Acta Tropica 153 (2016) 6469

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Acta Tropica
journal homepage: www.elsevier.com/locate/actatropica

Phenology and host preferences Phlebotomus perniciosus (Diptera:

Phlebotominae) in a focus of Toscana virus (TOSV) in South of France
C. Cotteaux-Lautard a, , I. Leparc-goffart b , J.M. Berenger c , S. Plumet b , F. Pages d
a
UMR-MD1, Transporteurs membranaires, Chimiorsistance et Drug-Design, Facult de mdecine, 27 boulevard Jean Moulin, 13385 Marseille cedex 05,
France
b
French National Reference Centre for Arboviruses, IRBA Armed Forces Biomedical Research Institute, 13013 Marseille, France
c
Aix Marseille Universit, Unit de Recherche en Maladies Infectieuses et Tropicales Emergentes (URMITE), UM63, CNRS 7278, IRD 198 (Dakar, Sngal),
Inserm 1095, WHO Collaborative Center for Rickettsioses and Other Arthropod-Borne Bacterial Diseases, Facult de Mdecine, 27 bd Jean Moulin, 13385
Marseille cedex 5, France
d
Regional Ofce of the French Institute for Public Health Surveillance (Cire OI, Institut de Veille Sanitaire), Saint-Denis, Runion, France

a r t i c l e

i n f o

Article history:
Received 16 June 2015
Received in revised form
21 September 2015
Accepted 27 September 2015
Available online 22 October 2015
Keywords:
Phlebotomus perniciosus
TOSV
Ecology
Garlaban

a b s t r a c t
This paper reports on an entomological survey performed over the period 20092011 in endemic focus of
peri-urban TOSV in South of France located from 24 km east of Marseille. Sand ies were captured using
CDC light traps set in sand y resting places overnight, and temperature, relative humidity and wind
were recorded to establish possible relations between meteorological factors and vector densities. The
most common species, of 5,432 specimens collected and identied, was Phlebotomus perniciosus (74%),
followed by Sergentomyia minuta (6%) and Phlebotomus ariasi (1%). Male ies were highly predominant
for all Larroussius species instead of S. minuta which counted (85%) of females. The results shed light
on the wide populations dynamic of P. perniciosus in France showing a diphasic seasonal trend with
two abundance peaks at the beginning of July and late August, when a mean temperature is from 23.3
to 25.7 C. Interestingly, these two peaks are corresponding to the peaks of occurrence of human TOSV
cases. Among the 1724 females collected, 549 (32%) were blood-fed. Based on the results of blood meal
analyses, P. perniciosus fed on large animals diversity (man, chicken, rabbit, others mammalians, etc.),
including bats that are the only species found naturally infected by TOSV. Results indicate that host
choice was probably related to its availability than specic attractiveness. Data presented conrm that
sand ies easily adapted to the periurban sites like, P. perniciosus may represent a public health concern
for pathogen transmission in similar Mediterranean environments.
2015 Elsevier B.V. All rights reserved.

1. Introduction
Phlebotomine sand ies (Diptera: Phlebotominae) are vectors
of Leishmania, Bartonella and phleboviruses affecting humans and
other vertebrates in warmers parts of the world. There populations were controlled particularly in leishmaniasis survey, and
recently for ARBOviroses (TOSV). In France, seven species have
been described: Phlebotomus perniciosus [Newstead, 1911], Phlebotomus ariasi [Tonnoir, 1921], Phlebotomus mascittii [Grassi, 1908],
Phlebotomus sergenti [Parrot, 1917], Phlebotomus papatasi [Scopoli,
1786], Sergentomyia minuta [Rondani, 1843] (Raynal, 1954) and
Phlebotomus perliewi [Parrot, 1930] (Izri et al., 1994). P. perniciosus, main vector of Leishmania infantum and phleboviruses in

Corresponding author. Fax: +33 4 91 32 46 06.

E-mail address: lautard.christelle@gmail.com (C. Cotteaux-Lautard).
http://dx.doi.org/10.1016/j.actatropica.2015.09.020
0001-706X/ 2015 Elsevier B.V. All rights reserved.

southeast of France, was found in 1920 for the rst time in Bouchesdu-Rhnes by Pringault (Raynal, 1954).
We report here a detailed study of sand ies from South of France
to further understand aspects of their ecology, and implication on
epidemiological risk.
2. Materials and methods
2.1. Study area
The studied site is located from 24 km east of Marseille (SN: 43,3396; SE: 5,5844), with a population density of
361 habitant/km2 . This peri-urban territory belongs to Garlabans massif, a calcareous formation with a maximum altitude of
731 m. Its vegetation is divided into forest (Pinus halepensis, Pinus
sylvestris, Quercus ilex and Quercus pubescens) and scrubland with
bushes and low plants. Our study area consists more precisely

C. Cotteaux-Lautard et al. / Acta Tropica 153 (2016) 6469

Fig. 1. Study area (

65

) located in periurban zone, about 25 km far from Marseille.

of Mediterranean-type maquis with cultivated hilly areas, mainly

with orchard (predominantly fruit trees) on 197 m of altitude,
surrounded by mountainous promontory (average altitude 600 m
above sea level) (Fig. 1). The place has a Mediterranean climate
with hot, dry summer (temperature values between 2535 C) and
maximum rainfalls during spring and autumn. In this area, TOSV
human cases have been reported by the regional health agency
and TOSV infected P. perniciosus (males and females) have been
caught during summer 2009 (Brisbarre et al., 2015). Traps have
been deployed in an old farm surrounded by olive groves and
individual houses in the bottom on a valley, where we can found
animals farm (rabbits chicken), pets (catsdogs), various wild animals (rodents, birds, reptiles, . . .) and human habitants. Dogs were
presents in the area but, there the number was limited by the burden of canine leishmaniasis that has discouraged habitants to have
them.

2.2. Sandy collection and identication

CDC light traps model 512 (John W. Hock, Gainesville, FL, USA)
for sand ies were set inside animal shelters (rabbit and chicken)
with low luminosity, favouring their presence (Izri et al., 1992),
before sunset and collected the next morning. These traps allow
catching signicantly more specimens of different species (Boussaa
et al., 2009), they were captured through out summer once a mouth,
from July 2009 to September 2009, and once a week from July
2010 to November 2011, with interruption between December and
February.
Insects were transported alive to laboratory where they were
frozen at 20 C and stored until analyses. At the rst time, insects
were separated into pools by sex, captures localization and date.
Sand ies were dissected; the head and genitalia were cut off
using sterile needles, cleared in MarcAndr solution, and then
mounted under a cover slip for microscopic identication. It was
based on examination of the pharyngeal armatures and spermathecae morphology (females) or external genitalia (males) (Lewis,
1982).

2.3. Meteorological data and analysis

Meteorological data, such as daily mean temperatures, high and
low extremes, precipitations, relative humidity and wind during
the study period, were recorded (http://www.previmeteo.com/, La
Destrousse). Data do not follow normal law, so Spearman correlation was used to express the relationship between sand ies
population and climate variables. Statistical tests were performed
using the SigmaPlot software (Systat software Inc., San Jos, California).
2.4. Blood meal determination and host preference analysis
Engorged females were conserved and then classied into three
levels: freshly fed, partially fed and late fed according to the amount
and colour of the blood in the intestine, bright red, dark red and
brown respectively. Blood and tissue samples were disrupted by
mechanical homogenization in Phosphate Buffered Saline-BSA 3%
(PBS; P3813-10PAK, SigmaAldrich, France). Identication of blood
meals is essential to the determination of host range and host preference of insect vectors.
Whole blood DNA was extracted from the abdomen of sand ies,
using the QiaAmp blood DNA mini Kit (Qiagen, 69,506, France) and
eluted in 50 l of elution buffer. DNA concentration was measured
using a Nanodrop 2000 spectrophotometer (W6807L, Thermoscientic Nanodrop, France). We used the primers L14841 (5 AAAAAGCTTCCATCCAACATCTCAGCATGATGAAA-3 ) and H15149
(5 -AAACTGCAGCCCCTCAGAATGATATTTGTCCTCA-3 ) (Dias et al.,
2010) to amplify a 305 bp segment of the cytochrome b gene
from the host DNA. The PCR reactions were performed in 25 l
total volumes, including 25 ng of total genomic DNA, 0,08 mM of
each nucleotide, 3 mM of MgCl2 , 1X PCR buffer, 0,4 M of each
primer and 0,04 units of GoTaq Flexi DNA Polymerase (M8306,
Promega, France). At each PCR a negative control containing distilled water instead of DNA was run in parallel. PCR products
were examined by electrophoresis in a 2% agarose gel with ethidium bromide and puried by using kit Wizard SV Gel and PCR
Clean-up System (A9285, Promega, France). The concentration and

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C. Cotteaux-Lautard et al. / Acta Tropica 153 (2016) 6469

Table 1
Spearman analyses on correlation between Phlebotomus perniciosus collected during
each year.

P. perniciosus 2009
P. perniciosus 2010

P. perniciosus 2010

P. perniciosus 2011

Spearman

P-value

Spearman

P-value

0.5

0.450

0.6
0.484

0.35
0.0748

integrity of each DNA samples were assessed by spectrophotometry

(W6807L, Thermoscientic Nanodrop, France) and were sequenced
directly in cycle sequencing reactions by using the primer H15149
(Big Dye, Applied Biosystem). We tested a total of 549 samples
yielded a PCR product that we could sequence. The hereby obtained
FASTA les were then used for species identication with the
nucleotidenucleotide basic alignment search tool (BLAST) in GenBank DNA sequence database (NCBI) (http://www.ncbi.nlm.nih.
gov/). The primers for the cytochrome b gene used here easily
amplify from human material. We therefore, took the following
precaution to exclude the possibility that the obtained human
sequences resulted from contamination of human DNA, either from
persons collecting the insects or working with the material in the
laboratory.
The remaining tissues (thorax, wings, legs and abdomen) were
suspended in 50 l of sterile Phosphate Buffered Saline-BSA3% with
microbeads (Lysin Matrix E, 6914,100, MP Biomedicals, France) and
crushed at 20 vibrations per second in a tissue homogenizer (TissueLyser, 1185,300, Qiagen, France). Lysated tissues were stored at
20 C until used for pathogens diagnostic.

3. Results
3.1. Sandies fauna composition and dynamic
Collecting site was positive for sand ies. During the 3 years
of study, 5432 sand ies were caught (68% of males) belonging to
the genera Phlebotomus and Sergentomyia. Among the members of
the subgenus Larroussius, P. perniciosus (74%) was the most represented, and then we nd S. minuta (6%) and P. ariasi (1%). The
study did not show a markedly different sand ies density and
composition between 20102011, with respectively 2251 (72% of
P. perniciosus) and 2657 (80% of P. perniciosus) captured specimens.
Results of 2009 did not be exploited on this part because of monthly
capture instead of weekly collection on 2010 2011, induced gap
on information. The rst positive collection of P. perniciosus was
recorded in mid-May and the last in early October (Fig. 2). The
adults were active during 6 months (MayOctober) showing a typical diphasic distribution in France, which normally is described
with a single peak from July to August on Cvennes (Rioux et al.,
1969).
As regards S. minuta, the rst specimen was collected in the end
of June and the last in mid-September (data not showed) of the
333 specimens collected (85%) were females. Lastly, P. ariasi were
collected occasionally on July, August and September on this site.
Additionally, we make correlation analyse between annual populations (Table 1), and between meteorological data recorded
during study and P. perniciosus population (Table 2). Dynamic of P.
perniciosus populations between each year do not have correlation
and were not affected by relative humidity and wind variations.
Weekly mean temperatures were positively correlated with P. perniciosus distribution. Indeed, the populations uctuation of P.
perniciosus follows the temperatures curb (Fig. 3). Two genders follow the same kind of diphasic dynamic during season. But, contrary
to laboratory data, which establish that sex ratio is 1 on emergence

(Dolmatova and Delina, 1966), our study in the eld found a sex
ratio of 2,4 (71% males).
3.2. Blood meal analysis
Blood-meal sources were successfully identied by DNA
sequencing from (47%) of female P. perniciosus. Among the 220
positive results, 68 (31%) contained avian blood and 149 (68%) contained mammalian blood (Table 3). More than (43%) of the sand
y specimens collected inside the rabbit and chicken house were
found to have fed on the animals occupying these respective shelters.
4. Discussion
Light trap captures allowed the identication of 5432 sand ies
belonging to 3 species, from 2 genera, conrming the large density
of phlebotomines fauna at the Garlaban, and that great difference
exists between collected species. The presence of P. perniciosus, P.
ariasi and S. minuta conrms previous data on sand ies population
in France under 200 m a.s.l. (Rioux and Golvan, 1969), and more particularly around Marseille (Bron M, 1994). S. minuta sand ies were
not continuously caught throughout the collecting period. Data are
conformed to Maroli and Bettini, 1975 observations on Italy in 1975.
Among the identied species, two (75%) presented a health public
concern; P. ariasi and P. perniciosus but only P. perniciosus was sufciently abundant to be of health concern. The low density of P.
ariasi could be explained by the peri-urban localisation of study, as
P. ariasi is a rural species (Rioux and Golvan, 1969).
P. perniciosus is considered as the most abundant species in the
Mediterranean-type vegetation where it is thought to be the principal vector involved in the transmission of pathogens. The range
of activity of P. perniciosus in this part of South France is clearly
bimodal. Indeed, this kind of evolution of P. perniciosus population
with a highest rate at the beginning and at the end of the warm
season is more current in Maghreb (Dedet et al., 1984), or in Italy
(Maroli and Bettini, 1977). The rst peak appears from end June to
the beginning of July during the two years study. It could result from
a massive emergence of larva in diapause during winter. The second
peak, more important, appears at the end of August and can spread
out September. It seems to represent a second generation lead during summer. These ndings, two peaks, corresponding with two
successive generations, separated from 6 to 7 weeks, is conformed
with the biological cycle of sand y in laboratory condition, 3545
days for complete development (Dolmatova. and Delina, 1966). In
2009, the repartition of TOSV cases in the PACA region was also
clearly bimodal with a rst peak of cases from May to July and
another one from the end of August to the end of September. (Six
et al., 2014). We can hypothesis that the rst peak of transmission
could be due to the emergence of transovarian infected females
during the rst peak of emergence.
Our results conrm that on peri-urban focus the dominant
sand y is P. perniciosus (Rioux et al., 1982), but diphasic seasonal
distribution is a particular data for France, because it was only
mentioned on studies around Marseille (Bron, 1994; Gillet, 1981).
This difference could be explain by specic warming climate which
increase summer season and allows two successive emergence
events. Environmentalmeteorological factors like mean daily temperatures, affect the density and distribution of sand ies. Beyond
these data, Brons study in 1994, suggested that bimodal tendency
of P. perniciosus would be explained by competition phenomenon
with other sand ies species like S. minuta. This hypothesis does
not be veried in our study because population peaks of these two
species are simultaneous (data not showed). On the other hand, as
show with results from 2009, the difference on trend population

C. Cotteaux-Lautard et al. / Acta Tropica 153 (2016) 6469

67

Fig. 2. Seasonal trends in Phlebotomus perniciosus density during three years of study ( 2009,  2010 and 2011).
Table 2
Spearman analyses on correlation between Phlebotomus perniciosus collected and meteorologicals data (weekly mean temperature, relative humidity and wind).
Weekly mean temperatures

P. perniciosus 2009
P. perniciosus 2010
P. perniciosus 2011

Relative humidity

Wind

Spearman

P-value

Spearman

P-value

Spearman

P-value

0
0.769
0.874

1
0.000308
0.0000002

0.4
0.212
0.0107

0.517
0.441
0.960

0.1
0.382
0.460

0.950
0.154
0.0310

Fig. 3. Density of male () and female () Phlebotomus perniciosus collected during the third year (2011) and variations in weekly temperature ().

with Rioux monophasic description in Cvennes could also be due

to data gap. Indeed, with monthly collection we cannot clearly see
the diphasic distribution of P. perniciosus population.
The high quantity of sand ies found in shelters can be explained
by the plentiful organic matter of the soil and as this is the natural habitat of these insects. The shelters are corresponding to the
ecotypes usually occupied by immature phlebotomines which are

organically rich moist soils (Feliciangeli, 2004). Indeed, the developmental stages were associated with a relatively stable, cool and
humid environment protected from sunshine and rain, rich in clay
and organic matter and particularly chicken or rabbit faeces (Pozio
et al., 1985; Bettini et al., 1986, 1991; Bettini and Melis, 1988;
Dougherty et al., 1993). Our results suggest this focus associates
characteristics of sand ies breeding site.

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C. Cotteaux-Lautard et al. / Acta Tropica 153 (2016) 6469

Table 3
Results of blood meal identication of sand ies female collected in 20102011.

Rabbit pens
Engorged females number
%
Chicken house
Number
%
Total
Engorged females number
%

Rabbit

Chicken

Human

Shrew

Bat

Cat

Cow

Amphibian

Other rodents

Other birds

43
28.5%

12
7.9%

20
13.2%

47
31.1%

12
7.9%

1
0.7%

1
0.7%

3
2.0%

11
7.3%

1
0.7%

2
2.9%

53
76.8%

6
8.7%

3
4.3%

1
1.4%

0
0.0%

0
0.0%

0
0.0%

2
2.9%

2
2.9%

45
20.5%

65
29.5%

26
11.8%

50
22.7%

13
5.9%

1
0.5%

1
0.5%

3
1.4%

13
5.9%

3
1.4%

On the other hand, information obtained on blood-meal sources,

could conrm that this shelter corresponding on a phlebotomine
sand y breeding site (Table 3). Undetermined blood meals seem
to be due to the sand y taking only a small amount of blood from
its host or having time to digest most of the meal before capture
(Table 3). Moreover, sand ies can feed on multiple hosts, like
mention for (16%) of P. perniciosus (De Colmenares et al., 1995),
which disrupt sequencing analysis. Our results suggest that local
population of P. perniciosus did not necessary imply a higher preference for a particular host. Availability, low defensive behaviour
and skin accessibility (Coulange, 2011) can explain frequent feeding on chikenrabbit. Animals in cellars represent a rich source of
blood and may serve as an important breeding place for sand ies
(Lane, 1986).
Sand ies capture and analyse on this collection site shows
that it present breeding sites characteristics, that suggest implications of shelters presence for the epidemiology in peri-urban
areas, where sand y females may bite humans.
The blood meal analysis showed the high diversity of P. perniciosus hosts. This lack of specicity is often a characteristic of zoonotic
diseases vectors. However, poultry and rabbits were always available to P. perniciosus more than (11%) fed on human, at least (28%)
fed on wild rodents and almost (6%) on bats. These data highlight
the role of P. pernicious as a bridge vector between wild fauna,
domestic fauna and humans. If transovarian transmission of TOSV
has been showed in lab and in the eld, it seems insufcient to
maintain a natural foci and the probable existence of a reservoir
or of amplicator host has been suggested. In the eld, TOSV has
been isolated in the brain of a bat in Italy (Verani et al., 1988). Bats
are currently considered of high concern for the emergence of new
strains of viral or bacterial diseases and are suspected to be the
natural source of many emergent viruses (i.e. nipah, hendra, cetar,
ebola, etc.). Further studies should assess the potential role of wild
rodents and bats as natural host of TOSV. Another point is the ability of P. perniciosus to feed on reptiles (1.4%) in situation where
other sources of blood meal are available. This is a new challenge
to the old dogma considering that Phlebotomus spp. fed only on
warm-blooded animals and that Sergentomyia spp. feed only on
cold-blooded animals (Berdjane-Brouk et al., 2012).
Our results show that by a majority P. perniciosus has no feeding
preferences and this vector species is an opportunistic feeder and
has an eclectic habit for food, adjusting its eating habits to the availability of hosts at anthropic environments (Bongiorno et al., 2003).
Blood-feeding behaviour studies have been critically important for
estimating the efciency of pathogen transmission and assessing
the relative human disease risk.
We did not nd a link between P. perniciosus abundance and
wind or relative humidity. This observation is probably due to
the resting habitat protecting them from adverse climatic conditions, which conrm that P. perniciosus is able to colonize domestic
environment (Rossi et al., 2008). Futhermore, our results conrm
bibliographic data on the necessity of 10 days with 18.9 C or 1
day with 20.3 C in order to activate the rst sand ies hatching

(Dolmatova and Delina, 1966). The optimal temperature for adults

P. perniciosus activity seems to be from 23.3 to 25.7 C. The sex ratio
is 2.4 (71% males) in our study, a information tallies with others
natural studies in Mediterranean region (Helal et al., 1987). We
could suppose that difference observes on wild collection is due to
the great mortality during females oviposition, like observed on
laboratory with (34.8%) of females surviving to exhaustion of laying eggs (Alarcn-Elbalet al., 2011). Also, blood meals taken can
be risky. In order to ripen ecological data, it could be necessary to
analyse the part of nullipare females and of young males (genitalia turned to 180 ). For two genders, it appears that mean weekly
temperature is positively correlated with trend population. And like
observe on Cvennes, temperatures decrease seems to reduce generations number and so risk of transmission. It important to note
that climate changes would enhance the number of days favourable
for transmission of pathogens due to higher density and activity
of sandies during a longer period, which will increase the phleboviruses incidence.
The data obtained in this research increased our knowledge,
showing that P. perniciosus can be considered the principal vector
in this region due to its high abundance and distribution. Sand y
adults were active from end of May until the third week of October.
Moreover, P. perniciosus fauna presents bimodal population trend
only recorded in Mediterranean basin in France. Phenological
observations may help to understand the phlebotomine-bornediseases epidemiology, and determine the optimal period of control
measure; because greatest is phlebotomine population, greatest are
transmissions risks. Environmentalmeteorological factors could
provide useful information on the spatial and temporal trends and
risks.
Acknowledgments
We greatfully thank the entomology staff of IRBA for their
support on the eld and M Killick-Kendrick for his knowledges
transmission. We also wish to thank Dr. Sebastien Emonet for the
constructive discussions on study design and the suggestions for
the manuscript drafting.
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