Abstract
This paper includes the summarized knowledge (of more than 40 years) on earthworms in Central Serbia, in the middle part of the Balkan Peninsula. The aim of this paper is to present new data on the earthworms for the study area. Also by analysing the newly reported species together with literature records, we establish the definitive list of known earthworm taxa. The list underlines earthworm diversity and provides a general overview of their distributions, zoogeographical positions, levels of dominance and ecological categories. During the current investigations in the different parts of Central Serbia, 36 earthworm species and subspecies belonging to 10 genera were recorded. Among them, 4 taxa represented the first findings in Central Serbia: Bimastos parvus (Eisen, 1874) Bimastos eiseni (Levinsen, 1884) Aporrectodea cemernicensis Mršić, 1991 and Lumbricus castaneus (Savigny, 1826). Consequently, the number of the earthworm species recorded for Central Serbia is raised to 46. Surprisingly, the peregrine B. parvus proved to be new species in the fauna of Serbia, including the study area, so now the total number of species for the whole Serbia has risen to 75. With respect to the zoogeographic situation, the majority of them belong to peregrine (36.96%), endemic (19.57%), and trans-Aegean species (13.04%). Summing up the endemics and Balcanic-Alpine species, 30.44% of the total lumbricid fauna in Central Serbia shows an autochthonous character.
Similar content being viewed by others
References
Blakemore RJ (2007) Japanese earthworms. In: Ito M, Kaneko N (eds) A series of searchable texts on earthworm biodiversity, ecology and systematics from various regions of the world. Yokohama National University, Tokiwadai. Yokohama, Japan
Blakemore RJ (2008) Cosmopolitan earthworms: an eco-taxonomic guide to the species, 3rd edn. Verm Ecology, Yokohama
Bouché MB (1972) Lombriciens de France. Écologie et sysématique. Institut National de la Recherche Agronomique, Articles de Zoologie-Écologie animale (Numéro hors-série)
Bouché MB (1977) Strategies lombriciennes. Ecological Bulletin Stockholm 25:122–132
Csuzdi CS, Zicsi A (2003) Earthworms of Hungary. Pedozoologica Hungarica No 1. Hungary: Natural History Museum and Hungary Academy of Sciences, Budapest
Csuzdi CS, Zicsi A, Mısırlıoğlu M (2006) An annotated checklist of the earthworm fauna of Turkey (Oligochaeta: Lumbricidae). Zootaxa 1175:1–29
Csuzdi CS, Pop VV, Pop AA (2011) The earthworm fauna of the Carpathian Basin with new records and description of three new species (Oligochaeta: Lumbricidae). Zool Anz 250:2–18. https://doi.org/10.1016/j.jcz.2010.10.001
Cvijić J (1922) Balkansko poluostrvo i južnoslovenske zemlje. Hrvatski Štamparski Zavod, Zagreb
EEA - Eur Environ Agency (2011) Biogeographic regions dataset. http://www.eea.europa.eu/data-andmaps/data/ds_resolveuid/b2515476c53448d39b499915cd34dde7. Accessed 6 June 2018
Fedorovich CV (1991) Fauna, landscape and habitat distribution of earthworms (Lumbricidae, Oligochaeta) in the Prutdniester River Bassins. Dissertation, Academy of Sciences of the Moldavian SSR, Chișinău, Moldova
Hackenberger DK, Hackenberger BK (2013) Checklist of the earthworm fauna of Croatia (Oligochaeta: Lumbricidae). Zootaxa 3710:1–30. https://doi.org/10.11646/zootaxa.3710.1.1
ISO 2361 (2005) Soil quality — Sampling of soil invertebrates — Part 1: Hand-sorting and formalin extraction of earthworms
Jakšić P (2008) Prime Butterfly Areas: A Tool for Nature Conservation in Serbia. HabiProt, Belgrade, Serbia
Karaman S (1972) Beitrag zur Kenntnis der Oligochaetenfauna Jugoslawiens. Biloški Vestnik 20:95–105
Karaman S (1983) The third contribution to the knowledge of the earthworms of Serbia. II Simpozijum о fauni SR Srbije. Zbornik, pp 51–53
Karaman S (1987) The fourt contribution to the knowledge of the earthworms of Serbia. Biosistematika 13:69–72
Karaman S, Stojanović M (1993) Аutekološka analiza lumbricida (Oligochaeta) okoline Kragujevca. Zbornik radova PMF 15:105–113
Karaman S, Stojanović M (1994) Kišne gliste južne Srbije. III Simpozijum o flori Jugoistiočne Srbije, Zbornik, pp 185–193
Karaman S, Stojanović M (1995) Contribution to the knowledge on the earthworms (Oligochaeta: Lumbricidae) in Montenegro. Arch Biol Sci 47:139–143
Karaman S, Stojanović M (1996a) New earthworm (Oligochaeta, Lumbricidae) records from Serbia (Yugoslavia). Bios 4:7–13
Karaman S, Stojanović M (1996b) Diverzitet faune kišnih glista Jugoslavije sa posebnim pregledom vrsta međunarodnog značaja. Biodiverzitet Jugoslavije 1:285–291
Karaman S, Stojanović M (1998) Biodiversity of Lumbricidial fauna (Oligochaeta, Lumbricidae) in valley meadows in Kragujevac depresion. In: Second international congress of the biodiversity, ecology and conservation of the Balcan fauna. Ohrid, Macedonia, p 99
Karaman S, Stojanović M (2002) Treći prilog poznavanja kišnih glista (Oligochaeta, Lumbricidae) južne i jugoistočne Srbije. VII Simpozijum o flori jugoistočne Srbije i susednih područja. Zbornik, pp 223–225
Karaman S, Stojanović M, Pešić S (1998) Promene biodiverziteta lumbricidne faune (Oligochaeta: Lumbricidae) u uslovima sukcesivne smene dolinskih livada Kragujevačke kotline. Ekologija 33:85–88
Kostecka J (1997) Ecology of Allolobophora cernosvitoviana, a species new for the polish earthworms fauna. Siol Biol Biochem 29:259–263
Kostecka J, Skoczeń S (1993) Earthworm (Oligochaeta: Lumbricidae) populations in four types of beech wood Fagetum carpaticum in the Bieszczady National Park (South-Eastern Poland). Part I. species composition, diversity, dominance, fre-quency and associations. Acta Zool Cracov 36:1–13
Lavelle P, Decaën T, Aubert M, Barot S, Blouin M, Bureau F, Margerie P, Mora P, Rossi JP (2006) Soil invertebrates and ecosystem services. Eur J Soil Biol 42:S3–S15. https://doi.org/10.1016/j.ejsobi.2006.10.002
Milutinović T (2014) Zoogeografija, diverzitet i konzervacioni status Lumbricidae (Annelida) zapadne Srbije. Dissertation, University of Kragujevac, Serbia
Milutinović T, Avramović S, Pešić S, Blesić B, Stojanović M, Mitrovski-Bogdanović A (2010) Contribution to the knowledge of pedofauna in Šumadija (Central part of Serbia). Biotechnol Biotechnol Equip 24:628–635. https://doi.org/10.1080/13102818.2010.10817911
Milutinović T, Milanović J, Stojanović M (2015a) Application of species richness estimators for the assessment of earthworm diversity. J Nat Hist 49:273–283. https://doi.org/10.1080/00222933.2013.791947
Milutinović T, Milanović J, Stojanović M (2015b) Threat status and distribution of the endemic species Allolobophora kosowensis kosowensis Karaman, 1968 (Oligochaeta, Lumbricidae) in the Balkans. J Nat Hist 49:471–481. https://doi.org/10.1080/00222933.2013.791946
Mršić N (1991) Monograph on Earthworms (Lumbricidae) of the Balkans I-II. SAZU, Ljubljana
Omodeo P (1989) Earthwoems of Turkey. Boll Zool 56:167–199. https://doi.org/10.1080/11250008909355639
Omodeo P, Rota E (1991) Earthworms of Turkey II. Boll Zool 58:171–181. https://doi.org/10.1080/11250009109355749
Perel TS (1964) Rasprostranenie doždovych červej (Lumbricidae) v ravninych lesach evropejskoj časti SSSR. Pedobiologia 4:92–110
Perel TS (1976) A critical analysis of the Lumbricidae genera system (with key to the USSR fauna genera). Révue d'Écologie et Biologie du Sol 13:635–643
Pop VV (1997) Earthworm vegetation soil relationships in the Romanian Carpathians. Soil Biol Biochem 29:223–229
Pop AA, Pop VV, Csuzdi CS (2010) Significance of the Apuseni Mountains (the Carpathians) in the origin and distribution of Central European earthworm fauna (Oligochaeta: Lumbricidae). Zool Middle East 51(Suppl 2):89–110. https://doi.org/10.1080/09397140.2010.10638462
Rota E (2005) Fauna Europaea, Oligochaeta, Lumbricidae. Fauna Europaea version 1.2. http://www.faunaeur.org. Accessed 26 June 2018
Rozen A, Kostecka J (1988) Allolobophora cernosvitoviana (Zicsi, 1967) (Oligochaeta, Lumbricidae), a new species of earthworm in Poland. Przegl Zool 32:199–202
Salomé C, Guenat C, Bullinger-Weber G, Gobat JM, Le Bayon RC (2011) Earthworm communities in alluvial forests: influence of altitude. vegetation stages and soil parameters Pedobiologia 54:S89–S98. https://doi.org/10.1016/j.pedobi.2011.09.012
Šapkarev J (1978) Kišne gliste Jugoslavije. Sadašnja taksonomska proučenost i njihova dalja istraživanja Biosistematika 4:293–304
Šapkarev J (1980) Prilog poznavanju kišnih glista (Lumbricidae) SR Srbije. Zbornik radova faune Srbije 1:165–179
Šapkarev J (1988) Contribution to the knowledge of the earthworm fauna of Serbia, Yugoslavia (Lumbricids of Šumadija). Fragmenta Balcanica 5:17–24
Šapkarev J (2002) Rasprostranjenje kišnih glista središnje Srbije. Zbornik radova o fauni Srbije SANU 6:307–318
Savić I (2008) Diversification of the Balkan fauna: Its origin, historical development and present status. In: Makarov SE, Dimitrijević RN (eds) Advances in arachnology and developmental biology. Serbia, SASA Publishing, Belgrade, pp 57–79
Schwerdtfeger F (1975) Ökologie der Tiere, Band 3: Synökologie. Verlag Paul Parey. Hamburg und Berlin
Sekulić J (2017) Faunistička i ekotoksikološka studija Lumbricidae (Annelida: Oligochaeta) centralne Srbije. Dissertation, University of Kragujevac, Serbia
Stojanović M (1989) Istraživanja kišnih glista okoline Kragujevca. III Simpozijum o fauni SR Srbije Zbornik rezimea 23
Stojanović M (1996) Faunističko-ekološka studija Lumbricida (Oligochaeta) Srbije. Dissertation, University of Kragujevac, Serbia
Stojanovic M, Karaman S (2003) Second contribution to the knowledge of earthworms (Lumbricidae) in Montenegro. Arch Biol Sci 55(1-2):55–58
Stojanović M, Karaman S (2005) Further contribution to the knowledge of the earthworms of Šumadija. Arch Biol Sci 57:127–133 https://doi.org/10.2298/ABS0502127S
Stojanović M, Karaman S (2006) Threat status and distribution of the earthworm genus Helodrilus Hoffmeister, 1845; sensu Zicsi 1985, on the Balkans and the neighboring regions. Biodivers Conserv 15:4601–4617. https://doi.org/10.1007/s10531-005-5823-9
Stojanović M, Karaman S (2007) Distribution of endemic species from the earthworm genus Serbiona (Oligochaeta, Lumbricidae) in Serbia. Arch Biol Sci 59:23–24 https://doi.org/10.2298/ABS0702001S
Stojanović M, Milutinović T (2014) The earthworms (Oligochaeta: Lumbricidae) of the Pannonian region of Serbia, Vojvodina Province: zoogeography and diversity. North-West J Zool 10:305–313
Stojanović M, Milutinović T, Karaman S (2008) Earthworm (Lumbricidae) diversity in the Central Balkans: an evaluation of their conservation status. Eur J Soil Biol 44:54–67. https://doi.org/10.1016/j.ejsobi.2007.09.005
Stojanović M, Sekulić J, Trakić T (2017) Distribution and threat status of endemic earthworm Allolobophora dofleini (Oligochaeta, Lumbricida) on the Balkan Peninsula. North-West J Zool 13(1):136–143
Stojanovic Petrovic M, Trakic T, Sekulic J (2017) Earthworms (Annelida: Oligochaeta) of Kragujevac basin: A review. Kragujevac J Sci (39):177–192
Stojanović M, Sekulić J, Trakić T (2018) Checklist of earthworms (Oligochaeta: Lumbricidae) from Serbia: a review. Zootaxa 4496(1):124–155. https://doi.org/10.11646/zootaxa.4496.1.9
Szederjesi T (2013) New earthworm records from the former Yugoslav countries (Oligochaeta: Lumbricidae). Opusc Zool Budapest 44:61–76
Szederjesi T, Csuzdi CS (2012) New earthworm species and records from Albania (Oligochaeta, Lumbricidae). Acta Zool Acad Sci Hung 58:259–274
Szederjesi T, Pop V, Csuzdi C (2014) New and little known earthworm species from peripheral areas of the Romanian Carpathians (Oligochaeta, Lumbricidae). Acta Zool Hung 60:85–107
Tischler W (1949) Grundzüge der terrestrischen Tierökologie. Fridrich Vieweg, Braunschweig
Trakić T, Valchovski H, Stojanović M (2016) Endemic earthworms (Oligochaeta: Lumbricidae) of the Balkan Peninsula: a review. Zootaxa 4189(2):251–274. https://doi.org/10.11646/zootaxa.4189.2.3
Valchovski H (2012) Checklist of earthworms (Oligochaeta: Lumbricidae) from Bulgaria: a review. Zootaxa 3458:86–102
Valchovski H (2017) New data on the distribution of earthworms (Oligochaeta: Lumbricidae) in Bulgaria, with the first record of Proctodrilus opisthoductus Zicsi, 1985 in the country. Acta Zool Bulgar 69:441–443
Zajonc I (1970) Synúzie dažďoviek (Lumbricidae) na lúkach Karpatskej oblasti Československa. Biologické práce 16:5–98
Zicsi A (1967) Beitrage zur Kenntnis der Ungarichen Lumbriciden Fauna. V. Acta Zool Hung 13:245–252
Zicsi A (1972) Ein neuer Wiederfund von Allolobophora dofleini Ude, 1922. Annales Universitatis Scientarium Budapestiensis de Rolando Eötvös Nominatae 14:241–245
Zicsi A (1985) Über die Gattungen Helodrilus Hoffmeister 1845 und Proctodrilus gen. n. (Oligochaeta, Lumbricidae). Acta Zool Hung 31:275–289
Zicsi A, Michalis K (1981) Übersicht der Regenwurm-fauna Griechenlands (Oligochaeta: Lumbricidae). Acta Zool Hung 27:239–264
Zicsi A, Michalis K (1993) Zwei neue Dendrobaena-Arten aus Griechenland (Oligochaeta: Lumbricidae). Acta Zool Hung 39:301–310
Zicsi A, Szlavecz K, Csuzdi CS (2011) Leaf litter acceptance and cast deposition by peregrine and endemic European lumbricids (Oligochaeta: Lumbricidae). Pedobiologia 54S:S145–S152. https://doi.org/10.1016/j.pedobi.2011.09.004
Acknowledgements
This work was supported by the Ministry of Education and Science of the Republic of Serbia (Grant No. 41010).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
ESM 1
(DOCX 26.2 kb)
Rights and permissions
About this article
Cite this article
Stojanović, M., Trakić, T. & Sekulić, J. New and additional records of earthworms (Annelida: Clitellata) from Central Serbia: First finding of Bimastos parvus (Eisen, 1874) in Serbia. Biologia 74, 269–278 (2019). https://doi.org/10.2478/s11756-018-00170-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.2478/s11756-018-00170-2