Caridina incolor, Feng & Chen & Guo, 2021

Feng, Shuo, Chen, Qing-Hua & Guo, Zhao-Liang, 2021, Integrative taxonomy uncovers a new stygobiotic Caridina species (Decapoda, Caridea, Atyidae) from Guizhou Province, China, ZooKeys 1028, pp. 29-47 : 29

Caridina incolor sp. nov. Figures 3 , 4 , 5

Material examined.

Holotype: Adult male (FU, 2018-11-27-01), tl 21.8 mm, cl 5.1 mm, rl 3.0 mm; Yaoshui Cave , Mengtang Village , Wangmeng Township , Daqikong scenic area, Libo County, Guizhou Province, China (25°17'1"N, 107°45'8"E, alt. 520.0 m), November 27, 2018.

Paratypes: 1 male (FU, 2018-11-27-02) tl 25.9 mm, cl 6.1 mm, rl 3.1 mm; 16 males (FU, 2018-11-27-03) tl 17.4-25.9 mm, cl 4.2-6.0 mm, rl 2.4-3.4 mm; 10 females (FU, 2018-11-27-04), tl 17.8-25.2 mm, cl 4.5-6.1 mm, rl 2.4-3.4 mm; cl 4.9-6.6 mm, same data as for holotype . Paratypes: 6 males (FU, 2018-11-27-05) tl 18.4-25.1 mm, cl 4.4-5.9 mm, rl 2.5-3.0 mm; 9 females (3 ovigerous) (FU, 2018-11-27-06), tl 17.5-25.0 mm, cl 4.5-6.0 mm, rl 2.4-3.1 mm; cl 5.0- 6.3 mm, same data as for holotype. Two samples from (FU, 2018-11-27-05) and three samples from (FU, 2018-11-27-06) were sequenced .

Comparative material examined.

Caridina sinanensis Xu, Li, Zhang and Guo 2020. Holotype: Adult male (FU, 2019-01-25-01), tl 16.7 mm, cl 4.8 mm, rl 1.5 mm; a cave river at Pengjiaao , Tangtou Town, Sinan County, Guizhou Province, southwestern, China (27°44'10"N, 108°11'58"E, alt. 294.7 m), January 25, 2019. Paratypes : 1 male (FU, 2019-01-25-02) cl 5.4 mm; 1 male (FU, 2019-01-25-03) cl 6.8 mm; 1 male (FU, 2019-01-25-04) cl 4.8 mm; 2 males (FU, 2019-01-25-05), cl 4.2-6.2 mm; 20 females (9 ovigerous) (FU, 2019-01-25-05), cl 4.9-6.6 mm.

Diagnosis.

Body and appendages without coloration, translucent. Rostrum slender, slightly elevated at base, reaching to base of 3rd segment of antennular peduncle to end of scaphocerite; straight, slightly sloping downwards, sometimes with tip turned upwards; rostral formula 6-10+11-27/4-15. First pereiopod carpus 0.83-0.91 × as long as chela, 2.3-2.7 × as long as high; chela 2.2-2.5 × as long as broad; fingers 1.1-1.4 × as long as palm. Second pereiopod carpus 1.3-1.4 × as long as chela, 5.4-5.6 × as long as high; chela 2.4-2.6 × as long as broad; fingers 1.6-1.8 × as long as palm. Third pereiopod propodus 3.8-4.0 × as long as dactylus, 13.6-14.4 × breadth, with 8-11 thin spines on the posterior and lateral margins. Fifth pereiopod propodus 4.0-4.7 × as long as dactylus, 17.6-20.5 × breadth, with 17-20 thin spines on the posterior and lateral margins, dactylus terminating in one claw, with 50-55 spinules on flexor margin. Endopod of male subrectangular, slightly wider proximally, length 0.39-0.46 × exopod length, 2.0-2.2 × proximal breadth, ending broadly rounded; inner margin slightly concave, bearing spine-like setae, outer margin slightly convex, proximally 1/3 bearing nearly equal length short spine-like setae, distally 2/3 bearing nearly equal length long spine-like setae, and top bearing nearly equal length stout spine-like setae; appendix interna well developed, arising from distal 1/3 of endopod, beyond the end of endopod, distally with cincinulli. Appendix masculina rod-shaped and gradually tapering into a triangular tip, reaching about 0.48-0.51 × length of endopod, with numerous long spined setae on proximal and distal regions; endopod reaching about 0.76-0.79 × length of exopod; appendix interna well developed, reaching about 0.58-0.78 × length of appendix masculina, with cincinulli distally. Uropodal diaeresis with 10-12 movable spinules. Females carry 10-15 eggs, size of undeveloped eggs (without eyespots) 0.83-0.88 × 1.18-1.26 mm.

Description.

Body (Figs 3A , 5C-F ): Slender, smooth, colorless, translucent, sub-cylindrical, and medium-sized, males up to 25.9 mm tl, females up to 25.2 mm tl.

Rostrum (Figs 3A , 4A , 5C-F ): 0.47-0.77 of cl, slender, slightly elevated at base, reaching to base of 3rd segment of antennular peduncle to end of scaphocerite; straight, slightly sloping downwards (55.8%, N = 43), tip sometimes turned upward (44.2%); armed dorsally with 17-27 teeth, including 6-10 (usually 5-8) on the carapace, with 4-15 (usually 5-8) ventral teeth; lateral carina dividing rostrum into two unequal parts, continuing posteriorly to the orbital margin.

Eyes (Figs 3A , 4A , 5C-F ) small, bullet-like, reduced, with a short stalk, lacking facets, cornea pigmentation has great variability in the eye phenotype, with the smaller pigmented cornea (79%, N = 43), or totally pigmentless and blind (21%).

Carapace (Figs 3A , 4A ): Smooth, swollen; antennal spine acute, fused with inferior orbital angle; pterygostomial angle angular, produced forward; pterygostomian spine absent.

Antennule (Fig. 3B ): Reaching slightly short of scaphocerite; stylocerite long, reaching end of the basal segment, basal segment robust, anterolateral angle with broadly produced sharp projection, reaching 0.25 length of 2nd segment; about 0.72-0.76 × of combined length of 2nd and 3rd segments, 2nd segment as long as 0.76-0.82 × of basal segment, 1.2-1.3 × of 3rd segment; all segments with sub-marginal plumose setae.

Antenna (Fig. 3C ): Peduncle about 0.44-0.58 × as long as scaphocerite; scaphocerite 3.1-3.8 × as long as wide, outer margin straight, asetose, ending in a strong sub-apical spine, inner and anterior margins with long plumose setae.

Mouthparts characteristic of the genus. Mandible with well-developed incisor and molar processes; left incisor process with a single short sharp outer tooth, two long stout inner teeth, 7 curving setae followed by a patch of long setae; molar process stout and with triturative surface (Fig. 3D ). Maxillula with broadly rounded lower lacinia, with several rows of marginal and submarginal plumose setae; upper lacinia elongate, medial edge straight, with 25-35 strong spinules and simple setae; palp simple, longer than wide, slightly expanded distally, with 4 simple setae at basal part and 6 at distal part (Fig. 3E ). Maxilla with well-developed scaphognathite, tapers posteriorly, with a regular row of long plumose setae and short marginal plumose setae continuing down the proximal triangular process distally, furnished with numerous long plumose setae; upper and middle endite with marginal, simple, denticulate setae, with plumose setae distally; lower endite with long simple marginal setae; palp shorter than the cleft of upper endite, wider than distal setose proximally (Fig. 3F ). First maxilliped palp broad, with terminal plumose setae; caridean lobe broad, with marginal plumose setae; exopodal flagellum well developed, with marginal plumose setae distally; ultimate and penultimate segments of endopod indistinctly divided; medial and distal margins of an ultimate segment with marginal and sub-marginal rows of simple, denticulate and plumose setae; penultimate segments with marginal long plumose setae (Fig. 3G ). The second maxilliped with endopodite ultimate and penultimate antennomeres fused, slightly concave, reflected against basal antennomeres, inner margin of ultimate, penultimate, and basal segments with long setae of various types; exopod flagellum long, slender with marginal plumose setae distally. Podobranchium comb-like (Fig. 3H ). Third maxilliped with three-segmented endopod, reaching slightly beyond scaphocerite; penultimate segment 0.89-0.96 × of the basal segment; distal segment 0.75-0.91 × of the penultimate segment, ending in a large claw-like spine surrounded by simple setae, preceded by about 7-9 spines on the distal third of the posterior margin, with a clump of long and short simple, serrate setae proximally; exopod flagellum well developed, about 0.25-0.34 × of the penultimate segment of endopod, distal margin with long plumose setae (Fig. 3I ).

First pereiopod (Fig. 3J ): Short, reaches the end of eyes; chela length 2.2-2.5 × breadth, 1.1-1.2 × length of the carpus; movable finger length 3.1-3.4 × breadth, 1.1-1.4 × length of the palm, setal brushes well developed; carpus excavated disto-dorsally, length 2.3-2.7 × breadth, about the same length of merus.

Second pereiopod (Fig. 4B ): Reaches about the end of 3rd antennular peduncle segment, slenderer and longer than the first pereiopod; chela length 2.4-2.6 × breadth, 0.73-0.77 × length of the carpus; movable finger length 4.5-4.8 × breadth, and 1.6-1.8 × length of the palm, setal brushes well developed; carpus length 5.4-5.6 × breadth, slightly excavated distally, 1.0-1.1 × length of merus.

Third pereiopod (Fig. 4C, D ): Reaches beyond the end of scaphocerite; dactylus length 4.4-4.7 × breadth, ending in prominent claw-like spine surrounded by simple setae, behind which bears 6-7 spines; propodus length 3.8-4.0 × of the dactylus, bearing 8-11 spinules on posterior margin, 13.6-14.4 × breadth; carpus length 0.65-0.72 × of the propodus; merus length 1.9-2.1 × of the carpus, with about 3 strong spines on the posterior margin.

Fourth pereiopod (Fig. 4E, F ): Reaches end of 3rd segment of antennular peduncle; dactylus length 4.2-5.0 × breadth, ending in prominent claw-like spine surrounded by simple setae, behind which bears 7-8 spines; propodus length 3.8-4.6 × of the dactylus, bearing 12-15 spinules on posterior margin, 14.6-17.4 × breadth; carpus length 0.58-0.73 × of the propodus; merus length 1.9 × of the carpus, with about 3 strong spines on the posterior margin.

Fifth pereiopod (Fig. 4G, H ): Reaches end of 3rd segment of antennular peduncle; dactylus length 4.2-5.6 × breadth, ending in prominent claw-like spine surrounded by simple setae, behind which bears comb-like row 50-55 spines; propodus length 4.0-4.7 × of the dactylus, bearing 17-20 spinules on posterior margin, 17.6-20.5 × breadth; carpus length 0.55-0.60 × of the propodus; merus length 1.5-1.6 × of the carpus, with about 3 strong spines on the posterior margin.

First four pereiopods with epipod. Branchial formula typical for the genus.

First pleopod (Fig. 4I ): Endopod of male subrectangular, slightly wider proximally, length 0.39-0.46 × exopod length, 2.0-2.2 × proximal breadth, ending broadly rounded; inner margin slightly concave, bearing spine-like setae, outer margin slightly convex, proximally 1/3 bearing nearly equal length short spine-like setae, distally 2/3 bearing nearly equal length long spine-like setae, and top bearing nearly equal length stout spine-like setae; appendix interna well developed, arising from distal 1/3 of endopod, reaching beyond the end of endopod, with cincinulli distally.

Second pleopod (Fig. 4J ): Appendix masculina rod-shaped and gradually tapering into a triangular tip, reaching about 0.48-0.51 × length of endopod, with numerous long spine setae on proximal and distal margins; endopod reaching about 0.76-0.79 × length of exopod; appendix interna well developed, reaching about 0.58-0.78 × length of appendix masculina, with cincinulli distally.

Telson (Fig. 4K ): 0.40-0.55 × of cl, shorter than sixth abdominal segment, 0.67-0.96 × length of the sixth abdominal segment, posteriorly tapering, with median projection, dorsal surface with 5 pairs of stout movable spine setae including the pair at posterolateral angles; posterior margin with 4 pairs of intermedial strong spiniform setae, sublateral pair shorter than lateral and inner pairs. Exopodite of the uropod bears a series of 10-12 movable spinules along the diaresis, the last one shorter than the lateral process (Fig. 3K ).

Females carry 10-15 eggs, size of undeveloped eggs (without eyespots) 0.83-0.88 × 1.18-1.26 mm.

Coloration (Fig. 5C-F ): Body and appendages are colorless and translucent; vestigial pigment present at the center of the cornea or without pigment; internal organs (gonads and hepatopancreas) are yellow; eggs in females brown.

Etymology.

Caridina incolor sp. nov. is named after the colorless and transparent body color.

Remarks.

Caridina incolor sp. nov. might be more closely related to the epigean species than to its supposed cave congeners. It is morphologically similar to C. guiyangensis Liang, 2002, from Guiyang, Guizhou Province in the long rostrum and indentation, the shape of endopod of the male first pleopod and appendix masculina. Although no molecular comparison with C. guiyangensis could be accomplished, C. incolor sp. nov. can easily be distinguished from the latter by the reduced eyes, colorless body and appendages (versus developed eyes and pigmentation in C. guiyangensis ); the long stylocerite, reaching to the end of the antennule basal segment (versus reaching 0.85 × of basal segment in C. guiyangensis ); the long penultimate segment of the 3rd maxilliped, which is distinctly longer than the basal segment and distal segment (versus penultimate segment as long as basal segment and distinctly shorter than distal segment in C. guiyangensis ); absence of a projection on the base of the inner margin of male first pleopod endopod (vs. with projection in C. guiyangensis ); and relatively large eggs, size of undeveloped eggs 0.83-0.88 × 1.18-1.26 mm (versus 0.63-0.75 × 1.05-1.13 in C. guiyangensis ). In comparison to other cave species within Caridina , C. sinanensis Xu, Li, Zhang & Guo, 2020, is most similar in sharing the long 6th abdominal segment, and the variably pigmented cornea. However, the new species differs from the latter by possessing a relatively long and slender rostrum which reaches beyond the end of the 3rd antennular peduncle segment (versus stouter, reaching to the end of the 2nd segment in C. sinanensis ); the long stylocerite, reaching to the end of the basal segment of the antennule (versus reaching 0.75-0.88 × of basal segment in C. sinanensis ); and completely different shape of the endopod of the 1st pleopod and appendix masculina of the 2nd pleopod in males (Fig. 4I, J , versus Fig. 4H, J, K in Xu et al. 2020).). There are another six atyids, Caridina acuta , C. caverna , C. demenica , C. jiangkou , C. sinanensis , and Neocaridina brevidactyla , that have been reported from nearby caves from Guizhou Province. Caridina incolor sp. nov. differs from N. brevidactyla in the completely different shape of the endopod of 1st pleopod and appendix masculina of the 2nd pleopod in males; lack of a hook-like projection on the posterior part of coxa of the 2nd pereiopod and a pterygostomian spine. C. incolor sp. nov. differs from all other cave species in having a long rostrum and stylocerite (with the longest rostrum and stylocerite amongst all known seven cave atyids); slender sixth abdominal segment which is distinctly longer than the telson (only C. sinanensis has a slender sixth abdominal segment that is slightly longer than the telson, other cave species have a stout sixth abdominal segment which is distinctly shorter than the telson); and an appendix masculina that is unique in shape and gradually tapers into a triangular tip. These taxa can be separated from each other by morphological differences as discussed in Xu et al. (2020).

Molecular phylogenetic results.

We analyzed 47 COI sequences in total. Five specimens of Caridina incolor sp. nov. were used in the molecular phylogenetic analysis shown in Figure 2 . Specimens assigned to Caridina incolor sp. nov. formed a clade distinct from other species. Caridina incolor sp. nov. is well distinguished from the other 16 atyids with a sequence divergence of 13.7% - 24.5% (COI). The sequence divergence between Caridina incolor sp. nov. and C. sinanensis is the closest. The topology of the Bayesian (BI) trees and the ML tree are basically similar. Phylogenetic trees revealed the relationship between Caridina incolor sp. nov. and 16 other species of atyids, with the posterior probability and bootstrap values from the BI and ML analysis shown in Figures 2 . According to Hebert, Ratnasingham and de Waard 2003, the genetic distances supports Caridina incolor sp. nov. as a new species.

Conservation.

Threats to cave shrimp are of concern due to the uniqueness of the habitat and increasing anthropogenic activities. Based on the information available, the Yaoshui Cave and its faunas are potentially at risk from excessive levels of external disturbance. Daqikong scenic area is famous for its marvelous primeval forests, steep canyons, spectacular caves, and underground rivers. Over the years, tourism to the region has improved the welfare of local residents and has become a major industry in this area. Moreover, new recreational trails and amusement facilities have been built in the scenic area. It is almost inevitable that these new projects will put great pressure and impact on caves and their faunas. In addition, land development and agriculture lead to habitat degradation and groundwater pollution, which also has a negative impact on the survival of this species.

So far, no freshwater shrimps are protected by the national legislation. The Announcement of the Ministry of Agriculture and Rural Areas of China has failed to categorize the strictly endemic cave species as Endangered (CITES Appendix aquatic wild species of China, no. 69, 2018). Caridina incolor sp. nov. is new to science and the conservation status remains unassessed. Using the criteria provided by the IUCN (2019) Red List Categories and Criteria (version 14) ( IUCN (2019)), the new species should be considered as a critically endangered (CR) species on account for its exceptional rarity, restricted distribution, and exposure to serious anthropogenic impacts.

The Yaoshui Cave, which is home to two unique and range-restricted species (atyid shrimp, Caridina incolor sp. nov., and loach fish, Oreonectes daqikongensis ) is biologically significant without question. These strictly-adapted cave species must be considered as important units for conservation, and devising an effective conservation strategy is clearly an urgent priority. It has also become obvious that there is a need to collect more baseline data, such as the exact population size, structure, natality, and mortality rates. Regular monitoring may be necessary to ensure populations are sustained in the face of further anthropogenic disturbances. Equally important, a captive breeding program of these cave species should be developed. In addition, we propose that non-invasive and non-destructive projects, such as eco-tourism, should be promoted. Last but not least, we also appeal to local farmers to lower the usage of agricultural pesticides, herbicides, and fertilizers to help reduce the amount of hazardous chemicals that are leeched into the groundwater.

Figures

Figure 2. Bayesian inference (BI) tree and maximum likelihood method (ML) tree of 16 atyids and outgroups (Palaemon modestus) based on the COI gene. Support values at the nodes represent posterior probability.

Figure 3. Caridina incolor sp. nov. A entire animal, lateral view B antennule C antenna D mandible E maxillula F maxilla G first maxilliped H second maxilliped I third maxilliped J first pereiopod K diaeresis of uropodal exopod A holotype B-K paratype (FU, 2018 - 11 - 27 - 02).

Figure 4. Caridina incolor sp. nov. A carapace and cephalic appendages, lateral view B second pereiopod C third pereiopod D dactylus of third pereiopod E fourth pereiopod F dactylus of fourth pereiopod G fifth pereiopod H dactylus of fifth pereiopod I first male pleopod J second male pleopod K distal margin of telson A-K paratype (FU, 2018 - 11 - 27 - 02).

Figure 5. Habitats, variable features, and live coloration of Caridina incolor sp. nov. A surrounding environment of Yaoshui Cave during the dry season B same site during the rainy season C-E variable rostrum and eye size in life F ovigerous female in life.