Parasitol Res (2014) 113:2295–2301 DOI 10.1007/s00436-014-3884-y

ORIGINAL PAPER

New record of the suspected leishmaniasis vector Phlebotomus (Transphlebotomus) mascittii Grassi, 1908 (Diptera: Psychodidae: Phlebotominae) — the northernmost phlebotomine sandfly occurrence in the Palearctic region Christian Melaun & Andreas Krüger & Antje Werblow & Sven Klimpel

Received: 17 February 2014 / Accepted: 24 March 2014 / Published online: 16 April 2014 # Springer-Verlag Berlin Heidelberg 2014

Abstract Although being typical Mediterranean faunal elements, phlebotomine sandflies have also been recorded in central Europe for several countries including Germany, where two species, Phlebotomus mascittii and Phlebotomus perniciosus, occur. In Europe, P. mascittii is the northernmostly distributed phlebotomine species. While P. perniciosus is a proven vector of leishmaniasis as well as various sandfly fever causing phleboviruses, the situation for P. mascittii is different. For this species, vector competence could not be proven yet, but is strongly suspected. During an entomological survey in July 2013, one female sandfly was caught in Giessen in the German state of Hesse. Adjacent to the collection site, different potential habitats could be found. Morphological examination of the cibarium, pharynx, and genitalia revealed the specimen as P. mascittii. This is the first reported occurrence for Hesse, and not only the northernmost documented occurrence for P. mascittii, but also of the whole subfamily in the Palearctic region. New records of proven or suspected vectors are of medical relevance because of potential Leishmania and/or Phlebovirus transmission and the awareness therefore in the public.

C. Melaun : A. Werblow : S. Klimpel (*) Institute for Ecology, Evolution and Diversity, Goethe-University (GU), Biodiversity and Climate Research Center (BiK-F), Senckenberg Gesellschaft für Naturforschung (SGN), Max-von-Laue-Str. 13, 60438 Frankfurt am Main, Germany e-mail: [email protected]

Keywords Phlebotomus mascittii . Palearctic region . Phlebotominae . Northernmost locality . Leishmaniasis . Vector

Introduction Several species of Phlebotomus are proven or suspected vectors of protozoan parasites of the genus Leishmania, the causative agents of leishmaniasis. Therefore, sandflies are of high medical importance, especially in the Mediterranean area where they are typical faunal elements (Aspöck et al. 2008). For a long time, the possible occurrence of phlebotomine sandflies in central Europe north of the Alps has been denied. However, in 1999, one male and three female Phlebotomus (Transphlebotomus) mascittii Grassi, 1908 were caught in three smaller towns in southwestern Baden Württemberg, Germany (all at 47° N) (Naucke and Pesson 2000). Subsequently, P. mascittii was found at additional localities in Baden-Württemberg and in Rhineland-Palatinate near to Cochem (50° 19' N/07° 15' E), which represented the northernmost occurrence so far (Naucke et al. 2008). In 2001, a second species, Phlebotomus (Larroussius) perniciosus Newstead, 1911, was also documented (Naucke and Schmitt 2003) from near Kaiserslautern (Rhineland-Palatinate, at 49° N). In summary, it should be noted that knowledge about phlebotomine sandflies in Germany is scarce, as is reflected by the patchily clustered localities, which are unlikely to resemble the whole distribution.

C. Melaun e-mail: [email protected]

Materials and methods

A. Krüger Department Tropical Medicine, Military Hospital Hamburg, Bernhard-Nocht-Str. 74, 20359 Hamburg, Germany

During an entomology survey BG-Sentinel traps (Biogents, Regensburg) in the CO2 version with a UV-light set were

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operated at various sites within and around the Hessian city of Giessen (Germany) from the beginning of June till the end of September 2013. Hereby, the traps were positioned at different types of landscape. Depending on the weather conditions, the sampling intervals were 4 to 14 days with a mean of 7, the operation time was 24 h, and some traps were equipped also with BG-Lure (Biogents) as an additional attractant. On July 19th, one female phlebotomine sandfly was caught with one of the UV-light equipped traps. After that finding, the survey was intensified on the specific collection site using more traps with UV-light. As the mesh aperture of the original ones was too large, the collection bags were modified in August. Therefore, a 20 denier tight was altered to a collection bag with fixation band. For the morphological identification, the specimen was left in 70 % ethanol for about 5 min, and then the distal part of the abdomen (for the examination of the genitalia) and the entire head (for the examination of the cibarium and pharynx; Fig. 1) were removed with fine forceps. The head and distal part of the abdomen were cleared by incubation in 1 M KOH until the dark-reddish eye pigment had mostly faded (about 30 min). The remaining corpse was returned in absolute ethanol. After being cleared, the genitalia and head were transferred onto a slide, slightly squashed under a coverslip, and then immediately examined and photographed under a light microscope with an attached digital camera. The morphological identification was carried out using the keys provided by Theodor (1958). The differences between the two species occurring in Germany are shown in Table 1.

Fig. 1 Pharynx of the sampled specimen of Phlebotomus mascittii from Giessen, Hesse, Germany

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Results and discussion The specimen could be determined without ambiguity as P. mascittii following the characters shown in Table 1. The collection site (50° 35′ 41.3124′′ N; 8° 42′ 3.3624′′ E) was grassland with adjacent wooden areas about 500 m away from the next houses; a garden settlement with allotments and wooden arbors is located around 300 m away from the collection site. As a variety of different habitats, from which phlebotomine sandfly immature stages have been described (Feliciangeli 2004), are situated in the close neighborhood of the collection site, it is difficult to estimate where a possible breeding site could be located. Nevertheless, the one with the highest probability is the garden settlement. Here, the wooden arbors could serve as resting places for the adults and the organic compost material as breeding sites for the larval stages. Phlebotomus mascittii was found in most entomological studies in low numbers (e.g., Maroli and Bettini 1977; Veronesi et al. 2007). This might be because P. mascittii seems to be less attracted by light than other phlebotomine species (Poeppl et al. 2013), which influences directly the catch rate. The actual finding represents the first one in the German federal state of Hesse, as well as the easternmost locality for the species in Germany, but not within the species’ distribution (Fig. 2). Nevertheless, the locality deserves special attention. When comparing it with others from Europe, it is situated north of these. Even the Nearctic localities for Lutzomyia vexator (Coquilett, 1907) from Alberta, British Columbia and Ontario (Harwood 1965; Downes 1972; Shemanchuk et al. 1978) and the one from Alberta for Lutzomyia aquilonia (Fairchild & Harwood, 1961) are situated at more southern latitudes than Giessen. Consequently, the recent finding is the northernmost phlebotomine sandfly record in the Palearctic, probably even worldwide, close to 51° of northern latitude. At the same time, this places the hitherto estimated northern distribution limit due to climatic conditions, which was thought to be at the latitude of Frankfurt, i.e., 50° 7′ N (Naucke 2007), around 50 km to the north. This result leads to the assumptions that phlebotomine sandflies are more widely distributed in central Europe than known so far and that they probably have been overlooked in central Europe for a long time. Reasons for this can be their small size, their occurrence in small numbers, collection difficulties, as well as failure in recognizing them by nonspecialists. In total, 29 Phlebotomus sp. are recognized from geographical and political European countries. Of these, 12 are proven and 13 are suspected vectors for leishmaniasis and 5 species are also known to be vectors for different kinds of phleboviruses and in Phlebotomus longicuspis Punique virus could be detected (Zhioua et al. 2010). The distribution and vector competence of these species are listed in Table 2. Central European Phlebotominae records are regarded as remnants of warmer

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Table 1 Morphological characters to differentiate Phlebotomus mascittii and Phlebotomus perniciosus (after Theodor 1958)

Phlebotomus mascittii

Phlebotomus perniciosus

Female

Male

Spermatheca without neck, almost tubular, with irregular segmentation and wide efferent ducts; pharyngeal teeth consist of unregular scales in the rear quarter Spermatheca with long neck and 8–12 regular segments; pharynx teeth in the rear quarter, with a few reaching further anteromedially

Aedoeagus not bifid, narrowed gradually, with rounded tip. At the tip half as wide as at the base Aedoeagus bifid, spikes of the tip of about the same size and pointed

periods instead of being the result of recent immigration due to global warming. Nevertheless, due to climate change, the number of suitable areas could increase and migration would not only take place from the south, but also from the remnant sites. Interestingly, the climatic conditions of the collection site are currently more

Fig. 2 Distribution of Phlebotomus mascittii in Germany and the adjacent countries (Naucke and Schmitt 2003; Depaquit et al. 2005; Steinhausen 2005; Naucke et al. 2011; Naucke and Lorentz 2012; Poeppl et al. 2013). The red dot represents the new record

suitable for P. mascittii than in the future according to the projections made (Fischer et al. 2011), while according to the same authors, it will become in the future more suitable for Phlebotomus ariasi Tonnoir, 1921, Phlebotomus neglectus Tonnoir, 1921, and P. perniciosus. The latter species is already known from Germany and a

Adlerius

Adlerius

Adlerius

Adlerius

P. halepensis Theodor, 1958

P. kyreniae Theodor, 1958

P. longiductus Parrot, 1928

Unknown

Yes (Giorgobiani et al. 2012)

(Armenia), (Azerbaijan), (Georgia), Turkey Spain

Larroussius

Larroussius

P. kandelakii Shchurenkova, 1929

Albania, Bosnia and Herzegowina, Croatia, Greece, Italy, Makedonia, Russia, Serbia, Slovenia

Larroussius

Larroussius

Larroussius

Larroussius

Larroussius

Larroussius

Paraphlebotomus

Paraphlebotomus

Paraphlebotomus

Paraphlebotomus

P. neglectus Tonnoir, 1921

P. perfiliewi Parrot, 1930

P. perniciosus Newstead, 1911

P. tobbi Adler et al., 1930

P. syracus Adler & Theodor, 1931

P. wenyoni Adler & Theodor, 1930

P. alexandri Sinton, 1928

P. caucasicus Marzinowsky, 1917

P. chabaudi Croset et al., 1970

P. jacusieli Theodor, 1947

Albania, (Azerbaijan), Cyprus, Greece, Turkey

Albania, (Azerbaijan), Bulgaria, Cyprus, Greece, Romania, Spain (Armenia), (Azerbaijan), Bulgaria, (Georgia), Greece, Makedonia Spain

(Georgia), Turkey

Albania, (Azerbaijan), Bosnia and Herzegovina, Bulgaria, Croatia, Cyprus, (Georgia), Greece, Hungary, Italy, Makedonia, Romania, Serbia, Slovenia, Turkey, Ukraine Albania, Andorra, (Azerbaijan), Bosnia and Herzegovina, Bulgaria, Croatia, Cyprus, France, Germany, Greece, Italy, Makedonia, Malta, Portugal, Romania, Serbia, Slovenia, Spain, Switzerland Albania, (Azerbaijan), Bosnia and Herzegovina, Croatia, Cyprus, (Georgia), Greece, Italy, Serbia, Slovenia, Turkey (Armenia), (Azerbaijan), (Georgia), Ukraine

Spain

Larroussius

Larroussius

P. langeroni Nitzulescu, 1930

P. longicuspis Nitzulescu, 1930

Yes (Depaquit et al. 2010)

Unknown

Yes (Jiménez et al. 2013)

Yes (Léger et al. 2000)

Unknown

Suspected (Croset et al. 1978)

Suspected (Rassi et al. 2012)

Yes (Guan et al. 1986)

Unknown

Unknown

Unknown

Unknown

Unknown

Unknown

Yes (Depaquit et al. 2010)

Yes (Maroli et al. 1987)

Suspected (Adler and Theodor 1957) Suspected (Coleman et al. 2007)

Yes (Depaquit et al. 2010)

Dogs, humans

Dogs, humans

Unknown

Dogs, humans

Unknown

birds (suspected), humans

Dogs, humans, rodents

Unknown

Dogs, humans

Unknown

Birds (suspected), humans

Hosts

Bats, humans (both suspected)

Unknown

Humans, rodents

Humans

Humans, rodents (both suspected)

Dogs, humans

Dogs (suspected), goats, sheeps

Birds, dogs, horses, humans, rodents, sheep

Birds, dogs (suspected), goats, horses, humans, sheep

Dogs (suspected), horses, humans, rodents

Suspected (Zhioua et al. 2010) Dogs, humans

Unknown

Unknown

Unknown

Yes (Depaquit et al. 2005)

Unknown

unknown

Suspected (Killick-Kendrick 1990) Yes (Antoniou et al. 2013)

Yes (Guerbouj et al. 2007)

Yes (Giorgobiani et al. 2012)

Unknown

Yes (Franco et al. 2010)

Larroussius

P. galilaeus Theodor, 1958

Cyprus, Turkey

Andorra, France, Italy, Portugal, Spain

Anaphlebotomus

P. simici Nitzulescu & Nitzulescu, 1931 P. fortunatarum Ubeda Ontiveros et al., 1982 P. ariasi Tonnoir, 1921

Unknown

Suspected (Lewis and Unknown Ward 1987) Suspected (Killick-Kendrick Unknown 1990) Suspected (Lupascu et al. 1977) Unknown

Phlebovirus vector

Leishmaniasis vector

Suspected (Killick-Kendrick 1990) Albania, Bosnia and Herzegowina, Bulgaria, Croatia, yes (Aransay et al. 2000) Greece, Makedonia, Romania, Serbia, Slovenia Spain Unknown

Bulgaria, Croatia, Hungary, Romania

Cyprus, Turkey

(Azerbaijan), (Georgia), Turkey

P. brevis Theodor & Mesghali, 1964 Adlerius

Adlerius

Distribution in Europe Albania, (Azerbaijan), Bosnia and Herzegowina, Bulgaria, Croatia, (Georgia), Greece, Hungary, Makedonia, Romania, Serbia, Ukraine (Azerbaijan), (Georgia), Greece, Malta

P. balcanicus Theodor, 1958

Subgenus

Table 2 European sandfly species with their distribution and vector abilities (after Defense Pest Management Information Analysis Center 2001; Naucke 2002)

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Paraphlebotomus

P. sergenti Parrot, 1917

(Azerbaijan)

Transphlebotomus Albania, Austria, Belgium, Croatia, Cyprus, France, Germany, Greece, Italy, Slovenia, Spain, Switzerland, United Kingdom (Jersey)?

Unknown Unknown

Unknown Suspected (Antoniou et al. 2013)

Yes (Jennings and Boorman 1983)

Yes (Antoniou et al. 2013)

Dogs, horses, humans

Unknown

Birds, dogs, horses, humans, sheep

Bats (suspected), humans

Dogs, bats (suspected), humans

Unknown

Unknown

Humans, rodents

Humans, rodents

Hosts

Unknown

Unknown

Phlebovirus vector

Suspected (Depaquit et al. 1998)

Suspected (Killick-Kendrick 1990) Suspected (Killick-Kendrick 1990) Yes (Alptekin et al. 1999)

Leishmaniasis vector

Countries which belong politically but not geographically to Europe are mentioned in parenthesis, records for Turkey can refer also to the Asian part of the country

P. economidesi Léger et al., 2000 P. mascitti Grassi, 1908

P. papatasi Scopoli, 1786

P. similis Perfiliew, 1963

Paraphlebotomus

P. mongolensis Sinton, 1928

Turkey

Distribution in Europe

Albania, (Armenia), (Azerbaijan), Bosnia and Herzegovina, Bulgaria, Croatia, Cyprus, France, (Georgia), Greece, Italy, Makedonia, Malta, Portugal, Romania, Serbia, Slovenia, Spain, Turkey, Ukraine Paraphlebotomus Albania, (Armenia), (Azerbaijan), Bosnia and Herzegovina, Bulgaria, Croatia, (Georgia), Greece, Makedonia, Romania, Serbia, Slovenia, Ukraine Phlebotomus Albania, (Armenia), (Azerbaijan), Bosnia and Herzegovina, Bulgaria, Croatia, Cyprus, France, (Georgia), Greece, Hungary, Italy, Makedonia, Malta, Portugal, Romania, Serbia, Slovenia, Spain, Turkey Transphlebotomus Cyprus

Paraphlebotomus

Subgenus

P. kazeruni Theodor, 1958

Table 2 (continued)

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proven vector for Leishmania infantum in the Mediterranean region (Ready 2010), where dogs are of particular importance as reservoir hosts. Depending on the region, the infection rate among stray dogs can be more than 50 %, locally even 90 % (Aspöck et al. 2008). Usually, dogs stay infected by the parasite for the whole life and can serve, even without showing symptoms, as a reservoir host and pass the parasite to other dogs (Poeppl et al. 2013). Numerous stray dogs from Mediterranean countries are brought to Germany by tourists or animal welfare organizations. In recent years, rising numbers of infected dogs have been imported to central Europe, leading to an increase of Leishmania and a possible establishment of the disease (Aspöck et al. 2008). Nowadays, around 20,000 infected dogs live in Germany (Naucke and Lorentz 2012). Several autochthonous cases of leishmaniasis have been reported from Germany in the last 13 years, involving mainly dogs, but also a horse as well as a child (Bogdan et al. 2001; Koehler et al. 2002; Naucke et al. 2008). Additionally, infected male dogs are able to infect healthy females, as Leishmania can shed in the male dogs’ semen. Just recently, the first verticalvenereal transmission of canine leishmaniosis was reported for Germany (Naucke and Lorentz 2012). Such transmission routes may facilitate dramatically the spread and possible establishment of the disease among dogs in central Europe. However, the endemic areas of leishmaniasis correspond mainly with the geographic distribution of the vector (Lewis 1974), and introduction of the vector in such areas can lead to an establishment of the parasite and hence of the disease. It is therefore crucial to confirm or rule out, respectively, the potential autochthonous source of each canine and human case, when potential vectors are also present. Due to the high morbidity of leishmaniasis, especially when immunosuppressed persons and young children are involved, the occurrence of the disease has to be acknowledged and properly communicated, as this is crucial for an early diagnosis as well as treatment (Aspöck et al. 2008). Therefore, it is essential to answer the question, whether P. mascittii is a competent leishmaniasis vector, especially concerning the fact that it bites humans as well as dogs. Although the vectorial capacity of P. mascittii is unproven, but regarded as possible (Antoniou et al. 2013), the species has to be taken into account when estimating future health risks concerning leishmaniasis or phleboviruses. Acknowledgments The present study was financially supported by the research funding programme “LOEWE—Landes-Offensive zur Entwicklung Wissenschaftlich-ökonomischer Exzellenz” of Hesse's Ministry of Higher Education, Research, and the Arts, by the SAW (Senate Competition Committee) grant (SAW-2014-SGN-3) of the Leibniz Association as well as the German Research Council (BiodivERsA grant no. DFG KL 2087/6-1).

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New record of the suspected leishmaniasis vector Phlebotomus (Transphlebotomus) mascittii Grassi, 1908 (Diptera: Psychodidae: Phlebotominae)--the northernmost phlebotomine sandfly occurrence in the Palearctic region.

Although being typical Mediterranean faunal elements, phlebotomine sandflies have also been recorded in central Europe for several countries including...
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