Trichogenes beagle, Pinna & Reis & Britski, 2020

Pinna, Mário De, Reis, Vinícius & Britski, Heraldo, 2020, A new species of Trichogenes (Siluriformes, Trichomycteridae), with a discussion on the homologies of the anterior orbital bones in trichomycterids and other loricarioids, American Museum Novitates 2020 (3951), pp. 1-28 : 3-19

Trichogenes beagle , new species

Figures 1, 2A, 3; table 1

HOLOTYPE: MZUSP 125019 , 35.5 mm SL, no data (see comments on Distribution below) . PARATYPES: MZUSP 124888 , 2 (1 c&s), 32.7–37.9 mm SL, supposedly collected with holotype .

DIAGNOSIS: Trichogenes beagle is distinguished from its two congeners, T. longipinnis and T. claviger , by: (1) the color pattern composed of small uniform-sized dark markings irregularly distributed on body, not forming any pattern (fig. 2A; vs. presence of both small and large round spots, with the latter aligned in parallel to base of anal fin); (2) the lack of dark concentrations around latero-sensory pores on head (vs. pores outlined in dark); (3) the presence of a faint white vertical band along the margin of the hypural plate, delimited anteriorly and posteriorly by darker areas (vs. equivalent dark band or vertical series of dark spots in same position); (4) the absence of differential dark concentration along the base of the dorsal fin (vs. well-defined dark band present); (5) the presence of a wide (ca. 25% of the depth of the anal fin) white band parallel to the base of the anal fin (vs. band absent in T. longipinnis and narrower than 20% of the depth of the anal fin in T. claviger ); (6) the lack of dark pigment concentration on the ventral area of opercular odontodes (vs. no differential dark pigmentation along area of opercular odontodes); (7) the barbular bone (see Discussion) articulating with the distal portion of the antorbital process of the lateral ethmoid (figs. 4, 5, 6; vs. barbular bone absent in T. claviger and articulating with the midlength of the antorbital process in T. longipinnis ); (8) the opercular odontodes continuously distributed along a large portion of the margin of the opercle (figs. 3, 7, 8; vs. opercular odontodes distributed in two separate patches); (9) the presence of some tricuspidate teeth on jaws (fig. 9; vs. none tricuspid). Further distinguished from T. claviger by having 8+9 principal caudal fin rays (fig. 3; vs. 7+8); I+8 dorsal-fin rays (vs. I+7); by the presence of a barbular bone (vs. absence). Further distinguished from T. longipinnis by the terminal mouth (fig. 1; vs. subterminal); the presence of ossification on the second hypobranchial (fig. 10; vs. second hypobranchial entirely cartilaginous); the presence of an anterodorsal clawlike process on the dorsal surface of the neural arch of each of the anterior four free vertebrae (fig. 11; vs. process absent); the interopercular odontodes extending onto the posterodorsal margin of the interopercle (figs. 3, 7; vs. odontodes mostly restricted to ventral and posterior margins of the bone); by the posterior naris broader than long (vs. round); by the presence of an entirely differentiated fleshy lobe laterally on the lower lip (vs. fleshy lobe mostly continuous with the lower lip); by the lack of any branched anal-fin rays (fig. 3; vs. most anal-fin rays branched in adults); the deeper head (head depth 70.4.–71.5% HL; vs. 50.3–62.8% HL); by the deep coronoid process of the lower jaw (vs. coronoid process comparatively less deep); by the presence of 36 free vertebrae (vs. 38 or 39); by the presence of 6 branchiostegal rays (fig. 12; vs. 7); by the absence of a pelvic splint (vs. pelvic splint present); by the presence of 9 pleural ribs (vs. 10 or 11); by a well-defined thin dark line along base of anal fin, formed by a regular row of slanted elongate spots on the distal portion of each pterygiophore (fig. 2; vs. no such line); by the lack of dark spots on the sides of head (fig. 2; vs. lateral surfaces of head with roundish spots); by the dark spots on body not extending onto base of caudal fin (fig. 2; vs. spots covering bases of principal caudal-fin rays); and by having the deepest part of the body at the middle of the abdomen, then continuously less deep posteriorly to the base of the caudal fin (vs. deepest part of the body at the origin of the anal fin, with the body depth approximately even, only slightly decreasing towards the caudal fin).

DESCRIPTION: Body blunt, deeper than broad anteriorly and gradually more compressed posteriorly to caudal fin. Anterior part of body and head, from snout to dorsal-fin origin, straight or in broad continuous convex arc. Dorsal profile of posterior region of body, from endpoint of dorsal fin to caudal-fin origin, mostly straight. Ventral profile variably convex (due to abdominal distension) broadly convex from snout to origin of pelvic fins, then straight along entire length of anal-fin base. Deepest part of body at middle of abdomen immediately anterior to pelvic-fin origin, then gradually less deep to base of caudal fin.

Head approximately as wide as deep, its depth approximately three-quarters or more of HL. Mouth terminal, positioned at middepth of head, with jaws equally long or upper jaw slightly longer than lower one. Upper and lower lips narrow. Upper lip continuous laterally with maxillary barbel. Lower lip smaller and narrower than upper lip, laterally differentiated into well-defined elongate fleshy lobe attached anteriorly on lip, separating lip from base of rictal barbel. Dentary teeth 15–17, disposed in three rows. Outer row with 6 or 7 large, distally expanded, compressed and slightly tan colored, with bicuspid and tricuspid teeth interspersed (figs. 9, 12), with round cusp edges, gradually smaller laterally, with lateralmost one or two teeth conical. Teeth on inner row smaller, less markedly expanded and less deeply bilobed than on outer one. Two rows mixing up laterally, with 2–4 lateral teeth conical. Premaxillary teeth similar to those on dentary, 15–18 in number and also disposed in two rows, with 6–7 teeth in outer row (figs. 9, 12). Difference in tooth morphology between rows similar to that described for dentary. Two or three lateralmost premaxillary teeth of inner row conical. Many replacement tooth cusps alongside inner tooth row on both dentary and premaxilla.

Center of eye located anterior to middle of HL, closer to lateral margin of head than to dorsal midline in dorsal view. Skin over eye thin and transparent, orbital margin free. Infraorbital laterosensory canal complete, with five ossicles plus lacrimal-antorbital anteriorly. Five infraorbital pores, first one positioned posterodorsally to eye, second one posteroventrally to it, third and fourth ones along ventral margin of eye and fifth one directly anterior to that, close to dorsal margin of maxillary barbel base. Anterior naris surrounded by short anterolateral integument tube, continuous posterolaterally with nasal barbel. Posterior naris large and wide, broader than long in shape, located directly posterior to anterior one and partly occluded by two partly continuous flaps of skin. Three pairs of barbels, maxillary one maximally reaching base of first pectoral-fin ray or slightly beyond. Rictal barbel inserted ventrally to maxillary one, reaching posterior tip of interopercular patch of odontodes. Nasal barbel originating on posterolateral region of anterior naris, reaching anterior margin of eye. Opercular odontodes disposed along posteroventral margin of opercle (fig. 8) with concentration of 6–7 small odontodes at well-defined distal opercular process with round expanded tip. Remaining 4–5 odontodes more or less evenly disposed in single irregular file. Interopercle with well-developed patch of odontodes, visible in lateral and ventral aspect of head. Odontodes extending onto dorsal margin of bone posteriorly. Approximately 20 interopercular odontodes distributed along entire ventral, posterior, and part of dorsal margin of interopercle. Dorsal odontodes four in number, forming well-defined roundish sawlike arrangement of erect small odontodes (fig. 7). Odontodes along ventral portion of interopercle disposed in two series, with those on outer row larger than those on inner row.

Branchial arches with ossified basibranchials 2 and 3, and cartilaginous basibranchial 4, plus anterior cartilaginous body putatively representing vestigial basibranchial 1 (otherwise absent in siluriforms). Hypobranchials mostly cartilaginous, except for ossified anterolateral tips of hypobranchials 1 and 2 (with former produced into differentiated anterolateral process). Gill rakers present on all ceratobranchials and on short sector of first epibranchial. Accessory cartilaginous element of ceratobranchial 4-segmented and connected with elongated posterior cartilage of ceratobranchial 5 by membrane (fig. 10). Epibranchials 1–3 bearing well-defined uncinated processes directed posteromesially, largest on third element. Upper pharyngeal toothplate only slightly larger than associated ossified portion of pharyngobranchial 4.

Pectoral fin large, with convex distal profile, its base immediately posterior to vertical through tip of interopercle, shorter than HL. Pectoral-fin rays I+9 (n = 3). Pelvic fin with round distal profile, its origin slightly posterior to vertical through tip of pectoral fin. Tip of pelvics extending posteriorly beyond origin of anal fin. Pelvic-fin rays I+6 (n = 3). First pelvic-fin ray (unbranched) shorter than others. Pelvic splint absent. Dorsal fin smaller than pectoral fin, its distal profile convex. Dorsal-fin origin closer to base of caudal fin than to tip of snout, and anterior to middle of anal fin. Dorsal-fin rays I+7 (1 ex with malformed posterior ray), plus single large procurrent ray anteriorly. Anal fin long, its distal profile straight or gently convex, with round posterior end. Last anal-fin ray adnate for 80% of its length. Origin of anal fin slightly anterior to middle of SL, its base longer than 50% of body length (excluding head). All anal-fin rays unbranched, numbering 31 (n = 1) or 32 (n = 2), plus 2 small procurrent rays anteriorly to the first segmented and unbranched ray (fig. 3). Caudal fin strongly bilobed, with 8+9 principal rays. Upper lobe longer than lower lobe. Procurrent caudal-fin rays 7–9 dorsally and 5–6 ventrally, plus one accessory segmented unbranched ray on each lobe (n = 3; fig. 3).

Lateral line extending in straight path along mid-lateral line, from posterior part of head to vertical through middle of pelvic fin, almost reaching vertical through origin of anal fin, internally corresponding to position of 10th free vertebral centrum. Lateral line continuous for anterior two-thirds, then prolonged as series of four short independent tubules. Total of 16 lateral-line pores, eight of which in anterior continuous portion and eight at interrupted portion (each tubule with two terminal pores). Eleven short lateral-line ossicles positioned between pore pair. Vertebrae 36 (n = 3; fig. 3). First anal-fin pterygiophore inserted posterior to hemal spine of 12th free vertebra (n = 3; fig. 3). First dorsal-fin pterygiophore inserted posterior to neural spine of 17th (2) or 18th (1) free vertebra (fig. 3). Dorsal-fin pterygiophores 7, anal-fin pterygiophores 31 (fig. 3). Pleural ribs 9. Branchiostegal rays 6.

COLORATION (fig. 1): Dorsal and lateral sides of body and head with uniform background scattering of small dark chromatophores, denser dorsally. Dark background abruptly ending near base of anal fin, forming broad white band parallel to base of anal fin, equivalent to approximately 25% of fin depth. Concentration of melanophores forming well-defined round or oblong spots scattered irregularly on dorsum and sides of body, not arranged in any specific pattern. Spots and background covering not entering caudal fin. Abdominal region white. Well-defined dark line on body along base of anal fin, formed by series of partly coalescent, elongate, and anteriorly slanted dark markings on distal portion of each anal-fin pterygiophore.

Such a dark line underlies broad white band mentioned above, forming striking contrast with it. Narrow vertical white bar over distal portion of hypural plate, formed by abrupt and well-defined lack of background melanophores.

Head with uniform covering of fine chromatophores, similar to background color of body but lacking larger spots of latter. Skin at dorsal platform of opercular odontodes darker than surrounding areas, forming dark spot. Ventral patch of opercular odontodes white, lacking any FIG. 8. Trichogenes beagle , sp. nov., MZUSP 124888, paratype, 37.9 mm SL, cleared and stained. Opercle, concentration of dark chromatphores. left side, with intact odontode armature. Interopercular odontode patch white. Posterior naris outlined in narrow white ring, then surrounded posteromesially by dark field. Laterosensory pores white, without any dark concentrations. Nasal, maxillary, and rictal barbels with fine scattering of dark chromatophores, densest on their dorsal surfaces and posterior margins. Rictal barbel lightest, with sparse dark chromatophores at base and white distally. Ventral part of head with dark fields on region of lower jaw and margin of lower lip. Dorsal, pectoral, and caudal fins with sparse dark chromatophores alongside individual rays, most pronouncedly along first pectoral-fin ray. Base of dorsal fin without any differential dark concentration. Anal and pelvic fins lacking dark pigment.

SEXUAL DIMORPHISM: The degree of development of the posterior opercular process in all three specimens available of T. beagle conforms to the female morphology described for T. claviger (see Pinna et al., 2010). Sexing of one paratype (now c&s) confirms that it is a female. More specimens are needed before additional inferences can be made about the possible presence of sexual dimorphism in T. beagle .

DISTRIBUTION: The geographical distribution of Trichogenes beagle is unknown at present, a result of the unlikely circumstances of its discovery. The three known specimens were found by one of the authors (V.R.) during a routine search for molecular samples of trichomycterids in a freezer at the Laboratory of Molecular Systematics – Beagle at the Department of Animal Biology, Universidade Federal de Viçosa. The specimens were in a plastic centrifuge vial, in good overall condition and clearly had been fixed in formalin before their preservation in alcohol, as evidenced by the transparent aspect of their eye lenses. No label was associated with the vial, which had “Cachoeira do Cobra” inscribed by hand in pen on the outside. Extensive and repeated inquiries with lab members revealed no memory of who might have collected the fish or placed the vial in that freezer. The equipment is used by lab students, faculty, and visiting professionals, and is intended as a convenience facility for temporary storage, although some material is occasionally abandoned, as was apparently the case with the T. beagle material. As a result, the name “Cachoeira do Cobra” was the only clue as to the provenance of the material, even though vials of that sort are often repeatedly reused and inscriptions on their outside may bear no relation with their current content. Search in gazetteers and Web resources revealed two potential candidates for a locality with that name, one in the Rio São José at the town São Gabriel da Palha and the other in the Rio Guandú at the town of Afonso Claudio, both tributaries of the Rio Doce basin, State of Espírito Santo. Field trips were made by the authors to the two localities in January 2019, but did not locate any specimens of Trichogenes . The former locality, a relatively large river with a varied community of fishes, did not seem likely as a Trichogenes habitat. The second site was a more fitting location—a relatively isolated mountain watercourse–although it too had many resident species, including one of Trichomycterus , and the river had recently been heavily impacted by recreational dam construction at the time of our visit. While the presence of Trichogenes cannot be ruled out in the yet-unsampled upper course, the specific locality called Cachoeira da Cobra did not have any Trichogenes on the occasion of our sampling. Thus, the geographical provenance of T. beagle remains a mystery. Most of the ichthyological material that finds its way to or through the Beagle Laboratory is derived from field activities in the broadly surrounding area, roughly covering the adjacent portions of southeastern State of Minas Gerais, southern State of Espírito Santo, and northern State of Rio de Janeiro. That area is drained by the basins of rivers Doce, Itapemirim, Itabapoana and Paraíba do Sul. This encompasses a large range of possibilities for future prospection, especially considering the narrowly restricted geographical ranges of other species of Trichogenes ( Pinna et al., 2010) .

ETYMOLOGY: The species epithet honors the Laboratory of Molecular Systematics – Beagle, Department of Animal Biology, Universidade Federal de Viçosa, the lab where the only specimens of the new species were found preserved.

REMARKS: The variety and degree of distinguishing characteristics in external morphology and internal anatomy between Trichogenes beagle and T. claviger , summarized in the Diagnosis above, suggest a relatively long history of divergence. Such differences are still larger between T. beagle and T. longipinnis . Matching the relative degree of similarity, some of the conditions shared between T. beagle and T. claviger are apomorphic and indicate that the two species are sister groups. Those include the presence of the median clawlike process on the anterior neural arches, the terminal mouth, the dark line and associated white band along the base of the anal fin, the lack of branched anal-fin rays and the broader than long posterior nostrils. Other unusual similarities between the two species, such as the lack of a pelvic splint and the compressed tooth cusps, are present also in Copionodontinae and thus are likely apomorphic at a broader level including the latter subfamily plus Trichogeninae , with reversals in T. longipinnis . Some of the differential characters among the three species of Trichogenes warrant further discussion. Vertebral number seems to be a consistent meristic difference between the species in the genus, because it displays surprisingly little variation ( Pinna et al., 2010). Trichogenes longipinnis has 38 (n = 9, holotype) or 39 (n = 5) vertebrae and all specimens of T. claviger have 35 (n = 18). Vertebral number in T. beagle (36, n = 3) is unique in the genus and falls between the values for the two other species, but the limited number of specimens available does not allow an estimate of variation. The same happens with pleural rib number (10 or 11 in T. longipinnis , 9 in T. beagle , and 8 in T. claviger ). The pattern of integumentary pigmentation also consistently differs among the three species of Trichogenes . In T. longipinnis , much variation is seen among populations (illustrated in Sazima, 2004), but it never matches that in T. claviger or T. beagle , with some pronounced qualitative differences. For example, the dark line along the base of the anal fin of the two latter species is never present in T. longipinnis . Uniquely in the genus, T. beagle lacks differentially large dark spots forming a series along the ventral part of the body and all its spots are small throughout their position in the body. Additionally, its spots are not disposed in a row anywhere on the body.

Additional Data on T. claviger

The field activities related to the search for T. beagle led our team to attempt to sample material representative of T. claviger as well. Much information from that experience is new and, considering the rarity of the species, it is worth recording them here. Sampling in the type locality was impossible because it is located on private land belonging to a large corporation to which access is repeatedly denied. So we directed our efforts to the surrounding areas, finally locating specimens in a different tributary to the Rio Itapemirim, also on private property (Fazenda Santa Clara) but with access granted by the owners. The new locality is near the type locality, approximately 3 km apart in straight line (fig. 13), in a different tributary to the Picada Comprida Creek. Still, it is an important record because it shows that T. claviger is composed of more than a single population and may in fact be spottily distributed in the region. Previous field efforts in the region have not been successful in locating records additional to the original type locality ( Sarmento Soares et al., 2018), confirming that the species is not readily found.

The creek is a small body of water (ca. 1 m wide and 10 cm deep for most of its course) with limited flow. The sector visited had gentle declivity and no major waterfalls and was shaded with secondary-growth gallery forest (fig. 14). Specimens of T. claviger were observed in two spots. One was a deep pool, ca. 1 m in diameter and 1 m deep, heavily covered by gallery thicket, with debris on the sides and bottom and no detectable current within its perimeter, although water movement was evident by constant outflow in one of the edges. Only two specimens were found at that site. The other spot was ca. 100 m downstream from the first one and consisted of a small depression, ca. 25 cm deep, in the main channel of the creek, immediately after a short (ca. 50 cm) shallow rapid sector. Substrate in that spot was sand interspersed with rocks, covered with a thin layer of mud. Margins were muddy. Water was clear, slightly cloudy, but quickly turned turbid by disturbance. The time of our visit was the peak of the dry season, although evidence of former water levels in the marginal vegetation indicated that the creek can be much larger at other times. Most of the extension of the creek visited by us had no specimens of T. claviger , which appears to concentrate in a few widely spaced preferred spots, at least during the low water period. Location of such spots and detection of specimens requires careful inspection of relatively long stretches of the creek. No other fish species was captured in the stream sector surveyed for T. claviger .

Observation of live specimens in the field and immediately after capture (see video 1 of live specimens in Supplementary Material, available online at doi.org/10.5531/sd.sp.38) shows that T. claviger is a midwater swimmer with constant swimming mode, much like T. longipinnis . Several specimens were seen gulping air from the surface and others expelling a bubble of air, showing that T. claviger has accessory air breathing, like many other trichomycterids and loricarioids. Specimens with air in their stomachs swim at an oblique angle, with the head pointing down, again like T. longipinnis . When captured in the net, specimens elbowed their way up the net walls with the aid of their interopercula, in fashion similar to that of T. longipinnis and most other trichomycterids (see video 2 of live specimens in Supplementary Material). The sexual dimorphism in opercle morphology previously reported for the species ( Pinna et al., 2010) is clearly visible in live specimens (fig. 15).

The general habits observed for T. claviger therefore are similar to those reported for T. longipinnis ( Sazima, 2004, and personal obs., M.P., V.R.). Their habitat, on the other hand, is markedly different. Trichogenes longipinnis occupies highly oligotrophic mountain streams with mostly rocky substrate, no mud at margins or bottom, steep altitudinal declivity, and mostly high-energy water current (although specimens concentrate on quiet deep pools, usually immediately downstream from waterfalls). As noted above, the kind of stream inhabited by T. claviger has pronouncedly divergent characteristics. This shows that the target habitats for searching new localities of Trichogenes species (including that of T. beagle ) must be kept considerably broad. Despite the dissimilarities, however, some parallels exist in the ecology of the two species, such as their preference for deeper sectors following waterfalls or rapids sectors (on a tiny scale in the case of T. claviger ), the spotty distribution within water bodies and the absence or paucity of cooccurring fish species.