Hyalella longipropodus Limberger, Graichen & Castiglioni, 2021

Limberger, Marcio, Castiglioni, Daniela Da Silva & Graichen, Daniel Ângelo Sganzerla, 2021, A new species of freshwater amphipod (Crustacea, Peracarida, Hyalellidae) from Southern Brazil, Zootaxa 5026 (2), pp. 182-200 : 184-193

Hyalella longipropodus Limberger, Graichen & Castiglioni , n. sp.

( Figs 2–7 )

Type material. HOLOTYPE: male, head length 0.62 mm, total body length 5.23 mm, Brazil, state of Rio Grande do Sul, municipilaty of Palmeira das Missões, locality of Capão Alto, Distrito de Santa Rosa (27°51’38.1”S- 53°15’12.0”W), MNRJ 028999 , December, 04 2014, Castiglioni, D. S. & Streck-Marx, M. T. colls . ALLOTYPE FEMALE, head length 0.50 mm, total body length = 4.19 mm, Brazil, state of Rio Grande do Sul, municipality of Palmeira das Missões, locality of Capão alto, Distrito de Santa Rosa (27°51’38.1”S- 53°15’12.0W), MNRJ 029000 , December, 04 2014, Castiglioni, D. S. & Streck-Marx, M. T. colls . PARATYPES: MNRJ 29001 (10 males and 10 females), with the same place and data as holotype. Measurements from paratypes: males - mean total body length 4.60 mm, mean head length 0.54 mm (n= 10); females - mean total body length 3.91 mm, mean head length 0.46 mm (n= 10) .

Type locality. Brazil, state of Rio Grande do Sul, municipality of Palmeira das Missões, Distrito de Santa Rosa, locality of Capão Alto (27°51’38.1”S- 53°15’12.0”W), spring ( Várzea river basin), 526 m ( Fig. 1 ) .

Diagnosis. Body surface smooth, epimeral plates not acuminate. Eyes pigmented. Antenna 1 shorter than antenna 2. Antenna 2 longer than half of body length. Mandible incisor toothed. Maxilla 1 palp minute, reaching less than half length the distance between base of palp and tip of setae on outer plate; inner plate slender, with two papposerrate apical setae. Maxilla 2, inner margin of inner plate with two papposerrate setae, being one of them stronger and longer. Gnathopod 1 propodus hammer shape, inner face with seven serrate setae, denticles as comb scales on distoposterior margin, posterior lobe of carpus with border pectinate. Gnathopod 2 propodus, elongated, irregular palm and with a triangular space between propodus and dactylus when this is closed, distoposterior margin of denticles as comb-scales, posterior lobe of carpus with border pectinate. Uropod 1inner ramus of male without curved setae apically. Uropod 3 peduncle with seven strong distal setae with accessory setae, ramus with 10 cuspidate setae with accessory setae. Telson longer than wider, apically rounded, with two simple setae and two small cuspidate setae with accessory setae on distal margin. Sternal gills on ventral surface of pereonites 2 to 7.

Description of male. Mean body length= 4.45 mm, mean head length= 0.53 mm (n= 10) ( Fig. 2 ). Body surface smooth. Epimeral plates not acuminate ( Fig. 3A ). Head smaller than first two thoracic segments, typically gammaridean, rostrum absent. Eyes pigmented, medium, ovoid, located between insertion of antennae 1 and 2 ( Fig. 3A ).

Antenna 1 less than half of body length, shorter than antenna 2, longer than peduncle of antenna 2; peduncle longer than head; flagellum of 11 to 12 articles, longer than peduncle, basal article not elongated; aesthetascs on flagellum, found on articles 5 (2), 6 (2), 7 (2), 8 (2) and 9 (2) distally ( Fig. 3B ). Antenna 2 longer than half of body length; peduncle longer than length of head; flagellum of 19 to 20 articles ( Fig. 3C ). Upper lip margin rounded, distally covered with several short setules on ventral and dorsal faces ( Fig. 3D ). Basic amphipodan mandible [in the sense of Watling (1993)], without palp; incisor toothed; left lacinia mobilis with five teeth; setae row on left mandible with three pappose setae, right mandible with two pappose setae; molar large, cylindrical, and triturative, accessory seta present ( Fig. 3E ). Lower lip lobes rounded without notches or excavations, with several small setules on dorsal and ventral faces ( Fig. 3F ). Maxilla 1 palp uniarticulate, short, reaching less than half length the distance between base of palp and tip of setae on outer plate, inner plate slender, smaller than outer plate, with two papposerrate apical setae and several simple setae on the margin; outer plate with nine serrate setae ( Fig. 3G ). Maxilla 2 inner plate subequal in length to outer plate, inner plate more slender than outer plate and with two papposerrate setae, being one of them stronger and longer, some serrulate and several simple apical setae; outer plate with abundant long simple apical seta; outer and inner plates with several setules distal ( Fig. 3H ). Maxilliped inner plates apically truncated, with three strong cuspidate distal setae, several pappose and simple setae apically and medially; outer plates larger than inner plates, apically truncated, apical, medial and facial simple setae; palp longer than outer plate, with four articles with several simple setae on margin; dactylus unguiform, smaller than third article, with simple setae and without comb-scales and distal nail ( Fig. 3I ).

Gnathopod 1 subchelate; coxal plate longer than wide with short simple setae on the anteromarginally; basis, ischium and merus with simple setae and without comb scales posteromarginally; carpus longer than wide, longer and wider than propodus, with strong and wide posterior lobe bearing polygonal pattern (border pectinate), two rows of denticles as comb-scales and a row of serrate setae, four serrate setae on ventral face; propodus length about two times maximum width (rectangular), hammer shape, inner face with seven serrate setae, distoposterior border with two cuspidate setae and denticles as comb-scales and three simple setae, anteroposterior border without combscales but with several simple setae; dactylus claw-like not surpassing the palm, with denticles as comb scales, with one plumose setae and some simple setae on inner margin ( Fig. 4A ). Gnathopod 2 subchelate; coxal plate longer than wide and with short simple setae on the margin; basis (long), ischium and merus with simple setae and without comb-scales posteromarginally; carpus wider than long, posterior lobe narrow, and with margin elongated with border pectinate with one row of serrate setae and two rows of denticles as comb scales; propodus elongated (length 1.65 maximum width), palm shorter than posterior margin, slope oblique, palm with irregular margin, with several long and short cuspidate setae with accessory setae and some simple setae, posterior margin with denticles as comb scales and two short and strong cuspidate setae with accessory setae and some simple setae; dactylus claw-like, shorter than propodus, with one plumose setae dorsally; triangular space between propodus and dactylus when this is closed ( Fig. 4 B-C). Pereopods 3 to 7 simple with merus, carpus and propodus posterior margins with clusters of 2–3 cuspidate setae with accessory setae; pereopods 3 to 7 dactylus less than half-length of propodus; pereopods 3 to 6 with similar size and pereiopod 7 slightly longer than others ( Fig. 5 A-E).

Pleopods not modified; peduncle slender; longest ramus longer than peduncle, with two coupling setae ( Fig. 5F ).

Uropod 1 longer than uropod 2; peduncle longer than rami with five cuspidate setae with accessory setae; inner ramus slightly longer than outer ramus with three cuspidate setae with accessory setae, six apical cuspidate setae (four with accessory setae), male without curved setae on inner side of ramus; outer ramus with four dorsal cuspidate seta with accessory seta and four distal cuspidate setae (two with accessory setae) ( Fig. 6A ). Uropod 2 outer ramus shortened; inner ramus with three dorsal cuspidate setae with accessory seta and six distal cuspidate setae (four with accessory setae); outer ramus with three dorsal and three distal setae; peduncle with three cuspidate setae with accessory setae ( Fig. 6B ). Uropod 3 peduncle rectangular, wider than ramus, with seven strong cuspidate setae with accessory setae distally and one marginal simple seta the other side; inner ramus absent; outer ramus uniarticulate, same length as peduncle, with seven to ten cuspidate setae (some longer than others) with accessory setae apically ( Fig. 6C ).

Telson wider than long, entire, apically rounded, with two long simple setae and two small cuspidate setae with accessory setae on distal margin, and three small plumose setae laterally close to each distal seta ( Fig. 6D ).

Coxal gills saclike, on gnathopod 2 and pereopods 3–6. Sternal gills tubular, on pereonites 2–7.

Female. Mean body length = 3.92 mm, mean head length= 0.46 mm (n = 10). Antenna 1 flagellum with 10 to 11 articles. Antenna 2 similar in shape to male, flagellum with 14 to 18 articles. Gnathopod 1 greater than gnathopod 2; similar to male gnathopod 1 in size and shape; dactylus claw-like with one plumose setae and with comb-scales; propodus inner face with five serrate setae, simple setae on the inner margin and comb-scales on posterodistal border and little comb-scales on anterodistal border; carpus with pectinate lobe with comb-scales and several serrate setae and three serrate setae and three serrate setae on ventral face; basis, ischium and merus without comb-scales ( Fig. 7A ). Gnathopod 2 different from male gnathopod 2 in shape and smaller; propodus length two times maximum width, anterodistal and posterodistal margins with comb-scales and seven (eight) and thee simple setae, respectively; propodus inner face with two serrate setae; carpus with pectinate lobe with comb-scales and two serrate setae and on ventral face; basis, ischium and merus without comb-scales ( Fig. 7B ).

Molecular analysis. The specimens of Hyaellla longipropodus n. sp. submitted to sequencing analysis presented a single haplotype for both COI and 16S genes. When these haplotypes were compared to sequences of other species, they always presented uncorrected p-distances greater than 19% (COI) and 29% (16S). In comparison to the sympatric species H. gauchensis , the genetic distance was 21% for COI gene and 31% for 16S gene. The differences between other species from the region varied from 19% with H. georginae to 38% with H. palmeirensis for COI gene and 29% with H. bonariensis to 31% with H. gauchensis ( Table 1 and Table 2). In phylogenetic comparisons,

both using COI and 16S genes, the tree topologies placed Hyalella longipropodus n. sp. in an isolated clade from the other species ( Fig. 8 ) with statistical support above 46 % bootstrap.

Etmology. The specific name, “ longipropodus ”, refers to the elongated propodus of gnathopod 2 of the males.

Habitat and ecological conservation. Freshwater, epigean, spring.

Several specimens of males (n = 46) and females (n = 38) of Hyalella longipropodus n. sp., including ovigerous females (n = 3) and couples in pre-copulation behaviour (n = 5) were sampled in the type locality (spring), December 4th, 2014, in which here is cattle raising. The spring had no riparian forest, but there were macrophytes of the genus Polygonum Linnaeus, 1753 and Lemna Linnaeus, 1753 . Spring water at the time of amphipod sampling had 19.8° C of temperature, 6.5 of pH, 51.1 μS/cm of conductivity and 7.9 mg /L of dissolved oxygen. It should be noted that the source is located at about 200 m from the residence and the water is collected to be used for human consumption. Beyond the spring, H. longipropodus n. sp. specimens were also sampled in a stream, two dams and in another spring on the same farm. It should be noted that on the rural property in which H. longipropodus n. sp. specimens were sampled, there aren’t any soybean plantation areas, but dairy cattle farming. However, in the surroundings there are several properties that cultivate especially soybeans, wheat and oats.

Remarks: Among the species of Hyalella found in South America, especially at Brasil, H. longipropodus n. sp. has similarities at the morphology of gnathopod 2 (irregular palm of the propodus) to H. pampeana Cavalieri, 1968 , H. minensis Bastos-Pereira & Bueno, 2013 and H. longistila Faxon, 1876 . Besides the propodus of gnathopod 2 is elongated similar to H. pampeana and H. longistila , and have a triangular space between the propodus and dactylus similar to H. pampeana . The new species has antenna 2 which is longer than those of other species that occurs at the state of Rio Grande do Sul, Brazil, but similar in length to H. kaigang Bueno & Araujo, 2013 , that has antenna 2 with 18 to 24 articles. Besides, it is the only species of state of Rio Grande do Sul, which does not have curved setae in the inner ramus of uropod 1, characteristics shared with the other species with occurrence in other Brazilian states. The species Hyalella longipropodus n. sp. have a several cuspidate setae in the outer ramus of the uropod 3 similar to H. imbya Rodrigues & Bueno, 2012 , another species found in state of Rio Grande do Sul and H. xakriaba Bueno & Araujo, 2013 , specie that occur in the state of Minas Gerais.

The state of Rio Grande do Sul is located geographically very close to Argentina, a country where ten species of Hyalella are known, of which three species also occur in Brazil ( H. curvispina Shoemaker, 1942 , H. pampeana and H. bonariensis ). Of the species that occurs in Argentina, H. longipropodus n. sp. resembles H. misionensis Colla & César, 2015 mainly by the absence of the curved seta on the inner side of the inner ramus of uropod 1 of males, the propodus of gnathopod 2 with the irregular palm and with a triangular space between the propodus and dactylus, telson shape and the number of apical setae, sternal gills present on thoracic segments 2 to 6 and the maxilla 2 with two papposerrate setae in outer plate. However, H. longipropodus n. sp. differs from H. misionensis by length of antenna 2, the number of serrate setae on the inner face of propodus, the number of cuspidate setae on the ramus of uropods 1 and 2 and the number of cuspidate setae on the ramus of uropod 3 ( Table 3).

Figures

FIGURE 1. Type locality (spring) of Hyalella longipropodus n. sp. Limberger, Graichen & Castiglioni in Palmeira das Missões municipality, state of Rio Grande do Sul, Southern Brazil.

FIGURE 2. Paratype male of Hyalella longipropodus n. sp. Limberger, Graichen & Castiglioni, Palmeira das Missões, Palmeira das Missões municipality, state of Rio Grande do Sul, Southern Brazil. Scale: 0.60 mm.

FIGURE 3. Hyalella longipropodus n. sp., Palmeira das Missões municipality, state of Rio Grande do Sul, Southern Brazil. Paratype, male. (A) habitus; (B) antenna 1; (C) antenna 2; (D) mandible; (E) upper lip; (F) Lower lip; (G) maxilla 1; (H) maxilla 2; (I) maxilliped. Scales: 0.65 mm for 2A; 0.5 mm for 2B, C; 0.2 mm for 2D–I.

FIGURE 4. Hyalella longipropodus n. sp. Limberger, Graichen & Castiglioni, Palmeira das Missões municipality, state of Rio Grande do Sul, Southern Brazil. Paratype, male. (A) gnathopod 1; (B) gnathopod 2. (C) propodus of the gnathopod 2 of male. Arrow indicates triangular space between propodus and dactylus. Scales: 3A—0.2 mm; 3B—0.5 mm.

FIGURE 5. Hyalella longipropodus n. sp. Limberger, Graichen & Castiglioni, Palmeira das Missões municipality, state of Rio Grande do Sul, Southern Brazil. Paratype, male. (A) peraeopod 3; (B) peraeopod 4; (C) peraeopod 5; (D) peraeopod 6; (E) peraeopod 7; (F) pleopod. Scales 4A to 4E—0.5 mm; 4F—0.2 mm.

FIGURE 6. Hyalella longipropodus n. sp. Limberger, Graichen & Castiglioni, Palmeira das Missões municipality, state of Rio Grande do Sul, Southern Brazil. Paratype, male. (A) uropod 1; (B) uropod 2; (C) uropod 3; (D) telson. Scales: 5A—0.5 mm; 5B to 5D—0.2 mm.

FIGURE 7. Hyalella longipropodus n. sp. Limberger, Graichen & Castiglioni, Palmeira das Missões municipality, state of Rio Grande do Sul, Southern Brazil. Paratype, female. (A) gnathopod 1; (B) gnathopod 2. Scales: 6A and 6B—0.2 mm.

FIGURE 8. Phylogenetic tree of Hyallela species used in this study.A) Maximum likelihood phylogenetic tree using sequences of the COI gene (T92+G+I). B) Maximum likelihood phylogenetic tree using sequences of the 16S rRNA gene (T92+G+I).