An updated list of chironomid species from Italy with biogeographic considerations (Diptera, Chironomidae)

Author(s): Rossaro, Bruno; Pirola, Niccolo; Marziali, Laura; Magoga, Giulia; Boggero, Angela; Montagna, Matteo | Abstract: In a first list of chironomid species from Italy from 1988, 359 species were recognized. The subfamilies represented were Tanypodinae, Diamesinae, Prodiamesinae, Orthocladiinae and Chironominae. Most of the species were cited as widely distributed in the Palearctic region with few Mediterranean (6), Afrotropical (19) or Panpaleotropical (3) species. The list also included five species previously considered Nearctic. An updated list was thereafter prepared and the number of species raised to 391. Species new to science were added in the following years further raising the number of known species. The list of species known to occur in Italy is now updated to 580, and supported by voucher specimens. Most species have a Palearctic distribution, but many species are distributed in other biogeographical regions; 366 species are in common with the East Palaearctic region, 281 with the Near East, 248 with North Africa, 213 with the Nearctic, 104 with the Oriental, 23 species with the Neotropical, 23 with the Afrotropical, 16 with the Australian region, and 46 species at present are known to occur only in Italy. On the basis of new findings in Italy and in nearby areas it is stated that the knowledge of chironomid fauna is still incomplete.


INTRODUCTION
Research on Chironomidae in Italy began in 1900 (Bezzi 1918), but with the exception of a few contributions (Marcuzzi 1949) the study of chironomids in Italy had a substantial progress only after the publication of the identification keys for their aquatic stages, larvae and pupae (Ferrarese and Rossaro 1981, Rossaro 1982a, Ferrarese 1983, Nocentini 1985. Information on species presence and distribution was very scanty before 1968, grew slowly up to 1976 and, in the following 30 years, the number of species known from Italy increased steeply. The list of species belonging to the subfamily of Orthocladiinae was reviewed by Rossaro (1979Rossaro ( , 1992a and of other subfamilies by Ferrarese (1982). Thereafter an updated list of species (Boormann et al. 1995, Ferrarese andRossaro 2001) had been made available on the website of the Checklist of the Italian Fauna (URL 1), but unfortunately, since its publication, the information present in this website has not been updated. Meanwhile revisions of some genera including also the adult stage were carried out (Rossaro 1992b, Rossaro and Lencioni 2000, Rossaro et al. 2003, Rossaro 2017). In addition, the distribution of chironomids in running waters (Rossaro et al. 2006) and in glacial areas (Rossaro et al. 2016) gave other contributions to the knowledge of Italian fauna. Chironomid research covers systematic, biogeographic and ecological problems. Italy is in the centre of the Mediterranean area, representing a natural bridge between Central Europe and Africa. In Italy, several very different water types and biotopes can be investigated: cold springs, glacier and alpine streams, large lakes (Garda, Maggiore, Como), large rivers (Po, Adige, Ticino, Adda, etc.), Mediterranean streams, brackish waters (Boggero et al. 2017), and coastal lakes. A very long list of species is to be expected and this is indeed the case, although at present the continuous progress suggests that chironomid knowledge is still very incomplete in Italy, as is in other regions including the relatively well studied West Palaearctic area.
The sampling effort pursued during recent decades was well below the need to have a uniform coverage across the country; entire regions such as Calabria and Basilicata are still almost unstudied (Fig. 1), while others were sampled only in very restricted periods (Sardegna, Sicilia). Only Lombardia, Valle d'Aosta, Trentino Alto Adige and Abruzzo were sampled with a reasonable frequency.
Water pollution of domestic and industrial origin, the capture of springs and the creation of reservoirs for water supply are unfavourable factors for the preservation of an autochthonous, highly diversified fauna and there is a serious risk that some species will disappear before being discovered. On the other hand, many eurytopic and euryoecious species may be favoured. The large spread of insecticides and water drainage to fight malaria in the Mediterranean countries after the Second World War significantly reduced the species living in marshes. Global warming with the risk of total disappearance of glacial areas is also a very serious matter of concern.
Chironomids are a very ancient group going back to the Triassic or even earlier (Cranston et al. 2012) so the possibility of dispersion in terms of available time was significant, but the stringent ecological needs of stenoecious species suggest a rather restricted distribution with possible endemism and risk of species extinctions. For this reason, chironomids provide an excellent system to study biogeographic questions.
The aim of the present paper is to give an updated list of the species present in Italy.

MATERIALS AND METHODS
The list of species is based on determinations of adult males when available, but some species are known only on the basis of pupal exuviae; in fewer cases only the larvae are available. Samples were collected with hand-nets, light traps, surface drift nets, and kick samplers (Rossaro 1982a). Larvae were collected alive in some sites and reared to adults in the laboratory under controlled conditions. In laboratoryreared material, larvae and pupae are associated with adults; this procedure is highly recommended, but requires a lot of experimental effort.  The species identified were mounted on slides according to Wirth and Marston (1968) and Rossaro et al. (2017). Most of the slides are deposited in the corresponding author's (Rossaro) personal collection. Some voucher specimens are deposited in the Ferrarese personal collection and at the Museo delle Scienze (Trento), Sergentia sp. is deposited in the CNR IRSA (Verbania Pallanza) collection and H. mediterraneus is deposited in the Senckenberg Naturmuseum Frankfurt (Germany) (Hirvenoja 1973).
Sampling efforts were made in different Italian regions, but Lombardia has been the most intensively sampled. The sites in which the most intensive sampling was carried out are shown in Figure 1, but sampling was carried out also in many other sites. Each sampling site can include many different stations and covers a large area. In some sampling sites, as in Ortles-Adamello (6), River Po (10), River Taro (12), Parco Nazionale d'Abruzzo (19) (see Figure 1), captures were made throughout the year. Sites sampled only at intervals are not reported in Figure 1.

RESULTS
A total of 580 species are now known to occur in Italy (Table 1, Table 2) and their distributions in Europe and in areas outside Europe are cited on the Fauna Europaea website (de Jong et al. 2014, URL 5). Other 28 species were previously cited as occurring in Italy (Boormann et al. 1995, Ferrarese andRossaro 2001), but at present we consider these species as misidentifications.
The discussion about the distribution of species is based on the information present in the Fauna Europaea website (URL 5), but this information has been updated considering contributions published later (Bitušík and Trnková 2019 It is well accepted that chironomid species distribution can be explained both by ecological and by biogeographical reasons. Cold-stenothermal species are restricted to highlands (most Diamesinae and a part of Orthocladiinae): species belonging to these two subfamilies are widespread in the Alps (Region 4) (Illies 1978, Fittkau and Reiss 1978, Griffith 2006, and many of them are also present in cold countries of Northern Europe. For some species a boreo-alpine vicariance has been proposed: Diamesa arctica (Boheman, 1865) is restricted to Scandinavia, while D. goetghebueri to the Alps, but new findings such as the presence of D. lindrothi in the Alps, contradicted the hypothesis that this species was restricted to the Arctic. Many species found in the Alps are not present in the Apennines, this is likely linked to the lack of glaciers in the latter (Rossaro et al. 2006).
The progress of knowledge in recent decades has been intensive. Three species (Syndiamesa nigra, Tokunagaia tonollii and Stilocladius montanus) were first reported as present only on the southern side of the Italian Alps, but not on the northern one (Rossaro 1988); S. montanus was also cited as present in the Apennines (Rossaro 1984). This supported the existence of cold-stenothermal species with an endemic distribution on the southern side of the Alps or with a wider southern distribution. To support this hypothesis it was observed that there were other cold-stenothermal species in the Mediterranean area belonging to the coldstenothermal genus Diamesa Lencioni 2015, Montagna et al. 2016a) as D.
lavillei Serra-Tosio, 1970 andD. thomasi Serra-Tosio, 1970 cited to be known only from the Pyrenees (Serra-Tosio 1973). To contradict this hypothesis new findings were highlighted; for example, D. veletensis Serra-Tosio, 1971 previously considered endemic from the Sierra Nevada (Spain) was later captured in the Atlas Mountains (Morocco) and in Mongolia, suggesting that the cited species has a much wider distribution including southern and oriental parts of the Palearctic Region (Serra-Tosio 1983). Diamesa thomasi was captured in Germany and Poland and D. lavillei in the Near East and Caucasus. The area of distribution of T. tonollii has been enlarged including England, Scandinavia and the Far East (Makarchenko and Makarchenko 2007) and the area of distribution of S. montanus was enlarged to include the northern side of the Alps, Spain, Germany, and Slovakia. The capture of other species of Stilocladius (S. clinopecten Saether, 1982) in the southeastern United States, S. intermedius and S. orientalis Makarchenko et Makarchenko, 2003(Wang 1998, Makarchenko and Makarchenko 2003 in the Eastern Palaearctic, Eastern European Russia and Finland, further supported the evidence of a much wider distribution of these species. To sum up, even if the existence of endemic species cannot be excluded, the progression of knowledge suggests a large area of distribution for many species. The lack of substantial differences in species composition of lakes on the northern and southern sides of the Alps convinced us that the Alps are not a zoogeographical barrier for chironomids, as suggested half a century ago (Reiss 1968) and confirmed by more recent contributions (Reiss 1986b, Laville andSerra-Tosio 1996, URL 2, URL 3).
The percentage of Mediterranean, Afroand Panpaleotropical species in Italy is of interest.
The halobiont species Baeotendipes noctivagus and Halocladius millenarius were included in the Mediterranean faunal component (Reiss 1977), but the former species is now also known from Bulgaria, Romania and Ukraine, while the latter is also present in the Canary Islands. Another Halocladius species is cited from Italy (H. mediterraneus), Corsica, Near East, Spain, Madeira Isle, so this species seems restricted to the Mediterranean area and Madeira. Other species captured in Italy and previously considered endemic Mediterranean species (Reiss 1977), but now known to have a more extended area, are: Virgatanytarsus albisutus, present also in Madeira, Canary Islands and Portugal, Polypedilum acifer Townes, 1945 which results widespread in Europe and present also in the Nearctic, while Harnischia angularis is widespread in Europe and present also in the Eastern Palaearctic and Oriental regions.
About Afro-and Panpaleotropical species, two species previously known with a Panpaleotropical distribution (Reiss 1985(Reiss , 1986a now extend their presence to the Mediterranean region and are restricted to southern areas in Italy. They are Chironomus calipterus, found in Sardegna, and Dicrotendipes peringueyanus, in Sicily. Polypedilum aegyptium was supposed to have an Afrotropical distribution, but was collected in northern Italy (Rossaro 1988); after a revision of the species it was discovered that it had been captured also in Sweden and in other 14 European countries. Pseudosmittia subtrilobata was supposed to be an Afrotropical species, but was captured in Sardegna (Boormann et al. 1995); a re-examination of the material deposited in the corresponding author's collection suggests P. subtrilobata is a junior synonym of P. trilobata even if they are both still considered valid species (Ferrington and Saether 2011). Another formerly supposed Afrotropical species is Tanytarsus formosanus Kieffer, 1911(= T. horni Goetghebuer, 1934, reported from Sicilia by Reiss (1977) and recently captured in other 7 European countries, as in Oriental and Australian regions; yet, no voucher specimens are available in the corresponding author's collection so its presence in Italy should be confirmed.
The following species are reported only from Italy in Fauna Europaea, but they are present outside Europe in other regions: Cricotopus (Paratrichocladius) pierfrancescoi presently known from the Eastern Palaearctic; Euryhapsis annuliventris present in the Nearctic, Hydrobaenus dentistylus present in the Near East, Limnophyes algerinus present in North Africa, Stenochironomus spatuliger known to occur in different Afrotropical countries (Freeman 1957), and that was captured in Italy in River Mincio (Mantova lakes).
About Polypedilum (Tripodura) pruina Freeman, 1954, it is of interest to emphasize that it was considered a valid species and not a junior synonym of P. (T.) aegyptium (Chattopadhyay 2000); if accepted as a valid species, P. (T.) pruina should be an Oriental species but could be present also in Italy. Another species with an interesting distribution is Polypedilum nubifer, apparently originating in the Australian region, but now present almost worldwide, except in the Afrotropical and Neotropical regions. It is an invasive species, recently found in the Nearctic (Wallace et al. 2009); its absence from the Afrotropical region should be confirmed because of its similarity with some Afrotropical species (Cranston et al. 2016); in Italy, it was collected in rice fields (Nocentini 1985, Ferrarese 1992, Rossaro and Cortesi 2013. It is interesting to note that a few species, such as Rheopelopia perda and Saetheria reissi, formerly reported as Nearctic, were later found in Europe including Italy, Euryhapsis annuliventris is still reported only in the Nearctic and in Italy.
The following species were described as new to science (Rossaro 1982b, Rossaro and Lencioni 2000, Rossaro 2017  Some notes on some species given in Table 1 and whose presence in Italy was unexpected are here added. Procladius (Holotanypus) freemani: this species was known in North America (Roback 1971) but more recently it was collected in the Russian Far East (URL 4), its presence in Italy (Fucino) is supported by an adult male with associated exuvia and suggests a major range expansion of this species.
Procladius (Holotanypus) denticulatus: this species is currently known only from the Nearctic (Roback 1971) and in Italy (Milano Botanical garden) where only pupal exuviae were collected; its presence should be considered as a tentative identification.

Ablabesmyia (Ablabesmyia) aspera:
formerly known only from the Nearctic (Roback 1971). The capture of an adult male in Italy in a disused clay quarry (Oasi Le Foppe, Lombardia) extends its range in the world.
Chaetocladius holmgreni: it appears to be a northern species present in Sweden and in Svalbard, its presence in Italy is supported by an adult male captured in the River Aso in Central Apennines.
Cricotopus gelidus: a northern species, a male was captured in Italy near a glacial stream (Estellette glacier), but it is also known from Romania and Austria.
Heterotrissocladius maereri: a northern species, only pupal exuviae from Italy (Bors glacial stream, Monte Rosa); its identification should be confirmed.
Limnophyes aagardii: northern species, but extended to the Russian Far East, and collected as adult males in Sardegna near a spring (Rio Mannu, Sardegna).

Orthocladius
(Eudactylocladius) priomixtus: apparently widespread but not generally confirmed in Europe, it was identified on the basis of an adult male collected in the River Acqualba in Northern Italy.
Psilometriocnemus europaeus: a northern species captured near a glacial stream in Adamello mountain group (Vedretta Lobbia).
Pseudorthocladius uniserratus: this species is described as Nearctic (Saether and Sublette 1983), only exuviae found in Italy (Lake Variola, Piemonte), but the species can be easily recognized on the basis of exuviae alone.
Boreoheptagyia ortladamellica: present in the Alps in Ortles Adamello mountain group. Its presence in other sites must be confirmed.
Chironomus (Chironomus) lugubris: with a northern European distribution, but known also from Switzerland and Hungary, in Italy captured in Oasi Le Foppe (Lombardia).
Beckidia tethys: described from Nearctic (Saether 1977), but present in Italy (River Po) and in the Balkans; another species of the same genus, B. zabolotzskyi was just known from Palaearctic including the Russian Far East.

CONCLUSIONS
Chironomids have represented important contributions in the development of biogeographic theories. They were a critical group in supporting transantarctic relationships (Brundin 1966), but unfortunately the lack of knowledge and uncertain information from large areas suggests caution in drawing conclusions about the significance of their distributions. As emphasized above, new findings often extended the distribution of some species greatly (Rossaro 1995). The examples given above for S. montanus and D. veletensis are instructive. In contrast, the discovery of new species with very restricted distribution suggests that the family may contain both widespread and very restricted distribution species. More extensive knowledge of chironomid species distributions is very desirable, at present there are many unexplored regions (see Figure 1 for Italy) and sampling was often concentrated in restricted areas. The resolution of many taxonomic questions will profit from molecular analysis (Montagna et al. 2016b), but new collections accompanied by traditional morphological analysis remain essential.
In conclusion, it can be stated that present knowledge is far from complete. Some regions in the Western Palaearctic are very well studied and revision of checklists is rather recent; 598 species were reported from France in 1990 (Serra-Tosio and Laville 1991), raised to 646 in a 1996 updated list (Laville and Serra-Tosio 1996); a species list from Corsica updated in 2012 included 368 species (Moubayed and Ashe 2012); a checklist of species in Germany updated in 2014 listed 987 species (Orendt et al. 2014); 780 species were reported from Finland updated in 2014 (Paasivirta 2014). Some countries in the Western Palaearctic are not well studied, even if recently some efforts were made; for example, the fauna of Albania included 35-40 species before a recent update (Bitušík and Trnková 2019) raising it to 85-90 species. Recent research (Plóciennik and Pešic 2012;Plóciennik et al. 2014Plóciennik et al. , 2016