FFS-22-02-Trajer-2017.html

Folia faunistica Slovaca 22 (2017) 7–12

Checklist, distribution maps, bibliography of the Hungarian Phlebotomus (Diptera: Psychodidae) fauna complementing with the climate profile of the recent sandfly distribution areas in Hungary

Attila János Trájer

MTA-PE, Limnoecology Research Group, Egyetem u. 10, H-8200 Veszprém, Hungary; attilatrajer@gmail.com
University of Pannonia, Department of Limnology, Egyetem u. 10, H-8200 Veszprém, Hungary

Key words

Phlebotomus

sandfly species

Hungary

Pannonian ecoregion

climate

Abstract

A checklist of sandflies containing 4 species from Hungary is given. The history of the scientific investigations of Phlebotomus species in Hungary was briefly reported. For each species the following data were provided: important synonyms, localities from Hungary with the reference of the publication. Distribution was mapped using the UTM system. Since climate conditions determine the distribution of sandfly species, the averages of monthly mean, maximum, minimum temperatures and the monthly precipitation values also were involved into the study. Most of the collecting sites can be found in 3 locations: in Budapest and its agglomeration, in the south-east part of Transdanubia and in the south-east part of the Great Hungarian Plain. It was found that Phlebotomus papatasi and Phlebotomus perfiliewi inhabit the coldest areas of sandfly distribution. Phlebotomus mascittii and Phlebotomus major neglectus occur in the warmer Transdanubian part of the country. The result of the cluster analysis for Hungarian occurrences of sandfly species based on the average values of monthly climatic variables showed the clear dichotomization of the north and south distribution areas. Data of monthly climatic factors of the four major distribution areas including temperature variables and monthly precipitation values is given.

Received 20 December 2016 ~ Accepted 25 January 2017 ~ Published 27 January 2017

© 2017 Faunima, Bratislava, e–ISSN 1336–4529 ISSN 1335–7522 www.ffs.sk

 

Introduction

There are more than 700 sandfly species worldwide and 17 species of sandflies and 3 subspecies of the Phlebotomus (Larroussius) major complex in Europe. Phlebotomus species are the vectors of several Leishmania pathogens and Phleboviruses in the Mediterranean parts of Europe where five species can transmit visceral leishmaniasis to humans, namely Phlebotomus (Larroussius) ariasi Tonnoir, 1921, Phlebotomus major neglectus Tonnoir, 1921, Phlebotomus (Larroussius) perfiliewi Parrot, 1930, Phlebotomus (Larroussius) tobbi Adler, Theodor et Lourie, 1930, and Phlebotomus (Larroussius) perniciosus Newstead, 1911 (Minter 1989; Léger et al. 2000). Most of the sandfly species are typical tropical and subtropical fauna elements, but some species are native to the temperate areas of Europe. In contrast to the members of Culicidae, sandflies and several other species of Psychoda breeds in wet, decaying organic materials and microbial mats. Some of them are synanthropic species which can breed in water-wells of bathrooms and showers and along the rifts of old buildings or in the cracks of the walls. The anthropogenic climate change is predicted to trigger the northward spread of sandfly species and Leishmania infantum in Europe including the whole Carpathian basin (Trájer et al. 2013). It seems that in the Pannonian ecoregion the observed and projected regional warming trends exceed the warming trends of Europe (Bartholy et al. 2007). The minimum temperature limit of the survival of larvae is about -4°C to 5 °C depending on the species and countries (Killick-Kendrick & Killick-Kendrick 1999; Naucke & Schmitt 2004; Rioux et al. 1984; Singh 1999). The January mean and mean minimum temperatures are important distribution liming factors of sandfly vectors in east and central Europe (Trájer et al. 2013). Urban heat island effect can help the survival of the extrazonal populations of sandfly species far north from their continuous distribution area in the Carpathian basin (Trájer et al. 2014; Bede-Fazekas & Trájer 2015).

The purpose of this paper was to provide a checklist on Phlebotomus species and the comparable climate data of the distribution areas of sandfly species in Hungary.

History

Studies on Hungarian sandfly fauna started in the 1930’s and only sparse data were published until the end of the 2000’s. The first paper on the observation of Phlebotomus species in Hungary was published in 1933 by Lörincz & Szentkirályi. They investigated the regional outbreak of an unfamiliar type of dermatitis which was affected about 30 patients in Hódmezővásárhely, south-east Hungary during the August of 1931. The etiologic connection between the papular or vesicular eruptions and the bites of Phlebotomus species was proved. The individuals of Phlebotomus macedonicus Adler et Theodor, 1931 (= Phlebotomus (Larroussius) perfiliewi) were found in the trapped materials. The insects were observed first in the August of 1931, but in the same month of 1932 the sandflies were observed again. Ivánovics (1953) mentioned the presence of Phlebotomus species in Hungary as the potential vector of Pappataci-fever. Szabó & Draskovits (1983) proposed the possible occurrence of Phlebotomus papatasi in the southern part of Hungary. They also mentioned the occurrence of Phlebotomus perfiliewi from Esztergom and the Gellért Hill cave, Budapest, based on the trappings of the National Public Health Service of Hungary which were performed sometimes in the 1960’s (Tánczos 2012). These observations can be handled as ‘uncertain occurrences’. The later surveys showed that the historical observations were not unfounded since two Phlebotomus species were observed in the agglomeration of the Capital and also two species in south-east Hungary. In 2007 – 2010 a countrywide survey was performed to investigate the presence of Phlebotomus species and canine leishmaniasis in Hungary. Tánczos (2012) summarized the results of the collection surveys in his doctoral dissertation and presented the detailed history of sandfly research in Hungary. Altogether the presence of 4 sandfly species was proved (Farkas et al., 2011; Tánczos 2012; Tánczos et al. 2012). In 2014, a minor survey was conducted for the investigation of the physical requirements of Phlebotomus major subsp. neglectus in Nagyharsány, Hungary (unpublished data) and another for the investigation of the proposed presence of sandfly species and Aedes albopictus Skuse, 1894 in the border region of south-west Hungary and Croatia (Trájer et al. 2016).

Material and methods

Taxonomy

Both of the nomenclature and taxonomy were based on the Fauna Europea zoological taxonomic index database (Wagner 2013).

Climate data

The January mean minimum temperatures, the monthly averages of mean, minimum, maximum temperatures and daily average precipitation values were derived from the European Climate Assessment Dataset (Haylock et al. 2008). The values were averaged for the period of January 1950 to December 2014 (the year of the last collecting survey in Hungary for sandfly species). Average values were calculated from the 0.25° grid within the domain including the certain collecting sites and almost the entire south Pannonian ecoregion. The latitudinal range of the whole frame was 45°00’N to 46°25’N, while the longitudinal was 16°45’°E to 21°00’E. The monthly average values of the used climate values were averaged according to the following grids (Table 1, 2).

Results

Checklist of sandfly species

Phlebotomus (Transphlebotomus) mascittii (Grassi, 1908)

Loc. Kapolcs – Bakony Mts, Veszprém County (Farkas et al. 2011; Tánczos 2012), Nagyharsány – Villány Hills, Baranya County (Farkas et al. 2011; Tánczos 2012), Törökbálint – Buda Mts, Pest County (Farkas et al. 2011; Tánczos 2012; Figure 1).

Phlebotomus (Larroussius) major neglectus (Tonnoir, 1921)

Loc. Nagyharsány – Villány Hills, Baranya County (Farkas et al. 2011; Tánczos 2012, Trájer et al. 2016) Törökbálint-Buda Mts, Pest County (Farkas et al. 2011; Tánczos 2012), Villánykövesd-Villány Hills, Baranya County (Farkas et al. 2011; Tánczos 2012; Figure 2).

Phlebotomus (Phlebotomus) papatasi (Scopoli, 1786)

Loc. Maroslele Maroslele – southern Hungary, Csongrád County (Farkas et al. 2011; Tánczos 2012; Figure 3).

Phlebotomus (Larroussius) perfiliewi (Parrot, 1930)

Loc. Földeák – southern Hungary, Csongrád County (Farkas et al. 2011; Tánczos 2012), Maroslele-southern Hungary, Csongrád County (Farkas et al. 2011; Tánczos 2012), Hódmezővásárhely – southern Hungary, Csongrád County (Lőrincz & Szentkirály 1933), Budapest (?) – Buda Mts, Budapest (Szabó & Draskovits 1983), Esztergom (?) – Danube Bend, Komárom – Esztergom County (Szabó & Draskovits 1983; Figure 4).

Climatic zoogeography of the sandfly fauna

The January mean minimum temperature, which is an important climatic limiting factor of the distribution of sandflies, showed notable differences between the main distribution areas in 1950 – 2014. Ph. papatasi and Ph. perfiliewi inhabit the coldest areas where the January mean minimum daily temperatures were the lowest C in 1950 – 2014 (mean: -3.95, maximum: 0.48 °C and the minimum: -12.55 °C). The winters were relatively mild in Törökbálint (belongs to the agglomeration of Budapest), where both Ph. major subsp. neglectus and Ph. mascittii were found (mean: -2.54, maximum: 2.70 and the minimum: -8.83 °C). Ph. mascittii also was observed in Kapolcs, where the winters are somewhat milder than in the distribution area of Ph. papatasi and Ph. perfiliewi, but colder than the climate of the agglomeration of Budapest (mean: -3.45, maximum: 1.15 and the minimum: -10.21 °C). Ph. major subsp. neglectus was also collected in Nagyharsány and Villánykövesd (mean: -3.25 to -3.40, maximum: 2.39 to 2.25 and the minimum: -10.72 to -11.09 °C; Figure 5).

The warmer, submediterranean Croatian areas (January mean minimum temperature is more than -2.37 °C) are close to the Nagyharsány-Villánykövesd area. The south-east Hungarian occurrences of sandfly species are situated north to the warmer south-west areas of Romania and north-east Serbia (Figure 6).

Based on the linear trend of the January mean minimum temperature data of 1950 – 2014, the most notable winter warming trends (3.9 – 3.6 °C per 65 years) were observed in the south-east parts of the Great Hungarian Plain and Vojvodina, Serbia, that about cover the south Hungarian distribution area of sandfly species (Figure 7).

The result of the cluster analysis for Hungarian occurrence grids of sandfly species based on the average values of monthly climatic variables showed the clear dichotomization of the north (A and B) and south (C and D) main distribution areas. The climates of the C and D distribution areas are more similar to each other than the climates of the A and B distribution areas’ (Figure 8).

Discussion

Altogether the presences of four Phlebotomus species were confirmed in Hungary in the last one hundred years: Ph. mascittii, Ph. major neglectus, Ph. papatasi and Ph. perfiliwei (Farkas et al. 2011; Lőrincz & Szentkirály 1933; Tánczos 2012; Trájer et al. 2016). Four major distribution areas were found. Most of the positive collecting sites can be found in south-west Hungary, in the south-east part of the Great Hungarian Plain and in the agglomeration of Budapest. It is noticeable that -excluding the uncertain observations- the composition of the recent sandfly faunas of south-east and west Hungary are different: Ph. perfiliewi and Ph. papatasi recently only presents in the south-east, Ph. neglectus and Ph. mascittii only in the Transdanubian (west) part of Hungary. The Transdanubian distribution of Ph. mascitti can be explained by the wider zoogeography of the species since it is the fauna element of the west Balkan. The population of this species in Törökbálint forms the most eastern, but not the most northern occurrence of the species in the Pannonian ecoregion since Dvorak et al. (2016) found Ph. mascitti in Slovakia. In contrast, Ph. papatasi and Ph. major subsp. neglectus can be found both in the south-east and south-west of the Pannonian ecoregion. Ph. perfiliewi presents in Serbia (Depaquit et al. 2013) and Croatia (Bosnić et al. 2006). These zoogeographical observations indicate that the Hungarian Phlebotomus fauna is also related to the east and the west Balkan sandfly faunas.

The recent warming trend of the south Pannonian ecoregion raises the possibility of the increasing abundance of sandfly species in the region and a possible faunistic exchange between the south-west and south-east sandfly faunas. Due to the heat island effect of the Capital’s agglomeration the winters are milder in Törökbálint, where both Ph. major subsp. neglectus and Ph. mascittii were found, than the winters of the south-western and south-eastern distribution areas of these species. The influence of heat island effect of Budapest on the overwintering potential of Ph. major subsp. neglectus and Ph. mascittii previously was studied by Bede-Fazekas & Trájer (2015) and Trájer et al. (2014).

Data of monthly climatic factors of the four major distribution areas including temperature variables and monthly precipitation values is given. This can be the basis of further climatic zoogeographical investigations of the Carpathian basin’s sandfly fauna.

References

Bartholy J, Pongrácz R, Gelybó RPG, 2007. Regional Climate Change Expected in Hungary for 2071-2100. Applied Ecology and Environmental Research 5: 1–17. doi: https://doi.org/10.15666/aeer/0501_001017

Bede-Fazekas Á, Trájer A, 2015. Potential urban distribution of Phlebotomus mascittii Grassi and Phlebotomus neglectus Tonn. (Diptera: Psychodidae) in 2021-50 in Budapest, Hungary. Journal of Vector Borne Diseases 52: 213.

Bosnić S, Gradoni L, Khoury C, Maroli M, 2006. A review of leishmaniasis in Dalmatia (Croatia) and results from recent surveys on phlebotomine sandflies in three southern counties. Acta tropica 99: 42–49. doi: 10.1016/j.actatropica.2006.06.009

Depaquit J, Bounamous A, Akhoundi M, Augot D, Sauvage F, Dvorak V, Chaibullinova A, Pesson B, Volf P, Léger N, 2013. A taxonomic study of Phlebotomus (Larroussius) perfiliewi sl. Infection, Genetics and Evolution 20: 500–508. doi: 10.1016/j.meegid.2013.10.006

Dvorak V, Hlavackova K, Kocisova A, Volf P. 2016. First record of Phlebotomus (Transphlebotomus) mascittii in Slovakia. Parasite 23, 48. doi: 10.1051/parasite/2016061

Farkas R, Tánczos B, Bongiorno G, Maroli M, Dereure J, Ready PD, 2011. First surveys to investigate the presence of canine leishmaniasis and its phlebotomine vectors in Hungary. Vector-Borne and Zoonotic Diseases 11, 7: 823–834. doi: 10.1089/vbz.2010.0186

Haylock MR, Hofstra N, Klein Tank AMG, Klok EJ, Jones PD, New M, 2008. A European daily high-resolution gridded dataset of surface temperature and precipitation. J. Journal of Geophysical Research (Atmospheres) 113: D20119. http://onlinelibrary.wiley.com/doi/10.1029/2008JD010201/epdf

Ivánovics G, 1953. Pappataci-fever. In: Human-pathogen viruses and rickettsies [Pappataci-láz. In: Emberi betegségeket okozó vírusok és rickettsiák]. Akadémiai kiadó. 117 pp.

Killick-Kendrick R, Killick-Kendrick M, 1999. Biology of sand fly vectors of Mediterranean canine leishmaniasis. In: Killick-Kendrick R (ed.): Canine leishmaniasis: an update. Proc. Int. Can. Leishm. Forum, Barcelona, Spain. Intervet International, Boxmeer, The Netherlands, pp. 26-31.

Léger N, Depaquit J, Ferté H, Rioux JA Gantier JC, Gramiccia M., Ludovisi A, Michaelides A, Christophi N, Economides P, 2000. [Phlebotomine sandflies (Diptera-Psychodidae) of the isle of Cyprus. II--Isolation and typing of Leishmania (Leishmania infantum Nicolle, 1908 (zymodeme MON 1) from Phlebotomus (Larroussius) tobbi Adler and Theodor, 1930]. Parasite (Paris, France) 7: 143–146.

Lőrincz F, Szentkirályi S, 1933. The Occurrence of P. macedonicus in Hungary. Contributions to the Determination of the European Species. Állattani Közlemények, 30: 160–169.

Minter DM, 1989. The leishmaniases. Geographical distribution of arthropod-borne diseases and their vectors. WHO/VBC/89.967: 93–106.

Naucke TJ, Schmitt C, 2004. Is leishmaniasis becoming endemic in Germany? International Journal of Medical Microbiology Supplements 293: 179–181. doi: 10.1016/S1433-1128(04)80036-6

Rioux JA, Aboulker JP, Lanotte G, Killick-Kendrick R, Martini-Dumas A, 1984. [Ecology of leishmaniasis in the south of France. 21. Influence of temperature on the development of Leishmania infantum Nicolle, 1908 in Phlebotomus ariasi Tonnoir, 1921. Experimental study]. Annales de Parasitologie Humaine et Comparée 60: 221–229.

Singh KV, 1999. Studies on the role of climatological factors in the distribution of phlebotomine sandflies (Diptera: Psychodidae) in semi-arid areas of Rajasthan, India. Journal of Arid Environments 42: 43–48. doi: 10.1006/jare.1999.0499 

Szabó J, Draskovits ÁD, 1983. Psychodidae-Ptyshopteridae [Lepkeszúnyogok, redős szúnyogok]. Fauna Hungariae, Diptera I., 4/C. Akadémiai Kiadó, Budapest. 13–16 pp.

Szentkiralyi S, Loerincz F, 1933. A peculiar dermatitis caused by the bites of Phlebotomus in Hungary. Dermatologische Wochenschrift 96: 289–296.

Tánczos B, 2012. The investigation of canine leishmaniasis and its vectors in Hungary [A kutya leishmaniózis és a parazita vektorainak vizsgálata Magyarországon]. Doctoral dissertation. Szent István University, Doctoral School of Veterinary Sciences. Available at: http://www.huveta.hu/bitstream/handle/10832/572/TanczosBalazsDissertation.pdf

Tánczos B, Balogh N, Király L, Biksi I, Szeredi L, Gyurkovsky M, Scalone A, Fiorentino E, Gramiccia M, Farkas R, 2012. First record of autochthonous canine leishmaniasis in Hungary. Vector-Borne and Zoonotic Diseases 12: 588–594. doi: 10.1089/vbz.2011.0906

Tánczos B, Farkas R, 2009. Phlebotomine sand flies (Diptera: Psychodidae) and their epidemiological importance. Literature review. Magyar Állatorvosok Lapja 131: 411–416.

Trájer AJ, Bede-Fazekas Á, Bobvos J, Páldy A. 2013. The effect of climate change on the potential distribution of the European Phlebotomus species and the parasite Leishmania infantum in 2011-2070. A climate envelope modeling approach. In: 2013 Conference of the International Society of Environmental Epidemiology (ISEE), the International Society of Exposure Science (ISES), and the International Society of Indoor Air Quality and Climate (ISIAQ) Abstracts Booklet., 2013.08.19 – 2013.07.23, Basel, Switzerland.

Trájer AJ, Mlinárik L, Juhász P, Bede-Fazekas Á. 2014. The combined impact of urban heat island, thermal bridge effect of buildings and future climate change on the potential overwintering of Phlebotomus species in a Central European metropolis. Applied Ecology and Environmental Research 12: 887–908.

Trájer A, Tánczos B, Hammer T, Bede-Fazekas Á, Ranvig K-A, Schoffhauzer J, Padisák J, 2016. The complex investigation of the colonization potential of Aedes albopictus (Diptera: Culicidae) in the south Pannonian ecoregion. Applied Ecology and Environmental Research, online first article. http://www.aloki.hu/indvolOF.htm

Wagner R, 2013. Fauna Europaea: Phlebotomidae. In: Beuk P & Pape T, Fauna Europaea: Diptera, Fauna Europaea version 2.6.2, http://www.faunaeur.org

 

Table 1. The delimiter coordinates and the correspondent grids of the collecting sites according to the used 0.25° resolution. For the visualization of the grids see Figure 5.

Locality (correspondent grid)

Longitude (N)

Latitude (E)

Kapolcs (A)

46.75 – 47.00

17.50 – 17.75

Törökbálint (B)

47.25 – 47.50

18.75 – 19.00

Villánykövesd (C)

Nagyharsány (C)

45.75 – 46.00

45.75 – 46.00

18.25 – 18.50

18.25 – 18.50

Hódmezővásárhely (D)

Földeák (D)

Maroslele (D)

46.25 – 46.50

46.25 – 46.50

46.25 – 46.50

20.25 – 20.50

20.25 – 20.50

20.25 – 20.50

Table 2. The monthly averages of mean, minimum, maximum temperature values and daily averages of precipitation. For the visualization of the grids see Figure 5.

Tmean – mean monthly temperature, Tmax – maximum monthly temperature, Tmin – minimum monthly temperature [°C], Prec/day – mean monthly precipitations expressed in daily precipitation values

Grid

Variable

I

II

III

IV

V

VI

VII

VIII

IX

X

XI

XII

A

Tmean

-0.87

0.95

5.33

10.55

15.39

18.77

20.61

20.07

15.91

10.72

5.19

0.78

Tmax

2.47

5.12

10.54

16.27

21.27

24.62

26.74

26.37

21.88

16.18

8.98

3.80

Tmin

-3.52

-2.33

1.24

5.74

10.19

13.65

15.24

14.70

11.05

6.40

2.33

-1.55

Prec/day

1.05

1.12

1.06

1.56

1.99

2.37

2.03

1.96

1.94

1.53

1.95

1.45

B

Tmean

-0.27

1.58

6.09

11.59

16.45

19.76

21.66

21.08

16.66

11.26

5.67

1.31

Tmax

2.29

4.81

10.41

16.65

21.72

25.01

27.18

26.77

22.08

16.02

8.55

3.62

Tmin

-2.59

-1.27

2.32

6.96

11.47

14.80

16.51

16.01

12.15

7.38

3.16

-0.78

Prec/day

1.13

1.10

0.95

1.23

1.74

2.03

1.54

1.57

1.34

1.27

1.75

1.40

C

Tmean

-0.39

1.54

6.14

11.51

16.49

19.83

21.59

21.05

16.77

11.48

5.79

1.29

Tmax

2.85

5.66

11.47

17.25

22.26

25.61

27.74

27.54

23.17

17.44

9.82

4.29

Tmin

-3.47

-2.12

1.41

5.98

10.64

13.93

15.38

14.87

11.18

6.54

2.40

-1.44

Prec/day

1.09

1.17

1.03

1.53

1.91

2.35

1.84

1.65

1.59

1.44

1.72

1.50

D

Tmean

-1.01

0.81

5.63

11.27

16.46

19.84

21.65

21.03

16.57

11.03

5.51

0.93

Tmax

2.30

5.00

11.21

17.33

22.51

25.88

28.11

27.86

23.39

17.41

9.75

3.97

Tmin

-3.98

-2.78

0.90

5.63

10.38

13.65

15.05

14.55

10.77

5.95

2.08

-1.77

Prec/day

0.86

0.91

0.86

1.23

1.59

2.07

1.56

1.40

1.26

1.04

1.32

1.28

 

 

 

 
 

Figure 1. The distribution of Ph. mascittii in Hungary (black rectangles: confirmed observations).

Figure 2. The distribution of Ph. major subsp. neglectus in Hungary (black rectangles: confirmed observations).

AJ Trájer — Folia faunistica Slovaca 22 (2017) 7–12

 
 

 

Figure 3. The distribution of Ph. papatasi in Hungary (black rectangles: confirmed observation).

Figure 4. The distribution of Ph. perfiliewi in Hungary (black rectangles: confirmed observations, dark grey rectangles: unconfirmed observations).

 

Figure 5. The mean January minimum daily temperature values in 1950-2014 according to the five grid of confirmed observations of Phlebotomus species.

AJ Trájer — Folia faunistica Slovaca 22 (2017) 7–12

 
 
 

Figure 6. The averages of the January mean minimum temperature values in the South Pannonian Ecoregion (45°00’N to 46°25’N – 16°45’°E to 21°00’E) in 1950 – 2014.

1 – Nagyharsány, 2 – Villánykövesd, 3 – Maroslele, 4 – Földeák

Figure 7. The trends of the January mean minimum temperature values in the South Pannonian ecoregion (45°00’N to 46°25’N – 16°45’°E to 21°00’E) according to the linear trend of the annual mean temperature values in 1950 – 2014.

1 – Nagyharsány, 2 – Villánykövesd, 3 – Maroslele, 4 – Földeák

Figure 8. Cluster analysis for Hungarian occurrence sites of sandfly species based on the average values of four monthly climatic variables are listed in Table 2.