A novel species of Heterophoxus Shoemaker, 1925 (Crustacea, Amphipoda, Phoxocephalidae) from southeast and southern Brazil, with an identification key to world species of the genus

This paper describes a novel species of the genus Heterophoxus Shoemaker, 1925 from Brazil. The material examined was collected during the Mini Biological Trawl Project, off southeast and southern Brazil’s coast off the states of Rio de Janeiro, Santa Catarina, and Rio Grande do Sul, ranging in depth from 25 to 128 meters. The new species, H. shoemakeri sp. nov., is similar to H. videns K.H. Barnard, 1930; however, the former species can be distinguished by: pereopod 7 basis posterior margin serrate with acute teeth, merus posterior margin not produced; epimeral plate 3 posteroventral corner with a longer acute projection, posterior margin almost straight; uropod 3 outer ramus article 2 clearly notable in both sexes. For Brazilian waters, this is the second record of the genus and the first species described with type material from the country. Besides that, we provide an identification key for the world species of Heterophoxus and a distribution map for the new species.


Introduction
The genus Heterophoxus Shoemaker, 1925 was erected with the type species H. pennatus Shoemaker, 1925 and shortly after, the species H. videns K.H. Barnard, 1930 andH. trichosus K.H. Barnard, 1932 were described based on material from Antarctica. In further work on the revision of the family Phoxocephalidae Sars, 1891, J.L. Barnard (1958) assigned the species Harpinia oculata Holmes, 1908 and Ha. ophthalmica Schellenberg, 1925 to Heterophoxus based on the following examined characters: presence of eyes, antenna 2 with an ensiform process on the fi rst article and short maxilliped palp, bearing a long seta. In the same research work, the author synonymized H. oculatus (Holmes, 1908) with H. pennatus, the type species of the genus. Jarret & Bousfi eld (1994) described H. ellisi Jarret & Bousfi eld, 1994 from the northern Pacifi c and invalidated J.L. Barnard's synonymy, stating that the character analysis by the author was not enough to support his decision. Therefore, the species H. oculatus and H. pennatus should be kept as valid. Griffi ths (1975) described H. cephalodens Griffi ths, 1975 and H. opus Griffi ths, 1975 with material from South Africa. Ren (1991) described H. pellusidus Ren in Ren & Huang, 1991 from the Antarctic region and Alonso (2012) described H. despard Alonso, 2012 from the Beagle Channel in Argentina.
So far, the only Heterophoxus species reported from Brazilian waters was H. videns, recorded from the state of São Paulo (Wakabara et al. 1991;Valério-Berardo 1992;Wakabara & Serejo 1998;Valério-Berardo et al. 2000;Rodrigues & Pires-Vanin 2012;Serejo & Siqueira 2018); however, none of these works present illustrations of the sampled specimens. The Brazilian record of H. videns is considered extralimital (Alonso de Pina et al. 2008), since the previous records of the species are from areas with very different water temperature conditions such as the Antarctic shelf and the Magellanic region. This work presents the fi rst species of Heterophoxus described with type material from Brazil.

Material and methods
The material examined was collected by the R/V Prof. Wladimir Besnard, off Brazil's southeastern coast off the states of Rio de Janeiro, Santa Catarina and Rio Grande do Sul in 1970 and 1971, with rectangular dredges at depths ranging from 25 to 128 meters. The campaign was organized by the Instituto Oceanográfi co, Universidade de São Paulo, in the scope of the Mini Biological Trawl (MBT) Project. All specimens are preserved in 70% ethanol and deposited at the Crustacea Collection of the Universidade do Estado do Rio de Janeiro (UERJ). For the taxonomic study, the mouthparts and appendages were dissected and mounted in glycerin gel slides. The drawings were made under an optical microscope with camera lucida, Motic BA-310, and digitalized with CorelDRAW 2018. The distribution map was built with the software QGIS 3.2.1. The setal classifi cation adopted in this paper follows Garm & Watling (2013) and the nomenclature of gnathopod palms is based on Poore & Lowry (1997).

Etymology
The species name is a tribute to Dr Clarence Raymond Shoemaker, for his worldwide contributions to the knowledge of the amphipods.  Fig. 1A. HEAD ( Fig. 2A). Eyes present, rounded, dark in alcohol; rostrum entire, unconstricted. Antenna 1 (Fig. 2B), peduncle article 1 stout, about 1.4× as long as wide, ventral margin with four brush setae, dorsal margin with setules and one pappose seta distally; article 2, short, ventral margin with seven long pappose setae, facial margin with one brush seta; article 3, short, ventral margin with two setae, facial margin with two brush setae and three simple setae distally; primary fl agellum 7-articulate; accessory fl agellum 5-articulate. Antenna 2 (Fig. 2C), peduncle article 1 ensiform; article 3, ventral margin with three pappose setae, dorsal margin with one long seta distally; article 4, ventral margin with long pappose setae, facial margin with two brush setae and a row of long setae extending to dorsal apex; article 5, about 0.7× the length of article 4, ventral margin with fi ve pappose, one brush seta and two distal setae; fl agellum 7-articulate. Left mandible (Fig. 2D), molar as a small hump with three bipectinate stout setae, incisor with fi ve teeth, lacinia mobilis fl abellate, accessory setal row with 10 multicuspidate stout setae, palpar hump medium; palp 3-articulate, article 1 short, article 2, curved, about 4.6× as long as wide, with one medial and two distal setae, article 3, about 1.2× as long as article 2, with two long setae medially, apex oblique, with six medium to long setae. Right mandible (Fig. 2E), molar as a small hump with three bipectinate stout setae, incisor with seven teeth, lacinia mobilis bifi d, with small cusps, accessory setal row with eight multicuspidate stout setae, palpar hump medium; palp 3-articulate, article 1 short, article 2, curved, about 4.7× as long as wide, with one proximal and three distal setae, article 3, about 1.4× as long as article 2, with two long setae medially, apex oblique, with seven medium to long setae. Maxilla 1 (Fig. 2G), inner plate with two plumose setae; outer plate, with nine stout multicuspidate setae; palp 2-articulate, article 2 with six setae forming a row medially and two stout plus two long setae apically. Maxilla 2 (Fig. 2H), inner plate subequal to outer plate, with nine plumose setae, medial margin with row of setules; outer plate, with eight long pectinate setae apically and two mid-lateral setae, lateral margin with row of setules. Maxilliped (Fig. 2F), inner plate with one short stout seta apically and six long plumose setae; outer plate with seven stout setae medially, two stout paposerrate setae apically and two long pappose setae laterally, with the exception of the proximalmost ones, these setae are strongly curved; palp, article 2, medial margin weakly setose, article 3 subrounded, weakly setose, article 4 subtriangular, with two setae on the sides, two apical setae and one long apical nail.

HABITUS. As in
PEREON. Gnathopod 1 (Fig. 3A), coxa, ventral margin expanded, convex, with 15 pappose setae; basis, about 2.4× as long as wide, posterior margin with four long plumose setae medially and three long setae distally; ischium small and subrectangular, posterior margin with one pappose and two simple setae; merus, posterior margin with fi ve pappose setae, facial margin with one long seta; carpus short, 1.2× as long as wide, anterior margin with one seta distally, posterior margin with seven long setae; propodus, 2.2× as long as wide, anterior margin with a tuft of setae distally, posterior margin weakly setose, with one stout seta defi ning palm, palmar hump large; palm acute; dactylus reaching palmar corner, outer margin with one short seta distally. Gnathopod 2 (Fig. 3B) slightly larger than gnathopod 1; coxa subrectangular, ventral margin with nine pappose setae, anterior margin very weakly concave; basis about 2.9× as long as wide, posterior margin with two long setae medially and three long pappose setae distally; ischium small and subrectangular, posterior margin with two long pappose setae and row of four pappose setae extending to facial margin; merus, posterior margin with six pappose setae, facial margin with one pappose seta; carpus short, subtriangular, slightly wider than long, anterior margin with one long seta distally, posterior margin with two pappose and two simple setae; propodus, 2× as long as wide, anterior margin with tuft of setae distally, posterior margin weakly setose, with one stout seta defi ning palm, palmar hump large; palm acute; dactylus reaching palmar corner, outer margin with one short seta distally. Pereopod 3 (Fig. 3C), coxa subrectangular, ventral margin with eight plumose setae; basis about 2.6× as long as wide, posterior margin with four long setae medially and four long pappose setae distally; ischium small and subrectangular, posterior margin with row of six pappose setae extending to facial margin; merus expanded anteriorly, anterior margin with fi ve pappose setae distally, posterior margin moderately setose with medium to long pappose setae; carpus, posterior margin moderately setose, with two stout setae, being the distalmost almost reaching apex of dactylus; propodus, posterior margin with six long setae; dactylus, about 50% the length of propodus. Pereopod 4 (Fig. 3D), coxa strongly expanded posteriorly, posterodorsal margin excavate, ventral margin with   12 plumose setae; basis, about 2.7× as long as wide, posterior margin with three long setae medially, posterodistal corner with one long pappose seta; ischium, small and subrectangular, posterodistal corner with two long pappose setae; merus, anteriorly expanded, posterior margin moderately setose with long pappose setae; carpus, anterior margin with one short seta distally, posterior margin moderately setose, facial margin with four setae, with two stout setae, being the distalmost almost reaching the apex of dactylus; propodus, anterior margin with two short setae distally, posterior margin with fi ve long setae; dactylus, about 55% as long as propodus. Pereopod 5 (Fig. 4A), coxa bilobate, expanded posteroventrally, posteroventral lobe with six pappose setae; basis, about 2.9× as long as wide, anterior margin with two long setae medially and three pappose and one simple seta distally, posterior margin with one long pappose seta medially; ischium small and subrectangular, anterior margin with three pappose setae distally; merus, anterior margin moderately setose, with three stout setae medially and a row of four stout setae extending to facial margin, posterior margin with four long pappose setae medially and one plumose and one stout seta distally; carpus, anterior margin moderately setose, with long pappose and stout setae, posterior margin with fi ve plumose and two stout setae medially, distally with three plumose and three stout setae; propodus, anterior margin with one stout and three pappose setae, posterior margin with one stout and four plumose setae medially, facial margin fi ve long and two stout setae distally; dactylus, about 70% as long as propodus. Pereopod 6 ( Fig. 4B), much longer than the remaining pereopods; coxa, weakly expanded posteroventrally, posterior margin with one short seta and covered with setules; basis, about 1.3× as long as wide, anterior margin convex, posterior margin concave, margins covered with plumose setae; ischium, small and subrectangular, anterior margin with two plumose setae; merus, 2.7× as long as wide, anterior margin with two stout setae, posterior margin with two plumose setae proximally, one stout and one long seta medially, and three stout setae distally; carpus, anterior margin with four sets of stout setae (2-2-2-3), posterior margin with three long and four stout setae; propodus, 8.6× as long as wide, anterior and posterior margins with long and stout setae; dactylus elongate, about 60% the length of propodus. Pereopod 7 (Fig. 4C), coxa, small and subrounded, posteroventral margin with one short seta and row of setules; basis, about 1.3× as long as wide, strongly expanded posteroventrally, exceeding half of merus, posterior margin serrate, with plumose setae in inter-dental notches; ischium, 1.5× as long as wide, distal lobe produced, anterior margin with two stout setae medially, anterodistal corner with three pappose setae; merus, anterior margin with four stout and three pappose setae, posterior margin with two stout setae distally; carpus, anterior margin with three setae, posterior margin with two plumose setae distally; propodus, anterior and posterior margins with two setae each; dactylus, elongate, slightly longer than propodus.

Remarks
The only species of the genus doubtfully cataloged for Brazilian waters is H. videns, recorded from São Paulo State. The original description of the species by K.H. Barnard (1930) and subsequent works with diagnoses and illustrations (Schellenberg 1931;Nicholls 1938; J.L. Barnard 1960) are not enough to make a complete comparison between H. shoemakeri sp. nov. and H. videns. The best-represented scheme of this species in which is possible to check important diagnostic characters was provided by Bellan-Santini (1972). Heterophoxus shoemakeri sp. nov. can be distinguished from H. videns by the following states of characters (H. videns characters in parentheses): mandible palp, article 2 curved (straight); maxilliped, outer plate with strongly curved stout setae (not curved); pereopod 6, basis, posterior margin concave (very weakly concave); pereopod 7, basis, posterior margin serrate with acute teeth (large rounded teeth), merus, posterior margin not produced distally (produced into a rounded lobe); epimeral plate 3, posteroventral corner with a long acute projection (short), posterior margin almost straight (sinuous); uropod 3, outer ramus, article 2 clearly present in both sexes (doubtful/absent in males).

Distribution
The species is known from the coasts of the states of Rio de Janeiro, Santa Catarina and Rio Grande do Sul (Fig. 7), between 25 and 128 meters depth.

Discussion
Heterophoxus shoemakeri sp. nov. presents a gap in its distribution along the Brazilian coast, since the species was not found off the states of São Paulo and Paraná during the present study. We believe that further works with a broader sampling effort will be able to report the species for the possibly missing locations.
According to Karaman (1980), there is a clear taxonomic problem within the subfamily Harpiniinae Barnard & Drummond, 1978, presenting a complex of genera. The genera Heterophoxus and Proharpinia Schellenberg, 1931 differ from the Harpinia complex only by the presence of eyes; nevertheless, it is known that the presence/absence of eyes within amphipods cannot be used as a generic distinctive character (Thurston & Bett 1993). Barnard & Drummond (1978) used male characters for a generic division within Harpiniinae, but male specimens of many species are poorly described or unknown, resulting in an obstacle in defi ning which genus some species belong to. The authors state that the use of certain taxonomic characters is dubious such as presence/absence of eyes, ensiform fi rst article of antenna 2 and a row of stout setae on uropods 1-2. Hence, the validity of the genera Heterophoxus, Proharpinia, Pseudharpinia Schellenberg, 1931 andHarpiniopsis Stephensen, 1925 is uncertain, and only new and more detailed studies will defi ne whether the four genera should be merged into one group. For now, we consider the four genera as valid and distinct from each other until molecular studies are done to solve these taxonomic issues.