New discoveries for the subfamily Phtisicinae Vassilenko, 1968 (Crustacea: Senticaudata) from the Brazilian coast

Amphipod material collected from Brazil on Ilha do Arvoredo, (Santa Catarina), Campos Basin, (Rio de Janeiro) and Espírito Santo Basin (Espírito Santo) in the southwestern Atlantic Ocean yielded new taxonomic findings for the subfamily Phtisicinae Vassilenko, 1968. Hemiproto wigleyi McCain, 1968, previously recorded from the Gulf of Mexico to the Caribbean Sea, is herein redescribed and recorded for the first time from the Brazilian coast. The type material of Phtisica verae Quitete, 1979, a poorly described species recorded from Brazil and based only on its original description, was examined and considered herein as a junior synonym of P. marina Slabber, 1769, a well-known and widely distributed species from the Atlantic Ocean and the Mediterranean Sea. In this paper, Phtisica marina is redescribed, with its two morphotypes of male gnathopod two, and compared with previous descriptions. The geographic distribution of both H. wigleyi and P. marina is provided. 


Material and methods
Samples of Phtisica marina and Hemiproto wigleyi were provided from two projects coordinated by CENPES/PETROBRAS: 1. Project HABITATS (Environmental Heterogeneity of the Campos Basin) with samples collected from the Campos Basin (25-150 m) from 2008 to 2009, using a Van Veen grab 92 × 80 × 40 cm (Ribeiro-Ferreira et al. 2017); 2. Project AMBES (Marine environmental characterization of the Espírito Santo Basin and north of the Campos Basin portion) with samples collected from the Espírito Santo Basin and north of the Campos Basin portion (12-150 m) from 2010 to 2013, using a Van Veen grab 92 × 80 × 40 cm and Box Corer 50 × 50 × 50 cm. Additionally, the type material of P. verae was loaned from the collection of the Department of Zoology / Instituto de Biologia / UFRJ (CDZRJ) and examined for comparison. In addition, some samples from Ilha do Arvoredo, Santa Catarina, were examined and included in the present analysis.
All material was preserved in 70% ethanol and deposited in the Crustacean Collection of the Museu Nacional (MNRJ). Due to the brittleness of the caprellidean body, the posterior legs (pereopods 5-7) often drop off during the sampling process and they were missing in most samples. The specimens were examined using notes on their most informative and well-preserved features. The most suitable specimens were selected for drawing and dissection. Specimens were dissected under a stereo microscope. Appendages and mouthparts were mounted on glass slides with gelatin-glycerol and illustrated with camera lucida using the optic microscope ZEISS Axioscope. The setal formula used for the last article of the mandibular palp complies with the formula proposed by McCain (1968). For general caprellid morphological nomenclature, see Guerra-García (2006).

Diagnosis
Antenna 1 slightly smaller than body length, flagellum with nine articles, articles 2-3 much longer than article 1. Antenna 2 flagellum with four articles. Gill pairs on pereonites 2-4.

Redescription
Head. Left mandible with 5-toothed incisor, 5-toothed lacinia mobilis, and two accessory plates, row of eight lateral setae; palp 3-articulate, last article setal formula 1-5-1. Right mandible with 5-toothed incisor, lacinia mobilis smooth, two accessory plates and a row of five slender setae; labium outer lobe wing-shaped, inner lobe small. Labrum apically acute. Maxilla 1 outer lobe with four robust apical setae, palp with six robust apical setae. Maxilliped palp second article with six lateral setae and two very small setae inserted at medium-lateral part, article 3 with distal row of five setae; distal article with three toothlike apical projections; outer plate serrate, four setae at top and one inserted at middle border; inner plate strongly serrate with pair of two pectinate acute projections at medial-distal apex, pair of robust setae on ventral-medial part.
abdomen. One pair of small anterior pyriform, appendages; pair of lobes smooth and pair of very elongate posterior appendages, 1-articulate, with three proximal and three distal setae.

Redescription
Head. Labrum outer and inner lobes well demarcated, inner lobe rounded and solid, with row of minute setae. Maxilla 1 outer lobe with five setae and two minute, robust setae; palp 2-articulate with three distal-lateral setae and row of six apical setae. Maxilla 2 external lobe with six apical setae; inner lobe with five apical setae. Left mandible incisor 5-toothed, lacinia mobilis 5-toothed and two accessory plates, row of 12 lateral setae, palp 3-articulate, first article with two distal setae, setal formula of last article 1-2-1-1; right mandible with incisor 5-toothed, lacinia mobilis 5-toothed with two accessory plates. Maxilliped inner plate with one subdistal robust seta and two robust setae on center-distal portion, outer lobe longer than inner lobe, with row of five lateral setae, palp article two enlarged with row of about 14 setae, article 3 with distal crown of setae.
abdomen. Proximal part slightly projected with one pair of 1-articulate pyriform appendages, two pairs of 2-articulate appendages and one pair of lobes. Abdomen tip smooth.
Female. 9.8 mm. Body smooth. Gill plates present on pereonites 2-4. Oostegites reaching end of pereopods 3-4 basis. Gnathopod 1 merus and carpus slightly setose, propodus ventral-lateral margin with fringe of slender setae. Proximal projection with two robust and one slender seta, propodus palm with row of small robust setae and small projections, dactylus serrate. Gnathopod 2 carpus minute, much smaller than merus, propodus nearly elliptical, more than two times as long as wide, with acute ventral projection and three robust setae, palm of gnathopod two membranous lobes absent, dactylus smooth. Pereopod 3 propodus with three robust setae at center, row of minute distal setae, sometimes not visible. Pereopod 4 similar to 3. Pereopods 5-7 not present in any of adult individuals examined.

Discussion
Hemiproto wigleyi was first described by McCain (1968) who stated that the mandible setal formula is very similar to that of Phtisica, which is confirmed in the present study, regarding mandible setal formula (1-5-1 pattern for both Phtisica and Hemiproto). Despite the resemblances, Hemiproto differs from Phtisica in the maxilliped plates armed (versus unarmed), gnathopod 2 basis more than three times as long as pereonite 2 (versus up to 1.5 times) and male abdomen with two pairs of 1-articulate appendages (versus two pairs of 2-articulate + 1 rudimentary).
This work presents the first record of H. wigleyi for the southwestern Atlantic Ocean (Figs 6-7).
Phtisica verae was originally described by Quitete (1979) from Angra dos Reis, Rio de Janeiro and Enseada do Flamengo, Ubatuba, São Paulo and has since then not been recorded from the Brazilian coast. The type material was accessed and compared with the material of Phtisica from Brazil deposited in the Crustacean Collection of the Museu Nacional / UFRJ. The present study acknowledges the existence of two male morphotypes of P. marina that were overlooked in Quitete's original description. Quitete (1979) described the following diagnostic characters for P. verae gnathopod 2, "carpus shorter than merus, propodus with greatest width at mid-length, presenting an irregular membrane at male's palm margin, with proximal spines". When observing the type material, we noticed that the carpus of the male gnathopod 2 is not considerably smaller in all specimens, only in the holotype P. verae Fig. 6. World distribution of Phtisica marina Slabber, 1769 andHemiproto wigleyi McCain, 1968. (0.5 times length of merus), but also in other material of Phtisica. Quitete (1979) pointed out some differences between P. verae and P. marina: 1) male antenna 2 longer than antenna 1 peduncle; 2) mandible setae not serrate (versus serrate); 3) maxilliped inner plate smaller than outer plate (versus subequal or longer); 4) male gnathopod 1 propodus with 3 robust proximal setae (versus four robust setae and dactylus smooth); 5) male gnathopod 2 propodus with one robust seta, two proximal minute setae and an irregular membrane (versus two proximal robust setae, without membrane); 6) pereopods 3-4 with four grasping setae (versus three grasping setae). Examining the type material of P. verae and additional comparative material, we concluded that these differences are inconsistent to establish a new species based on the following observations 1) antenna 1 is considerably longer than antenna 2, varying according to size and development of individuals of P. verae (Figs 3, 5), which were also observed in P. marina, with antenna 2 varying from half-length or up to ¾ of antenna 1 peduncle; 2) morphology of mandible setae was essentially the same, all of them naked (not pectinate) as in the samples of P. marina. The setal formula showed a variation already observed by McCain (1968) (1-2-1 to 1-6-1), having a setal formula of individuals with 1-2-1 or 1-3-1 ; 3) maxilliped inner plate is subequal in length to outer plate, including Quitete's material, differing only from P. antillensis; 4) male gnathopod 1 propodus has four robust proximal setae as described for P. marina. McCain (1968) suggests a range from 4-5 setae while Krapp-Schickel (1993) reported five proximal setae; 5) gnathopod 2 (morphotype II), propodus with three robust proximal setae and three membranous lobes; 6) adult males of P. marina showed five to six robust setae on pereopods 3 and 4, while younger specimens showed three to four setae, therefore we noticed that this character is age dependent and should be used with caution. Moreover, adult males (morphotype II) show a unique recurved shape of pereopod 3 propodus.
In conclusion, Quitete (1979) described the morphotype II as a new species, but she overlooked some intraspecific variation and characters of morphotype II already observed by Sars (1895) and later on by Krapp-Schickel (1993) for P. marina. Based on these observations, the authors propose that P. verae is a junior synonym of P. marina and the genus now includes only two species, P. marina and P. antillensis.
Phtisica marina differs from P. antillensis by male gnathopod 2 carpus 0.5 times as long as than merus (versus two times longer), palm indent located at proximal part of propodus (versus medial) and pereopods 3 and 4 propodus with 4-5 setae in both sexes (versus lacking setae).
Phtisica marina was first described by Slabber (1769) with simple illustrations. The setal formula postulated by McCain (1968), ranging from 1-1-1 to 1-6-1 is in accordance to all specimens observed. Male gnathopod 1 with 4-5 setae grasping setae is in accordance to McCain (1968) and Krapp-Schickel (1993). The present material presents male gnathopod 2 with two morphotypes (Fig. 4). Sars (1895) also described male gnathopod 2 with two morphotypes, being 'type I' with three membranous lobes as the present material. McCain (1968) described only male 'type II', whereas Krapp-Schickel (1993) also illustrated male gnathopod 2 with two morphotypes, with no morphotype designations. Regarding pereopods 3-4, McCain (1968) and Krapp-Schickel (1993) pointed out three small setae on the propodus and Sars (1895) described four robust setae. Nevertheless, the present material shows 3-5 setae, which suggests that this variation range should be added to the species diagnosis. None of afore-mentioned taxonomic works correlates variations in Phtisica marina morphology to its geographical distribution.
Variations in male amphipods behavior and morphology have been observed in Jassa Leach, 1814 (Corophiida: Ischyroceridae), a mate-guarding amphipod genus, known to dissociate sexual activity from physiological maturity and to have dimorphic secondary sex characters in the male (Clark 1997). It is suggested that delay in sexual activity and dimorphism at maturity are responses to competition among males, thus creating different 'male types'. However, further studies on the ontogenetics of Phtisica marina are necessary to address such questions, as whether morphotypes correspond to late life-stages or constitute different individuals, which underlying events are involved, or how such variations may occur.