ridge of major chela palm (often poorly developed); pf—fossa (socket) of major chela pollex; vs—ventral shoulder of major / minor chela palm; vtg—ventral transverse groove of major / minor chela palm (also known as ventral notch).

FIGURE 5. Alpheus euphrosyne De Man, 1897: neotype, male (cl 16.6 mm) from Surabaya, Java, Indonesia (RMNH Crus. D.49669); A—habitus, dorsal view; B—frontal region, dorsal view; C—major (left) chela in situ, mesial view; D—same, lateral view; E—minor (right) chela in situ, dorsal view. Refer to A for scale.

FIGURE 6. Alpheus euphrosyne De Man, 1897: male (cl 16.4 mm) from Angsila, Thailand (MNHN-IU-2018-5593); A— frontal region, dorsal view; B—telson, dorsal view; C—ventromesial carina of first article of antennular peduncle, lateral view; D—antennal basicerite, lateral view; E—third maxilliped, lateral view; F—second pereiopod, lateral view; G—third pereiopod, lateral view; H, I—same, dactylus, mesial (H) and dorsal (I) views; J—fifth pereiopod, lateral view; K—same, propodus and dactylus, mesial view; L—second pleopod, appendices masculina and interna, anterior view; M—left uropod, dorsal view; N—right uropod, detail of distolateral angle.

FIGURE 7. Alpheus euphrosyne De Man, 1897: male (cl 16.4 mm) [A–G] and female (cl 18.0 mm) [H] from Angsila, Thailand (MNHN-IU-2018-5593); A—major (right) cheliped, chela, carpus and distal part of merus, mesial view; B—same, chela, lateral view; C—same, coxa to carpus, lateral view; D—same, dactylus, lateral view; E—male minor (left) cheliped, chela, carpus and distal part of merus, mesial view; F—same, chela, lateral view; G—same, coxa to carpus, lateral view; H—female minor chela, lateral view.

FIGURE 8. Alpheus euphrosyne De Man, 1897: male (cl indet.) from Satun, Thailand, in lateral (A) and dorsal (B) views (deposition unknown). Photographs courtesy of Rueangrit Promdam.

FIGURE 9. Alpheus euphrosyne De Man, 1897: male (cl 16.8 mm) from Pattani, Thailand (ZRC 2014.0672), in dorsal view (A), with details of the frontal area and chelipeds (B). Photographs courtesy of Sukree Hajisamae.

FIGURE 11. Alpheus eurydactylus De Man, 1920: lectotype, male (cl 13.8 mm) from Surabaya, Java, Indonesia (RMNH Crus.D.49670 = ZMA Crus.D.102536); A—cephalothorax and chelipeds, dorsal view; B—frontal region, dorsal view; C, D— major (left) cheliped, mesial view, with slightly different angles and illuminations (slightly more ventral and enhancing mesial subdistal ridge on pollex in D). Refer to A for scale.

FIGURE 14. Alpheus eurydactylus De Man, 1920: male (cl 16.4 mm) from Pattani, Thailand (ZRC 2014.0672) [A–H, J–N]; ovigerous female (cl indet.) from Johor, Malaysia (MNHN-IU-2018-5598) [I]; A—frontal region, dorsal view; B—telson, dorsal view; C—ventromesial carina of first article of antennular peduncle, lateral view; D—antennal basicerite, lateral view; E—third maxilliped, lateral view; F—second pereiopod, lateral view; G—third pereiopod, lateral view; H—same, dactylus, dorsal view; I—same, ischium, lateral view; J—fifth pereiopod, lateral view; K—same, propodus and dactylus, mesial view; L—same, basis and ischium, lateral view; M—second pleopod, appendices masculina and interna, anterior view; N—right uropod, dorsal view.

FIGURE 15. Alpheus eurydactylus De Man, 1920: male (cl 16.4 mm) from Pattani,Thailand (ZRC 2014.0672) [A–G]; ovigerous female (cl indet.) from Johor, Malaysia (MNHN-IU-2018-5598) [H]; A—major (right) cheliped, chela, carpus and distal part of merus, lateral view; B—same, ischium to carpus, lateral view; C—same, chela and carpus, mesial view; D—same, dactylus, lateral view; E—male minor (left) cheliped, chela and carpus, mesial view; F—same, chela, lateral view; G—same, ischium to carpus, lateral view; H—female minor chela, lateral view.

FIGURE 16. Alpheus eurydactylus De Man, 1920: male (cl indet.) from Can Gio, Vietnam (ZMMU) [A]; female (cl indet.) from the same locality (ZMMU) [B, C]; male (cl indet.) from near Bangkok, Thailand (deposition unknown) [D]: A—habitus, dorsal view; B, D—same, lateral view; C—major cheliped, mesial view. Photographs courtesy of Ivan N. Marin (A–C) and Sukkrit Nimitkul (D).

FIGURE 19. Alpheus microrhynchus De Man, 1897: neotype, male (cl 16.3 mm) from Kabupaten Sambas, Kalimantan Barat, Indonesia (ZRC 2000.2193); A—habitus, dorsal view; B—frontal region, dorsal view; C—major (right) cheliped, lateral view; D—same, mesial view; E—minor (left) cheliped, lateral view; F—same, mesial view. Refer to A for scale.

FIGURE 21. Alpheus microrhynchus De Man, 1897: ovigerous female (cl indet.) imported to Germany from Thailand [A]; ovigerous female (cl indet.) imported to Singapore from Thailand [B–E]: A, B—habitus, lateral view; C—pleon and tail fan, dorsal view; D—pleon, ventrolateral view E—frontal region and chelipeds, dorsal view. Aquarium-kept specimens, probably not preserved / deposited. Note the low number and large size of developing embryos inA and D. Photographs courtesy of Chris Lukhaup (A) and Paul Ng (B–E).

FIGURE 22. Alpheus microrhynchus De Man, 1897: female (cl indet.) imported to Singapore from Thailand; A, B—habitus, dorsal view (with one Singapore dollar coin, diameter 22.4 mm, for scale in B); C—detail of frontal margin; D—major (right) chela, mesial view; E—posterior pleonites and tail fan, d orsal view. Aquarium-kept specimen, probably not preserved / deposited. Photographs courtesy of Paul Ng.

FIGURE 23. Alpheus cyanoteles Yeo & Ng, 1996: ovigerous female (cl indet.) [A, B] and female (cl indet.) [C, D] from an unknown locality in southern Johor, Malaysia;A—habitus, lateral view; B—same, dorsal view; C—same, lateral view; D—detail of frontal margin of carapace and left antenna, lateral view. Aquarium-kept specimens, probably not deposited. Photographs courtesy of C.H. Wah (A, B) and Heok-Hui Tan (C, D).

FIGURE 24. Alpheus cyanoteles Yeo & Ng, 1996: male (cl 9.5 mm) from Sungei Tementang, southern Johor, Malaysia (OUMNH.ZC. 2013.05.6); A—habitus, dorsal view; B—frontal region, dorsal view; C—tailfan, dorsal view; D—chelipeds (major chela widely opened), mesial view; E—H.H. Tan and S. De Grave collecting A. cyanoteles in its natural habitat, a small stream in southern Johor. Photographs by the author.

FIGURE 51. Distributional maps for species of Alpheus treated in this study: A—A. eurphrosyne De Man, 1897; B—A. eurydactylus De Man, 1920; C—A. richardsoni Yaldwyn, 1971; D—A. microrhynchus De Man, 1897; E—A. cyanoteles Yeo & Ng, 1996; F—A. nomurai sp. nov.