Urocaridella arabianensis, Akash & Purushothaman & Madhavan & Ravi & Hisham & Sudhakar & Kumar, 2020

Akash, S., Purushothaman, P., Madhavan, Manu, Ravi, Charan, Hisham, T. Jafer, Sudhakar, M. & Kumar, T. T. Ajith, 2020, Urocaridella arabianensis n. sp., a new Palaemonid shrimp (Crustacea, Decapoda Palaemonidae) from Lakshadweep Islands, India with taxonomic comparison on the genus Urocaridella Borradaile, 1915, Zootaxa 4816 (1), pp. 49-66 : 51-62

Urocaridella arabianensis n. sp.

( Figs. 1–5 )

Material examined: Holotype: NBFGR / PALUARA-01, Female (CL 13 mm), Arabian Sea, Off Agatti Island, Lakshadweep, India, 10°50’26”N, 72°11’97”E, 1–3 feet depth, August 2019.

Description: Rostrum ( Fig. 2A, B ) slender and long, 1.7–2.1 times as long as carapace, strongly curved upwards anteriorly, extended beyond the end of antennular peduncle; dorsal margin of rostrum bearing three pairs (Basal, Middle and Distal) in appeared widely spaced teeth with a strong epigastric tooth on middle of the carapace. Basal pair of teeth are larger than other two pairs found in above the orbit, inner margin of teeth is serrated distally, 2 nd tooth slightly larger than 1 st one with a row of 2–3 long plumose setae on rostrum underneath of each tooth ( Fig. 2B ); midrostral pair of teeth are glabrous, set wider apart, without fine serrate on inner margin and two long plumose setae underneath of each tooth; distal pair teeth glabrous, spinose, with row of long plumose setae and most posterior teeth set slightly above between level of midrostral pair of dorsal one, last ventral tooth situated posteriorly to distal pair of dorsal teeth, terminally sharp and spinose.

Carapace glabrous, laterally compressed, well developed antennal spine with well-produced orbital angle. Branchiostegal spine is prominent and smaller than the antennal spine, which is situated slightly in back of the anterior margin of carapace, pterygostomine region is rounded. Eyes are large with the globular shaped cornea, eyestalk looks bulbous, eyestalk and cornea were separated by a groove ( Fig. 2C ).

Antennular peduncle ( Fig. 2E ) reaching near to the distal margin of scaphocerite, 0.85 times as long as scaphocerite; basal segment broad, thin, anterior margin lobate with long setae, lateral outer margin anteriorly with a spine, 4.6 times as long as the second segment, 1.9 times as long as third segment. Stylocerite spiniform arising in posterior of the basal peduncle; second segment of antennular peduncle, shorter than third segment, anterio-laterally lobate with long plumose setae. Antennular flagellum are long, tapered; upper flagellum biramous, basally 6 segments fused, contains 57–60 segments; lower flagellum thin almost equal to upper one with 53–55 segments. Antennal scaphocerite ( Fig. 2D ) 3.7 times as long as wide, inner margin convex with long plumose setae and anteriorly rounded, outer margin slightly concave with the prominent tooth in latero-distally.

Mandible ( Fig. 2F ) without palp, molar process stout and provided with 3 strong obtuse teeth, incisor process short and truncate tip armed with 3 broad teeth. Maxillula ( Fig. 2G ) with bilobed palp, the upper lobe with numerous spines on distal margin and lower lobe with small hook-shaped setae. Maxilla ( Fig. 2H ) with simple palp, basal endite bilobed with long setae distally, exopod with well-developed lobe, flagellum broad, densely setose distally. The first maxilliped ( Fig. 2I ) with basial and coxal endites short, broad, flattened and fringed with short simple setae. Second maxilliped ( Fig. 2J ) have a large epipod and long exopod fringed with setose distally, fourth and fifth segments fringed with numerous long setae distally. Third maxilliped ( Fig. 2K ) slender; coxa with rounded lateral plate, bearing slender exopod barely extended middle of antipenultimate article; endopod slender and reaching to distal end of carpocerite; antipenultimate article somewhat twisted, 1.3 times as long as penultimate segments, ultimate segment tapering with numerous terminal spinule and setae, 0.5 times as long as penultimate segments.

First pereopod ( Fig. 3A,B ) slender and reaching distal end of antennal scaphocerite; fingers subequal, concave with small terminal tooth with tuft of setae distally, inner margin of fingers with long setae and 1.05 length of palm; outer margin of dactylus with 4–5 row of log numerous setae; chela 0.7 times long as carpus length; carpus subcylindrical, 5.7 times long as the width of distal end of carpus, 2.5 times long as palm, with transverse row of short setae (10–12) on inner distal margin; merus cylindrical, longer than carpus (1.1 times); ischium stout, 0.66 times long as merus.

Second pereopod ( Fig. 3C, D ) reaching the level of terminal end of rostrum, exceeding length of 1 st pereopod; fingers are long, slender, 0.86 times long as palm, hooked edges with the row of setae on internal margin; carpus subcylindrical, 1.8 times as long as palm, 10 times long as the width of distal end; merus cylindrical, equal length to carpus; ischium long, 0.92 times long as merus.

Ambulatory pereopods ( Fig. 3 E–G & 4A–C) are long and slender; third pereopod is reaching near to distal end of rostrum; dactylus short, simple, curved and terminally sharped end with long setae, about 0.14 length of propodus; propodus long as to carpus about 1.4 times, 11 times as long as dactylus, ventral margin with 10–12 ventral spiniform setae including a distal pair; merus slender and longer than about 1.7 times of carpus length, unarmed; ischium about 0.41 of merus length. Fourth pereopod little extended beyond the tip of rostrum; dactylus similar to 3 rd pereopod; propodus 9 times as long as dactylus with 9–11 spiniform setae including a distal pair; carpus short, 0.66 times as long as propodus; merus long, slender, 1.06 times as long as propodus, 1.6 times as long as carpus. Fifth pereopod: propodus 9.5 times as long as dactylus; carpus short, 0.65 times as long as propodus; merus long, slender, 0.95 times as long as propodus, 1.45 times as long as carpus.

First pleopods shorter than second ( Fig. 4D ), exopod broad and outer margin fringed with long setae; endopod short and 0.4 times long as exopod. Appendix interna of second pleopod ( Fig. 4E ) is short, reaching middle of the exopod, distal outer margin fringed with setae; exopod and endopod broad and outer margin with long setae.

arabianensis n. sp. Anp=Antennular peduncle; CL=Carapace length; CW=Carapace width; Prp=propodus; RL=Rostrum length; sp=spine, TeL=Telson length.

Abdominal somites ( Fig. 3H ) smooth, 3.2 times as long as carapace; 1 st three abdominal somite broadly rounded and 3 rd abdominal tergite produced dorso-posteriorly and rounded; fourth and fifth abdominal segments posteriordorsally rounded, letro-meadially produced a spine-like projection, postero-ventrally produced leaf-like angular end; sixth abdominal segment elongate, 2.3 times long as the fifth segment, produced pointed end at postero-ventral angle, petero-medially extended triangular projection with sharp end.

Telson ( Fig 4F, G ) slender, 0.72 times long as sixth abdominal segment, bearing two pairs of movable minute dorsal spines on posterior half of the telson, posterior margin produced triangular with 3 pairs of spines, 1 st lateral spine very shorter than others, 2 nd pair slender, long and 0.11 times long as telson length, 2.7 times long as 3 rd pair of spine. Uropods exceeding the length of telson; Endopods of uropods smaller than exopod, leaf-like structure, lateral margin fringed with long setae; exopods with pair of distal spines and outer most spine, outer margin not bearing setae, inner and posterior end fringed with long setae.

Coloration in life: Carapace and abdomen ( Fig. 5 ) translucent with sparsely scattered bright red and whitish spots, one white dot in posterior-dorsally and two dots in lateral sides of carapace, fifth and sixth abdominal somites almost fully translucent without spots. Dorso-posterior end of third abdominal tergites contains two red bars. Rostrum white in colour with red band sub-terminally, dorsal-ventral marginal teeth pale red. Antennule and antennular flagellum are dark red. Antennal scale is transparent with margin red in colour. Eyestalk with translucent, cornea with semi-transparent or ash in colour with dark spots dorsally. First and second pereopods almost white or translucent; bases of palm, carpus with a red coloured band; fingers are white; merus and ischium contain scattered red dots. Third to fifth pereopods of dactylus, propodus white with small red dots; carpus distally with red band, merus and ischium white or transparent with red dots dorsally. Pleopods are translucent with outer margin reddish. Midlateral spine of 4 th and 5 th abdomens are reddish. The base of uropods and telson has a red colour band with white dots, continues with a red dot on each of the uropod and reddish in posterio-distally.

Distribution and habitat: Underwater surveys have been conducted at different islands of Lakshadweep. Urocaridella arabianensis n. sp. is so far observed only from the type locality, i.e., Agatti Island (10°50’26”N, 72°11’97”E; 10°50’04”N, 72°10’51”E), Lakshadweep at the depth of 1–3 feet at low tide.

These shrimps were occurred in the shallow waters at Agatti Island, however they are frequently noticed in the bottom curve of the coral boulder. Aggregation of these shrimps were mostly in the bottom of dead coral, where light penetration is very low, darkening area and so the species is may be a free-living browser. Also, we observed that most of the specimens are matured and berried females (eggs are eye stalked), which indicates, the bottom region serve as shelter and schooling place.

Live specimens of Urocaridella arabianensis n. sp. were collected in two sampling sites at Agatti Island, 10°50’26”N, 72°11’97”E (1) and 10°50’04”N, 72°10’51”E (2). Few pipefish ( Doryrhamphus sp) was also observed together, however U. arabianensis n. sp. (~95%) was dominated. The salinity of the region was ranged from 35– 35.5 ppt and temperature with 27–27.5˚C. Faunal assemblage and habitat of U. arabianensis n. sp. was documented as video, but the spatial distribution of the species was not able to documented, as the shrimp found on the bottom of the reef boulder. The habitat, where shrimps collected are dominated with common coral Montipora Blainville, 1830 , Tombstone coral Coeloseris mayeri Vaughan, 1918 , Brain coral Symphyllia Milne Edwards & Haime, 1848 , Knob coral Favia stelligera (Dana, 1846) , Staghorn coral Acropora Oken, 1815 . In addition, Black nose cardinalfish, Rhabdamia cypselura Weber, 1909 ; Bluestripe Snapper, Lutjanus kasmira (Forsskal, 1775) ; Indo-Pacific sergeant, Abudefduf vaigiensis (Quoy & Gaimard, 1825) ; Yellowbelly damselfish, Amblyglyphidodon leucogaster (Bleeker, 1847) ; Twinspot damselfish, Chrysiptera biocellata (Quoy & Gaimard, 1825) ; Bluehead fish, Thalassoma janseni (Bleeker, 1856) ; Yellow boxfish, Ostracion cubicus Linnaeus, 1758 ; Black-blotched porcupinefish Diodon liturosus Shaw, 1804 and Bicolor cleaner wrasse, Labroides bicolor Fowler & Bean, 1928 were also noticed.

In the sampling site 2, 85% of U. arabianensis n. sp. with Doryrhamphus sp were observed. They were collect- ed from the bottom of the coral, Montipora , Coeloseris , Symphyllia , where salinity and temperature were noticed, 36 ppt and 28˚C respectively. The co-occurred species are L. kasmira , A. vaiiginensis , T. janseni , and T. janseni .

Biological features (Size and reproductive): 29 females and 26 males (N = 55) were measured for documenting the carapace length (cl) of U. arabianensis n. sp. Overall size frequency of both sexes are represented in Fig. 6A . The mean size (CL ± SE) of females was 8.1 ± 0.4 mm (ranges 4–13 mm); while males 7.0 ± 0.41 mm (ranges 3–11 mm). Further, the most abundant individuals were observed between 7–8 mm CL for females and 3–5 mm CL for males. The CL of ovigerous female was noticed from 9–13.0 mm. Out of the 29 females, only six were carrying eggs and the mean value of fecundity was 185 (ranged from 170– 190 eggs). The largest ovigerous female (CL 13.0 mm) have the maximum eggs (190) and the smallest ovigerous female (CL 9.0 mm) have 175 eggs. Eggs are oblong shaped, fourth post-naupliar stage and the length ranged from 0.4–0.57 mm and width varied from 0.35–0.45 mm ( Fig. 6B ).

Etymology: The species is named after the Arabian Sea, where Lakshadweep islands are scattered and 55 specimens of the new species were collected from one among the islands.

Paratypes: 9 females (CL 6–13 mm), 7 males (CL 5–11 mm) Arabian Sea , off Agatti Islands, Lakshadweep, India, 10°50’04”N, 72°10’51”E, 1–3 feet, August 2019 .

Remarks. This new species increases the number of species as eight in the genus Urocaridella described worldwide ( Holthuis, 1950; Bruce, 1967; Fujino & Miyake, 1969; Chace & Bruce, 1993; Yokes & Galil, 2006; Wang, Chan & Sha, 2015; Prakash & Baeza, 2018) and also increased the number of species as two, reported in India ( Radhakrishnan et al., 2012; Samuel et al., 2016). The species is easily identifiable as a member of Urocaridella based on several morphological characters. Rostrum armed 2 strong basal teeth with elevated into semblance of crest; carapace with strong epigastric teeth at about middle of dorsal surface, present a submarginal branchiostegal spine, absence of hepatic spine or branchiostegal suture; posterior pairs of ambulatory pereopods slender with simple dactylus and not biunguiculate, which is shorter than propodus; endopod 1st pleopod in male contains appendix interna ( Chace & Bruce, 1993).

The present new species of the genus, Urocaridella is close relation to U. pulchella , U. cyrtorhyncha and also to U. urocaridella with the structure of rostrum, orientation of the dorsal rostral spination and the postero-dorsal part of the third segment, which is expanded backwards roundly. Among the said three species, the rostrum strongly upcurved and bears larger teeth dorsally (6+1) ( Fujino & Miyake 1969; Chace & Bruce, 1993; Yokes & Galil, 2006). However, U. arabianensis n. sp. can be differed from other species of the genus by size (length) and the number of dorsal and ventral teeth of the rostrum, size of pereopods, and the relation of 5 th and 6 th abdominal length ( Table 2). Urocaridella arabianensis n. sp. have rostrum, which is 1.7 to 2.1 times as long as carapace, 10 ventral rostral teeth, carpus of 1 st pereopod is 2.5 times long as palm, carpus of 2 nd pereopod 1.8 times as long as palm, presence of a spine in latero-middle of fourth and fifth abdomens, sixth abdominal segment 2.3 times long as fifth segment. Where, in U. pulchella , rostrum 1.5 times long as carapace, carpus of the second pereopod 1.5 times long as palm, sixth abdominal segment 2.0 times long as the fifth segment. U. cyrtorhyncha differed by presences of 9 ventral teeth in rostrum, carpus longer than the palm of first pereopod (1.5 times), propodus of pereopod 3 rd to 5 th are 7 times as long as the dactylus ( Fujino & Miyake, 1969; Prakash & Baeza, 2018). U. urocaridella is distinguished by the presence of eight dorsal and 9–11 ventral teeth in rostrum, the propodus of the fifth pereopod 4 times long as dactylus, mandible with well-developed 2-segmented palp ( Chace & Bruce, 1993). U. degravei differed with presences of 9 ventral rostral teeth, stylocerite falls well behind the middle of the basal segment, carpus of first and second pereopod is about 1.3 times as long as the palm, propodus of the fifth pereopod is about 8.5 times as long as the dactylus. U. antonbruunii and U. liui were well distinguished by the presence of triangular hump and triangular cap overhanging strongly produced in postero-dorsal part of the third abdominal segment, respectively. Next, U. vestigialis varied from the U. arabianensis n. sp. with the presence of six ventral rostral teeth, 5 th abdominal pleuron strongly acute postero-ventrally; mandible with vestigial palp, propodus of the fifth pereopod is about 5 times as long as the dactylus ( Chace & Bruce, 1993).

Colour patterns are most important taxonomic character for the genus Urocaridella and are mostly species-specific ( Prakash & Baeza 2018). The colour pattern of Urocaridella arabianensis n. sp. is similar to U. pulchella and U. antonbruunii , where the carapace, rostrum and abdominal region had red and white spots and translucent and two red bars present on the dorsal region of the third abdominal somite. However, U. arabianensis n. sp. is differed by having red dots on propodus, carpus, merus and ischium of the last three pereopods. The exopods and endopods of the uropods are having lined red and white blotches, which is also similar in U. pulchella and U. antonbruunii and red spots in U. urocaridella . Few specimens of U. arabianensis n. sp. colour pattern observed that pale red dots on the body and legs and fully transparent on the body ( Fig. 5 ).

Recently, Khalaf & Khalaf (2018) has described a new species Urocaridella renatekhalafae Khalaf in Khalaf & Khalaf, 2018 from the Fujairah and Khorfakkan Sea, East Coast of United Arab Emirates, Gulf of Oman, which was accepted as junior synonym to U. cyrtorhyncha (WoRMS, 2020). They have described about the colouration and biological characters of the species, however, illustration about the morphological characters are totally lacking. Accordingly, the colour patterns in pereopods, abdomen and telson of U. renatekhalafae were similar to U. arabianensis n. sp. But, U. renatekhalafae is distinguished from U. arabianensis n. sp. by comprising of fully long white coloured rostrum without sub-terminal red band, antennas and antennules are red in colour with some white dots at the base and carapace with two white dots in posterior-dorsally and four dots in laterally in irregular shape.

Phylogenetic analysis: Seven COI sequences were generated for Urocaridella arabianensis n. sp. and six of the sequences being identical with one haplotype differing by only one base ( Fig. 7A ). Three sequences of Urocaridella species retrieved from Genbank and used for phylogenetic study. There were 555 positions in the final dataset. The new species sequences had a monophyletic clade and sister to U. pulchella ( KY197952 ) from the Mediterranean Sea (coast of Egypt) with high genetic distance (14.7–15.1%) ( Table 3). U. antonbruunii ( KY197951 ) and U. degravei ( KY197953 ) were shown far to U. arabianensis n. sp. with the distance of 19.8–20.02% and 22.6–22.8%, respectively ( Fig. 7A ).

Additionally, the phylogenetic relationships between the new species and other congeners were analyzed using the Maximum Likelihood and Bayesian inference methods with the sequences of 16S rRNA (456 bp),18S rRNA (650 bp) and Histone 3 (295 bp) genes. Sequences of 16S ( Fig. 7B ) gene KC515050 ( U. pulchella ), KC515049 ( U. antonbruunii ), KP179006 ( U. cyrtorhyncha ) sequences showed very low genetic distances (0.0–0.4%) and named as different species which may be missed identified and the similar result was noticed by Prakash & Baeza (2018) also. Phylogeny of 18S and H3 gene sequences also supporting significantly to the new species ( Fig. 8A & B ).

In the concatenated analysis, the combined data matrix contains 24 nucleotide sequences of in-group taxa and 3 sequences of out-group taxa. The combined data set (16S, 18S and H3) was 1430 bp long including 5 indels and an outgroup species ( Fig. 9 ). The in-group taxa have 56 parsimony-informative of 116 variable characters with 61% of A+T base frequency. The tree topology was supported by>80% bootstrap support from the ML analysis and posterior probabilities from the BI analysis for all the nodes, which is similar to individual tree topologies. The three specimens of the U. arabianensis n. sp. clustered together into a monophyletic clade with U. antonbruunii , U. cyrtorhyncha and U. pulchella . Similarly, Prakash & Baeza (2018) noticed, that misidentification of two sequences of U. pulchella and U. antonbruunii from Japan ( Kou et al., 2013) and one sequence of U. cyrtorhyncha from Singapore ( Carvalho et al., 2016), which found to be a single clade. Accordingly, we conclude that the individuals of U. antonbruunii ( Japan) , U. pulchella ( Japan) and cyrtorhyncha ( Singapore) are might be the synonyms of U. arabianensis n. sp.

Figures

FIGURE 1. Urocaridella arabianensis n. sp.: holotype, female (CL 13 mm) from Agatti Island, Lakshadweep, India.

FIGURE 2. Urocaridella arabianensis n. sp. Holotype, Female (13 mm): lateral view of carapace (A); close view of distal teeth of rostrum (B); eye (C); Antennal scaphocerite (D); Antennular peduncle (E); mandible (F); maxillula (G); Maxilla (H); Maxilliped I (I); Maxilliped II (J); Maxilliped III (K).

FIGURE 3. Urocaridella arabianensis n. sp. Holotype, Female (13 mm): Pereopod I (A); chela of Pereopod I (B); Pereopod II (C); chela of Pereopod II (D); Pereopod III (E); Pereopod IV (F); Pereopod V (G); lateral view of Abdominal pleura (H).

FIGURE 4. Urocaridella arabianensis n. sp. Holotype, Female (13 mm): Chela of pereopod III (A); Chela of Pereopod IV (B); Chela of Pereopod V (C); 1st Pleopod (D); Appendix interna (E); Uropod (F); Posterior end of telson (G). Scale bar=0.5 mm.

FIGURE 5. Urocaridella arabianensis n. sp. in live condition (A & B)

FIGURE 6. Biological features of Urocaridella arabianensis n. sp. from Agatti Island, Lakshadweep, India. Size frequency (A); Eggs with eyestalk (B).

FIGURE 7. The phylogenetic tree topology for Urocaridella arabianensis n. sp. with congener species based on COI (A), 16S (B) genes sequences using Bayesian inference (BI)/maximum likelihood (ML) analyses.

FIGURE 8. The phylogenetic tree topology for Urocaridella arabianensis n. sp. with congener species based on 18S (A) and H3 (B) genes sequences using Bayesian inference (BI)/maximum likelihood (ML) analyses.

FIGURE 9. Concatenated analysis for the species of Urocaridella arabianensis n. sp. with congener species using Bayesian inference (BI) and maximum likelihood (ML) based on one mitochondrial (16S) and two nuclear gene sequences (H3, 18S).