NORTH-WESTERN JOURNAL OF ZOOLOGY 13 (2): 326-336 ©NwjZ, Oradea, Romania, 2017 Article No.: e161805 http://biozoojournals.ro/nwjz/index.html

New records from the Central Zagros Mountain, with description of a new species

Robabeh LATIF1, Masoumeh MALEK1* and Csaba CSUZDI2

1. School of Biology and Center of Excellence in Phylogeny of living organisms, College of Science, University of , Tehran, Iran. E-mails: [email protected], [email protected] 2. Department of Zoology, Eszterházy Károly College, Eger, Hungary. E-mail: [email protected] *Corresponding author, M. Malek, E-mail: [email protected]

Received: 25. January 2016 / Accepted: 22. June 2016 / Available online: 27. July 2016 / Printed: December 2017

Abstract. The earthworm fauna of Iran is inadequately known. Up till now only 20 species were recorded for the country including 9 autochthonous and 11 peregrine species. The Zagros Mts. of Iran possesses unique geographical and climatic conditions that support a rich biota. Surprisingly enough the earthworm fauna of the region has not been studied earlier. A new survey carried out in the Central Zagros Mountain resulted in recording 24 earthworm species distributed in two families, (22 species) and Acanthodrilidae (two species) including 6 new country records (Aporrectodea longa, D. pentheri, D. semitica, Microscolex dubius, Microscolex phosphoreus) and furthermore a species new to science; Eisenia omranii sp. nov. According to the zoogeographic composition, out of the 24 species recorded, 14 are widely introduced peregrine ones and 10 are autochtonous of East-Mediterranean origin. In comparison with previously surveyed Elburz region with 14 recorded earthworm species, the Zagrosian earthworm fauna proved to be much richer in term of species number.

Key words: Lumbricidae, Acanthodrilidae, Central Zagros, new records, new species.

Introduction rani (1973) and following Csuzdi & Zicsi (2003) regarded Aporrectodea trapezoides (Dugès, 1828) as The earthworm fauna of Iran is quite poorly synonym of Ap. caliginosa (Savigny, 1826). known. Until the early 1970s, there were only four Recently a new species Eisenia malekae Szeder- species recorded for the country, three widely dis- jesi, Latif & Csuzdi, 2014 was added to the fauna tributed peregrine worms (Aporrectodea caliginosa raising the number of of Iran to 22 (Savigny, 1826), Ap. rosea (Savigny, 1826) and Eis- (Szederjesi et al. 2014). eniella tetraedra (Savigny, 1826) and a native spe- Despite the increasing sampling activity in cies Perelia persiana (Michaelsen, 1900) (Michaelsen some parts of Iran, little information is available 1900, Černosvitov 1941). The first broader earth- about the earthworm fauna in the Zagros Moun- worm campaign was launched by Ghassem Ali tain although it represents a special ecoregion in Omrani targeting five larger ; the the Palearctic (mountain forest steppe ecoregion Caspian Sea region, environs of Teheran, , No. PA0446) and harbors many rare or endan- and the region of the Persian Gulf. During gered species (WWF 2016). The present study is this study Omrani collected altogether 233 earth- aimed to obtain a better knowledge on the earth- worm samples and recorded 18 species belonging worm fauna of this remote and still pristine re- to the families Lumbricidae and Megascolecidae gion. (17 and 1 species respectively) (Omrani 1973). During the last decade the earthworm re- search of Iran gained a new momentum and sev- Material and Methods eral papers have been published adding new data to the earthworm fauna of different regions of the Study area The area studied is located in the western and southwest- country such as the Central Elburz Mts. (Latif et al. ern Iran and is a part of the Alpine-Himalayan mountain 2009), (Ezzatpanah 2010) chain. This region consists of forested and pastured and Teheran Province (Mirmonsef et al. 2011). mountain ranges. The climate is generally sub-humid These results have been summarized by Farhadi et continental with winter precipitation. The Zagros are lo- al. (2013) listing 19 earthworm species recorded for cated on the boundary between the Arabian and Eurasian Iran, however they forget mentioning Allolobo- tectonic plates (Agard et al. 2005). phoridella parva (Eisen, 1874) listed earlier by Om-

Earthworms from the Zagros Mountain, Iran 327

were placed in 4% formalin (Csuzdi & Zicsi 2003). Each bottle was labeled with information of GPS, location, PH, soil moisture and date from which it was collected (Ap- pendix 1). All mature specimens were dissected and ex- amined morphologically. For taxonomic identification the keys in Csuzdi & Zicsi (2003) and Sims & Gerard (1999) and Perel (1979) were used.

Results

In this study, 24 species belonging to 11 genera

Figure 1. Type locality of Eisenia omranii sp. nov (marked and two families of earthworms have been re- with circle). corded. Most of the taxa belong to the genera Den- drobaena Eisen, 1873 and Aporrectodea Örley, 1885 (6 and 5 species, respectively).The definitive list of Method earthworm taxa currently known from the region Investigations were carried out during 3 different peri- ods: in June 2013, July 2014 and Apr. 2015. Samples were is given in Table 1. Of these, five species (Aporrec- obtained from 105 localities at different sites representing todea longa, Dendrobaena pentheri, D. semitica, Micro- various habitats. In some sites, earthworms were sampled scolex dubius, M. phosphoreus) are new records for following two complementary approaches: qualitative the country, and one species Eisenia omranii sp. and quantitative sampling. Adults were collected by dig- nov. proved to be new for science. ging and hand sorting of a 25 cm × 25 cm × 15 cm deep In the frequency of occurrence analysis of the soil monolith. After collection earthworms were trans- identified species in the investigated area, Aporrec- ferred to the laboratory and washed to remove soil. The adult specimens were anaesthetized and killed in 15% todea trapezoides appears to be the most wide- and 75% ethanol, respectively. After one day, samples spread taxon. The next most common species are

Table 1. Comparison of the earthworm species found in the Central Zagros and the Elburz regions.

Species Central zagros Central elburz Chorotype Aporrectodea caliginosa (Savigny, 1826) + + peregrine Ap. trapezoides (Dugés, 1828) + + peregrine Ap. rosea (Savign, 1826) + + peregrine Ap. jassyensis (Michaelsen, 1891) + + Circum-Mediterranean *Ap. longa (Ude, 1885) + - peregrine Bimastos parvus (Eisen, 1874) + - peregrine Dendrobaena byblica (Rosa, 1893) + + Circum-Mediterranean D. hortensis (Michaelsen, 1890) + + peregrine D. orientalis Černosvitov, 1940 + - East -Mediterranean D. octaedra (Savign, 1826) + + peregrine *D. pentheri (Rosa, 1905) + - East -Mediterranean *D. semitica (Rosa, 1893) + - East -Mediterranean D. veneta (Rosa, 1886) + + peregrine Dendrodrilus rubidus (Savigny, 1826) + + peregrine Eisenia fetida (Savigny, 1826) + + peregrine E. malekae (Szederjesi, Latif & Csuzdi, 2014 + - endemic E. omranii sp. nov. + - endemic Eiseniella tetraedra (Savigny, 1826) + + peregrine Helodrilus patriarchalis (Rosa, 1893) + - East -Mediterranean Healyella syriaca (Rosa, 1893) + - East -Mediterranean lacteum (Örley, 1881) + + peregrine Perelia kaznakovi (Michaelsen, 1910) + + East -Mediterranean Dichogaster bolaui (Michaelsen, 1891) - + peregrine *Microscolex dubius Fletcher, 1887 + - peregrine *M. phosphoreus (Dugés, 1837) + - peregrine Amynthas corticis (Kinberg, 1867) - + peregrine

*New records for the Iranian earthworm fauna. 328 R. Latif et al.

Aporrectodea rosea (Savigny, 1826), Helodrilus patri- , Bisheh Fall 29.06.2014. ZUTC archalis (Rosa, 1893) and E. fetida ((Savigny, 1826), 5820, 2ex. Province, Ghalegah respectively. 30.04.2014. ZUTC 5822, 3ex. Kermanshah Provine, Karand 02.05.2014. ZUTC 5823, 2ex. Kermanshah List of species Province, Gillane- Gharb 03.05.2014. ZUTC 5824, 2 Family: Lumbricidae (Rafinesque-Schmaltz, ex. , Sarabe- Ghanbar 1815) 03.05.2014. ZUTC, 5825 8ex. Kermanshah Prov- Aporrectodea caliginosa (Savigny, 1826) ince, 04.05.2014. ZUTC 2826, 5ex. - Aporrectodea caliginosa: Csuzdi and Zicsi 2003: 75 shah Province, Ghaledez 29.05.2014ZUTC 5827, (for complete synonymy) 3ex. Lorestan Provine, Pole-Dokhtar 18.06.2014. Material examined: ZUTC 5801, 3 ex. Lorestan ZUTC 5828, 2ex. Hamedan Province, Famenin Province, Robate-Namaki 28.06.2013. ZUTC 5802, 20.06.2014. ZUTC 5829, 4 ex. Hamedan Province, 5ex. Lorestan Province, Sarabe-Honam 28.6.2013. Shahrak- Village 20.06.2014. ZUTC 5830, 2ex. ZUTC5803, 1ex. Lorestan Province, Sarabe- Presk Hamedan Province, Sarabe-Gian 20.06.2014. 29.06.2013. ZUTC 5804, 3ex. Lorestan Provine, Ecology: endogeic Koohdasht 29.06.2013. ZUTC 5805, 2ex. Lorestan Diagnosis: Clitellum on segment (24)25–32, Province, Chamar Village 30.06.2013. tubercles on segments 29–31. Dorsal pores are Ecology: endogeic readily visible, especially on the clitellum, 60–130 Diagnosis: Clitellum and tubercula respec- segments. tively extend on segments 27–34, 31–33. Tubercula Aporrectodea jassyensis (Michaelsen, 1891) bipartite, pigmentation absent, colour whitish- Aporrectodea jassyensis: Csuzdi & Zicsi 2003: 87 (for grey. Some specimens have extended prostomium complete synonymy) into a proboscis-like structure, 80–100 segments. Material examined: ZUTC 5831, 3 ex. Ker- Aporrectodea trapezoides (Dugès, 1828) manshah Province, 29.04.2014. ZUTC Aporrectodea trapezoides: Blakemore 2008: 503-506 5832, 2ex. Kermanshah Province, Ghalegah (for complete synonymy). 30.04.2014. ZUTC 5833, 5ex.Kermanshah Province, Material examined: ZUTC 5806, 5 ex. Kerman- Eslamabad 02.05.2014. ZUTC 5834, 2ex. Kerman- shah Province, Kangavar 29.04.2014. ZUTC 5807, shah Provine, Sarabe- Ghanbar 02.05.2014. ZUTC 2ex. Kermanshah Province, Shooshmi Village 5835, 2ex. Hamedan Province, 1.05.2014. ZUTC 5808, 3ex. Lorestan Province, 19.05.2014. ZUTC 5836, 3 ex. Hamedan Province, Mahdasht 02.05.2014. ZUTC 5809, 1ex. Kerman- Toyserkan 30.05.2014. shah Provine, Eslam abad 02.05.2014. ZUTC 5810, Ecology: endogeic. 2ex. Kermanshah Province, Sarabe- Karand Diagnosis: Clitellum extends on 29–35, tuber- 02.05.2014. ZUTC 5811, 5 ex. Kermanshah Prov- cles on 1/n 31, 32–34, body 100–120 segments, ince, Gillane- Gharb 03.05.2014. ZUTC 5812, 2ex. color pale. Lorestan Province, Aligoodarz 28.05.2014. ZUTC Aporrectodea longa (Ude, 1885) 5813, 5ex. Hamedan Province, Ghahavand Aporrectodea longa: Csuzdi and Zicsi 2003: 89 (for 18.06.2014. ZUTC 5814, 3ex. Hamedan Provine, complete synonymy) Baban Village 18.06.2014. ZUTC 5815, 2ex. Material examined: ZUTC 5837, 2 ex. Lorestan Hamedan Province, Shahrak Village 19.06.2014. Province, Koohdasht 29.04.2014. ZUTC 5838, 2ex. ZUTC 5816, 4 ex. Hamedan Province, Sarabe- Gian Kermanshah Province, Ghilane-Gharb 03.05.2014. 19.06.2014. ZUTC 581, 2ex. Hamedan Province, ZUTC 5839, 2ex. Kermanshah Province, Nosood 20.06.2014. 04.05.2014. Ecology: endogeic Ecology: endo-anecic Diagnosis: Clitellum and tubercula respec- Diagnosis: Clitellum extends on 27–35, tuber- tively on segments 27–34, 31–33. Tubercula band- cles on 1/n 31, 32–34, body length 90–160mm, shaped, dorsal surface light to dark brown, 100– color dark brown. 180 segments. Bimastos parvus (Eisen, 1874) Aporrectodea rosea (Savigny, 1826) Bimastos parvus: Blakemore 2008: 537 (for complete Aporrectodea rosea: Csuzdi & Zicsi 2003: 92.(for synonymy) complete synonymy) Material examined: ZUTC 5840, 2 ex. Kerman- Material examined: ZUTC 5818, 3 ex. Lorestan shah Province, Eslam abad 02.05.2014. Province, Kakareza 28.06.2014. ZUTC 5819, 3ex. Ecology: epigeic Earthworms from the Zagros Mountain, Iran 329

Diagnosis: Clitellum extends on 24–31, tuber- Material examined: ZUTC 5851, 1 ex. Kermanshah cles absent, body 60–95 segments, color usually Province, Mahidasht 02.05.2014. reddish, sometimes pale and at two ends of the Ecology: epigeic body appears rosy. Diagnosis: Clitellum extends on 24–33, tuber- Dendrobaena byblica complex (Rosa, 1893) cles on 30–32 and ribbon-shaped, color red-violet Dendrobaena byblica complex: Blakemore 2008: 547. especially on dorsum. Material examined: ZUTC 5841, 2 ex. Kerman- Dendrobaena pentheri Rosa, 1905 shah Province, Nosood 01.05.2014. ZUTC 5842, Dendrobaena pentheri: Perel 1979: 234 (for complete 2ex. Kermanshah Province, 02.05.2014. synonymy). ZUTC 5843, 2ex. Kermanshah Province, Material examined: ZUTC 5852, 2 ex. Lorestan 04.05.2014. Province, Ab sefid Fall 30.04.2013ZUTC 5853, 2ex. Ecology: epigeic Hamedan Province, Alvand 20.06.2014. ZUTC Diagnosis: Clitellum extends on segments 24– 5854, 2ex. Hamedan Province, Alvand 20.06.2014. 30, saddle-shaped, tubercles on 25–27. The size ZUTC 5855, 2 ex. Hamedan Province, Meryanaj and shape of tubercles are different. Some are 18.06.2014. very small in size, the bigger ones are colorless Ecology: epigeic with very small male pore. The others have dark Diagnosis: Clitellum on segment 25–34 (35), red to violet pigmentation while the male pore tubercles on segment 28–32, color dark violet, easily seen. length 90–150 mm, Male pore small. Remarks: Dendrobaena byblica is a highly vari- Dendrobaena semitica (Rosa, 1893) able species complex showing an extended Dendrobaena semitica: Csuzdi & Pavlíček 1999: 477 Circum-Mediterranean distribution (Csuzdi et al. (for complete synonymy). 2011). To clear the status of the 20 or so synonym Material examined: ZUTC 5856, 2 ex. Hamedan names in this complex (Csuzdi 2012), a detailed Province, Meryanaj 20.06.2014. ZUTC 5857, 2ex. molecular study would be needed (Szederjesi, Pop Kermanshah Province, Sahneh 02.05.2014. & Csuzdi 2014, Szederjesi 2017). Ecology: epigeic Dendrobaena hortensis (Michaelsen, 1890) Diagnosis: Clitellum is consistently on seg- Dendrobaena hortensis: Csuzdi and Zicsi 2003: 119 ments 26–33, tubercular bands consistently on (for complete synonymy) segments 31–33. Color striped red-violet. Material examined: ZUTC 5844, 3 ex. Kerman- Dendrobaena veneta (Rosa, 1886) shah Province, Tagh 02.05.2014. ZUTC 5845, 2ex. Dendrobaena veneta Csuzdi and Zicsi 2003: 127 (for Kermanshah Province, Gillane-Gharb 01.05.2014. complete synonymy) ZUTC 5846, 2ex. Kermanshah Province, Harsin Material examined: ZUTC 5858, 2 ex. Kermanshah 03.05.2014. ZUTC 5847, 2 ex. Kermanshah Prov- Province, Javanrood 01.06.2014. ZUTC 5859, 2ex. ince, Sarabe-Holi 04.05.2014. ZUTC 5848, 3ex. Kermanshah Province, Sarabe-Harsin 02.05.2014. Kermanshah Province, Nosood 01.05.2014. ZUTC ZUTC 5860, 1ex. Kermanshah Province, Sahneh 5849, 2ex. Kermanshah Province, 02.05.2014 04.05.2014 Ecology: epigeic Ecology: epigeic Diagnosis: Clitellum extends on segments 27– Diagnosis: Clitellum on segment 27–33, tuber- 33, saddle-shaped, tubercles on 30–½32, color red- cles on segment 30–31, pigmentation often trans- dish. versely striped, 55–150 segments. Dendrobaena octaedra (Savigny, 1826) Dendrodrilus rubidus (Savigny 1826) Dendrobaena octaedra: Csuzdi and Zicsi 2003: 121 Dendrodrilus rubidus: Csuzdi & Zicsi 2003: 132 (for (for complete synonymy) complete synonymy) Material examined: ZUTC 5850, 2 ex. Lorestan Material examined: ZUTC 5861, 2 ex. Kerman- Province, Aleshtar 28.06.2014. shah Province, Nodesheh 01.05.2014. ZUTC 5862, Ecology: epigeic 2ex. Kermanshah Province, Hajij Village Diagnosis: Clitellum extends on segments 28– 02.05.2014. 33, saddle-shaped, tubercles on 31–33, color dark Ecology: epigeic red. Diagnosis: Clitellum extends on segments 27– Dendrobaena orientalis Cernosvitov 1940 31, tubercles on 29–30, color red-violet. Csuzdi & Pavlíček 1999: 475 (for complete synon- Eisenia fetida (Savigny, 1826) ymy) Eisenia fetida: Csuzdi and Zicsi 2003: 143 (for com- 330 R. Latif et al. plete synonymy) Material examined: ZUTC 5863, 2 ex. Lorestan Province, Rahimabad 29.06.2013. ZUTC 5864, 2ex. Kermanshah Province, Sarabe-Holi 30.04.2014. ZUTC 5865, 3ex. Kermanshah Province, Nosood 01.05.2014. ZUTC 5866, 2 ex. Kermanshah Prov- Figure 2. Diagram of the ince, Qasre- shirin 01.05.2014. ZUTC 5867, 2ex. setal arrangement of Kermanshah Province, Eslamabad 02.05.2014. Eisenia omranii sp. nov. aa, ab, bc, cd, dd ZUTC 5868, 3ex. Kermanshah Province, Koo- = setal intervals. sevand 03.05.2014. ZUTC 5869, 1 ex. Lorestan

Province, Nosood 01.05.2014. ZUTC 5870, 2ex. Hamedan Province, Rezini 18.06.2014. ZUTC 5871, Etymology. The new species is named in hon- 2ex. Hamedan Province, Malhamdareh 20.06.2014. our of Dr. Ghasem Ali Omrani who initiated the ZUTC 5872, 5 ex. Lorestan Province, Par Spring earthworm researches in Iran. 30.06.2013. ZUTC 5873, 2ex. Hamedan Province, External characters: Holotype 72 mm long and Hassan Gheshlagh 18.06.2014. ZUTC 5874, 1ex. 4 mm wide, number of segments 118. Paratypes Kermanshah Province, Kangavar 04.05.2014 55–72 mm in length and 4–4.5 mm in diameter. Ecology: epigeic. Number of segments 115–118. Setae closely paired, Diagnosis: Clitellum on segment 26–32, tuber- setal arrangement after the clitellum cles on segments 28–31, dorsal surface brown-red, aa:ab:bc:cd:dd = 11:1.6:8:1:32 (Fig. 2). Colour dark and pigmentation often absent from furrows, 60– brown on the dorsum and somewhat lighter on 110 segments. However, differentiation of Eisenia the ventrum. Head epilobous, first dorsal pore in fetida and E. andrei Bouché, 1972 is very difficult 4/5. Clitellum extends on 25(26)–34, tubercles on due to the high morphological similarity (Szeder- 30–1/n34 (Fig. 3). Spermathecal pores two pairs in jesi & Valchovski 2016). 9/10–10/11 in setal line d. Male pore on 15 me- Eisenia malekae Szederjesi, Latif & Csuzdi 2014 dium sized, confined to its own segment. Eisenia malekae Szederjesi, Pavlicek, Latif & Csuzdi, Nephridial pores irregularly alternated between 2014: 284. setal line b and above d. Glandular tumescences Material examined: ZUTC 5875, 1 ex. Kerman- on segments 9–11ab. shah Province, Karand 02.05.2014. Internal characters: Septa 6/7–8/9 thickened. Ecology: epigeic Testes and male funnels in 10, 11 covered with pe- Diagnosis: Clitellum on 27, 28–41, 42, tubercles rioesophageal testis sacs. Four pairs of vesicles in on 37, 38–41. Color alive dark red-violet, con- 9–12, those in 9 and 10 small; spermathecae two served pale. pairs in 9/10–10/11, open near d. Calciferous Eisenia omranii Latif, Malek & Csuzdi sp. nov. glands in 11–12 without distinct diverticula, Figures 2-3 Hearts in segments 7–11 a pair of small extraoe- Holotype. ZUTC 5876. Kermanshah Province, sophageal vessels in 12. Nephridial bladders sim- Iran, N 34° 22' 4.2''E, 47° 45' 57.0''. Leg. R. Latif, E. ple, sausage-shaped. Typhlosolis T-shaped, large. Hosseini & A. Kazemi. 4.05.2014. Deposited in the Longitudinal musculature is of pinnate type. earthworm collection of University of Tehran. Ecology: endo-epigeic Paratypes. ZUTC 5877, 5 ex. locality and date Remarks. The new species is near to E. tran- same as that of the Holotype. Deposited in the scaucasica (Perel, 1967), however differs from it in earthworm collection of University of Tehran. the position of the clitellum and tubercles (26–36

Figure 3. The lateral view of the anterior external features of E. omranii sp. nov. showing the clitellar organs. Mp = male pore, Tb = tubercles. Scale bar = 1 mm. Earthworms from the Zagros Mountain, Iran 331

Table 2. Distinguishing characters of Eisenia omranii. “(12)” in the Calciferous glands column refers to the position of the calciferous diverticula “(-)” denotes the missing diverticulum.

Calciferous Species Clitellum Tubercles Spermatheca Vesicles Musculature Head glands Eisenia kontschani Szederjesi, 26–37, ½38 32–36 9/10, 10/11 d 9–12 11–13 (-) pinnate tanylobous Pavlícek & Csuzdi, 2014 Eisenia malekae Szederjesi, 27,28–41, 42 37,38–41 9/10, 10/11 d 11, 12 11–12 (12) pinnate epilobous Latif & Csuzdi, 2014 Eisenia malevici 29–36 31,32–36 9/10, 10/11 d>M 11, 12 11, 12 (11) pinnate epilobous Perel, 1962 Eisenia muranyii ½24–35 28–1/n33 9/10, 10/11 d 9–12 11–12 (12) fasciculated epilobous Szederjesi & Csuzdi, 2015 Eisenia omranii sp. nov. 25,26–34 30–1/n34 9/10, 10/11 d 9–12 11–12 (-) pinnate epilobous Eisenia transcaucasica 26,½26–36 31–35 9/10, 10/11 cd 9–12 ½10–12 (-) fasciculated epilobous (Perel, 1967)

vs. 25,26–34 and 31–35 vs. 30–¼34 respectively). segment 15, surrounded by a genital ridge situ- The two species differs in the longitudinal muscu- ated on segment ½14–16. lature as well (it is fasciculate in transcaucasica and Helodrilus patriarchalis (Rosa, 1893) pinnate in the new species). According to the cli- Helodrilus partiarchalis: Szederjesi et al. 2014a: 566 tellar organs. the new species shows similarity (for complete synonymy) with E. breviclitellata Kvavadze, 1985 and E. mu- Material examined: ZUTC 5887, 2 ex. Kerman- ranyii Szederjesi & Csuzdi, 2015 as well (cl. 25– shah Province, Sarpole-zahab 02.05.2014. ZUTC 33,34, tb. 29–33 and cl. ½ 24–35, tb. 28–1/n33 re- 5888, 1ex. Kermanshah Province, Pahn reshid spectively) however both latter species are un- Spring 02.05.2014. ZUTC 5889, 1ex. Kermanshah pigmented. Furthermore. breviclitellata possesses Province, Ghare soo river 02.05.2014. ZUTC 5890, large calciferous diverticula in 10–12 (Table 2). 2 ex. Kermanshah Province, Sarabe- Holi This is why Szederjesi et al. (2014) noted that E. 03.05.2014. ZUTC 5891, 2ex. Kermanshah Prov- breviclitellata might belong to a different genus. ince, Sarabe-Fas 03.05.2014. ZUTC 5892, 2ex. Lore- stan Province, Pole-dokhtar 29.05.2014. ZUTC Eiseniella tetraedra (Savigny, 1826) 5893, 2ex. Lorestan Province, waterland Lafaneh Eiseniella tetraedra: Csuzdi and Zicsi 2003: 153 (for 29.05.2014. complete synonymy) Ecology: endogeic Material examined: ZUTC 5882, 2 ex. Kerman- Diagnosis: Clitellum extends on segments (21), shah Province, Sarabe- Karand 02.05.2014. ZUTC 22, 23–33, 34 saddle-shaped. Tubercles usually on 5883, 2ex. Lorestan Province, Nojian Fall ½30–½33. Male pore on 15, great slit. 29.04.2014. ZUTC 5884, 3ex. Hamedan Province, (Örley, 1881) 18.06.2014. ZUTC 5885, 2 ex. Lorestan Prov- Octolasion lacteum: Csuzdi and Zicsi 2003: 197 (for ince, Kashkan River 01.05.2014. ZUTC 5842, 2ex. complete synonymy) Kermanshah Province, Bell Fall 29.06.2013. Material examined: ZUTC 5896, 2 ex. Ecology: epigeic Hamedan Province, Kaboodarahang 30.05.2014. Diagnosis: Clitellum on segments 23–26, tu- ZUTC 5897, 2 ex. Kermanshah Province, Harsin bercles on segments 24–25. Tail with characteristic 04.05.2014. tetrahedral shape. Ecology: endogeic Healyella syriaca (Rosa, 1893) Diagnosis: Clitellum on segments 30–35, tu- Healyella syriaca: Szederjesi et al. 2014a: 566 (for bercles on segments 31–34, male pore is obvious complete synonymy) and its glandular crescents extends across furrow Material examined: ZUTC 5894, 3ex. Hamedan 14/15. Province, Toyserkan 29.05.2014. ZUTC 5895, 3 ex. Perelia kaznakovi (Michaelsen, 1910) Hamedan Province, Kaboodarahang 30.05.2014. Perelia kaznakovi: Csuzdi and Pavlíček 2005: 79 (for Ecology: epi-endogeic complete synonymy) Diagnosis: Clitellum on segment 26–32, tuber- Material examined: ZUTC 5898, 2 ex. cles lacking. Color grey, sometimes with reddish Hamedan Province, Sarabe-Farsban 20.05.2014. hints, setae distant. Male pores on posterior part of ZUTC 5899, 2 ex. Hamedan Province, Sarajbe-Gian 332 R. Latif et al.

20.05.2014. omranii sp. nov is new to science. Ecology: endogeic With these data the number of earthworm Diagnosis: Clitellum extends on segments 27– species recorded for Iran is raised to 28. Two of 35, tubercles on 32–34, large species, and pigmen- these newly recorded species (Microscolex dubius tation absent. and M. phosphoreus) are peregrine, introduced Family: Acanthodrilidae Claus, 1880 worldwide by anthropogenic activities. The two Microscolex phosphoreus Dugés, 1837 Microscolex species have perhaps of S. American Microscolex phosphoreus: Sims & Gerard 1985: 140 origin, and are common over the whole Mediter- (for complete synonymy) ranean area (Pavlíček et al. 2003). Microscolex Material examined: ZUTC 5901, 1 ex. Ker- dubius is more widespread and it survives in manshah Province, Taghbostan 01.05.2014. summer as resistant cocoons in the dry surface soil Ecology: endogeic (Doube & Auhl 1998). We found Bimastos parvus, Diagnosis: Clitellum annular on segments 13– native in North America, along water courses with 17 incomplete ventrally on the first and last seg- some organic material in the water. The autoch- ments, prostomium epilobous. Spermathecal pores thonous species, Dendrobaena pentheri prefers soil in 8/9, prostatic pores on segment 17. which includes abundant organic material. This Microscolex dubius (Fletcher, 1887) species is abundant in Northern Turkey and Microscolex dubius: Szederjesi et al. 2014a: 568 (for common in the Caucasus (Pavlíček & Csuzdi complete synonymy) 2006). Its area stretches to the west as far as the Material examined: ZUTC 5900, 1 ex. Ker- Karpathos Island (Szederjesi 2015). manshah Province, Taghbostan 01.05.2014. Another autochthonous species belonging to Ecology: endogeic the genus Dendrobaena is D. semitica endemic in the Diagnosis: Medium-sized worms, 60–65 mm East-Mediterranean Region and distributed in the in length and 4 mm. in diameter. Unpigmented, Levant. The remaining newly recorded species clitellum yellowish. Clitellum on 13–16, covering Aporrectodea longa belongs to the endo- anecic eco- slightly 17 as well. Prostomium epilobous. Sper- logical group and have widespread distribution in mathecae lacking, prostatic pores on 17. the palearctic region. We have found Ap. longa in many stations in the Zagros Mts. but surprisingly it was not found in the Elburz region (Latif et al. Discussion 2009). This phenomenon can be related to the obli- gate diapause period reported for this species Before we launched this survey, there was little in- which lasts from as early as May to September or formation available on earthworm species compo- October (Edwards & Bohlen 1996). sition in this region. Here we report on 24 species Healyella syriaca, is another autochthonous of earthworms belonging to 11 genera of Lumbri- species shared with the Levant and most probably cidae and two species in the family Acanthodrili- has an Anatolian origin (Omodeo & Rota 1999). dae. Earthworm habitats in the surveyed area are Up to now this species has also not been found in populated by both native and introduced earth- Central Elburz region of Iran (Latif et al. 2009). worm species. The most commonly encountered In the Zagros region the most abundant earthworms in Iran belong to the family Lumbri- earthworm along the river banks was Helodrilus cidae. patriarchalis, this species prefers highly moist soils Csuzdi and Zicsi (2003) recognized four large or can be found in the very banks of streams. In biogeographic domains including: the Franco- the same habitats in the Central Elburz region Iberian, Aegean, Turanian, and North American however, we have observed Eiseniella tetraedra as a domains in the distribution area of endemic lum- dominant species and H. patriarchalis has not been bricids. Lumbricid earthworms in Iran show recorded so far. This species shows a typical East faunistic affinities with the Turanian and Aegean Mediterranean distribution with its range stretch- subdomains (Ezzatpanah et al. 2010). ing from Crete through Anatolia and the Levant Out of the 24 species recorded here, Aporrecto- (Csuzdi et al. 2006, Pavliček et al. 2003) to the dea longa (Ude, 1885), Dendrobaena pentheri Rosa, Transcaucasus (Perel 1967, Kvavadze 1985). Based 1905, D. semitica (Rosa, 1893), Microscolex dubius on previous surveys (Omrani 1973) this species (Fletcher, 1887) and M. phosphoreus (Dugès, 1837) was recorded as Helodrilus oculatus Hoffmeister, are new records to the fauna of Iran and Eisenia 1845. Because completely adult specimens of H. Earthworms from the Zagros Mountain, Iran 333 patriarchalis are found only for a short period in as well. the year, this has resulted in the description of Aporrectodea rosea was recorded together with several synonym names for this species (Szederjesi Ap. caliginosa in most stations but Ap. caliginosa et al. 2014). was more sensitive to low moisture levels than Ap. Dendrobaena byblica, Dendrobaena veneta and rosea. Aporrectodea caliginosa is one of the most Aporrectodea jassyensis are three autochthonous abundant earthworm species in Paleartic grass- species with Anatolian-Caucasian origin. Dendro- land regions and the most commonly found in ag- baena byblica share the same clitellar position with ricultural ecosystems across the temperate zone. It the typical East Mediterranean form but differ in is known that these species resemble each other in many characters such as the coloration, size, and ecological preferences. The same results were re- type of prostomium. In a previous study, the D. ported for these species by Mirmonsef et al. (2011) byblica specimens collected in the Elburz region, in Central Elburz region. were darker, smaller and possessed fewer seg- Out of the 24 species recorded in Zagros Mts., ments in comparison with the Zagrosian ones. Ac- 14 are introduced and 10 species are autochtho- cording to Csuzdi & Pavlicek (1999) and Szeder- nous (Aporrectodea jassyensis, Dendrobaena byblica, jesi, Pop & Csuzdi (2014), D. byblica probably D. orientalis, D. pentheri, D. semitica, D. veneta, Eis- represents a superspecies containing several valid enia malekae, E. omranii sp. nov, Helodrilus patriar- species. chalis, and Perelia kaznakovi). Regarding the num- Dendrobaena orientalis is one of the autochtho- ber of autochthonous species of this region, the nous species in the Middle East (Pavliček et al. Zagrosian fauna is richer than the Central Elburz 2010). It has already been reported in the spring region with five autochthonous species recorded, habitat from the Zagros region by Farhadi et al. however the two regions share 13 species. (2013). Other recorded species in this region is E. Taking into account the earthworm composi- malekae; distribution of this species might be asso- tion of the Zagros Region, we can conclude that ciated to moist oak forest. the earthworm fauna has more zoogeographic af- Aporrectodea jassyensis is a Trans-Aegean spe- finities with the Levantine than with the Anatolian cies (Stojanovic & Milutinovic 2014), which prefer fauna. To evaluate the earthworm faunistic simi- woody areas (Sims & Gerard 1999); it was re- larities between Turkey, Levant and Iran, more corded only at six localities. Dendrobaena veneta data are needed especially on molecular level to was collected under litter and other organic mate- clear the phylogenetic and phylogeographic rela- rial in a woody area which is typical habitat for tionships between the shared species. this species. In the present study, the species richness is not equally distributed among the genera. Most of the species ascribed to the genus Dendrobaena, How- Acknowledgments. We would like to thank the Research ever, this is not surprising because one of the dis- Affairs of the University of Tehran and the National Science Foundation of Iran for the financial support. tribution centers of the genus is in the East- Thanks are extended to Mr. Kazemi, Mr. Roohi Aminjan, Mediterranean (Omodeo & Rota 2008). Mr. Mirmonsef and Ms. Hosseini for their help with Among the peregrine species recorded for the sampling. Zagros Mts., Aporrectodea trapezoides is one of the most common. It is abundant and dominant in humid plots like riversides, forests, and farming areas. Aporrectodea rosea is also very frequent in References cultivated fields. This latter species occurs in two Agard, P., Omrani, J., Jolivet, L., Mouthereau, F. (2005): morphological forms, Some samples associated Convergence history across Zagros, Iran; constraints from with grassy habitats. with large-sized adults and collisional and earlier deformation. International Journal of Earth Sciences 94: 401–419. less distinct tubercles and a much smaller one Blakemore, R.J. (2008): Cosmopolitan Earthworms (3rd Edition) with sterile male reproduction system near river- Verm Ecology, Yokohama, Japan. pp. 757. side. We suppose that this condition is possible Černosvitov, L. (1940): On some Oligochaeta from Palestine. The Annals and Magazine of Natural History 11(6): 438–447. due to parthenogenesis. In one station we have Černosvitov, L. 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+ Appenidx 1 – 1 ½ pages

Appendix 1. Sampling localities.

St.Name GPS coordinate PH Soil Moisture 1 Kangavar N 34° 29' 08.7''E 48° 55' 54.9'' 7 35% 2 Tagh-Bostan N 34° 23' 11.0''E 47° 07' 51.2'' 7 35% 3 Paveh N 34° 27' 6.01''E 47° 01' 8.5'' 5 60% 4 Norooz abad N 34° 28' 35.3''E 46° 55' 19.5'' 7 50% 5 Soror-e Olia Village N 34° 48' 27''E 46°32' 55.2'' 7 35% 6 GHalegah N 34° 54' 6.0''E 46° 28' 36.2'' 7 40% 7 Shahoo N 34° 55 51.6''E 46° 28' 5.9'' 7 50% 8 Paveh- Sarabe- Hooli N 35° 2' 47.5''E 46° 22' 6.6'' 7 40% 9 Hajij N 35° 09' 36.02''E 46° 19' 19.9'' 7 4.5% 10 Hajij Village N 35° 09' 34.08''E 46° 20' 23'' 7 70% 11 Bell fall N 35° 10' 4.01''E 46° 20' 57.06'' 4 40% 12 Hajij Village N 35° 09' 47.8''E 46° 17' 54.8'' 7 60% 13 Nodesheh N 34° 28' 35.3''E 46° 55' 19.5'' 7 40% 14 Marivan N 35° 12' 56.2'' E 46°13' 23'' 7 60% 15 Nosood N 35° 10' 32.2''E 46° 12' 11.4'' 7 40% 16 Shooshmi Village N 35° 10' 43.9''E 46° 11'16.04'' 7 35% 17 Neisaneh N 35° 08' 16.5''E 46° 13' 51.9'' 7 75% 18 Sefidab Village N 34° 59' 16.2''E 46° 14' 5.6'' 5.5 30% 19 Mahidasht N 34° 18' 44.02''E 46° 41' 16.8'' 7.5 45% 20 Eslam abad N 34° 07' 24.08''E 46° 3015.06'' 8 60% 21 Karand N 34° 12' 48.9''E 46° 18' 10.0'' 8 45% 22 Sarabe- Karand N 34° 17' 10.3''E 46° 14' 56.1'' 7 80% 23 Sare-Pole Zahab N 34° 25' 32.2''E 45°50' 44.1'' 7 45% 24 GHasre Shirin N 34° 31' 45.2''E 45° 35' 21.7'' 7 45% 25 Ghasre Shirin N 34° 32' 11.7''E 45° 37' 38.7'' 7 50% 26 Gillane- Gharb N 34° 01' 16.6''E 46° 25' 35.0'' 6.5 45% 27 Sarabe- Ghanbar N 34° 02' 35.01'' E 46° 17' 40.7'' 7 80% 28 Pahne Rashid Spring N 34° 03' 6.04''E 46° 05' 34.07'' 7 85% 29 Sarabe- Ghillane-Gharb N 34° 07' 46.0''E 45° 56' 19.8'' 7 70% 30 Gharesoo River N 34° 25' 45.5''E 46° 51' 47.0'' 7 85% 31 Sarabe-Harsin N 34° 16' 40.4''E 47°25' 54.1'' 5.5 75% 32 Harsin N 34° 31' 45.2''E 45° 35' 21.7'' 7 55% 33 Pasar Village N 34° 14' 10.7''E 47° 22' 55.3'' 7 60% 34 Sorkhedeh Village N 34° 15' 14.1''E 47° 22' 59.0'' 7 45% 35 Ghaladziar Village N 34° 15' 36.08''E 47° 34' 41.0'' 7 80% 36 Sarabe- Garoos N 34° 22' 4.2''E 47° 45' 57.0'' 7 55% 37 Songhor N 34° 46' 47.0''E 47° 36' 47.8'' 6.5 45% 38 Kahriz Spring N 34° 46' 29.4''E 47° 36' 32.7'' 7 85% 39 Abdol Spring N 34° 30' 16.0''E 47°57' 27.8'' 7 85% 40 Sarabe-Fash N 34° 35' 50.5''E 47° 54' 47.2'' 7 70% 41 Robate- Namaki N 33° 35' 55.1'' E 48° 17' 50.4'' 7 55% 42 Kakareza Village N 33° 43' 13.3''E 48° 14' 57.3'' 6 45% 43 Alashtar N 33° 42' 37.7'' E 48° 16' 43.3'' 6.5 35% 336 R. Latif et al.

St.Name GPS coordinate PH Soil Moisture 44 Honam Village N 33° 47' 55.4''E 48° 14' 15.9'' 4.5 60% 45 Sarabe- Honam N 33° 48' 28.4'' E 48°18' 42.7'' 5 75% 46 Peresk Spring N 33° 49' 21.5'' E 48° 24' 24.4'' 7 85% 47 Sarabe- Peresk N 33° 49' 21.5''E 48° 24' 24.4'' 7 80% 48 Vardeh Village N 33° 27' 06.7''E 48° 15' 41.5'' 7 55% 49 Koohdasht N 33° 31' 33.6'' E 48° 07' 07.9'' 7 55% 50 Kashkan N 33° 27' 00.0'' E 48° 15' 37.3'' 6.5 80% 51 Bisheh fall N 33° 19' 52''E 48° 52' 45.7'' 7 85% 52 Chamar Village N 33° 25' 51.1''E 49° 11' 57.3'' 5 55% 53 Par Spring N 33° 13' 42.5'' E 49° 36' 36.9'' 5 85% 54 Dare- Takht River N 33° 25' 36.6'' E 49° 24' 23.2'' 5 85% 55 Pachenar N 33° 21' 57.2'' E 49° 22' 48.5'' 7 55% 56 Absephid Fall N 33° 08' 45.1'' E 49° 41' 01.4'' 7 80% 57 Visiar N 33° 08' 45.1'' E 49° 41' 01.4'' 7 70% 58 Afarineh Fall N 33° 18' 49.8'' E 47° 53' 21.6'' 6 85% 59 Talabe- Lafaneh1 N 33° 05' 14.7'' E 47° 42' 08.4'' 8 45% 60 Talabe- Lafaneh2 N 33° 05' 14.3'' E 47° 42' 14.1'' 8.5 50% 61 Valiasr Village N 33° 04' 56.4'' E 47° 41' 51.1'' 8 60% 62 Pole Dokhtar N 33° 05' 2.9'' E 47° 43' 46.1'' 5.5 55% 63 Saimareh River N 33° 50' 4.0'' E 47° 32' 11.4'' 4.5 85% 64 Novzhian Fall N 33° 17' 49.7'' E 48° 27' 52.5'' 5 85% 65 Nozhian Spring N 33° 15' 51.4'' E 48° 31' 22.3'' 8 85% 66 Nozhian N 33° 13' 32.0'' E 48° 33' 44.1'' 6 85% 67 Nozhian N 33° 17' 50.9'' E 48° 27' 41.6'' 7 55% 68 Nozhian N 33° 17' 53.8'' E 48° 27' 25.9'' 8 60% 69 Gol taft N 33° 17' 46.9'' E 48° 26' 42.9'' 8 65% 70 Sarabe-PirHassan N 33° 15' 28.2'' E 48° 27' 09.4'' 8 50% 71 Aligoodarz N 33° 26' 19.9'' E 49° 26' 51.0'' 7 65% 72 Abe sephid N 33° 21 34.9'' E 49° 44' 22.0'' 7 50% 73 Abesephid fall N 33° 07' 49.8'' E 49° 39' 29.9'' 6.5 85% 74 Abesephid N 33° 07' 50.3'' E 49° 39' 29.0'' 7 80% 75 Aligoodarz N 32° 59' 59.7'' E 49° 35' 20.2'' 7 55% 76 Razan N 35° 22' 19.32''E 49° 1' 43.62'' 8 50% 77 Abdarmani Spring N 35° 22' 11.10''E 49° 1' 41.52'' 7 80% 78 Ghahavand N 35° 5' 35.16''E 48° 58' 8.22'' 7.5 55% 79 Baban Village N 35° 12' 18.42''E 48° 46' 13.44'' 8 45% 80 Kaboodar Ahang Spring N 35° 12' 18.72'' E 48°46' 12.78'' 5.5 85% 81 N 34° 44' 55.38'' E 48° 26' 25.86'' 6 75% 82 Tarikdareh N 34° 43' 25.7''E 48° 26' 18.18'' 5.5 55% 83 Shahrestaneh Village N 34° 42' 49.92''E 48° 22' 21.84'' 7 55% 84 Hooshpil Village N 34° 39' 18.72''E 48° 22' 46.2'' 7 60% 85 Bili Spring N 34° 34' 12.54''E 48° 25' 51.96'' 7 85% 86 Chashkhore village N 34° 27' 54.72'' E 48° 16' 2.52'' 7 55% 87 Dehmosa Village N 34° 19' 3.15''E 43° 9' 30.48'' 6 50% 88 Shahrak Village N 34° 16' 25.68'' E 48°9' 3.30'' 6 50% 89 Rezini Village N 34° 15' 26.82'' E 48° 7' 56.76'' 8 50% 90 Rezini Village N 34° 15' 41.9''E 48° 7' 43.62'' 8 50% 91 Rezini Village N 34° 15' 32.04''E 46° 7' 15.605'' 8 50% 92 Sarabe- Farsban N 34° 15' 32.10''''E 48° 7' 15.6'' 6 65% 93 Sarabe- Gian N 35° 22' 11.10''E 49° 1' 41.52'' 7.5 60% 94 Meriyanaj N 34° 48' 17.70'' E 48° 23' 28.62'' 6 55% 95 Gian Village N 34° 52' 84''E 48° 24' 5.40'' 6 50% 96 Saleh abad Village N 34° 55' 22.26'' E 48°19' 49. 08'' 7.5 60% 97 Hassan gheshlagh Village N 34° 55' 22.14'' E 48° 19' 49.14'' 6 55% 98 Saleh abad N 34° 57' 13.44''E 48° 20' 19.56'' 6.5 45% 99 Malham dareh N 34° 49' 47.82''E 48° 8' 37.02'' 7 60% 100 Asad abad N 34° 48' 59.9''''E 48° 5' 54.48'' 7 70% 101 Viraii Village N 34° 43' 3.66''E 48° 13' 16.68'' 7 50% 102 Alvand N 34° 43' 3.54''E 48° 13' 16.56'' 7 50% 103 Ganjnameh Fall N 34° 45' 46.38''E 48° 26' 13.98'' 6.5 85% 104 Moradbeig N 34° 44' 33.12''E 48° 30' 8.64'' 7 60% 105 Alvand N 34° 44' 33.12''E 48° 40' 8.64'' 7 55%