Branchiobdella turkestanensis

Hosts. Pontastacus kessleri (Schimkewitsch, 1886) [as Astacus kessleri; for the generic assignment, see Crandall and De Grave (2017)]. Habitat. Present in the branchial chambers of the host (Subchev & Gelder 2010). Affinities. Although species of Branchiobdella are found in both the Euro-Mediterranean and East Asian subregions (Bănărescu 1990), each subregion has its own distinct set of species (Gelder 2019: 488). Branchiobdella turkestanensis is one of five, small (less than 3.0 mm long) Euro-Mediterranean species in this genus (Karaman 1967). Four of these have a spindle-shaped body, while Branchiobdella balcanica Moszyński, 1938, has a slightly dorso-ventrally flattened body with lateral ‘ shoulders’ on segment 4. Branchiobdella italica Canegallo, 1928, and Branchiobdella pentadonta Whitman, 1882, have long, thin glandular atria, leaving both B. kozarovi and B. turkestanensis with short glandular atria that also live on closely related crayfish species, Pontastacus leptodactylus (Eschscholtz, 1823) and P. kessleri respectively, in the southeastern Euro-Mediterranean subregion. With the reexamination of the MNHW material and its designation as a new species, B. turkestanensis, it was necessary to review the morphology of B. kozarovi to support the separation of the two species. The type description by Subchev (1978) contained a number of errors and omissions; these were corrected in a subsequent detailed description by Gelder et al. (1994 b). As reported in the Materials and methods section, the type material was unavailable for loan so other Bulgarian specimens and information were used. Subchev (1978: 78) reported the body length of preserved mature B. kozarovi ranged from 1.0 to 1.7 mm, while the topotypic specimens that I examined (unpub. data) had a mean length of 1.2 mm (n = 14) and range of 0.8 to 1.7 mm. Branchiobdella kozarovi from Ukraine reach over 3.0 mm long (Boshko 1983) or, more precisely, range from 0.9 to 3.5 mm according to Kolesnykova et al. (2008: Fig. 1 a, b). A photograph of a well-preserved specimen from the Netherlands with a scale bar, was calculated to be 4.0 mm long, but the text affirmed a range of body length of just 1.1 to 2.5 mm (Kolesnykova et al. 2012: 102). The longer specimens require further investigation, but they are not relevant here. Subchev (1978) described the jaws of B. kozarovi as being more than half as high as wide when seen in frontal view, but in his fig. 3 these dimensions are almost the same. He noted the presence of “ five or six teeth ” but made no mention of a dental formula. In the 14 specimens I examined (unpubl. data), the jaws were reniform and the dental formula was either 5 / 5 (five specimens), 6 / 5 (5), 5 / 6 (2), 6 / 6 (1) or 7 / 5 (1). Kolesnykova et al. (2008: 79) reported a predominance of 5 / 5, with 5 / 6 and 5 / 7 occurring rarely. The spermatheca length in B. kozarovi is x 1.2 the segment’s diameter, with its duct about subequal to the length of the spindle-shaped bulb that includes an ental process (Fig. 1 H) (modified from Gelder et al. 1994 b: fig. 1) and this agrees with the report in Kolesnykova et al. (2008: Fig. 2). Although the bulb’s diameter varies with the amount of sperm it contains, the length remains about the same. The thick, short glandular atrium is curved although not always pronounced, and the vas deferens reportedly enters into the glandular atrium towards the latter’s ental end (Gelder et al. 1994 b) or at its mid-point (Kolesnykova et al. 2008: fig. 2). The muscular atrium is subequal in length to that of the glandular atrium. The length and position of oviducts are not used as taxonomic characters; however, it is notable that Kolesnykova et al. (2008: fig. 2) showed a pair of long oviducts apparently opening to the exterior of segment 8 (her XII). If this is correct, their length and failure to open on the external surface of segment 7 would be unique to this species of branchiobdellidan. The diagnostic characteristics often employed to identify branchiobdellidan species, such as external features of the body, body length, dental formulae and shape and size of the jaws, are not significantly different in B. turkestanensis and B. kozarovi. These two species are separable from each other by differences in the morphology of the spermatheca and male reproductive organs, specifically their size, length and shape. Most noticeably, in B. turkestanensis (Fig. 1 G) these organs are approximately half the relative size of those in B. kozarovi (Fig. 1 H). In B. turkestanensis the spermatheca length is about 0.6 x the segment’s diameter, and the ovoid bulb is about x 1.5 longer than the duct. In contrast, the spermatheca in B. kozarovi is about equal or longer than the segment diameter, with a terete bulb and ental process together being similar in length to the duct. Branchiobdella turkestanensis has a terete glandular atrium that is less than half as long as the muscular atrium, while B. kozarovi has a curved, wide and tubular glandular atrium that is subequal in length to the muscular atrium. Among branchiobdellidans, differences of this sort have previously been considered sufficient to justify the separation of B. italica from B. pentadonta (Gelder et al. 1994 a: 181) and Cambarincola vitrea Ellis, 1918 from Cambarincola osceola Hoffman, 1963 (Hoffman 1963: 325).

(Figure 1 A – H)

Description. Small, about 2.0 mm long, with the body increasing in diameter from segment 1 to a maximum in segment 7 and tapering to segment 10. The posterior attachment disc, segment 11, is usually about the same diameter as the head. The rounded head is equal to or larger in diameter than segment 1, but clearly separated from it (Fig. 1 A). The holotype is 2.2 mm long with 16 paratypes ranging from 1.2 to 2.6 mm in length. Peristomium consists of a rounded, smooth dorsal and ventral lip and a slight median emargination on the latter; the peristomium is separated from the head by a shallow sulcus. Small oral papillae surround the mouth. The jaws are similar, brown, and kidney-shaped to ovoid, with the dorsal being larger than the ventral. A thickened portion supports the teeth while a thinner frontal plate extends below (Fig. 1 B, C, D, F; white portion). A large tooth is located on or near the jaw’s mid-point, with smaller lateral teeth providing a dental formula of 6 / 5, dorsal jaw 40.0 μm wide with ventral 33.0 μm (Fig. 4 B, C) in the holotype. A deep sulcus is present in the pharynx’s mid region. Dorsal segmental body ridges are absent along with segmental supernumerary muscles, while shallow sulci indicate the position of segments and annuli. Lateral epidermal glands are present on segments 8 and 9, but do not form lobe-like extensions. The anterior pair of nephridial pores on segment 3 were not visible. A clitellum over segments 5, 6 and 7 is thin. The male reproductive system consists of one pair of testes in segment 5, and developing spermatozoa fill the coelomic cavity (Fig. 1 A). A pair of sperm funnels in segment 5, each pass into a vas efferens that joins with its contralateral partner to form a short vas deferens which passes into segment 6 and enters the glandular atrium’s mid-region (Fig. 1 G). The glandular atrium is terete or spindle-shaped, length x 0.3 the segment diameter (Fig. 1 G). The ectal end of the atrium passes into the tubular muscular atrium, about x 0.6 the length of the segment’s diameter, before passing into the spheroidal muscular bursa. The ectal half of the muscular atrium contains the tubular, eversible penis when retracted. The ental end of the retracted penis extends into the dorsal bursal atrium above an internal horizontal sulcus that connects to a vertical, folded tube that opens externally through the genital pore. The glandular and muscular atria can lie either laterally (Fig. 1 A) or vertically in the segmental coelom depending on the pressure from the gut (Fig. 1 G). The spermatheca in segment 5 is club-shaped, about x 0.6 the length of the segment’s diameter, with an ovoid glandular spermathecal bulb, x 0.6 the organ’s length with the remaining x 0.4 being the muscular spermathecal duct (Fig. 1 G). Variations. The body length ranges from 1.2 to 2.6 mm with a mean of 2.0 mm (n = 18). The prominence or absence of the median emargination on the ventral lip is dependent on the degree of swelling imposed by the preservative. The width of the tooth base on the dorsal jaw is usually wider than that on the ventral, although examples were found with the same width. The dental formula ranges from 5 / 5 to 8 / 6 (teeth-bases being 31.0 to 50.0 μm wide), although 6 / 5 and 5 / 5 predominate. The volume of the coelomic cavity in segment 5 varies with the number of developing spermatozoa, so that at maximum maturity it presses the anterior and posterior septa outwards, causing them to bulge into segment 3 and almost hide the organs in segment 6 (Fig. 1 A). The ovoid spermathecal bulb varies in size reflecting the volume of inseminated sperm.

Diagnosis. Small, 1.2 to 2.6 mm long terete body, head equal to or larger in diameter than segment 1; peristomium rounded, smooth lips, slight median emargination on ventral lip; oral papillae present; two jaws small brown, kidney to ovoid shape, dorsal larger, one large tooth middlemost, smaller teeth laterally, 6 / 5; deep sulcus in pharynx; dorsal segmental body ridges absent; segments 8 and 9 lateral epidermal glands present; thin clitellum; segment 5 one pair of testes, developing spermatozoa, a pair of sperm funnels each pass into a vas efferens, join forming short vas deferens, enters glandular atrium’s mid-region in segment 6; glandular atrium terete, length x 0.3 the segment diameter joins tubular muscular atrium, length about x 0.6 segment diameter, connects to spheroidal muscular bursa; eversible penis in muscular atrium’s ectal half; segment 5 spermatheca club-shaped, length about x 0.6 segment diameter, ovoid glandular spermathecal bulb, x 0.6 organ’s length, muscular spermathecal duct about x 0.4 organ’s length.

Distribution. Fergana Valley, Uzbekistan, and Turkistan, Kazakhstan.

Etymology. The specific name is a 3 rd- declension Latin adjective derived from the reported collection area of Turkestan, and the toponymic suffix - ensis, with an ending that matches the feminine generic name.

Type material. The holotype (NHMW-EV- 4669 m) and 17 paratypes (NHMW-EV- 4669 a-l and n-o), all housed in the Natural History Museum Vienna (Naturhistorisches Museum Wien) in Austria, were mounted on slides after being removed along with excised gills from one Astacus kessleri Schimkewitsch, 1886, in the same museum (Inv. No. 1345). The latter had been collected on Mr. Krausse’s land (or “ Domaine ”) in Turkestan, from the headwater region of the Syr-Darya; however, this region is located in the Fergana Valley, Uzbekistan, but was once called the Turkestan Province of Siberia (Cortambert 1880).