The tubificids (Annelida, Oligochaeta) of Lake Trasimeno and Lake Piediluco in Central Italy, with a study of SEM morphology of some species

Enzo GORETTI, Caterina MARCUCCI, Alessandra DI VEROLI, Angelisa FABRIZI, Elda GAINO
477 115


Freshwater oligochaetes are studied worldwide because of their relevance as bioindicators in aquatic ecosystems. Nevertheless, species identification is still difficult because it is mainly based on the male reproductive system. The morphology of the chaetae offers an additional set of characters and the fine organization of these elements can help in solving crucial aspects allowing specific attribution. In spite of this, somatic chaetae are poorly investigated under scanning electron microscopy (SEM). A SEM analysis of the chaetae has been carried out on the tubificids Branchiura sowerbyi, Limnodrilus hoffmeisteri, Tubifex tubifex, and Psammoryctides barbatus from Trasimeno and Piediluco lakes (Central Italy). In particular, the chaetal pattern of B. sowerbyi is comparable to that described for specimens from the tropical regions of Asia, and T. tubifex shows the chaetal pattern typical of the nominal species; the palmate chaetae of P. barbatus are characterized by 15-20 fringes, each of them with a distal end thinner and folded backwards. In addition, B. sowerbyi is the dominant species in Lake Trasimeno, whereas it is lacking in Lake Piediluco, where the tubificids are primarily represented by T. tubifex.


Key words: Tubificids, chaetae, scanning electron microscopy

Full Text:



Arslan N, Şahìn Y (2006). A preliminary study on the identification of the littoral oligochaete (Annelida) and Chironomidae (Diptera) fauna of Lake Kovada, a national park in Turkey. Turk J Zool 30: 67–72.

Beauchamp KA, Kathman RD, McDowell TS, Hedrick RP (2001). Phylogeny of tubificid oligochaetes with special emphasis on Tubifex tubifex (Tubificidae). Mol Phylogenet Evol 19: 216–224.

Bouché ML, Biagianti-Risbourg S, Arsac F, Vernet G (1999a). An original decontamination process developed by the aquatic oligochaete Tubifex tubifex exposed to copper and lead. Aquat Toxicol 45: 9–17

Bouché ML, Biagianti-Risbourg S, Vernet G (1999b). A light and scanning electron microscope study of the morphology of the chaetae of Tubifex tubifex in a non-polluted medium. Hydrobiologia 411: 39–44.

Bouché ML, Habets F, Biagianti-Risbourg S, Vernet G (2000). Toxic effects and bioaccumulation of cadmium in the aquatic oligochaete Tubifex tubifex. Ecotox Environ Safe 46: 246–251.

Brinkhurst RO (1971). A guide for the identification of British aquatic Oligochaeta. Freshwater Biological Association Scientific Publication No. 22. Kendal, UK: Wilson and Sons.

Brinkhurst RO (1996). On the role of tubificid oligochaetes in relation to fish disease with special reference to the Myxozoa. Annu Rev Fish Dis 6: 29–40.

Brinkhurst RO, Gelder SR (2001). Annelida: Oligochaeta, including Branchiobdellidae. In: Thorp JH and Covich AP, editors. Ecology and Classification of North American Freshwater Invertebrates. 2nd ed. San Diego, CA, USA: Academic Press, pp. 431–463.

Brinkhurst RO, Jamieson BG (1971). The Aquatic Oligochaeta of the World. Edinburgh, UK: Oliver and Boyd.

Campaioli S, Ghetti PF, Minelli A, Ruffo S (1994). Manuale per il riconoscimento dei macroinvertebrati delle acque dolci italiane. Vol. 1°. Trento, Italy: Provincia Autonoma di Trento (in Italian).

Caramelo C, Martinez-Ansemil E (2012). Morphological investigations of microdrile oligochaetes (Annelida, Clitellata) using scanning electron microscopy. Turk J Zool 36: 1–14.

Chapman PM (2001). Utility and relevance of aquatic oligochaetes in ecological risk assessment. Hydrobiologia 463: 149–169.

Chapman PM, Brinkhurst RO (1984). Lethal and sublethal tolerances of aquatic oligochaetes with reference to their use as a biotic index of pollution. Hydrobiologia 115: 139–144.

Chapman PM, Brinkhurst RO (1986). Setal morphology of the oligochaetes Tubifex tubifex and Ilyodrilus frantzi (Capillatus) as revealed by SEM. Proc Biol Soc Wash 99: 323–327.

Chapman PM, Brinkhurst RO (1987). Hair today, gone tomorrow: induced chaetal changes in tubificid oligochaetes. Hydrobiologia 115: 45–55.

Crottini A, Marotta R, Barbuto M, Casiraghi M, Ferraguti M (2008). The world in a river? A preliminary analysis of the 16S rDNA variability of Tubifex species (Clitellata: Tubificidae) from the Lambro River. Mol Phylogenet Evol 48: 1189–1203.

Di Veroli A, Selvaggi R, Goretti E (2012). Chironomid mouthpart deformities as indicator of environmental quality: a case study in Lake Trasimeno (Italy). J Environ Monitor 14: 1473–1478.

Di Veroli A, Selvaggi R, Pellegrino RM, Goretti E (2010). Sediment toxicity and deformities of chironomid larvae in Lake Piediluco (Central Italy). Chemosphere 79: 33–39.

Drake CM, Elliott JM (1982). A comparative study of three air-lift samplers used for sampling benthic macro-invertebrates in rivers. Freshwater Biol 12: 511–533.

Egeler P, Römbke J, Meller M, Knacker T, Nagel R (1999). Bioaccumulation test with tubificid sludgeworms in artificial media – development of a standardisable method. Hydrobiologia 406: 271–280.

Envall I, Gustavsson LM, Erséus C (2012). Genetic and chaetal variation in Nais worms (Annelida, Clitellata, Naididae). Zool J Linn Soc-Lond 165: 495–520.

Erséus C, Wetzel MJ, Gustavsson L (2008). ICZN rules – a farewell to Tubificidae (Annelida, Clitellata). Zootaxa 1744: 66–68.

Finogenova NP, Arkhipova NR (1994). Morphology of some species of the genus Aulodrilus Bretscher. Hydrobiologia 278: 7–15.

Holmquist C (1983). What is Tubifex tubifex (O.F. Müller) (Oligochaeta, Tubificidae)? Zool Scr 12: 187–201.

Ladle M, Bird GJ (1984). The biology of Psammoryctides barbatus (Grube) in English chalk streams. Hydrobiologia 115: 109–112.

Lauritsen DD, Mozley SC, White DS (1985). Distribution of oligochaetes in Lake Michigan and comments on their use as indices of pollution. J Great Lakes Res 11: 67–76.

Lom J, Dykovà I (2006). Myxozoan genera: definition and notes on taxonomy, life cycles terminology and pathogenic species. Folia Parasit 53: 1–36.

Ludovisi A, Gaino E (2010). Meteorological and water quality, changes in Lake Trasimeno (Umbria, Italy) during the last fifty years. J Limnol 69: 174–188.

Marcucci C, Caffara M, Goretti E (2009). Occurrence of actinosporean stages (Myxozoa) in the Nera River system (Umbria, central Italy). Parasitol Res 105: 1517–1530.

Martin P, Martinez-Ansemil E, Pinder A, Timm T, Wetzel MJ (2008).

Global diversity of oligochaetous clitellates (Oligochaeta; Clitellata) in freshwater. Hydrobiologia 595: 117–127. Milbrink G (1983a). An improved environmental index based on the relative abundance of the oligochaete species. Hydrobiologia 102: 89–97.

Milbrink G (1983b). Characteristic deformities in tubificid oligochaetes inhabiting polluted bays of Lake Vänern, Southern

Sweden. Hydrobiologia 106: 169–184. Milbrink G (1994). Oligochaetes and water pollution in two deep Norwegian lakes. Hydrobiologia 278: 213–222.

Milbrink G, Timm T, Lundberg S (2002). Indicative profundal oligochaete assemblages in selected small Swedish lakes. Hydrobiologia 468: 53–61.

Ohtaka A, Nishino M (1999). Studies on the aquatic oligochaete fauna in Lake Biwa, Central Japan. II. Records and taxonomic remarks of nine species. Hydrobiologia 406: 33–47.

Paunović M, Miljanović B, Simić V, Cakić P, Djikanović V, JakovčevTodorović, Stojanović D, Veljković B (2005). Distribution of non-indigenous tubificid worm Branchiura sowerbyi (Beddard, 1892) in Serbia. Biotechnol Biotec Eq 3: 91–97.

Pearson RG, Litterick MR, Jones NV (1973). An air-lift for quantitative sampling of the benthos. Freshwater Biol 3: 309–315.

Posati S (2003). Il lago di Piediluco. Analisi e metodi di tutela. ARPA

Umbria, Agenzia Regionale per la Protezione Ambientale. Perugia, Italy: Cornicchia Grafiche (in Italian). Raposeiro PM, Ramos JC, Costa AC (2009). First record of Branchiura sowerbyi Beddard, 1892 (Oligochaeta: Tubificidae) in Azores. Aquatic Invasions 4: 487–490.

Rota E (2008). Oligochaeta. Biol Mar Mediterr 15: 380–385.

Svensson JM, Enrich-Prast A, Leonardson L (2001). Nitrification and denitrification in a eutrophic lake sediment bioturbated by oligochaetes. Aquat Microb Ecol 23: 177–186.

Swayne H, Day M, Wetzel MJ (2004). Limnodrilus hoffmeisteri

(Annelida: Oligochaeta: Tubificidae) in Pop’s Cave, Wisconsin, USA. J Cave Karst Stud 66: 28–31. Tachet H, Richoux P, Bournaud M, Usseglio-Polatera P (2010). Invertébrés d’eau douce. Systématique, biologie, écologie. Paris, France: CNRS Éditions (in French).

Timm T (1980). Distribution of aquatic oligochaetes. In: Brinkhurst RO, Cook DG, editors. Aquatic Oligochaete Biology. New York, NY, USA: Plenum Press, pp. 55–77.

Timm T (2012). About the scientific names of paraphyletic taxa. Turk J Zool 36: 139–140.

Wolf K, Markiw ME (1984). Biology contravenes taxonomy in the Myxozoa: new discoveries show alternation of invertebrate and vertebrate hosts. Science 225: 1449–1452.