First Records of Dacian Endemic Species Dendrobaena Clujensis Pop 1938 (Clitellata; Lumbricidae) in Serbia

Introduction

Earthworm fauna of Balkan is very diverse [2] and, though mostly well studied, somewhere it is still insufficiently investigated. The genus Dendrobaena Eisen 1873 is represented by 92 species [3], of which 25 are endemics of the [4]. In Serbia, the genus Dendrobaena is represented by as many as 14 species, of which only four are endemic– Dendrobaena kozuvensis [1], Dendrbaena rhodopensis, Dendrobaena serbica Karaman 1973 and Dendrobaena zicsi Karaman 1973. Although the earthworm fauna of Serbia (as well as Kopaonik Mountain) is comparatively well investigated [5- 7] there are no data about the presence of Dendrobaena clujensis Pop, 1938 in the country.

The aim of the paper is to show the distribution of the Dacian endemic species D. clujensis in this part of Europe supported by new findings (new records from Serbia) and provide information on some morphological and ecological characteristics of the species.

Materials and Methods

The specimens for this study were collected in 2021., on the eastern slopes of Kopaonik Mountain (43°16’N, 20°49’E). The samples were collected in the pasture and conifer forests of the mountain. Earthworms were collected by the formalin method, digging (0.4 x 0.4 m2) and hand sorting. The earthworms were hand-sorted, then fixed in 96% alcohol, with the label on which the necessary were marked data. Species identification was done in accordance with the key by [1,7,8]. The specimens were deposited at the Earthworm Collection of the University of Kragujevac, Serbia (CEKUS). The map of the distribution of the species was created with Google Maps.

Results and Discussion

Morpho-anatomical descriptions of the species are given below. Differences in character states as found in the literature are inserted.

Dendrobaena clujensis Pop 1938

(Figure 1)

Dendrobaena clujensis Pop 1938: 137.

Figure 1: External morphology of Dendrobaena clujensis. Fixed specimen (a). Schematic drawing according to Šapkarev [7] (b) and Pop (1938) (c)

Dendrobaena clujensis Zicsi 1966: 395; Zicsi 1968: 137; Zicsi 1982: 443.

Dendrobaena clujensis Easton 1983: 478. Kritodrilus clujensis Omodeo & Rota 1989: 184. Dendrobaena clujensis Mršić [2]: 644; Qiu & Bouché 1998: 194; Csuzdi & Zicsi [8]: 112; Pop et al. [9]: 63; Csuzdi [10]: 97-99; Szederjesi [11]: 176.

Dendrobaena alpina mavrovensis Šapkarev 1971; 160; Šapkarev 1978: 62; Mršić 1991:630. New synonym Material examined: CEKUS/3492 1 exp., Serbia, Kopaonik Mt. (Jelak), 43º.3’ N, 20º.85’ E, coniferous forest, M. Stojanović, T. Trakić, J. Sekulić and F. Popović, 10.06.2021. CEKUS/3493 2 exp., Serbia, Kopaonik Mt. (Metodje), 43º.3’ N, 20º.88’ E, coniferous forest, M. Stojanović, T. Trakić, J. Sekulić and F. Popović, 10.06.2021. CEKUS/3494 2 exp., Serbia, Kopaonik Mt. (Jaram), 43º.28’ N, 20º.82’ E, pasture, M. Stojanović, T. Trakić, J. Sekulić and F. Popović, 16.07.2021.

Morphological description. External morphology. Body pigmentation dark violet in live specimens (Pop redviolet; Csuzdi & Zicsi dark red violet). White-beige homogeneous color in fixed specimens. Length 88–136 mm (Pop 60–120 mm; Csuzdi & Zicsi 70–100 mm) diameter 3.3–5 mm (Csuzdi & Zicsi 4.2–4.9 mm). Number of segments 135–167 (Pop 120–150; Csuzdi & Zicsi 110–157). Prostomium epilobous. First dorsal pore in 5/6. Male aperture on 15 between setae b–c, small, confined into own segment. Setae widely paired, setal arrangement after the clitellum: aa:ab:bc:cd:dd = 2:1:1.3:1:2.5. Glandular papillae surround setae ab on segments 10., 12., 15., 16., 33 and 34. (Csuzdi & Zicsi glandular papillae in 12 ab). Clitellum saddle-shaped in segments 26, 27–33. (Pop 27, 28– 33; Csuzdi & Zicsi (27), 28–33). Tubercula pubertatis in segments 30–32. (Pop 30–32, ½33; Csuzdi & Zicsi 30–32, ½33).

Internal anatomy. Septa 7/8–11/12 or thickened and muscular. Hearts in segments 6–11. Calciferous glands with clear diverticula in 11, 12, last pair of lateral hearts in 10. Crop in segments 15–16, gizzard in segments 17–19. The typhlosole is trifid. Testes in 10 and 11, ovaries in 13. Two pairs of testes in 10, 11 and three pairs of seminal vesicles in 9, 11, 12. Spermathecae two pairs in 9/10, 10/11 open close to setal line d. Nephridial bladders are sausage-shaped. Typhlosole bifid, the cross section of longitudinal muscle layer is of pinnate type.

Ecology: It was already noted that D. clujensis inhabits forest, and pasture vegetation as well as arable land [8,10-15]. Dendrobaena clujensis is characterized as a hill-mountain species that was recorded at altitudes of 600 to 2000 m a.s.l. Regarding ecological categories, it belongs to the epi-anecic species. This species has a remarkable adaptation to life in the soil and feeds on the litter layer.

Dendrobaena clujensis is a Dacian endemic, characteristic of the northern autochthonous part of Apuseni Mts. in Romania [9,10,15,16]. Also, this species was recorded on eastern part of Hungary [8]. The first record of the species from the Balkans Peninsula was in 1971 in North Macedonia [1]. Namely, the subspecies Dendrobaena alpina mavrovensis was found and described by Šapkarev [1] at the Duv site near the Mavrovo Mountain. Mršić confirmed the validity of the mentioned subspecies. Later, Csuzdi et al. [17] indicated that the Dendrobaena alpina group contains about 15 nominal species including several apparently synonymous species. The similarity of these species can be characterized by the position of the clitellum on segments 26, 27 to 33, 34 and tubercles around 30–32. On the other hand, these species show great taxonomic variability in terms of pigmentation, the number of seed sacs and the position of the spermatheca [17]. According to the earthworm database Csuzdi [3], the subspecies D. alpina mavrovensis is considered a junior synonym of the species D. clujensis, due to the identical taxonomic characters shown in Table 1. Further, the locality from North Macedonia (Mavrovo Mt.). represent the southernmost limit of the species’ natural range for now (Figure 2).

Figure 2: Geographical distribution of the species Dendrobaena clujensis (Circles – literature data; Square – new record).

Table 1: A comparison of some of the important taxonomical characters of the species Dendrobaena clujensis with the junior synonym Dendrobaena alpina mavrovensis.

Conclusion

The individuals found by us at Kopaonik Mt. are the first documented record of the species in Serbia. Thus, D. clujensis represents a new species for the Serbian earthworm fauna. The main reasons for this species’ presence in Serbia are presumably ecological factors and the complex paleography of this part of the Balkan. An ecological explanation could include numerous local factors such as climate, altitude, soil type, food availability, presence of predators and competition, which interact with the internal properties of organisms, which together determine its distribution. Besides, Kopaonik Mt. is characterized by a complex geological structure, which is directly related to its position within the transition zone between the Adria and European plates [18]. The eastern part of the mountain is of autochthonous origin, it was created as a result of the collision of the Dacia and eastern Vardar zone. Therefore, the current areas of Dacian endemic species that appear and expand are undoubtedly the result of the so-called isolation effect and climate changes in the Paleocene and Eocene, when the land was a system of smaller or larger islands, which changed their contours during geological history. This may have led to the speciation of Dacian endemic taxa– Cernosvitovia mehadiensis mehadiensis (Rosa 1895), Cernosvitovia mehadiensis boscaiui (Pop 1948), D. clujensis and Octodrilus gradinescui (Pop 1938) in Serbia.

Acknowledgement

This work was supported by the Serbian Ministry of Science, Technological Development and Innovation (Agreement Nos. 451- 03-47/2023-01/200378, 451-03- 47/2023-01/200122, and 451- 03-47/2023-01/200032).

Conflict of Interest

The authors have no conflicts of interest to declare that are relevant to the content of this article.

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