Redescription of two subterranean amphipods Niphargus molnari Méhely, 1927 and Niphargus gebhardti Schellenberg, 1934 (Amphipoda, Niphargidae) and their phylogenetic position

Dorottya Angyal; Gergely Balázs; Valerija Zakšek; Virág Krízsik; Cene Fišer

doi:10.3897/zookeys.509.9820

. 2015 Jun 24;(509):53–85. doi: 10.3897/zookeys.509.9820

Redescription of two subterranean amphipods Niphargus molnari Méhely, 1927 and Niphargus gebhardti Schellenberg, 1934 (Amphipoda, Niphargidae) and their phylogenetic position

Dorottya Angyal ^1,², Gergely Balázs ³, Valerija Zakšek ⁴, Virág Krízsik ⁵, Cene Fišer ⁴

PMCID: PMC4493343 PMID: 26175603

Abstract Abstract

A detailed redescription of two endemic, cave-dwelling niphargid species of the Hungarian Mecsek Mts., Niphargus molnari Méhely, 1927 and Niphargus gebhardti Schellenberg, 1934 is given based on newly collected material. Morphology was studied under light microscopy and with scanning electon microscopy. Morphological descriptions are complemented with mitochondrial cytochrome c oxidase subunit I (COI) sequences as barcodes for both species and with notes on their ecology. Using three independent molecular markers we showed that Niphargus gebhardti belongs to the clade distributed between Central and Eastern Europe, whereas phylogenetic relationship of Niphargus molnari to the rest of Niphargus species is not clear. The two species from the Mecsek Mts. are phylogenetically not closely related. Both species need to be treated as vulnerable according to IUCN Red List of Threatened Species.

Keywords: Hungary, Mecsek Mts., Niphargus, redescription, morphology, phylogeny, endemism, SEM

Introduction

Fragmented mountain areas in East-Central Europe had been suggested to be centres of endemisms that evolved through a complex geological history including Eocene marine regression-transgression cycles and Pleistocene glacial cycles (Hou et al. 2013, Meleg et al. 2013, Mamos et al. 2014). The Mecsek is one of these isolated mountain ranges, that is situated in Southern Hungary and surrounded by Pannonian plains. The closest mountain ranges are the Croatian Papuk Mts. (80 km) and the Hungarian Transdanubian Mts. (150 km) (Fig. 1). The area is small of approximately 545 km². In biological sense, it is populated by numerous endemic species the origin of which may date back to Tertiary and which therefore apparently have survived mass extinctions in glacial periods. The upper geological layers comprise of Triassic and Jurassic limestones and dolomites, where extensive karstification has created over 200 caves. The subterranean environment of the area harbours numerous terrestrial and aquatic highly endemic invertebrates, known only from one or a few caves. Although the region apparently harbours an important piece of European and Hungarian natural heritage, until now only one species, the Hungarian blind snail (Bythiospeum hungaricum (Soós, 1927)) has been protected by law. A serious impediment for conservation biology is that our knowledge of species is only limited, beginning with poor taxonomic descriptions. The aim of this study is to bridge this gap at the most basic level. We morphologically redescribe and present phylogenetic relationships of two amphipod species from the genus Niphargus, both endemic to this area.

Figure 1. — Location of the Mecsek Mts. and the nearby isolated mountain ranges within Europe.

Niphargus molnari Méhely, 1927 was described from the stream of the Mánfai-kőlyuk Cave (Méhely 1927). The description is not detailed, as it contains only a few information about the body lenght, the pereonits, the pleon segments, the first antenna, the uropods and the telson, and two drawings about the epimeral plates and the pereion segments. Further drawing of the right lacinia mobilis can be found in Méhely’s summarizing work (Méhely 1941). At approximately the same period the species was also studied by Schellenberg, who analysed samples fom Abaligeti Cave. In his early study he first treated it as Niphargus leopoliensis molnari (Schellenberg, 1933), but later he acknowledged its species status and supplemented description with data about the seta number of the palpus of the first maxilla (Schellenberg 1935). The species was found in the Mánfai-kőlyuk Cave (Gebhardt 1933, 1934, 1963, 1967) and in the stream of the Abaligeti Cave too (Gebhardt 1934, 1963, 1967). Recently, the species was found in other two localities, the Spirál Sinkhole and the Vadetetős Sinkhole (Angyal and Balázs 2013). During our research in the caves of the Western Mecsek between 2010 and 2013, the species could not have been re-collected on the type locality, which is supposedly related to the artificial utilization of the Mánfai-kőlyuk Cave. The intrusive introduction of waterworks in the 1960-s and 1970-s has caused irreversible changes in the cave’s character, hidrology and ecosystem (Angyal 2012).

Niphargus gebhardti Schellenberg, 1934 was described from the pools formed by dripping water of the Abaligeti Cave, originally as Niphargus foreli gebhardti (Schellenberg 1934). Brief description reports on only few characters, like the pereopods, the antennae and the mouth parts, and two drawings about the second gnathopod’s propodus and the telson. Later the author gave additional data on the body length and the telson (Schellenberg 1935). Gebhardt mentioned the species’distribution from pools of the Abaligeti Cave’s main passage in various papers (Gebhardt 1934, 1963, 1967). The species rank was proposed for the first time in Méhely’s synthetic work (Méhely 1941), wherein a drawing of the pleopod’s retinacles and some data about the lacinia mobilis are also presented. Dudich (1941) discussed ‘Niphargus foreli gebhardti’ from the Abaligeti Cave as a fauna element of the historical Hungary. More recent sampling revealed new records of the species from Vadetetős Sinkhole, Szajha-felső Sinkhole, Spirál Sinkhole, Gilisztás Cave and Trió Cave (all Mecsek Mts.; see Angyal and Balázs 2013).

The holotypes of both species are either in an unknown place or had been destroyed. Although we identified the distinguishing characters of Niphargus gebhardti and Niphargus molnari, and presented comparative drawings of them (Angyal and Balázs 2013), the morphology of both species is unsuficiently known and cannot be used in a broader comparative research of Niphargus. In order to follow modern trends in taxonomy, we revised all possible sources of data that might increase the robustness of taxonomic conclusions (Padial et al. 2010). We provide a detailed and richly illustrated redesription of Niphargus molnari and Niphargus gebhardti with cytochrome c oxidase subunit I (COI) sequences as barcodes. We also present comparative scanning electron micrographies which are – to our knowledge – the first comparative micrographies of Niphargus. Moreover, we present phylogenetic relationships of both species within the genus Niphargus using three independent molecular markers and summarize field observations that may indicate species’ ecology.

Material and methods

Sampling sites and sampling

Samples for the redescription were collected in the Abaligeti Cave (N46°8'11.89", E18°6'59.40"), which is located in Southern Hungary, Western Mecsek in Abaliget village, near Pécs city. The altitude of the cave entrance is 219 m above sea level. With its three collaterals and the main passage, the total length of the cave is 2000 m. Its lowest point below the entrance is 10 m, while its highest point is 38 m. Shallow pools of water in the cave are of two types: some are formated by dripping water of the dripstones whereas others are filled during floods and contain residual water. The cave was regulary visited between 2010 and 2013 to characterize its fauna. For the morphological and molecular taxonomic analysis in total 18 and 20 specimens of Niphargus molnari and Niphargus gebhardti respectively were collected on 23 March 2013. Niphargus molnari was found in the stream of the Western 2. collateral and Niphargus gebhardti was collected from a permanent pool in a lateral chamber of ‘Karthago romjai’ hall in the main passage and from a pool at the end of Western 2. collateral, near Akácos Sinkhole’s entrance (Fig. 2). An additional specimen of Niphargus gebhardti for molecular studies was collected from a pool of the Szajha-felső Sinkhole (46°8'5.4"N, 18°7'8.22 E) 30 m vertical distance and 100 m horizontal distance from the entrance. The cave is situated in the area of a platform right above the Abaligeti Cave, 283 m above sea level. The two caves are supposedly connected, their entrances are approximately 1 km from each other (Dezső 2011). Specimens were collected using entomological (soft) forceps and were fixed and stored in 96% ethanol.

Figure 2. — Distribution of the two species within the Abaligeti Cave. 1 *Niphargus* *molnari* along the stream of the Western 2. collateral 2 *Niphargus* *gebhardti* in a permanent pool of ’Karthago romjai’ 3 *Niphargus* *gebhardti* in a permanent pool near the Akácos Sinkhole’s entrance.

Morphological studies

Cleared and stained exoskeletons of 10 (Niphargus molnari) and 11 (Niphargus gebhardti) specimens were dissected under a Leica MZ75 and a Leica M125 stereomicroscope. Slides were examined using a Leica DM 1000 light microscope. Drawings were made using a drawing tube mounted on the light microscope. Measurements were made using the AnalySIS Program Package, the computer was connected with a Zeiss Axioscope II light microscope. In total 230 morphological characters on each speciemens were examined according to the characters of the DELTA program package (Fišer et al. 2009) which were recorded in an Excel data matrix. Scanning micrographs of two individuals of each species about the main characters were made with a HITACHI S-2600 N scanning electron microscope. Specimens were placed in absolute alcohol for one day, then cleaned in an EMAG Emmi-16 Ultrasonic Cleaner and dried out on air. Dry samples were sticked onto holders and were sputter-coated by gold-palladium. Micrographs were digitally edited.

Molecular studies

DNA extraction was performed using QIAamp DNA Microcit® (Qiagen) or Sigma Aldrich GenElute Mammalian Genomic DNA Miniprep Kit® following the manufacturer’s instructions. Only a few pereopods were used for DNA isolation of each animal. The following primer pairs were used for PCR amplifications of COI, 28S rDNA fragment and histone (H3). For COI: LCO 1490 – HCO 2198 (Folmer et al. 1994), for 28S rDNA: 28S lev2 – 28S des2 or 28S rtest2 (Verovnik et al. 2005, Zakšek et al. 2007) and H3aF2–H3aR2 (Colgan et al. 2000) for histone (H3). Details on PCR conditions are listed in Suppl. material 1. PCR products were cleaned using Roche High Pure Purification Kit® or Exonuclease I and Alkaline Phosphatase (Fermentas, Germany) according to manufacturer’s instruction. The fragments were sequenced in both directions using PCR amplification primers using ABI 3130 sequencer in the Laboratory of Molecular Taxonomy in Budapest or Macrogen Europe (Amsterdam, The Netherlands). Contigs were assembled and sequences were edited using Geneious Pro 5.5.6. (Biomatters, New Zeland).

Phylogenetic analysis

In order to recover phylogenetic relationships of Niphargus molnari and Niphargus gebhardti within the genus Niphargus, a dataset of three molecular markers were complied, using available Niphargus sequences from previous studies (see Suppl. material 2 for references) and Synurella ambulans as outgroup taxon (Švara et al. submitted, Meleg et al. 2013). Altogether 104 taxa were included in the final dataset. List of taxa and sequences with GenBank accession numbers used in the analyses are listed in Suppl. material 2. The sequences were aligned using MAFFT 7 (Katoh and Standley 2013). Each sequence alignment was concatenated to the joint dataset and analysed as a single dataset in phylogenetic analysis. The length of combined dataset, including sequences of COI, 28S rDNA and H3 was 2068bp. A general time-reversible model with a proportion of invariant sites and a gamma distribution of rate heterogeneity (GTR+I+Γ) assuming six discrete gamma categories was chosen as the most appropriate model according to AIC and BIC criteria, using ModelGenerator (Keane et al. 2006). Phylogenetic relationships were reconstructed with Bayesian inference (BA) using MrBayes v3.2 (Ronquist and Huelsenbeck 2003). Two parallel searches with four chains each were run for 20 million generations, sampled every 1000^th generation. After discarding the ﬁrst 25% of the sampled trees, the ﬁnal tree was constructed according to the 50% majority rule. MrBayes phylogenetic analysis was run on the CIPRES Science Gateway, www.phylo.org (Miller et al. 2012).

Results

Redescription of Niphargus molnari Méhely, 1927: Order Amphipoda Latreille, 1816: Suborder Gammaridea Latreille, 1802: Family Niphargidae G. Karaman, 1962: Genus Niphargus Schiödte, 1849

Niphargus molnari

Méhely, 1927

Niphargus molnari sp. n.: Méhely 1927 type locality: Mánfai-kőlyuk Cave; Data from the original description is available in Suppl. material 3.
Niphargus leopoliensis molnari : Schellenberg 1933, samples from the Abaligeti Cave, morphological data.
Niphargus molnari : Schellenberg 1935, morphological data.
Niphargus leopoliensis molnari , Niphargus molnari: Gebhardt 1933, 1934, 1963, 1967 distributional data
Niphargus molnari : Méhely 1941 additional morphological data.
Niphargus molnari : Angyal and Balázs 2013 morphological and distributional data.

Material examined for redescription.

7 females and 3 males from the stream of the Western 2. collateral of the Abaligeti Cave (Cadastre number: 4120-1, Hungarian Cave Cadastre), collected in 23 March 2013 (leg. D. Angyal and A. Illés), dissected and mounted on slides; additional 4 specimens not dissected. Slides were deposited in the Collection of Crustaceans of the Hungarian Natural History Museum with the following codes: N.MOL-02, N.MOL-03, N.MOL-04, N.MOL-06, N.MOL-07, N.MOL-08, N.MOL-09, N.MOL-10, N.MOL-11, N.MOL-12. Diagnostic voucher number of specimen used for molecular studies: NB555 (Niphargus molnari, coll. data: Abaligeti Cave, Western 2. collateral, stream, 23 March 2013, leg. D. Angyal & A. Illés).

COI Gen Bank Accession Number: KP967552

Diagnosis.

Small to medium-sized niphargid; epimeral plate III postero-ventral corner sharply inclined. Telson with 3–4 apical spines, 1–3 lateral spines, 0–2 lateral plumose setae, 0–2 spines in cleft, dorsal surface with 1–3 spines in mediobasal position. Maxilla I outer lobe with 7 spines, 1.-3. pluri-toothed, 4.-7. variable (uni-, bi-, pluri-toothed). Gnathopod I and gnathopod II dactyli with single seta on outer margin. Gills II-VI ovoid, approximately same size as pereopod VI coxa, posterior margin slightly concave. Pleopods I-III with 2 retinacles on each. Uropod I lenght of endopodite: length of exopodite ratio as 1.00: (1.00–1.20) on males and 1.00: (1.15–1.18) on females. Uropod III sexually dimorphic, exopodite rod-shaped, distal article of exopodite on males 83–115% of proximal article length and 18–73% on females.

Description.

Body and telson. Small to medium-sized species, females are 6.4 mm to 9.0 mm, males are 7.8 mm to 10.6 mm. Head length up to 13% of body length; rostrum absent. Pereonites I–VI without setae; pereonite V, VI, VII with 1 postero-ventral seta each. Pleonites I–III with 3–6 setae along dorso-posterior margin (Fig. 3). Epimeral plate II ventral and posterior margins straight or sinusoid, ventro-postero-distal corner approximately perpendicular and pointed; along ventral margin 1–3 spiniform setae; along posterior margin 4–6 thin setae (Figs 3, 4). Epimeral plate III ventral margin convex and posterior margin straight, ventropostero-distal corner sharply inclined, strongly produced; along ventral margin 2–3 spiniform setae; along posterior margin 4–6 thin setae (Figs 3, 4). Urosomite I postero-dorso-laterally with 1–2 spiniform seta; urosomite II postero-dorso-laterally with 2–3 spiniform setae; urosomite III without setae. Near insertion of uropod I 1 spiniform seta (Fig. 3).

Figure 3. — *Niphargus* *molnari*, male from the Abaligeti Cave, lateral view. Telson, mouthparts and pleopods II-III are not drawn.

Figure 4. — *Niphargus* *molnari*, scanning electron micrographs. A epimeral plates (Ep1-3 = epimeral plates 1-3) B honeybee-cell pattern on the exosceleton (tipical feature of amphipods) C pleopod with two retinacles (pl-r = pleopod ramus, ret = retinaculum) D retinaculi on the pleopod (ret = retinaculum) E gnathopod II propodus (prop = propodus, sup-spine = supporting spine, dact = dactylus) F palmar region of gnathopod II propodus (dent-spine = denticulated spine, sup-spine = supporting spine, n = nail, palm-spine = palmar spine).

Telson length: width as 1.0: 0.6–0.8; cleft 71–87% of length; lobes apically rounded. Telson spines (per lobe): 3–4 apical spines; lateral margins with 1–3 spine, 0–2 plumose setae; 0–2 in cleft spines, dorsal surface with 1–3 basal spines in mediobasal position (Figs 4, 9). Length of apical spines 20–25% of telson length.

Figure 9. — *Niphargus* *molnari*, t = telson, upI = uropod I, upII = uropod II, upIII-f = female’s uropod III, upIII-m = male’s uropod III.

Antennae and mouthparts. Antenna I 35–48% of body length. Flagellum with up to 19 articles; each article with 1 long aesthetasc. Peduncle article 1: 2: 3 proportions 1.0: 0,78 (0.72–0.88): 0,4 (0.36–0.46). Proximal article of peduncle dorso-distally slightly produced. Accessory flagellum biarticulated; distal article shorter than one-half of the proximal article. Lengths of antennae I: II as 1.0: 0.50. Flagellum of antenna II with 6–8 articles. Lengths of peduncle articles 4: 5 as 1.0: (0.84–0.95); flagellum 54–70% of peduncle length (articles 4 + 5) (Fig. 5).

Figure 5. — *Niphargus* *molnari*, aI = antenna I, aII = antenna II, mxI = maxillaI, mxII = maxilla II, md-R = right mandibula, lm = lacinia mobilis, inc = incisor, md-L = left mandibula, lb = labium, mxpe: maxilliped.

Inner lobes of labium longer than half of outer lobes (Fig. 5).

Left mandible: incisor with 5 teeth, lacinia mobilis with 4 teeth; between lacinia and molar 6–9 thick, serrated setae, long seta at base of molar absent (Fig. 5).

Right mandible: incisor processus with 4–5 teeth, lacinia mobilis with several small denticles (more then 12), between lacinia and molar 6–7 thick, serrated setae, long seta at base of molar present. Proportions of mandibular palp articles 2: 3 (distal) as 1.0: 1,20 (1.17–1.32). Proximal palp article without setae; second article with 9–11 seta in 5–6 groups; distal article with 1 group of 3–5 ’A setae’; 3 groups of ’B setae’; 16–24 ’D setae’; 3–5 ’E setae’ (Fig. 5).

Maxilla I distal palp article with 2–3 apical and subapical setae. Outer lobe of maxilla I with 7 spines, 1–3 spines are always pluri-toothed with 3–6 lateral tooth while 4–6 spines are uni-, or bitoothed. Inner lobe with 1–2 setae (Fig. 5).

Maxilla II inner lobe slightly smaller than outer lobe; both of them setose apically and subapically, number of setae is approximately 13–23 per lobe (Fig. 5).

Maxilliped palp article 2 with 11–17 rows of setae along inner margin; distal article with dorsal seta and group of small setae at base of nail. Maxilliped outer lobe with 6–12 flattened, thick setae and 3–8 serrated setae; inner lobe with 2–3 flattened, thick setae apically and 5–9 serrated setae (Fig. 5).

Coxal plates. Coxal plate I width: depth as 1.00: 1.03 (0.89–1.16), of flattened rhomboid shape, antero-ventral corner subrounded; anterior and ventral margin of coxa I with 3–6 setae (Fig. 6). Coxal plate II width: depth as 1.00: 0.84 (0.76–0.95); anterior and ventral margin with 5–8 setae. Coxal plate III width: depth as 1.00: 0.82 (0.71–1.00); along antero-ventral margin 4–7 setae (Fig. 7). Coxal plate IV width: depth as 1.00: 1.03 (1.26–0.88); posteriorly concave; along antero-ventral margin 5–7 setae (Fig. 7). Coxal plates V-VI: anterior lobe well developed; along posterior margin 1 seta (Fig. 7). Coxal plate VII half-egg shaped, along posterior margin 1 seta (Fig. 7). Gills II-VI ovoid, with approximately same size as coxa VI (Fig. 7).

Figure 6. — *Niphargus* *molnari*, gpI = gnathopod I, gpII = gnathopod II.

Figure 7. — *Niphargus* *molnari*, ppIII = pereopod III, ppIV = pereopod IV, ppV = pereopod V, g = gill, oost = oostegit.

Gnathopods. Basis width is 38 (33–45)% of basis length. Gnathopod I ischium with 4–8 posterodistal setae in 1 row. Carpus length 62 (57–75)% of basis length and 87 (80–100)% of propodus length. Anterior margin of carpus only with distal group of setae; carpus posteriorly with transverse rows of setae proximally and a row of lateral setae, posterior enlargment small. Propodus subquadrate, palm convex. Along posterior margin 6–8 rows of denticulated setae. Anterior margin with 10–17 setae in 2–3 groups, antero-distal group with 6–12 setae. Group of 2–4 facial setae below (proximal of) palmar spine; 2–4 single surface setae present. Palmar corner with palmar spine, single supporting spine on inner surface, and 3 (rarely 4) denticulated, thick spiniform setae on outer side. Nail length 36 (34–37)% of total dactylus length; along anterior margin single seta; along inner margin 4–5 setae (Fig. 6).

Gnathopod II basis width: length as 1.0: 0.26 (0.21–0.29). Ischium with 2–6 postero-distal setae. Carpus length 56 (50–61)% of basis length and 86 (71–94)% of propodus lenght. Anterior margin of carpus only with distal row of setae; carpus posteriorly with transverse rows of setae proximally, a row of lateral setae; postero-proximal bulge small, positioned proximally. Propodus medium-sized (sum of length, diagonal and palm length measures up to 19 (15–21)% of body length) and larger than propodus of gnathopod I (1.0: 0.57 (0.65–0.85)). Propodus rectangular, palm convex. Posterior margin convex with 6–9 rows of denticulated setae. Anterior margin with 10–20 setae in 3–5 groups; antero-distal group with 7–9 setae. 1 group of 2–3 facial setae below (distal of) palmar spine; 1–4 individual surface setae present. Palmar corner with strong palmar spine, single supporting spine on inner surface, and 1 denticulated, thick spiniform seta on outer side. Nail length 31 (22–36)% of total dactylus length. Along anterior margin single seta; along inner margin 4–6 short setae (Figs 4, 6).

Pereopods III-IV. Proportions of pereopods III: IV as 1: 0.95 (0.93–0.97). Dactylus IV 45 (39–51)% of propodus IV; nail length 47 (39–52)% of total dactylus length. Dactyli III–IV with one dorsal plumose seta, one spine-like seta at the base of the nail, and tiny seta near the spine-like seta (sometimes not visible or absent). Additional spiniform setae on posterior margin are absent (Fig. 7).

Pereopods V-VII. Proportions of pereopods V: VI: VII as 1.00: 1.4 (1.37–1.54): 1.5 (1.42–1.61). Pereopod VII length 47 (42–52)% of body length. Basis V-VII narrow with convex posterior margins. Basis V width is 70 (60–78)% of length, basis VI is 67 (59–76)% of length and basis VII is 66 (56–76)% of length. Basis V with small posterodistal lobe, posterior margin with 8-13 setae, anterior margin with 6-8 groups of setae. Dactylus V with one dorsal plumose seta, one spine-like seta at the base of the nail, and tiny seta near the spine-like seta (sometimes not visible or absent). Additional spiniform setae on posterior margin are absent (Fig. 7). Basis VI with small posteriodistal lobe, posterior margin with 9–14 setae, anterior margin with 6–10 setae. Dactylus VI with one dorsal plumose seta (sometimes not visible or absent), one spine-like seta at the base of the nail, and tiny seta near the spine-like seta (sometimes not visible or absent). Additional spiniform setae on posterior margin are absent (Fig. 8).

Figure 8. — *Niphargus* *molnari*, ppVI = pereopod VI, ppVII = pereopod VII, plpII = pleopod II.

Basis VII posterior margin with 6–13 setae, anterior margin with 6–11 groups of setae. Total number of basis setae is 15–21. Dactylus VII length 26 (24–29)% of propodus VII length; nail length 26 (16–33)% of total dactylus length. Dactylus VII with one spine-like seta at the base of the nail. Additional spiniform setae on posterior margin are absent (Fig. 8).

Pleopods. Pleopods I-III with 2-hooked retinacles. Pleopod II rami of 16–20 articles each (Figs 4, 8).

Uropods. Uropod I basipodite with 6 dorso-lateral and 6 dorsomedial spinifom setae. Length ratio endopodite: exopodite as 1.00: 0.89 (0.83–1.0); rami slightly curved. Endopodite total setae number 2–4 in 2–3 groups, apically 5 spinifom setae. Exopodite with 2–7 spines; apically 5 spinifom setae (Fig. 9).

Uropod II endopodite: exopodite length as 1.00: 0.81 (0.77–0.9) (Fig. 9).

Uropod III up to 38–46% (males) and 12–42% (females) of body length. Basipodite with no lateral seta and 3–6 apical spiniform and thin setae. Endopodite 58–61% (males) and 48–70% (females) of basipodite length, endopodite apically with 1–2 thin-flexible and spiniform setae; laterally 0–1 seta. Exopodite of uropod III rod-shaped, distal article of exopodite 83–115% (males) and 18–73% (females) of proximal exopodite article length. Proximal article with 4–5 groups of plumose, thin-flexible and spiniform setae along inner margin and 4 groups of thin-flexible and spiniform setae along outer margin. Distal article with 3–6 apical setae; lateral setae only in males (Fig. 9).