Redescription of Schizodon dissimilis and appraisal of the dark barred species of the genus (Characiformes: Anostomidae)

Schizodon dissimilis is redescribed on the basis of syntypes and non-type specimens from the Parnaíba, Jaguaribe and Mearim rivers, and lectotype and paralectotypes are designated. Schizodon dissimilis is distinct from the Amazonian and southeastern Brazil congeners by having four dark brown vertical bars without a midlateral dark brown stripe or a dark blotch on caudal peduncle. When compared with the northeastern Brazilian Schizodon and those from the São Francisco river, and with the remaining dark barred species S. australis , S. borellii , S. corti, S. fasciatus and S. intermedius , it is diagnosed by a combination of lateral line scale counts, color pattern and body proportions. The color pattern distinguishes S. dissimilis from S. fasciatus and the meristic and morphometric data are important in separating S. dissimilis from S. intermedius and S. borellii . Schizodon dissimilis and S. fasciatus have disjunct distributions, with the first occurring in northeastern basins, and the second widely distributed through the Amazon basin and rivers draining northward from the Guyana Shield. Schizodon intermedius and S. borellii are respectively native to the upper Paraná and Paraguay river basins while S. australis is known from the Paraná-Uruguay system and S. corti was described from Maracaibo, Venezuela.


Introduction
The anostomid genus Schizodon was created by Agassiz for the species S. fasciatus described by Spix, Agassiz (1829) from Brazilian rivers. In his revision of anostomid fishes, Myers (1950) recognized Schizodon as a genus with eight serrate teeth on each jaw. That dental character remained the diagnostic feature for Schizodon until recently, when Sidlauskas, Vari (2008) added that the second and third teeth of premaxilla have four cusps, and the distal margin of the main lobe of the symphyseal dentary tooth has three distinct cusps. Those authors also proposed two osteological synapomorphies for Schizodon, the wide ascending process of the anguloarticular and a torsion in the medial flange of the mesocoracoid. Although the genus is broadly accepted and relatively well defined, its species-level taxonomy and relationships still need further study.
A redescription of Schizodon dissimilis (Garman, 1890) is needed, and indeed overdue. In this study, we evaluate the members of Schizodon fasciatus species group and redescribe Schizodon dissimilis (Garman, 1890) based on examination of the syntypes of this species from the rio Poti and additional specimens from the rivers Parnaíba, Poti, Jaguaribe and Mearim. Meristic and morphometry were taken on four commonly misidentified species in the Schizodon fasciatus group (S. dissimilis, S. fasciatus, S. borellii and S. intermedius) following Garavello (1994). Meristics included counts of premaxillary and dentary teeth, and counts of scales in the lateral line, predorsal series, transverse series, preanal series and circumpeduncular series. Measurements taken point-to-point with the help of digital calipers included: standard length, head length, trunk length, body depth, predorsal distance, snout length, interorbital distance, orbital diameter, caudal peduncle depth, first anal-fin ray length, ninth anal-fin ray length, interopercular distance, head depth, premaxillary length and mandibular width. Head length was taken from the tip of the snout to the posterior bony margin of the opercle. Meristic and morphometric characters were obtained for a total of 107 specimens of S. dissimilis (n=26 specimens) S. fasciatus (n=28); S. borellii (n=27) and S. intermedius (n=26).

Multivariate morphometric analysis:
Principal component analysis (PCA) was used to explore morphometric differences between S. borellii, S. dissimilis, S. fasciatus and S. intermedius. In this analysis fifteen measurements were taken on 81 specimens of S. dissimilis (n=13), S. fasciatus (15), S. borellii (n=27) and S. intermedius (n=26). PCA was performed on the natural logarithms of the measurements using the covariance matrix in accordance with Bookstein et al. (1985) and sheared thereafter in accordance with Macleod (1990). This sheared principal component analysis (PCA) removes the influence of a general size factor on the second principal component axis (PC2) and subsequent axes (Humphries et al., 1981). The eigenvectors resulting from the shearing procedure were analyzed to determine whether the species considered in the analysis differ in shape. Results of the sheared PCA on component axes II and III are represented by a scatterplot graph, while meristic and morphometric data on S. dissimilis and S. fasciatus are presented in a separate table.

Results
In the unsheared principal component analysis, PC1 explained 93.9% of the total variance. PC2 and PC3 explained 1.7 and 1.5% of the total variance, respectively (Tab. 1). After shearing, PC2 alone failed to discriminate between the four species analyzed (S. borellii, S. dissimilis, S. fasciatus, S. intermedius); however, a scatterplot of the sheared PC2 and sheared PC3 (Fig. 1) separated S. intermedius from the other three species, and separated S. dissimilis from S. intermedius and S. borellii. Measurements loading most heavily on the sheared PC2 were: ninth anal-fin ray length (-0.66) and pre-maxillary length (0.40), and in the PC3 were: ninth anal-fin ray length (0.52), body depth (-0.47), head depth (-0.37), orbital diameter (0.33), first anal-fin ray length (-0.28), caudal peduncle depth (-0.24), and head length (0.23) (Tab. 2). Although there are no conspicuous morphometric differences between S. dissimilis and S. fasciatus, the latter is readily distinguished by the presence of a dark brown blotch on the base of caudal peduncle that is absent in the other three species.   Diagnosis. Schizodon dissimilis is a member of the Schizodon fasciatus species group distinguished by having four conspicuous dark brown bars along the trunk and lacking any sort of dark stripe or elongate blotch along the lateral-line scale row vs. having a dark midlateral stripe running from the opercle to the caudal peduncle (some specimens of S. knerii, S. isognathus, S. scotorhabdotus and S. nasutus) or from the vertical through the dorsalfin origin to the caudal peduncle (S. vittatus, and some specimens of S. knerii, S. altoparanae and S. jacuiensis); or a dark elongate blotch on caudal peduncle (S. altoparanae, S. nasutus, S. platae, S. rostratus and some specimens of S. knerii). Schizodon dissimilis is distinguished by other members of the S. fasciatus species group by having 42-43 lateral-line scales vs. 40-42 in S. borellii and S. intermedius, 44-45 in S. fasciatus and S. corti, 44-46 in S. australis. It is further distinguished from S. australis by possessing 4 transverse scale rows above and 4-4.5 below the lateral line (vs. 5.5/5.5 in S. australis). Schizodon dissimilis is further distinguished from S. australis, S. corti and S. fasciatus by the lack of a dark blotch on the base of the caudal peduncle (vs. the presence of such a blotch in S. australis, S. corti and S. fasciatus). Schizodon dissimilis is distinguished by S. intermedius in relative values of body depth in SL (3.9 to 4.9, mean 4.0 in S. dissimilis vs. 2.9 to 3.9, mean 3.5 in S. intermedius). The color pattern of S. dissimilis is most similar to that of S. intermedius and S. borellii, and the meristic characters of S. dissimilis and S. borellii overlap partially. Despite the morphological similarity between these species, both are considered distinct herein based on their morphometric separation in the sheared PCA and their allopatric distribution. Molecular data are also informative on the distinction among S. dissimilis, S. fasciatus, S. borellii and S. intermedius (see discussion section below).
Description. Morphometric and meristic data of S. dissimilis are presented in Tab. 3. Body fusiform; greatest body depth at or just anterior to dorsal-fin origin. Dorsal profile of head gently curved from snout tip to vertical through anterior margin of eye, rising nearly straight to vertical through posterior margin of opercle, then leveling off to dorsal-fin origin; predorsal region from vertical through posterior margin of opercle to dorsal-fin base slightly convex, forming gentle hump; dorsal-fin base straight, slightly descending; profile from dorsal-fin to adipose fin straight, descending more gradually than dorsal-fin base; caudal peduncle slightly concave. Ventral profile from lower jaw to anal-fin insertion slightly convex with point of maximum inflection at pelvic-fin insertion; base of anal-fin straight, ascending; caudal peduncle slightly concave.
Mouth small, upper and lower jaws horizontally aligned with median region of orbit when the mouth is closed. Upper and lower lips smooth. Maxillary slightly curved along ventral margin and widening posteriorly into a flat rhomboidal plate. Each premaxillary and dentary with four serrate teeth (n=26 including lectotype), forming serrated cutting edge. Teeth slightly graded in size; symphysal teeth largest on each jaw; most distant tooth from symphysis much smaller. Anterior and posterior nostrils horizontally aligned with upper lip and upper quarter of orbit. Infraorbitals large; supraorbital positioned at anteriodorsal margin of orbit. Branchiostegal rays and opercular membrane connected at isthmus.

Tab. 3.
Morphometrics of Schizodon dissimilis and S. fasciatus expressed as percentages of SL and HL. Meristic data with numbers of specimens with each count in parenthesis. All lectotype data in millimeters. All specimens of S. dissimilis (n=26 including lectotype) with one extremely small anterior unbranched ray in dorsal fin followed by two major unbranched rays and seven branched rays with the first one longest. Anal fin with two unbranched rays, the first shorter than the second, followed by eight branched rays; first branched anal-fin ray slightly longer than unbranched rays; posterior margin of anal-fin slightly convex. Fleshy cover at base of anterior dorsal and anal fin rays extended. Pectoral fin with two unbranched and 15 branched rays; shape of extended pectoral fin almost triangular. Pelvic fin with one unbranched and eight branched rays; origin at vertical through base of first or second branched dorsalfin ray. Adipose fin elongate, length approximating three dorsal scales; origin at vertical through base of first or second branched anal-fin ray. Caudal fin with 10 principal rays; rays heavily ramified in adults; lobes blunt with rounded margins.
Lateral line scales: 42-43 (43 in lectotype). All lateral line scales pored, including those over caudal-fin rays; sixteen regular scale series around caudal peduncle just posterior to adipose-fin insertion in all specimens including lectotype. Four major scale rows dorsal to lateral line and 4 to 4.5 below lateral line at dorsal fin origin (lectotype 4/I/4); incomplete series of scales on base of dorsal and anal fins; predorsal scales 11-12 (11 in lectotype); scales in preanal series 33-35 (35 in lectotype); circumpeduncular scales series 16 (including the lectotype).

Color in alcohol.
Overall ground color brown dorsal to lateral line between opercle and caudal peduncle, light yellowish beginning one or two scale series ventral to lateral line, abdomen and lower caudal peduncle especially pale. Dorsal surface of head brown; ventral surface of head, gular region and branchiostegal membrane yellowish. Sides with four distinct inclined dark brown vertical bars; intensity of dark brown coloration varies among specimens, but number of bars always four. First bar about five scales anterior to dorsal-fin insertion; second bar ventral to dorsal-fin insertion; third situated between end of dorsal-fin base and adipose-fin origin; fourth ventral to adipose fin insertion. First and fourth bars three or four scales wide, second bar two scales wide, third bar two or three scales wide. Opercle brown with hyaline fleshy flap. Unbranched rays of anal, pectoral and pelvic fins occasionally with dark melanophores; fins otherwise hyaline, including adipose fin. Caudal fin with superior lobe slightly brown and inferior lobe conspicuously brown.

Discussion
On the color patterns of Schizodon species. Garavello (1994) discussed the color pattern of dark bars in Schizodon australis, S. borellii, S. corti, S. dissimilis, S. fasciatus, and S. intermedius. The six species together comprise the Schizodon fasciatus group defined by having dark brown bars throughout ontogeny, although the bars may vary in intensity. Schizodon fasciatus, S. australis and S. corti, exhibit four dark brown bars and an additional dark brown blotch on the caudal peduncle throughout their ontogeny. On the other hand, S. dissimilis, S. borellii, and S. intermedius never possess this dark brown caudal peduncle blotch at any stage of their development. Sidlauskas et al. (2007) considered the horizontally striped color pattern of S. scotorhabdotus to be stable throughout its development but variable in intensity. That may well be true for the remaining species of Schizodon. Adults of other species, such as S. rostratus, S. nasutus, and S. altoparanae exhibit a dark brown horizontally elongated blotch on the base of caudal peduncle, differentiating them from S. jacuiensis, S. isognathous, and some specimens of S. knerii, which normally have an elongate mid-lateral dark stripe aligned with a shortened dark brown blotch at the lateral-line terminus. Schizodon knerii varies in color pattern, with some specimens having only three large inconspicuous brown bars on trunk, not combined with a horizontally elongate blotch on the caudal peduncle.
The similar color pattern of the transversally brown barred Schizodon resulted in misidentifications of species from distinct river basins. Besides Fowler (1941) and Roberts (1973), Sales et al. (1984) applied the name S. fasciatus to specimens from northeastern Brazil, which we consider to be S. dissimilis. The reference of Sarmiento et al. (2014) to S. dissimilis for the Bolivian Amazon drainages may be considered a misidentification. In addition, the barred Schizodon species from the Parana-Paraguay system was misidentified as S. fasciatum fasciatum by Ringuelet et al. (1967), using specimens from the Paraná River in Argentina, and also misidentified as Schizodon aff. dissimile by Géry et al. (1987) using specimens from the Paraguay river. This kind of error suggests that those authors did not recognize Schizodon borellii (Boulenger, 1900).
Schizodon dissimilis, S. borellii, and S. intermedius share the same color pattern, but recent molecular studies on Schizodon barred species (Santos, 2018 and Ramirez et al., in preparation) show separation among these three species. Evidence from the COI gene suggests a close relationship between S. borellii and S. intermedius, while S. dissimilis is genetically distant from these two species. These molecular analyses also suggest that the taxonomy of the barred Schizodon species-level still needs further study to elucidate the group's true diversity.

On the misidentifications of Schizodon barred species in
Parana-Paraguay and northeastern basins. Géry (1987: 378) cited Schizodon aff. dissimile from the Paraguay River, perhaps misidentifying specimens of Schizodon borellii (Boulenger, 1900). The problem stems from Boulenger's (1895: 2, 3) description of the genus Nanognathus and species Nanognathus borellii based on a single specimen from "S. Pablo, Argentina". Later, Nanognathus was considered a synonym of Characidium (Crenuchidae: see Buckup in Reis et al., 2003: 88), and Characidium borellii is currently a valid species. A few years later, Boulenger (1900: 2) described Anostomus borellii based on a single specimen from Carandasinho (=Carandazinho), MT, Brazil, and this species is currently allocated to Schizodon (Anostomidae). Boulenger named both species after Alfredo Borelli, the collector of the type specimens in the Paraguay River system. The use of the same specific name for both species from the same river basin led to complex misconceptions concerning the barred species of Schizodon, as discussed below. Eigenmann, Kennedy (1903: 512) identified specimens from the Paraguay River at Asuncion and Estancia La Armonia as Anostomus fasciatus (= Schizodon fasciatus) but Eigenmann, Ogle (1907: 7) later identified specimens from Paraguay as Anostomus borellii (= Schizodon borellii). Thus, Eigenmann apparently recognized that he had incorrectly identified the specimens in the first article co-authored with Kennedy.
Finally, we examined the specimens from Russas, Ceará, Brazil assigned to S. fasciatus by Fowler (1941: 175). Those specimens, ANSP 69491 (3) and ANSP 69494 (1), collected by Ihering in 1936 and sent to Fowler, are herein identified as S. dissimilis. Also, the specimen MCZ 46796 (1, cleared and stained), cited by Roberts (1973) as S. fasciatus is more likely S. dissimilis. Robert's specimen is from Parnaíba River in northeastern Brazil whereas S. fasciatus is native to the Amazon and north-flowing drainages of the Guyana Shield.
On the geographic distribution of the Schizodon transversal brown barred species. Garavello (1994: 187) discussed the disjoint distributions of the six species with dark bars: S. australis, S. borellii, S. corti, S. dissimilis, S. fasciatus, and S. intermedius. Schizodon dissimilis is restricted to the isolated northeastern rivers Itapecuru, Parnaíba, Mearim, Poti, and Jaguaribe, while S. corti is known only from the type locality in the Maracaibo drainage of Venezuela. Schizodon fasciatus occurs in the Guianas and throughout the upper and central Amazon in Peru, Colombia and Brazil. Schizodon borellii and S. intermedius are restricted to the Paraguay and upper Paraná basins, respectively, while S. australis is common in the Uruguay River.
Schizodon dissimilis, S. rostratus, and S. knerii occur in the north and northeastern rivers of Brazil and have distributions similar to the northeastern species of Curimatidae studied by Vari (1988). In that study, Vari (1988) revealed disjunct distributions for some curimatid genera that suggest two regions of endemism. Vari's northeastern area of endemism is marked by the endemic species Curimata macrops Eigenmann, Eigenmann, 1889 from the Parnaíba River and Psectrogaster saguiru (Fowler, 1941) from rivers of Ceará state. In addition, Fowler (1941: 175) reported Caenotropus labyrinthicus (Kner, 1858) from Parnaíba River, a species that Vari et al. (1995) also recognized from the Poti River. Vari's second area of endemism for Curimatidae extends from São Francisco to the coastal rivers of Rio de Janeiro.
The distribution of Schizodon dissimilis coincides with the northeastern endemic area proposed by Vari (1988) for curimatids. Furthermore, brown barred Schizodon species do not occur in the neighboring São Francisco River or in the isolated coastal basins from Bahia to Rio de Janeiro. However, other species of Anostomidae occur in both northeastern Brazil and in the São Francisco basin, such as Leporinus piau Fowler, 1941and Leporinus taeniatus Lutken, 1875(Birindelli et al., 2013, blurring the distinctiveness of those endemic areas. This is the expected pattern since, as showed by Dagosta, de Pinna (2017), all regions and South American basins are historically (and compositionally) hybrid. Their ichthyofaunal composition are mosaics of divergent elements of different origins, mostly from neighboring regions/basins.