Perla pallida Guérin-Méneville, 1843

Teslenko, Valentina A., Palatov, Dmitry M. & Semenchenko, Alexander A., 2024, Overview of the Caucasian Perla Geoffroy, 1762 (Plecoptera: Perlidae) based on morphological and molecular data with description of two new species, Zootaxa 5507 (1), pp. 1-56 : 31-38

Perla pallida Guérin-Méneville, 1843

Figs. 102‒127

Guérin-Méneville, 1843: 393−394;

Pictet, 1841: 192, pl. XIII, fig. 13;

Klapálek, 1923: 46−48, fig. 22;

Zhiltzova, 1956: p. 660 (distribution in the Kura R. Basin, Trialetsky Range);

Sivec & Stark, 2002: 23, figs. 43−45,“ Type 1”;

Murányi et al., 2021: 73 (distribution, Azerbaijan)

Perla pallida was originally described by Guérin-Méneville (1843) based on a male from the Caucasus without indicating the type locality. The original description was supplemented by Pictet (1841). Later, the species was redescribed by Klapálek (1923) on Caucasian specimens from Azerbaijan, Georgia, and Turkey. These specimens subsequently became neotypes and are stored in the Natural History Museum of Wien (NHMW) ( Murányi et al. 2021). The primary types were presumably lost during the 19th century. The current concept of the species is based on these Caucasian specimens ( Sivec & Stark 2002). Taking into account differences in egg structure, Sivec & Stark (2002) considered P. pallida to be a species complex of three or more species or subspecies distributed in the Caucasus, Anatolia, Balkans, and Carpathians.

Diagnosis. Mesal field on tergum 9 of male slightly expanded anteriorly and posteriorly, width slightly greater than length; longitudinal serrated ridges (10−12) closer to anterior and lateral margins; posterior margin avoids serrated ridge rows ( Figs. 106 , 108 ). Hemitergites are strong, narrowed towards the rounded apex, and hook wide at the base with a weak notch distally ( Figs. 104, 106 , 108 ). The tube of the penis is 1.6 times the length of the sac and has a constriction before the sac; the sac is large, wider than the tube, and covered with a patch of coarse triangular spines, forming a wide, loose triangular apical brush; the spines of the brush along the lateral edges of the sac are absent; ventrally, the brush end is triangular; dorsally, the edge of the apical brush is semi-rounded ( Figs. 108−111 ). Egg oval; collar with flanged rim that is incised and distinctly wider than the neck; the collar sides covered ribs; chorion smooth, covered with follicle hexagonal cell impressions, limiting at the corners by six tiny round punctuations and by six small, slit-shaped punctuations located between them; cells have boundaries, a central depression, and one pore on the floor; pore and hexagonal punctuation are different in size ( Figs. 112‒119 ). The micropylar orifices lack rims ( Figs. 117−118 ). Head of larvae with a large trapezoidal pale spot expanding from the anterior ocellus to the labrum base; the lateral edges of the spot with two pair pointed projections; paired projections near the labrum wide; a thin pale M-line delimiting the spot from below; the epicranial sutures brown ( Figs. 120−121 ). Anal gills are absent.

Complimentary description. The coloration, external structures of the male and female genitalia, eggs, and appearance of larva in our material generally correspond to existing descriptions of P. pallida ( Guérin-Méneville 1843; Pictet 1841; Klapálek 1923; Sivec & Stark 2002; Zhiltzova & Cherchesova 2003), although the resemblance with Carpathian populations is also noticeable ( Kis 1974, Teslenko & Zhiltzova 2009, their figs. 314–318), with the exception of the distinctive features of the penis described below.

Adult habitus. The main body color is yellow-brown ( Fig. 102 ). The head is mostly yellow; the M-line is yellow and moderately defined ( Figs. 102, 105 ). The interocellar area bears a dark brown spot reaching the M-line and directed to compound eyes above yellow posterior tentorial pits; the posterior edge between the lateral ocelli with a solid pale line ( Figs. 105 ). The female head is darker due to a larger dark brown spot in the interocellar area, with more distinct lateral edges approaching the M-line and the posterior tentorial pits closely but not going beyond them ( Fig. 105 ). A triangular light brown spot, widening towards the anterior margin of the clypeus, is in front of the M-line and anterior ocellus; the antenna is brown ( Figs. 102–103, 105 ). Occiput bears a wide, V-shaped brown spot in the area of the epicranial suture and stem, the spot is darker and more pronounced on females ( Figs. 103, 105 ).

Pronotum is trapezoidal, narrowed, and rounded posteriorly ( Figs. 102‒103, 105 ). The anterior and posterior margins arched, the lateral margins straight, the anterior corners almost straight; yellow, with a narrow dark brown stripe along the anterior and posterior margins; the lateral margins with a relatively wide dark sinuous band sometimes the lateral edges bent down, and the dark band is not visible dorsally ( Figs. 102‒103, 105 ). The medial pronotal band is brown and relatively narrow, widening more anteriorly than posteriorly; lateral pronotal fields have dark, rounded, patches on which light rugosities are visible ( Figs. 103, 105 ). Legs yellow; femur with a narrow longitudinal grayish band close to the outer edge and a narrow dark brown band distally; tibia with a short, narrow transverse brownish band in the basal third; tarsi brown apically ( Fig. 102 ). The cerci are long, projecting far beyond the end of the wings; they are bicolored, with each segment yellowish at the base and brown distally. The wings are yellow with dark brown veins ( Fig. 102 ).

Male. Tergum 8 medially with a membranous furrow narrowed posteriorly; posterolateral humps and posterior tergal margins covered with dense, relatively long setae ( Fig. 106 ). Tergum 9 with a sclerotized mesal field; width is slightly greater than length; slightly expanded anteriorly and posteriorly; posterior margin with a small membranous notch in the middle ( Figs. 106 , 108 ). Longitudinal serrated ridges (10−12) cover the mesal field closer to the anterior and lateral margins; the posterior margin avoids serrated ridge rows ( Figs. 106 , 108 ). Hemitergites are strong and slightly narrowed towards the rounded apex ( Figs. 104, 106 , 108 ). In dorsal view, the hemitergal hook (not cleared) is wide at the base, with a weak notch on the inner edge in the distal 1/3 ( Fig. 104 ); the top of the hook and inner edge are covered with sensilla basiconica ( Figs. 104, 106 , 108 ). The artificially everted penis carries a tube that is 1.6 times the length of the sac, a tube with a noticeable constriction in the distal third before the sac, covered dorsally with densely arranged longitudinal rows of serrate sclerites, changing into scales with small spines or without them ( Figs. 108‒111 ). The base of the tube is membranous, with paired patches of round spine bases laterally ( Figs. 110– 111 ). Ventrally, the tube is partly membranous and covered with rows of oval-elongated or polygonal sclerites with or without small spines, the same as on the dorsal surface ( Figs. 111 , A−C). The membranous sac is spherical and large; the sac width exceeds the tube width by 1/3; in dorsal view, the sac bears two rounded lobes at the base and a central tongue-shaped lobe narrowed to the sac base; ventrally, the sac bears two rounded lobes ( Figs. 108‒111 ). The apex of the sac is covered with a patch of rather coarse triangular brown spines, forming a relatively wide, loose apical brush, reaching almost to the middle of the tongue-shaped lobe ( Figs. 108, 110‒111 , D); there are no spines along the lateral edges of the sac. Ventrally, the apical brush ends with a triangular protrusion; dorsally, the edge of the brush is semi-rounded ( Figs. 108, 110–111 ). The configuration of the apical brush of the penis in the Caucasian population differs from the pattern of P. pallida from the Romanian Carpathians ( Kis 1974, Teslenko & Zhiltzova 2009, their fig. 317), which is wide and covers the sac completely.

Female. The subgenital plate is typical of several Perla species, occupying>1/2 of sternum 8 width and has a small bilobed projection posteromedially. The lobes are small, pointed, and covered with reddish setae; the lateral edges of the lobes are slightly beveled; and the lobes slightly protrude beyond the anterior margin of the sternum 9 ( Fig. 107 ).

Egg. Oval of medium size, with mean dimensions of 452×300 μm (n=8) ( Fig. 111 ). The anchor plate is mushroom-shaped and covered with globular bodies gathered in small groups ( Figs. 113, 116 ). The collar has a flanged rim, which is incised and distinctly wider than the neck ( Figs. 114‒116 ). The sides of the collar have prominent, continuous ribs extending from the shoulders to the rim ( Figs. 114, 116 ). The chorion surface is smooth and pitted; the chorion is covered throughout with follicle hexagonal cell impressions, limiting at the corners by six tiny round punctuations and six small, slit-shaped punctuations located between them; cells are separated from adjacent ones by expressed boundaries; the cell floor has one pore, and the pore and hexagonal punctuations are different in size ( Figs. 118‒119 ). A central depression in the cell flow is well pronounced in eggs from the Armenian population ( Figs. 113, 116‒117 ). The ring of micropyles is located ca. 1/3 of the egg length removed from the anterior pole, the micropylar orifices without rims ( Figs. 112–113, 117‒118 ).

Larva. The appearance of the larva agrees well with the description by Zhiltzova & Cherchesova (2003). The body is brown with contrasting pale patterning, covered with short dark clothing hairs, and has a dorsomesal band of erect silky white setae that is more pronounced on the last abdominal terga ( Figs. 120–121 ). The head is brown, bearing a large trapezoidal pale spot expanding from the anterior ocellus to the labrum base; the lateral edges of the spot with two pair pointed projections; paired projections near the labrum are wide; a thin pale M-line medially delimiting the spot from below; an interocellar area with a short slit-shaped pale spot between lateral ocelli; and the epicranial sutures are brown ( Figs. 120–121 ). Mandible strongly sclerotized, outer edge rounded, base with tuft of thin setae at outer edge; mandibular teeth strongly pointed; left mandible with 5 teeth; right mandible with 6 teeth; the number and arrangement of rows of short setae on the molar areas of the left and right mandibles is the same as in other species ( Fig. 122 ). Lacinia bidentate, teeth are pointed, terminal tooth strongly curved, subapical tooth less curved, and extending ca. 2/3 of terminal tooth length. Below the subapical tooth, there is a small downward-sloping projection with 3–4 submarginal setae ( Fig. 123 ). The marginal fringe of setae along the inner lacinial margin is complete ( Fig. 123 ). Abdomen brown, each tergum with two transverse pale spots on the sides of the medial line and paired small pale spots laterally; in the female larva, the spots on the last abdominal terga are faintly visible ( Figs. 120–121 ). The anal gills are absent. The legs pale, the femur darkened basally and distally, with a dark spot in the distal half close to the outer edge; the tibia basally has a short brown band on the outer edge ( Figs. 120–121 , 124 ). The fine pilosity between dark short spines in the cercal circlet is the same as that of other Perla species ( Figs. 125−127 ). A dorsal longitudinal fringe of swimming hairs is tightly pressed to the segments; the length and density of long silky hairs decrease towards the cercal apex ( Figs. 125–127 ). On the middle and apical cercal segments, long and thin intercalary setae are visible; their length exceeds the length of fine circlet hairs ( Figs. 126‒127 ).

DNA barcoding. GenBank accession numbers are PP216457‒PP216461. Sequences of P. pallida from the Caucasus showed deep COI divergence between populations from Macedonia (AEG1356), Croatia (AAL2357), Croatia (AEK2845), and Slovenia, Croatia (AEB9929), whose minimum p-distances were 8.1%, 4.8%, 4.7%, and 2.8%, respectively ( Table 2 ). However, the phylogenetic analysis showed that this species is polyphyletic ( Fig. 160 ). In addition, P. pallida under BINs AAL2357 and AEB9929 cannot be distinguished using COI barcodes due to other species related to these BINs. Considering that P. pallida was originally described from the Caucasus, this casts doubt on the validity of European populations.

Material examined. Caucasus, Russia, Republic North Ossetia-Alania: 1 larva, Prigorodny District, Mairamadag River, Terek River Basin , altitude 690 m above sea level, 42.993308 N, 44.49815 E, 17.07.2021, coll. D. Palatov ; 1♂, Alagirsky District, Komdon River near Upper Tsey village , Terek River Basin , altitude 1832 m above sea level, 42.803514 N, 43.933395 E, 25.07.2021, coll. D. Palatov ; Krasnodar Kray: 2♂, Gelendzhik, Papay River, 2.5 km below Novosadovy farm, Pshada River Basin, altitude 195 m above sea level, 44.569305 N, 38.42889 E, 8.06.2021, coll. D. Palatov ; 6♂, 1♀, 3 larvae, District of the Sochi City, Plastunka village , 3rd tributary of the Kutarka River , Sochi River Basin , altitude 143 m above sea level 43.672794 N, 39.772125 E, 21.07.2022, coll. D. Palatov.

Additional material. Armenia, Syunik marz: 4♂, 1♀, Tzav River, about 3 km above the village Tzav , before the fork in the valley, altitude 2500 m above sea level, 39.316400, N 46.251943 E, 20.07.2014, coll. D. Palatov.

Distribution. Widespread in the Caucasus: Russia, North Ossetia-Alania, Krasnodar Kray; Armenia, Georgia, Azerbaijan, Turkey ( Anatolia) ( Zhiltzova 1956; Zwick 1975; Sivec & Stark 2002; Darilmaz et al. 2016; Murányi et al. 2021).

Figures

FIGURE 160. Ultrametric Bayesian inference (BI) tree inferred from the cytochrome c oxidase I (COI) gene fragment and the results of species delineation of the genus Perla Geoffroy, 1762, and out-group Kamimuria coreana. Bayesian posterior probabilities (> 0.7) are noted above the tree nodes. Vertical bars correspond to molecular operational taxonomic units by ASAP, mPTP, GMYC, and BINs of BOLD. The color of the specimens indicates the development stage of stoneflies in accordance with the legend, while the sequences obtained in this study are in bold.

FIGURES 102‒107. Perla pallida Guérin-Méneville, 1843. Caucasus, Russia, Krasnodar Kray, Papay River, Pshada River Basin; 3rd tributary Kutarka River, Sochi River Basin. 102. Male habitus, dorsal. 103. Male, head and pronotum, dorsal. 104. Male, hemitergal hook, lateral. 105. Female, head and pronotum, dorsolateral. 106. Male, abdominal tip, mesal plate and hemitergites, dorsal. 107. Female, abdominal tip, ventral.

FIGURES 108‒111. Perla pallida Guérin-Méneville, 1843. Caucasus, Russia, Krasnodar Kray, 3rd tributary Kutarka River, Sochi River Basin. Male. 108. Abdominal tip, mesal plate, hemitergal hooks, and artificially everted penis, dorsal, cleared. 109. Penis, ventral. 110. Chaetotaxy of the penis, dorsal. 111. Chaetotaxy of the penis, ventral. A. Oval scales with small spines. B. Leaf-shaped scales with small spines. C. Densely arranged longitudinal rows of heavy sclerotized serrate sclerites. D. Pointed brown spines in the apical brush.

FIGURES 112‒119. Perla pallida Guérin-Méneville, 1843. Caucasus, Russia, Krasnodar Kray, 3rd tributary Kutarka River, Sochi River Basin; Republic of North Ossetia-Alania, Prigorodny District, Mairamadag River, Terek River Basin. Armenia, Syunik Marz, Tzav River. Egg. 112. Appearance with micropylar row, lateral. 113. Appearance with mushroom-shaped anchor plate and micropylar row, lateral. 114. Collar with flanged rim and raised ribs, lateral. 115. Collar, dorsal. 116. Collar with anchor, covered with globular bodies, flanged rim and raised ribs, lateral. 117‒118. Chorion structure with micropylar row. 119. Chorion structure with follicle hexagonal cell impressions.

FIGURES 120‒121. Perla pallida Guérin-Méneville, 1843. Caucasus, Russia, Krasnodar Kray, 3rd tributary Kutarka River, Sochi River Basin; Republic of North Ossetia-Alania, Prigorodny District, Mairamadag River, Terek River Basin. Larva. 120. Habitus, female, dorsal. 121. Habitus, male, dorsal.

FIGURES 122‒127. Perla pallida Guérin-Méneville, 1843. Caucasus, Russia, Krasnodar Kray, 3rd tributary Kutarka River, Sochi River Basin; Republic of North Ossetia-Alania, Prigorodny District, Mairamadag River, Terek River Basin. Larva. 122. Left and right mandibles, ventral. 123. Left lacinia, galea, maxillary palpus, ventral. 124. Right hind leg, dorsal. 125−127. Chaetotaxy of the left cercus, lateral. 125. Basal cercal segments. 126. Middle cercal segments. 127. Apical cercal segments.