Epeorus (Belovius) latifolium Uéno, 1928

Epeorus (Belovius) latifolium Uéno, 1928 View in CoL ( Figs 5–9 View FIGURE 5 View FIGURE 6 View FIGURE 7 View FIGURE 8 View FIGURE 9 )

[ Japanese name "Erumon-hirata-kagerou"]

Epeorus latifolium View in CoL : Uéno 1928: p. 34, pl. 7, figs 6, 6a–6o (nymph) [ JAPAN: Hokkaido]; Uéno 1931b: p. 192, fig. 2 (male imago) [ JAPAN: "middle Japan " i.e. adjacent region of Nagano Prefecture]; Uéno & Okamoto 1932: p. 1959, fig. 3859 (male imago) [ JAPAN]; Imanishi 1934: p. 389 (nymph, imago) [ JAPAN: Kyoto]; Imanishi 1940: p. 248, fig. 36 (nymph) [ KOREA, Northeast CHINA]; Tshernova 1949: p. 146, figs 6, 7 (nymph) [ RUSSIA: Altai]; Uéno 1950: p. 123, fig. 306 (male imago, female imago) [ JAPAN]; Tshernova 1952: p. 251 (nymph) [ RUSSIA]; Uéno 1959: p. 55 (nymph) [ JAPAN]; Gose 1962: p. 20, fig. 1-11-4 (nymph) [ JAPAN]; Gose 1979: p. 44, figs 12, 16 (nymph, male imago) [ JAPAN]; Braasch 1979: p. 243, figs 2, 4, 7, 9, 11, 14d–f, 15, 16 (nymph) [ JAPAN]; Okazaki 1984: p. 20, fig. 10 (egg) [ JAPAN]; Gose 1985: p. 16, figs 37, 38 (nymph) [ JAPAN]; Kobayashi 1988: p. 297, figs 4, 5 (nymph) [ JAPAN]; Ishiwata & Inada 1996: p. 41, fig. 8 (nymph) [ JAPAN]; Ishiwata 2002, p. 22, figs 178, 179, (nymph, male imago) [ JAPAN: Kanagawa]; Quan et al. 2002, p. 253 (nymph) [Northeast CHINA]; Ishiwata & Takemon 2005b: p. 105, figs 45-9, 47-9 (male imago, nymph) [ JAPAN]; Maruyama 2016: p. 172, figs 1-171f, 1-177, 1-271, 1-272, 1-273, 1-274 (male imago, female imago, male subimago, female subimago) [ JAPAN: Hyogo]; Ishiwata et al. 2018: p. 126, figs 45-9, 47-9 (male imago, nymph) [ JAPAN]; Ishiwata & Fujitani 2018: p. 33, pl. 22, fig. 3 (egg) [ JAPAN].

Epeorus (Epeorus) latifolium View in CoL : Byong & Bae 1984: p. 5, pl. 2, figs a–f, pl. 15, fig. b (male imago, female imago, male subimago, female subimago, nymph) [ KOREA].

Epeorus (Belovius) latifolium View in CoL : Tshernova 1981: p. 329, fig. 9 (male imago) [ JAPAN]

Iron uenoi Matsumura, 1933: p. 98 , pl. 21, fig. 16 (male imago) [ JAPAN: Hokkaido]. SYN. NOV.

Epeorus uenoi View in CoL : Ishiwata et al. 2018: p. 126, fig.13 (male imago) [ JAPAN]; Ishiwata & Fujitani 2018: p. 33, pl. 22, figs 7, 8 (egg) [ JAPAN]. SYN. NOV.

Materials examined. Type specimens: We investigated the Aquatic Insects Collection at The Kyoto University Museum in 2019 but were unable to find the holotype of E. latifolium . Ishiwata (2018) also noted that the types and other materials collected by Uéno were missing. Syntypes of Iron uenoi Matsumura, 1933 (identification label by Imanishi, 1933, " Iron uenoi Imanishi, Det. K. Imanishi 1933 ". All dried specimens.): 3 male imagines, "Maruyama [in Kanji 円山], 5/27" (collection years not listed), one with other labels ( Fig. 32 View FIGURE 32 ): "Type Matsumura" (red label) and " Epeorus uenoi Matsumura. Det. by S. Ishiwata, 1992" (identification label by Shin-ichi Ishiwata, 1992); 2 male imagines, "Sahoro [in Katakana サホロ, probably meaning Sapporo], 5/27" (collection years not listed); 1 male imago, "Sahoro [in Katakana サホロ, meaning Sapporo], 5/26" (collection years not listed); 1 male imago, "Sapporo, Matsumura; 2/ VI '08" (with collection date June 2nd, 1908); 1 male imago, "Maruyama [in Kanji 円山], 6/7" (collection years not listed). Other specimens: JAPAN, HOKKAIDO, ISHIKARI: [1.] Sapporo-shi, Minami-ku, Jozankei, Toyohira-gawa Riv., mainstream, 678 m a.s.l. (42°47'57.0"N, 141°10'14.3"E), 5 mature male nymphs and 1 mature female nymph, 15.VIII.2003, K. Saito; ditto, 1 mature female nymph, 18.X.2003, K. Saito; [2.] Sapporo-shi, Minami-ku, Jozankei , Izarisawa-gawa Stream (a tributary of Toyohira-gawa Riv. ), 568 m a.s.l. (42°51'18.4"N, 141°10'34.0"E), GoogleMaps 2 mature male nymphs and 1 mature female nymph, 14. VI.2007, K. Saito; ditto, GoogleMaps 3 mature male nymphs and 5 mature female nymphs, 11.IX.2007, K. Saito; [3.] Sapporo-shi, Minami-ku, Jozankei , Toyohira-gawa Riv. , upstream of confluence of mainstream and Ekiteisawa-gawa Stream , 514 m a.s.l. (42°51'18.1"N, 141°08'59.0"E), GoogleMaps 1 mature male nymph and 1 mature female nymph, 12.VI.2003, K. Saito; [4.] Sapporo-shi, Minami-ku, Jozankei, Usubetsu-gawa Stream (a tributary of Toyohira-gawa Riv.), 472 m a.s.l. (42°54'33.5"N, 141°07'28.9"E), GoogleMaps 1 mature female nymph, 11.V.2002, K. Saito GoogleMaps ; ditto, 1 mature female nymph, 08.IX.2002, K. Saito GoogleMaps ; ditto, 1 mature male nymph, 06.VII.2003, K. Saito; [5.] Sapporo-shi, Minami-ku, Jozankei , Shirai-gawa Stream (a tributary of Toyohira-gawa Riv. ), the confluence of Shirai-gawa Stream and Migimata-gawa Stream , 450 m a.s.l. (42°59'39.6"N, 141°04'42.9"E), GoogleMaps 3 mature male nymphs and 3 mature female nymphs, 6.VI.2004, K. Saito; [6.] Sapporo-shi, Minami-ku, Jozankei, Otarunai-gawa Stream (a tributary of Toyohira-gawa Riv.), 502 m a.s.l. (43°04'22.4"N, 141°06'34.8"E), four mature male nymphs and 2 mature female nymphs, 11.V.2002, K. Saito; ditto, GoogleMaps 4 mature male nymphs and 6 mature female nymphs, 6.VII.2002, K. Saito GoogleMaps ; ditto, 1 mature male nymph and 2 mature female nymphs, 7.iv.2019, T. Takayanagi GoogleMaps ; ditto, 3 mature female nymphs, 21.IX.2019, T. Takayanagi; [7.] Sapporo-shi, Minami-ku , Jozankei , Otarunai-gawa Stream (a tributary of Toyohira-gawa Riv. ), 394 m a.s.l. (43°01'56.1"N, 141°07'42.9"E), GoogleMaps 1 mature male nymph, 18.VI.2007, K. Saito; [8.] Sapporo-shi, Minami-ku, Jozankei, Shirai-gawa Stream (a tributary of Toyohira-gawa Riv.), 300 m a.s.l. (42°58'37.7"N, 141°08'16.4"E), GoogleMaps 1 mature male nymph, 14.VI.2005, K. Saito GoogleMaps ; ditto, 1 mature female nymph, 13.VIII.2005, K. Saito GoogleMaps ; ditto, 1 mature male nymph, 07.IV.2019, T. Takayanagi; [9.] Sapporo-shi, Minami-ku , Jozankei , Usubetsu-gawa Stream (a tributary of Toyohira-gawa Riv. ), 353 m a.s.l. (42°56'29.4"N, 141°07'47.3"E), GoogleMaps 2 mature male nymphs, 07.IV.2019, T. Takayanagi ; [10.] Sapporo-shi , Minami-ku , Toyama, Kannonzawa-gawa Stream (a tributary of Toyohira-gawa Riv. ), 267 m a.s.l. (42°58'31.0"N, 141°15'30.0"E), GoogleMaps 2 male imagines, 2 female imagines, 1 mature female nymph and 1 immature nymph, 29.V.2018, T. Takayanagi GoogleMaps ; ditto, 1 mature male nymph and 1 immature nymph, 04.XI.2018, T. Takayanagi GoogleMaps ; ditto, 1 mature female nymph, 19.III.2019, T. Takayanagi GoogleMaps ; ditto, 5 male imagines and 4 female imagines, 23. V.2019, T. Takayanagi GoogleMaps ; ditto, 1 mature female nymph, 16.XII.2019, T. Takayanagi GoogleMaps ; ditto, 1 mature male nymph, 10. V.2020, T. Takayanagi GoogleMaps ; ditto, 5 male imagines, 29.V.2020, T. Takayanagi; [11.] Sapporo-shi, Minami-ku , Toyotaki , Toyohira-gawa Riv. , mainstream, 188 m a.s.l. (42°57'38.4"N, 141°13'50.9"E), GoogleMaps 2 mature male nymphs, 21.V.2020, T. Takayanagi; [12.] Sapporo-shi, Minami-ku, Makomanai, Toyohira-gawa Riv., mainstream, 82 m a.s.l. (42°59'02.5"N, 141°20'23.5"E), GoogleMaps 4 mature female nymphs, 12.IV.2019, T. Takayanagi; [18.] Sapporo-shi, Nishi-ku, Heiwa, Kotonihassamu-gawa Stream (a tributary of Shin-kawa Riv.), 312 m a.s.l. (43°03'25.3"N, 141°12'40.6"E), GoogleMaps 1 mature male nymph, 03.V.2020, T. Takayanagi; [19.] Chitose-shi, Shikotsuko-onsen, Shirisetsunai-gawa Stream (an inlet stream of Lake Shikotsu-ko ), 289 m a.s.l. (42°46'39.0"N, 141°24'05.8"E), GoogleMaps 1 mature male nymph, 2 mature female nymphs and 1 immature nymph, 23.V.2019, T. Takayanagi GoogleMaps ; ditto, 7 mature female nymphs, 21.IX.2019, T. Takayanagi GoogleMaps ; ditto, 2 mature male nymphs and 3 mature female nymphs, 09.IX.2020, T. Takayanagi GoogleMaps ; ditto, 2 mature male nymphs and 2 mature female nymphs, 01. VI.2021, T. Takayanagi GoogleMaps ; ditto, 1 mature male nymph and 1 mature female nymph, 15.VIII.2021, T. Takayanagi; [20.] Chitose-shi, Bifue, Bifue-gawa Stream (an inlet stream of Lake Shikotsu-ko ), 257 m a.s.l. (42°43'47.9"N, 141°15'18.2"E), 2 mature male nymphs, 07.IV.2019, T. Takayanagi GoogleMaps ; ditto, 1 mature female nymph, 23. V.2019, T. Takayanagi; [23.] Eniwa-shi, Banjiri, Rarumanai-gawa Stream (a tributary of Chitose-gawa Riv. ), 305 m a.s.l. (42°51'56.1"N, 141°20'31.5"E), 1 mature male nymph, 07.IV.2019, T. Takayanagi GoogleMaps .

Nymph (mature, in ethanol), redescription ( Figs 5–7 View FIGURE 5 View FIGURE 6 View FIGURE 7 , based on specimens collected from type locality [19.]).

Body length 10.0– 14.5 mm (male), 10.0– 15.5 mm (female). Cercus length ca. body length x 1.2.

Head. Shape ellipsoid. Color yellowish-brown to reddish-brown with pale markings. Compound eyes dark gray to black. Ocelli dark gray. Antennae brown. Anterior margin densely covered with hair-like setae extending to lateral margins. Dorsal surface of head covered with fine hair-like setae. Sparse longer fine hair-like setae located posteriorly to the eyes ( Figs 6a, b View FIGURE 6 ). Labrum: anterior and lateral margins evenly convex, anterior margin concave medially. Ventral surface with long antero-lateral bristles, row of short setae and brush of median fine hair-like setae on each side. Dorsal surface medially with four long adjacent bristles and two long bristles near each side of antero-lateral margin, and scattered variable-length setae ( Fig. 7a View FIGURE 7 ). Mandibles: each outer incisor with three apical teeth and serrated margins, inner incisor with two apical teeth (right mandible) or four apical teeth (left mandible) and both inner incisors sharply serrated, right inner incisor slender and almost straight. Tuft of long setae on the base of inner incisor of right mandible, tuft of long setae and one brachy-pulmose seta on the base of inner incisor of left mandible ( Figs 7b, c View FIGURE 7 ). Maxillae: one long, feather-like seta at base of apical tooth complex, some specimens with two setae on right maxilla ( Fig. 28a View FIGURE 28 ). Hypopharynx: superlinguae distally widened, lingua shape subquadrate. Labium: labial palps two segmented, outer margin of proximal segment with sparse, thick setae. Distal segment with sparse, hair-like setae on outer margin and dense, brush-like setae on distal 1/3 area. Glossae and paraglossae with long, dense setae.

Thorax. Yellowish-brown to reddish-brown with pale markings dorsally ( Figs 5a, d View FIGURE 5 ). Ventrally white ( Figs 5b, e View FIGURE 5 ). Pronotum roundly projecting laterally ( Fig. 29a View FIGURE 29 ). Long hair-like setae on medial line to posterior margin of pronotum. Long hair-like setae on medial line to posterior area of mesonotum. Legs. Each anterior face of femur with dark brown transverse markings on its proximal, medial, and distal parts and hypodermal black spots on its base and middle ( Fig. 6c View FIGURE 6 ). Dorsal edge of femur with dense long blade-like setae, ventral edge with sparse short bluntly pointed spines. Femoral surface with diversely shaped setae: oblong, spatulate or semi-circular, those near ventral edge tend to be oblong, and those near dorsal edge tend to be semi-circular ( Fig. 7d View FIGURE 7 ). Tibia with two dark-brown markings on base and middle parts and long hair-like setae on dorsal edge ( Fig. 6c View FIGURE 6 ). Tarsus darker in proximal area and dorsal edge with long hair-like setae ( Fig. 6c View FIGURE 6 ). Tarsal claw with 4–5 small denticles.

Abdomen. Terga yellowish-brown to reddish-brown, each tergum III–IX with a pair of dark spots. Tergum VII tends to be darker ( Figs 5a, d View FIGURE 5 ). Sterna white to slightly brown ( Figs 5b, e View FIGURE 5 ). Each surface of tergum with a cluster of long setae located to each side of midline. Posterior margin of each tergum with long setae and denticles which are uniform, sturdy and arranged in an even line ( Figs 7k View FIGURE 7 , 31a View FIGURE 31 ). Tergum I–VII each with three postero-lateral projections, ventral one blunt, lateral one pointed and bending slightly upward, and dorsal one blunt ( Fig. 30a View FIGURE 30 ). Posterior margin of sternum IX shape round with shallow medial emargination and covered with hair-like setae medially to laterally ( Figs 7i, j View FIGURE 7 ). Dorsal surface of cercus with a row of fine setae. Gills. Gills III and IV largest in size, VII smallest. Each gill with variably sized dark-violet spots on its posterior half, ground color slightly purple ( Fig. 6d View FIGURE 6 ). Gills II–VII with dark colored anal-proximal projections ( Figs 6d View FIGURE 6 , 7f, g View FIGURE 7 ). Costal margin of gill I with fine hair-like setae. Costal margin of gills II–VII with rough surface of spines and distal margin with fine setae. Each gill plate with filaments forming a fan-shape together. Gill VII without longitudinal fold ( Fig. 7h View FIGURE 7 ).

Male imago (in ethanol), redescription ( Fig. 8 View FIGURE 8 ).

Body length 11.0– 13.4 mm. Cercus length ca. body length x 3.0. Forewing length 12.6–14.3 mm.

Head. Yellowish-brown. Frons shape triangular. Compound eyes dark-gray to black, gray to greenish-gray when alive. Ocelli light-gray with black border ( Fig. 8g View FIGURE 8 ).

Thorax. Ground color yellowish-brown to translucent, musculature visible. Each side of pronotum dark. Mesonotum with dark-brown markings on adjacent parts of sutures and scutellum ( Fig. 8g View FIGURE 8 ). Mesopleuron with dark-brown to black speckles. Metathorax color dark-brown with black speckles ( Fig. 8a View FIGURE 8 ). Wings. Hyaline, veins and axillary cord brown. Forewing with black markings on costal brace ( Fig. 8e View FIGURE 8 ). Pterostigmatic area cloudy. Hindwing without markings. Legs. Whitish brown.Anterior face of each femur with dark linearly shaped spot and elliptic spot. Fore tarsus longest with each segment becoming shorter distally ( Figs 8b–d View FIGURE 8 ). Tarsal claws dissimilar, one hooked-shape and the other oblong.

Abdomen. Yellowish-brown, translucent with each posterior margin of tergum dark-brownish. Segments VIII– X yellowish white, internal organs and tissues visible ( Fig. 8a View FIGURE 8 ). Posterior margin of styliger plate roundly extended, forceps base with developed projection which has spines on its surface. Forceps four segmented, color dark-brown, with short comb-like spines on inner surface, fourth segment with sharp setae on its surface. Apical part of each penis lobe with proximally-oriented spine, titillators absent ( Fig. 8f View FIGURE 8 ). Cercus brown.

Female imago (in ethanol) ( Fig. 9 View FIGURE 9 ).

Body length 11.1–11.6 mm. Cercus length ca. body length x 2.2. Forewing length 13.2–15.0 mm.

Head. Yellowish-brown. Compound eyes gray to dark gray. Ocelli as in male imago.

Thorax. Coloration as in male imago ( Fig. 9a View FIGURE 9 ). Wings. Vein coloration as in male imago. Forewing slightly more expanded than in male ( Fig. 9a View FIGURE 9 ). Legs. Coloration and markings as in male imago. Fore tarsus not elongated. Of all tarsal segments, fourth is shortest, other segments almost equal in length ( Figs 9b–d View FIGURE 9 ). Tarsal claws dissimilar as in male imago.

Abdomen. Yellowish-brown, greenish eggs visible when alive. Posterior margin of subgenital plate almost straight. Posterior margin of sternum IX rounded with shallow emargination ( Fig. 9e View FIGURE 9 ). Cercus brown.

Diagnosis and comparison. Nymph. The nymphs of this species and the following species have variably sized dark-violet spots on their gills, in contrast to the other three species in the study area. See counterparts of the next species for a detailed comparison. Male imago. This species lacks penial titillators in contrast to all other species in the study area.

Remarks. Nymph. The specimens here identified as E. latifolium agree with the original description ( Uéno 1928). Body coloration may vary depending on the environment: specimens from more open and brighter parts of the river tend to have paler coloration, while those from darker, shaded areas exhibit darker coloration. Consequently, descriptions of coloration may vary according to each author's observations. Male imago. Almost all features correspond to the description by Uéno (1931b), though the color of cerci is notably different. In Uéno (1931b), its color was described as "white". Although we can't explain this difference, we identify this species as E. latifolium based on the genetic collation of the nymph and morphological correspondence as a whole. Female imago. This is the first description of the female imago. Subgenus attribution. This species is the type species of the subgenus Belovius .

The species concept of this species has been ambiguous since its original description. It was first described as a new species based on nymphal specimens collected in the Shirisetsunai-gawa Stream, Chitose, Hokkaido (locality [19.] in this study), in September ( Uéno 1928). The following year, Horasawa (1929) reported nymphal, male-subimaginal, and male-imaginal stages based on materials collected from central Honshu at the beginning of September. However, this report was based on a misidentification (Ishiwata 2018). Uéno (1931b) described the male imago based on materials from central Honshu, listing Horasawa’s work (1929) in the synonymy. However, critical discrepancies existed in the imaginal morphology descriptions, including differences in forewing markings and penis shape. Unfortunately, the materials examined in these studies are likely lost (Ishiwata 2018; Author’s investigation 2019). Further confusion about species delineation among “ latifolium -like” species was first noted by Imanishi (1940), and these issues remain unresolved (discussed below). This study investigated genetic and morphological features of nymphal specimens from the type locality and strongly suggests that only one “ latifolium - like” species exists in this area, thus confirming the species concept of E. latifolium as described above.

Epeorus uenoi was described by Matsumura in Illustrated Common Insects of Japan under the name " Iron uenoi Imanishi " ( Matsumura 1933), but authorship should be attributed to Matsumura ( Ishiwata 2001a). We concluded that this species is a junior subjective synonym of E. latifolium for the following reasons: 1) the genital structures of the E. uenoi syntypes match our observations of E. latifolium , displaying no titillators, a triangular styliger plate, and proximally oriented spines on the top of each penis lobe ( Fig. 32d View FIGURE 32 ); 2) all syntypes were collected in late May to early June, aligning with the first emergence period of E. latifolium identified in this study.

Emergence periods and habitat. Fully mature nymphs and imagines were collected from early May through October. Mature nymphs collected in spring are larger (13 mm to 15 mm) and become smaller in later seasons. This species was observed upstream in the Makomanai district (locality [12.]) of the Toyohira-gawa River.

Distribution. Japan (Hokkaido, Honshu, Shikoku, and Kyushu), Korea, China (Northeast), and Russia (Altai, Far East).