The Paradox Negative Effects of the mid-Pliocene Warming on the Climatic Suitability of Six Mediterranean Sandfly Species in Europe


  • Attila J. Trájer Pannon Egyetem



Neogene, Phlebotomus, Climate Change, Environmental Suitability Modelling, Bioclimatic Variables


The Pliocene era could be the last time when sandfly (Diptera: Psychodidae) species were widespread in Europe. Within the Pliocene, the mid-Pliocene period is an important model period in the investigation of the future effects of anthropogenic climate change. In this study, the mid-Pliocene potential distribution of six Mediterranean sandfly species was modelled based on the M2 mid-Pliocene cold and mid-Pliocene warm paleoclimatic reconstructions. It was found that the cold period’s potential occurrence of sandfly species could be notably more extended than the distribution of the taxa in the warm period. The difference is less expressed in the case of the West Mediterranean species, but it is particularly visible in the circum-Mediterranean and East Mediterranean taxa. It can be concluded that not the changes in the mean annual temperature, but the increase of the precipitation patterns and the wetter climate of the mid-Pliocene warm period resulted in the observed differences. The results imply that the use of mid-Pliocene warming as a model of the present climatic changes can be handled with caution in the performing of biogeographic proxies for vector sandflies related to the anthropogenic climate change.


Alten, B. (2010). Speciation and Dispersion Hypotheses of Phlebotomine Sandflies of the subgenus Paraphlebotomus (Diptera: Psychodidae): The Case in Turkey. Hacettepe Journal of Biology and Chemistry, 38(3), 229–246.

Alvar, J., Vélez, I. D., Bern, C., Herrero, M., Desjeux, P., Cano, J., Jannin, J., den Boer, M., & WHO Leishmaniasis Control Team. (2012). Leishmaniasis worldwide and global estimates of its incidence. PloSOne, 7(5), e35671.

Amante, C., & Eakins BE. (2009). Arc-Minute Global Relief Model: Procedure. ETOPO1 1 Arc-Minute Global Relief Model: Procedures, Data Sources and Analysis. NOAA Technical Memorandum NESDIS, NGDC-24, 19 pp.

Aspöck, H., Gerersdorfer, T., Formayer, H., Walochnik, J. (2008). Sand flies and sandfly-borne infections of humans in Central Europe in the light of climate change. Wiener klinische Wochenschrift, 120(4), 24–29.

Azar, D., Nel, A., & Geze, R. (2003b). Use of Lebanese amber inclusions in paleoenvironmental reconstruction, dating and paleobiogeography. Acta zoologica cracoviensia, 46(Suppl. Fossil Insects), 393–398.

Azar, D., Perrichot, V., Néraudeau, D., & Nel, A. (2003a). New psychodids from the Cretaceous ambers of Lebanon and France, with a discussion of Eophlebotomus connectens Cockerell, 1920 (Diptera, Psychodidae). Annals of the Entomological Society of America, 96(2), 117-126.[0117:NPFTCA]2.0

Bede-Fazekas, À., Tràjer, A.J. (2013). Ornamental plants as climatic indicators of arthropod vectors. Acta Universitatis Sapientiae, Agriculture and Environment, 5(1), 19–39.

Bogri, A., Solodovnikov, A., Żyła, D. (2018). Baltic amber impact on historical biogeography and palaeoclimate research: oriental rove beetle Dysanabatium found in the Eocene of Europe (Coleoptera, Staphylinidae, Paederinae). Papers in Palaeontology, 4(3), 433–452.

Brown, J.L., Hill, D.J., Dolan, A.M., Carnaval, A.C., Haywood, A.M. (2018). PaleoClim, high spatial resolution paleoclimate surfaces for global land areas. Scientific Data, 5(1), 1–9.

Caruso, A., Blanc-Valleron, M.M., Da Prato, S., Pierre, C., Rouchy, J.M. (2020). The late Messinian “Lago-Mare” event and the Zanclean Reflooding in the Mediterranean Sea: New insights from the Cuevas del Almanzora section (Vera Basin, South-Eastern Spain). Earth-Science Reviews, 200(2020), 102993.

Chalghaf, B., Chemkhi, J., Mayala, B., Harrabi, M., Benie, G.B., Michael, E., Salah, B. (2018). Ecological niche modeling predicting the potential distribution of Leishmania vectors in the Mediterranean basin: impact of climate change. Parasites & Vectors, 11(1), 461, pp. 2–9.

Chandler, M., Rind, D., & Thompson, R. (1994). Joint investigations of the middle Pliocene climate II: GISS GCM Northern Hemisphere results. Global and Planetary Change, 9(3–4), 197–219.

Cross, E.R., & Hyams, K.C. (1996). The potential effect of global warming on the geographic and seasonal distribution of Phlebotomus papatasi in southwest Asia. Environmental Health Perspectives, 104(7), 724–727.

Depaquit, J., Ferte, H., Leger, N., Killick‐Kendrick, R., Rioux, J.A., Killick‐Kendrick, M., Hanafi, H.A., Gobert, S. (2000). Molecular systematics of the phlebotomine sandflies of the subgenus Paraphlebotomus (Diptera, Psychodidae, Phlebotomus) based on ITS2 rDNA sequences. Hypotheses of dispersion and speciation. Insect Molecular Biology, 9(3), 293–300.

Depaquit, J., Ferté, H., Léger, N., Lefranc, F., Alves-Pires, C., Hanafi, H., Maroli, M., Morillas-Marquez, F., Rioux, J-A., Svobodova, M., Volf, P. (2002). ITS 2 sequences heterogeneity in Phlebotomus sergenti and Phlebotomus similis (Diptera, Psychodidae): possible consequences in their ability to transmit Leishmania tropica. International Journal for Parasitology, 32(9), 1123–1131.

Depaquit, J., Grandadam, M., Fouque, F., Andry, P.E., & Peyrefitte, C. (2010). Arthropod-borne viruses transmitted by Phlebotomine sandflies in Europe: a review. Eurosurveillance, 15(10), 19507.

Depaquit, J., Léger, N., Ferté, H. (1998). The taxonomic status of Phlebotomus sergenti Parrot, 1917, vector of Leishmania tropica (Wright, 1903) and Phlebotomus similis Perfiliev, 1963 (Diptera-Psychodidae) (1990). Morphologic and morphometric approaches. Biogeographical and epidemiological corollaries. Bulletin de la Societe de pathologie exotique, 91(4), 346–352.

Dinesh, D.S., Ranjan, A., Palit, A., Kishore, K., Kar, S.K. (2001). Seasonal and nocturnal landing/biting behaviour of Phlebotomus argentipes (Diptera: Psychodidae). Annals of Tropical Medicine and Parasitology, 95(2), 197–202.

Doha, S., Shehata, M.G., El Said, S., El Sawaf, B. (1991). Dispersal of Phlebotomus papatasi (Scopoli) and P. langeroni Nitzulescu in El Hammam, Matrouh Governorate, Egypt. Annales de parasitologie humaine et compare, 66(2), 69–76.

Dolan, A.M., Haywood, A.M., Hunter, S.J., Tindall, J.C., Dowsett, H.J., Hill, D.J., Pickering, S.J. (2015). Modelling the enigmatic late Pliocene glacial event—Marine Isotope Stage M2. Global and Planetary Change, 128(2015), 47–60.

Dowsett, H.J., Barron, J.A., Poore, R.Z., Thompson, R.S., Cronin, T.M., Ishman, S.E., Willard, D.A. (1999). Middle Pliocene paleoenvironmental reconstruction: PRISM2. US Geological Survey open file report, 99(535), 236, pp. 1–23.

Elnaiem, D.A., Connor, S.J., Thomson, M.C., Hassan, M.M., Hassan, H.K., Aboud, M.A., Ashford, R.W. (1998). Environmental determinants of the distribution of Phlebotomus orientalis in Sudan. The American Journal of Tropical Medicine and Hygiene, 92(8), 877–887.

Erdei, B., Hably, L., Kázmér, M., Utescher, T., Bruch, A.A. (2007). Neogene flora and vegetation development of the Pannonian domain in relation to palaeoclimate and palaeogeography. Palaeogeography, Palaeoclimatology, Palaeoecology, 253(1-2), 115–140.

Esseghir, S, Ready, P.D., Ben-Ismail, R. (2000). Speciation of Phlebotomus sandflies of the subgenus Larroussius coincided with the late Miocene-Pliocene aridification of the Mediterranean subregion. Biological Journal of the Linnean Society, 70(2), 189–219.

Esseghir, S., Ready, P.D., Killick‐Kendrick, R., Ben‐Ismail, R. (1997). Mitochondrial haplotypes and phylogeography of Phlebotomus vectors of Leishmania major. Insect Molecular Biology, 6(3), 211–225.

Fischer, D., Moeller, P., Thomas, S.M., Naucke, T.J., Beierkuhnlein, C. (2011). Combining climatic projections and dispersal ability: a method for estimating the responses of sandfly vector species to climate change. PLOS Neglected Tropical Diseases, 5(11), e1407.

González, C., Wang, O., Strutz, S.E., González-Salazar, C., Sánchez-Cordero, V., Sarkar, S. (2010). Climate change and risk of leishmaniasis in North America: predictions from ecological niche models of vector and reservoir species. PLOS Neglected Tropical Diseases, 4(1), e585.

Hanson, W.J. (1961). The breeding places of Phlebotomus in Panama (Diptera, Psychodidae). Annals of the Entomological Society of America, 54(3), 317–322.

Harzhauser, M., Piller, W.E. (2007). Benchmark data of a changing sea—palaeogeography, palaeobiogeography and events in the Central Paratethys during the Miocene. Palaeogeography, Palaeoclimatology, Palaeoecology, 253(1–2), 8–31.

Haywood, A. M., Chandler, M. A., Valdes, P. J., Salzmann, U., Lunt, D. J., & Dowsett, H. J. (2009a). Comparison of mid-Pliocene climate predictions produced by the HadAM3 and GCMAM3 General Circulation Models. Global and Planetary Change, 66(3-4), 208-224.

Haywood, A. M., Valdes, P. J., & Sellwood, B. W. (2000b). Global scale palaeoclimate reconstruction of the middle Pliocene climate using the UKMO GCM: initial results. Global and Planetary Change, 25(3-4), 239-256.

Haywood, A.M., & Valdes, P.J. (2004). Modelling Pliocene warmth: contribution of atmosphere, oceans and cryosphere. Earth and Planetary Science Letters, 218(3–4), 363–377.

Haywood, A.M., Valdes, P.J., Sellwood, B.W. (2000). Global scale palaeoclimate reconstruction of the middle Pliocene climate using the UKMO GCM: initial results. Global and Planetary Change, 25(3-4), 239–256.

Hill, D.J. (2015). The non-analogue nature of Pliocene temperature gradients. Earth and Planetary Science Letters, 425(2015), 232–241.

Hinkelman, J. (2019). Spinaeblattina myanmarensis gen. et sp. nov. and Blattoothecichnus argenteus ichnogen. et ichnosp. nov. (both Mesoblattinidae) from mid-Cretaceous Myanmar amber. Cretaceous Research, 99(2019), 229–239.

Ibrahim Abdelwahab, A., Abdoon, M.A. (2005). Distribution and population dynamics of Phlebotomus sand flies (Diptera: Psychodidae) in an endemic area of cutaneous leishmaniasis in Asir Region, Southwestern Saudi Arabia. Journal of Entomology, 2.1(2005), 102–108.

Jacob, D., Podzun, R. (1997). Sensitivity studies with the regional climate model REMO. Meteorology and Atmospheric Physics, 63(1-2), 119–129.

Jansen, E., Overpeck, J., Briffa, K.R., Duplessy, J-C., Joos, F., Masson-Delmotte, V., Olago, D., Otto-Bliesner, B., Peltier, W.R., Rahmstorf, S., et al. (2007). Palaeoclimate. In S. Solomon, D. Qin, M. Manning, Z. Chen, M. Marquis, K.B. Averyt, M. Tignor, H.L. Miller (Eds.), Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, United Kingdom: Cambridge University Press.

Jiang, D., Wang, H., Ding, Z., Lang, X., Drange, H. (2005). Modeling the middle Pliocene climate with a global atmospheric general circulation model. Journal of Geophysical Research: Atmospheres, 110(D14), 1–14.

Kaddumi, H.F. (2007). Amber of Jordan, the oldest prehistoric insects in fossilized resin (3rd ed.). Amman, Jordan: Publications of the Eternal River Museum of Natural History.

Kasap, O.E., Alten, B. (2006). Comparative demography of the sand fly Phlebotomus papatasi (Diptera: Psychodidae) at constant temperatures. Journal of Vector Ecology, 31(2), 378–385.[378:cdotsf];2

Kasap, O.E., Dvorak, V., Depaquit, J., Alten, B., Votypka, J., Volf, P. (2015). Phylogeography of the subgenus Transphlebotomus Artemiev with description of two new species, Phlebotomus anatolicus n. sp. and Phlebotomus killicki n. sp. Infection, Genetics and Evolution, 34(2015), 467–479.

Kemp, D. (1990). Global environmental issues: a climatological approach. London, United Kingdom and New York, United States: Routledge.

Koch, L.K., Kochmann, J., Klimpel, S., Cunze, S. (2017). Modeling the climatic suitability of leishmaniasis vector species in Europe. Scientific reports, 7(1), 1–10.

Kottek, M., Grieser, J., Beck, C., Rudolf, B., Rubel, F. (2006). World map of the Köppen-Geiger climate classification updated. Meteorologische Zeitschrift, 15(3), 259–263.

Krzeminski, W., Krzeminska, E., Kubisz, D., Mazur, M., & Pawlowski, J. (1997). Preliminary report on a Pliocene fauna from western Hungary. Studia Naturalia, 10(1997), 174–192.

Lacaze, B., Dudek, J., & Picard, J. (2018). GRASS GIS Software with QGIS. QGIS and Generic Tools, 1(2018), 67–106.

Liu, Z., Pagani, M., Zinniker, D., DeConto, R., Huber, M., Brinkhuis, H., Shah, S.R., Leckie, L.M., & Pearson A. (2009). Global cooling during the Eocene-Oligocene climate transition. Science, 323(5918), 1187–1190.

Lőrincz, F., Szentkirályi, S. (1933). The Occurrence of P. macedonicus [=Phlebotomus perfiliewi] in Hungary. Contributions to the Determination of the European Species. Állattani Közlemények, 30(1933), 160–169.

Mahamdallie, S.S., Pesson, B., & Ready, P.D. (2011). Multiple genetic divergences and population expansions of a Mediterranean sandfly, Phlebotomus ariasi, in Europe during the Pleistocene glacial cycles. Heredity, 106(5), 714–726.

Martinetto, E., Momohara, A., Bizzarri, R., Baldanza, A., Delfino, M., Esu, D., Sardella, R. (2017). Late persistence and deterministic extinction of “humid thermophilous plant taxa of East Asian affinity (HUTEA) in southern Europe. Palaeogeography, Palaeoclimatology, Palaeoecology, 467(2017), 211–231.

Martins-Melo, F.R., da Silveira Lima, M., Ramos Jr, A.N., Alencar, C.H., & Heukelbach. J. (2014). Mortality and case fatality due to visceral leishmaniasis in Brazil: a nationwide analysis of epidemiology, trends and spatial patterns. PloSOne, 9(4), e93770.

Moo-Llanes, D., Ibarra-Cerdeña, C.N., Rebollar-Téllez, E.A., Ibanez-Bernal, S., Gonzalez, C., & Ramsey, J.M. (2013). Current and future niche of North and Central American sand flies (Diptera: Psychodidae) in climate change scenarios. PLoS Neglected Tropical Diseases, 7(9), e2421.

Naucke, T.J., & Pesson, B. (2000). Presence of Phlebotomus (Transphlebotomus) mascittii Grassi, 1908 (Diptera: Psychodidae) in Germany. Parasitology Research, 86(4), 335–336.

Nesis, K.N. (2003). Distribution of recent Cephalopoda and implications for Plio-Pleistocene events. Berliner paläobiologische Abhandlungen, 3(2003), 199–224.

Pielowska, A., Sontag, E., & Szadziewski, R. (2018). Haematophagous arthropods in Baltic amber. Annales Zoologici, 68(2), 237–249.

Poinar Jr, G. (2007). Early Cretaceous trypanosomatids associated with fossil sand fly larvae in Burmese amber. Memórias do Instituto Oswaldo Cruz, 102(5), 635–637.

Popov, S.V., Shcherba, I.G., Ilyina, L.B., Nevesskaya, L.A., Paramonova, N.P., Khondkarian, S.O., & Magyar, I. (2006). Late Miocene to Pliocene palaeogeography of the Paratethys and its relation to the Mediterranean. Palaeogeography, Palaeoclimatology, Palaeoecology, 238(1–4), 91–106.

Rajesh, K., & Sanjay, K. (2013). Change in global climate and prevalence of visceral leishmaniasis. International Journal of Scientific and Research Publications, 3(1), 2250–3153.

Ready, P.D. (2008). Leishmaniasis emergence and climate change. Revue scientifique et technique, 27(2), 399–412.

Robert, C., &Kennett, J.P. (1997). Antarctic continental weathering changes during Eocene-Oligocene cryosphere expansion: Clay mineral and oxygen isotope evidence. Geology, 25(7), 587–590.<0587:ACWCDE>2.3.CO;2

Sloan, L.C., Crowley, T.J., & Pollard, D. (1996). Modeling of middle Pliocene climate with the NCAR GENESIS general circulation model. Marine Micropaleontology, 27(1–4), 51–61.

Stebner, F., Kraemer, M.M.S., Ibáñez-Bernal, S., & Wagner, R. (2015). Moth flies and sand flies (Diptera: Psychodidae) in Cretaceous Burmese amber. PeerJ, 3(2015), e1254.

Stuckenberg, B.R. (1975). New fossil species of Phlebotomus and Haematopota in Baltic Amber (Diptera: Psychodidae, Tabanidae). Annals of the Natal Museum, 22(2), 455–464.

Trájer, A. J. (2019). The potential impact of climate change on the seasonality of Phlebotomus neglectus, the vector of visceral leishmaniasis in the East Mediterranean region. International Journal of Environmental Health Research, 4(2019), 1–19.

Trájer, A. J., Hammer, T., & Padisák, J. (2018b). Reflection of the Neogene–Quaternary phylogeography in the recent distribution limiting climatic factors of eight Mediterranean Phlebotomus species (Diptera: Psychodidae). Journal of Natural History, 52(27-28), 1763-1784.

Trájer, A., Tánczos, B., Hammer, T., & Padisák, J. (2018a). Solar radiation and temperature conditions as the determinants of occurrence of Phlebotomus neglectus Tonnoir (Diptera: psychodidae). Journal of the Entomological Research Society, 20(2), 13-27.

Trájer, A.J. (2017). Checklist, distribution maps, bibliography of the Hungarian Phlebotomus (Diptera: Psychodidae) fauna complementing with the climate profile of the recent sandfly distribution areas in Hungary. Folia Faunistica Slovaca, 22(2017), 7–12.

Trájer, A.J., & Sebestyén, V. (2019). The changing distribution of Leishmania infantum Nicolle, 1908 and its Mediterranean sandfly vectors in the last 140 kys. Scientific reports, 9(1), 1–15.

Trájer, A.J., Bede-Fazekas, Á., Hufnagel, L., Horváth, L., & Bobvos, J. (2013). The effect of climate change on the potential distribution of the European Phlebotomus species. Applied Ecology and Environmental Research, 11(2), 189–208.

Tsirigotakis, N., Pavlou, C., Christodoulou, V., Dokianakis, E., Kourouniotis, C., Alten, B., & Antoniou, M. (2018). Phlebotomine sand flies (Diptera: Psychodidae) in the Greek Aegean Islands: ecological approaches. Parasites & Vectors, 11(1), 97–97.

VECTORNET. (2020). Phlebotomine sandflies maps. [accessed 2020 September 23]

Whitesitt, J.E. (2012). Boolean algebra and its applications. USA: Courier Corporation.

WHO leishmaniasis. [accessed 2020 September 23]

Wolfe, A.P., Tappert, R., Muehlenbachs, K., Boudreau, M., McKellar, R.C., Basinger, J.F., & Garrett, A. (2009). A new proposal concerning the botanical origin of Baltic amber. Proceedings of the Royal Society B: Biological Sciences, 276(1672), 3403–3412.

Wu, C., Liu, C., Yi, H., Xia, G., Zhang, H., Wang, L., Li, G., & Wagreich, M. (2017). Mid-Cretaceous desert system in the Simao Basin, southwestern China, and its implications for sea-level change during a greenhouse climate. Palaeogeography, Palaeoclimatology, Palaeoecology, 468, 529–544.

Yaghoobi-Ershadi, M.R., Akhavan, A.A., & Mohebali, M. (2001). Monthly variation of Leishmania major MON-26 infection rates in Phlebotomus papatasi (Diptra: Psychodidae) from rodent burrows in Badrood area of Iran. Medical Journal of The Islamic Republic of Iran, 15(3), 175–178.

Yang, S., Galbraith, E., & Palter, J. (2014). Coupled climate impacts of the Drake Passage and the Panama Seaway. Climate Dynamics, 43(1–2), 37–52.




How to Cite

Trájer, A. J. (2020). The Paradox Negative Effects of the mid-Pliocene Warming on the Climatic Suitability of Six Mediterranean Sandfly Species in Europe. Biosis: Biological Systems, 1(4), 141-156.