SEARCH

SEARCH BY CITATION

Keywords:

  • Sand flies;
  • fauna;
  • abundance;
  • seasonal activity;
  • altitude;
  • diversity;
  • similarity

ABSTRACT:

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

This paper presents the results of an entomological survey in an endemic focus of cutaneous leishmaniasis in the Cukurova region of Turkey. A total of 8,927 specimens belonging to eight Phlebotomus and two Sergentomyia species were captured with sticky papers and CDC light traps from 52 stations. Phlebotomus tobbi Adler, was found to be the most abundant species. Sand fly activity started in May and ended in October. Abundance was highest in August. According to the frequency distributions among certain temperature intervals the observed number of individuals was significantly different from the expected values between 22–24° C and 28–30° C. There was no significant correlation between the abundance of sand flies and altitude. However, sand fly species showed great aggregation at the 100–199 m and 200–299 m altitude intervals. The Shannon–Weinner index indicated no difference between the diversity and abundance of sand flies at different altitudes. Diversity and evenness reached maximum values at 500 m. Jaccard's coefficient indicated that similarity was the highest between 0–99 and 300–399, 0–99 and 500–599 and 100–199 and 200–299 m and lowest between 100–199 and 300–399 and 100–199 and 500–599 m.


INTRODUCTION

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

Phlebotomine sand flies are vectors of Leishmania parasites in Anatolia. Twenty-six species (or subspecies recently raised to species level) belonging to the Phlebotomus and Sergentomyia genera have been described within Anatolia (Houin et al. 1971, Lewis 1982, Ozbel et al. 1995, Volf et al. 2002, Yaman and Dik 2006, Simsek et al. 2007), with nine of these species being proven or probable vectors of human leishmaniasis in the Old World (Killick-Kendrick 1990).

Geographically, Anatolia is a unique landmass with substantial ecological and climatic heterogeneity and constituting a bridge between the three continents of Europe, Asia, and Africa. Anatolia presents numerous suitable habitats for the proliferation of both the vector and the parasite and, coupled together with its importance as a north-south/east-west corridor, can play a vital role in the epidemiology and spread of leishmaniasis.

Two clinical types of leishmaniasis have been recorded in Turkey: cutaneous leishmaniasis (CL) caused by Leishmania tropica (Wright 1903) (Volf et al. 2002) and L. infantum (Svobodova et al. 2009) and visceral leishmaniasis (VL) caused by L. infantum. CL is highly endemic in the south and southeast of Anatolia while VL is endemic along the Aegean and Mediterranean coasts, however it can occur sporadically in other regions as well (Ozbel et al. 1995, Ok et al. 2002, Volf et al. 2002, Yaman and Ozbel 2004).

Recently, the Cukurova Basin, situated in south Anatolia, has become an endemic focal point for CL research due to the significant increase in the number of CL cases over the past ten years. Previous studies have shown a large diversity and abundance of sand fly species within the region, with most of the species being proven vectors of CL (Simsek et al. 2007, Svobodova et al. 2009). Recently, Svobodova et al. (2009) identified the etiological agent of CL in the Cukurova Region as L. infantum, and P. (Larroussius) tobbi was clearly shown to be the vector of CL within the basin. Additionally, since the Cukurova Region is a crossroad between western and eastern Anatolia, and since almost 70% of the region is covered by agricultural plantations, the immigration and emigration rates in the basin are high. This raises the importance of the area with regard to epidemics of leishmaniasis, and the also wide-range distribution of sand fly species.

All of the above makes it necessary to re-evaluate the sand fly fauna of the Cukurova Region, taking into account population densities and seasonal dynamics of sand fly populations within the region. Determining faunal compositions and seasonal dynamics of vector species is crucial for controlling and designating factors responsible for the transmission of such diseases as CL and VL. Therefore, the aim of this research was to evaluate the sand fly fauna of the Cukurova Region, its distribution in relation to altitude and climatic factors, and to present the results of a one year monitoring study detailing the seasonal dynamics of sand fly species.

MATERIALS AND METHODS

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

The study area

The Cukurova Basin is approximately 28,000 km2 in area, surrounded by the Taurus Mountains on the west and north, Amanos Mountains on the east and the Mediterranean Sea on the south. The plain is nourished by the Seyhan and Ceyhan rivers, flowing respectively from the west and east directions. The present study was carried out within the Tarsus, Adana and Osmaniye provinces and their surrounding areas (Figure 1).

image

Figure 1. Map of the study area showing the main sites sampled, the main geographical barriers between the sites, and cities. (▴) indicates the sampling sites.

Download figure to PowerPoint

The Cukurova Basin has a temperate climate with long summers and short and rainy winters. The regional climate is also suitable for sand flies and the warm season coincides reasonably well with their life cycle (Lewis 1982, Volf et al. 2002). The mean annual precipitation is 636.8 mm for Adana and 761.0 mm for Osmaniye. The relative humidity and mean annual temperature is 66% and 18.7° C for Adana and 67% 19.6° C for Osmaniye provinces.

Most of the area is fertile (mollisol and alluvial soil) and used for agricultural activities but Pinus and Abies forests are also cultivated. The villages are usually surrounded by citrus orchards and cotton fields, these being most common in the eastern part. Residents live in single-family houses built from briquette, adobe, stone, and cement surrounded by gardens with henhouses and sheep or cattle sheds. Altitudes range from sea level up to 530 m.

Sand fly collection and identification

Fifty-two villages were selected as sampling stations (Table 1, Figure 1). Sand flies were sampled monthly both indoors and outdoors from April to October, 2006 using standard CDC light traps (John W. Hock, U.S.A.), sticky papers, and mouth aspirators (Alexander 2000). In every village light traps were placed 1.5 meters above ground, in houses or animal shelters, and they were activated between 18:00 and 06:00, two nights per month. Sticky traps were rolled up and placed in holes within walls surrounding chicken coops, animal shelters, houses, or gardens. They were set up and collected together with the light traps. Mouth aspirators were used in indoor collections during the daytime.

Table 1.  Sampling stations in the study area
VillagesCoordinateAltitudeVillagesCoordinateAltitude
  1. (*)number of data loggers placed in the villages.

  2. a North; b East

 NaEb  NE 
Kulak (KUL)*36 47 37.734 52 01.81 mKüçük Tüysüz (KTUY)*37 02 57.036 05 31.478 m
Dedepınarı (DDP)*36 55 36.635 28 56.44 mBelören (BEL)*36 48 42.235 33 20.999 m
Bahşiş (BAH)36 49 36.234 53 08.66 mBaklalı (BAK)37 02 11.235 38 16.6124 m
Bebeli (BBL)36 38 24.735 29 30.07 mKoyunevi (KOY)*37 17 21.335 39 23.6146 m
Adalı (ADA)36 38 04.835 32 33.07 mÇelemli (CEL)*36 50 48.135 39 02.4162 m
Yaramış (YAR)36 49 19.135 02 50.08 mDöşeme (DOS)37 25 28.135 51 59.2175 m
Yemişli (YEM)36 39 18.635 21 31.09 mCamili (CAM)*37 20 19.535 36 38.5181 m
Eğriağaç (ERA)*36 46 40.835 26 50.49 mÇağşak (CAG)37 09 12.836 20 02.9184 m
Cine (CIN)36 47 49.035 15 37.910 mTepeçaylak (TCK)*37 03 33.635 03 34.7188 m
Hacı Hasan (HCH)36 43 37.535 16 34.210 mTepecikören (TEP)*37 21 50.835 37 38.9189 m
Çağbaşı (CBS)36 51 53.935 03 53.415 mTehçi (TEH)*37 09 14.836 20 01.9192 m
Kızıltahta (KZT)36 45 01.335 34 43.516 mKarakütük (KKK)*37 24 40.136 07 15.8217 m
Yalnızca (YLN)36 46 31.635 24 53.818 mSarımazı (SMZ)36 58 21.535 58 32.4222 m
Ziyalı (ZIY)36 49 35.435 34 22.418 mDutlupınar (DUT)37 01 39.736 01 03.7222 m
Doğankent (DK)*36 50 51.935 20 19.020 mTüysüz (TUY)*37 01 56.436 04 41.5228 m
Yumurtalık (YUM)*36 46 55.435 47 44.522 mGüneri (GUN)37 26 45.935 46 52.8235 m
Zeynepli (ZEY)36 44 14.435 34 43.525 mOtluk (OT)*37 18 05.235 31 05.3237 m
Çiftlikler (CIF)36 58 52.635 52 34.526 mGökbüket (GOK)37 07 39.135 32 48.6244 m
Mercimek (MER)*37 06 19.135 47 31.133 mAydın (AY)*37 24 35.635 35 43.8278 m
Yenice (YEN)*36 58 39.235 02 57.442 mZerdali (ZER)37 24 18.235 37 51.2292 m
Hamamköy (HAM)37 19 08.735 49 02.845 mSofular (SOF)*37 22 53.936 14 20.0316 m
Narlık (NAR)*36 55 03.635 51 14.348 mKızyusuflu (KIZ)**37 19 54.836 12 36.7373 m
Aydınlar (ADL)37 21 35.536 00 45.145 mAkçakoyunlu (AKC)37 11 15.436 25 13.3373 m
İsalı (ISA)*36 55 11.935 43 04.962 mGedikli (GED)37 30 10.135 51 40.5381 m
Bucak (BUC)*37 26 54.435 54 19.566 mDüziçi (DUZ)**37 15 52.636 28 27.1521 m
Tumlu (TUM)37 08 49.935 42 26.366 mKesmeburun (KES)37 15 52.936 28 27.0530 m

Specimens were stored in 96% alcohol for morphological identification. Identifications were based on the morphology of male genitalia and female spermathecae and pharynges using the keys of Theodor (1958), Lewis (1982), and Killick Kendrick et al. (1991). Both preparation and identification of specimens were made individually.

Determination of climatic variations

In order to determine whether local variations in temperature and relative humidity might affect sand fly abundance or activity, 28 data loggers (iButton hygrocron, DS 1923) were placed throughout the study area (Table 1) in locations associated with the placement of traps. They were programed to record temperature and humidity every 6 h starting from April, 2006 until May, 2007. Temperature and humidity data were summarized as monthly means and all comparisons between locations were conducted using monthly averages of recorded parameters.

Data analysis

Abundance and seasonal activity parameters were calculated on direct monthly counts. Ecological comparisons between altitudes were performed with PAST, Paleontological Statistics Software ver. 2.00 (Hammer et al. 2001). Shannon-Weiner species diversity index and Jaccard's coefficient were used to estimate species diversity and similarity between altitudes, respectively. The formulae are presented below:

  • image

where s is the number of species and pi is the proportion of total samples belonging to the i-th species.

  • image

where A is the number of species sampled from community a, B is the number of species sampled from community b, and C is the number of species sampled from both communities.

RESULTS

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

Sand fly fauna

A total of 8,927 specimens (6,102 male and 2,825 female) belonging to ten phlebotomine species was collected from 42 of the sampled 52 villages. P. tobbi (67.48%), P. perfiliewi – galilaeus (21.75%), and P. papatasi (4%) were found to be the most prevalent species in the study area. Less frequent species were identified as S. dentata (3.76%), P. sergenti, (1.4%), S. theodori (0.20%), and P. syriacus/neglectus (0.97%), while P. alexandri (0.02%), P. perfiliewi – perfiliewi (0.01%), P. brevis (0.01%), were rare. P. syriacus/neglectus, P. perfiliewi – perfiliewi, P. perfiliewi / galilaeus were counted as a single species due to systematical ambiguities attached with these taxa (Table 2). P. tobbi, P. papatasi, and P. sergenti were present in almost all sampling sites.

Table 2.  Number (N) and relative abundance (%) of sand fly species collected in the study area.
SpeciesNaFemaleMale%b
  1. aTotal number of specimens collected by CDC light traps, sticky papers and indoor aspirators from all sampling stations.

  2. bRelative abundance: nx/N * 100, nx: number of individuals belonging to species x, N: total number of sampled individuals.

P. tobbi60241844418067.48
P. perfiliewi – galilaeus1942374156821.76
P. papatasi3911931984.38
S. dentata336308283.76
P. sergenti12572531.4
P. syriacus – neglectus8719680.97
S. theodori181530.2
P. alexandri2020.02
P. brevis1010.01
P. perfiliewi – perfiliewi1010.01
TOTAL892728256102100

Seasonal dynamics of sand fly populations

According to all data loggers placed within the study area, average temperatures and RH% were 21.0° C and 65.6% respectively. Maximum and minimum temperatures were 30.4° C in August and 12.2° C in January, while relative humidity was 53.4% in December and 77.1% in February, respectively. There were no significant linear correlations between the abundance of sand fly populations, average monthly temperature and average monthly relative humidity (r2temperature=0.0696, p=0.13; r2humidity=0.0698; p=0.11). However, the frequency of occurrence of sand flies within certain temperature intervals was assessed using a X2 test. We determined five temperature intervals corresponding to 20–22, 22–24, 24–26, 26–28 and 28–30° C. The X2 test determined that the observed number of sand flies was significantly different from the expected between 22–24° C (7.6% of the population) and 28–30° C (86% of the population) temperature intervals (X2= 24235.79 df= 4, p=0.00), under the assumption of equal frequencies in all temperature intervals.

Sand fly activity within the region started at the beginning of May and lasted until the month of October coinciding with the increase and decrease of the average temperatures within the region. Abundance reached its peak values in August when average temperatures were also at a maximum (30.4° C) (Figure 2). The relative abundance of each species by month during the active season is shown in Table 3. P. tobbi was the predominant species during the active season, reaching its highest density in August (2202 specimens; 24.67%) . Although no P. perfiliewi – galilaeus were found in May, it was the second most predominant species during the study period. On the other hand, P. papatasi and P. sergenti were continuously abundant during the season, even though their abundance was very low compared to P. tobbi. While only one specimen of P. papatasi was found in April, the species reached its highest density in May. Other species like P. syriacus / neglectus and Sergentomyia spp. were rare throughout the study period.

image

Figure 2. Seasonal dynamics of the sand fly species in the study area. (*) log transformed.

Download figure to PowerPoint

Table 3.  Monthly number (N) and relative abundances (%) of sand fly species during the active season in the Cukurova Region.
MonthsAprilMayJuneJulyAugustSeptemberOctoberTotal
SpeciesN%N%N%N%N%N%N% 
P. tobbi00.0016560.0078465.7765774.66220257.00169683.3052076.476024
P. perfiliewi – galilaeus000012510.49536.02145737.721688.2513920.441942
P. papatasi11009634.91715.96707.95802.07602.95131.91391
S. dentata0020.7313010.91667.50721.86653.1910.15336
P.sergenti0062.18413.44131.48340.88261.2850.74125
P. syriacus – neglectus0051.82403.36101.14130.34180.8810.1587
S. theodori000000111.2540.1020.1010.1518
P. alexandri0010.3600000010.05002
P. brevis0000000010.0300001
P. perfiliewi – perfiliewi000010.08000000001
Total1 275 1192 880 3863 2036 680 8927

Altitudinal distribution of sand fly species

Sampling stations were grouped into 100 m altitude intervals between sea level and 599 m. Unfortunately, no suitable sampling station was found between 400–499 m. The relative abundance of each species within altitudinal ranges is given in Table 4. P. tobbi, P. syriacus / neglectus, and S. dentata were found in every altitude interval, while the second most abundant species within the region P. perfiliewi/galilaeus was sampled only between 100–299m. No specimens of P. papatasi and P. sergenti were found between 300–399m and 500–599 m, respectively. There was no significant linear correlation between the abundance of sand flies and altitude (r2altitude=0.019; p=061). However a X2 test evaluating the frequency of occurrence of sand flies within different altitudinal intervals indicated that P. tobbi, P. perfiliewi / galilaeus, P. syriacus / neglectus and S. dentata were mainly aggregated between 100–199 m and 200–299 m (X2= 2113.508 df= 20, p=0.00).

Table 4.  Number (N) and relative abundance (%) of sand fly species collected at different altitude ranges of the Cukurova Region.
SpeciesAltitudinal ranges (m)
 0–99100–199200–299300–399500–599Total
 19 sitesa10 sites7 sites5 sites1 site42 sites
 N%N%N%N%N%N%
  1. aNumber of sampling sites at each altitudinal ranges.

P. tobbi20561.56433065.30129376.4018474.801244,4602467,48
P. perfiliewi – galilaeus00190228.70402.360000194221,75
P. papatasi80242654412.4200518,53914,38
S. dentata3610.80640.9721412.60208.1327,413363,76
P. sergenti92.70320.48593.482510.20001251,40
P. syriacus – neglectus30.90150.23442.60176.91829,6870,97
S. theodori00170.2610.060000180,20
P. alexandri0010.0210.06000020,02
P. brevis0010.0200000010,01
P. perfiliewi – perfiliewi0010.0200000010,01
Total333 6628 1693 246 27 8927 

The Shannon–Weinner index (H) indicated no difference between the diversity and abundance of sand flies distributes at different altitudes (Table 5). Diversity and evenness reached maximum values at 500 m. Evenness values were relatively low between 100–199 m (0.24). This along with high richness values (10) is most probably due to the predominance of P. tobbi (65.3%) within this interval.

Table 5.  The Shannon-Weiner diversity index (H), evenness (E) and richness (S) for the sand fly species at different altitude ranges of Cukurova Region.
Altitude (m)HES
  1. aA higher value of H indicates greater diversity than a lower value. The evenness (E) is calculated by dividing H by the maximum value for a given population.

0–991.020.565
100–1990.870.2410
200–2990.860.298
300–3990.840.584
500–5991.230.854

Jaccard's coefficient (IJaccard) measuring similarity between sand fly communities indicated that similarity was the highest between 0–99 and 300–399 m (0.8), 0–99 and 500–599 m (0.8) and also between 100–199 and 200–299 m (0.8) while low values were recorded between 100–199 and 300–399 m (0.4), and 100–199 and 500–599 m (0.4).

DISCUSSION

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

In the present study, eight Phlebotomus and two Sergentomyia species were identified. All known and suspected vectors of leishmaniasis in Turkey are present in the study area. These species were already determined in previous studies carried out in the Cukurova Basin together with P. simici, P. trancaucasicus, and P. halepensis, which were not found in this survey (Simsek et al. 2007, Svobodova et al. 2009).

Similar to previous studies, P. tobbi, the vector of L. infantum in the Cukurova Basin (Svobodova et al. 2009), was found to be the most dominant species (67.48%) (Simsek et al. 2007, Svobodova et al. 2009), while P. perfiliewi/galilaeus was the second most abundant species in the study area (21.76%) (Erisoz Kasap et al. 2009). P. papatasi, which accounted for only 4.38% of all collected samples from the study area, was represented in small populations. In contrast, this species is fairly abundant in the Sanliurfa region, which is the endemic focus of CL in Turkey and the Konya provinces, constituting respectively, 45% and 78% of all collected samples (Toprak and Ozer 2005, Yaman and Dik 2006). Together with P. syriacus/neglectus (0.97%) and S. dentata (3.76%), P. sergenti, the proven vector of L. tropica in the southeastern part of Turkey (Volf et al. 2002) represented a small proportion of the total catch (1.4%) . The low density of this species has been observed by others as well (Alten et al. 2003, Toprak and Ozer 2003, Simsek et al. 2007).

There is strong evidence that the distribution of sand fly populations in Turkey are highly correlated with altitudinal and bioclimatic clines (Belen et al. 2004, Erisoz Kasap and Alten, 2005, Belen and Alten 2006, Simsek et al. 2007). The Cukurova Region has a typical Mediterranean climate with long summers and short and rainy winters, which permits the proliferation of large populations of sand flies. Sand fly activity within the region started in May and ended in October, and abundance reached peak values in August when average temperatures were at a maximum (30.4° C). Although altitude has important consequences on population dynamics of insects via reduction of season length as one climbs to higher altitudes, these effects could not be observed in this study as the altitudinal differences between sampling sites were not great enough to cause any difference in season length.

P. tobbi, a typical eastern Mediterranean species (Lane et al. 1988), was the most abundant and active species during the season. Both the abundance of P. tobbi and P. perfiliewi/galilaeus peaked in August, although the activation of the latter started one month later. This delay was also observed in previous studies (Erisoz Kasap et al. 2009). Likewise, Swalha et al. (2003) found that P. tobbi appeared to reach a peak during the driest month (July), whereas P. perfiliewi numbers peaked during August in the Palestinian West Bank. In his study on the role of climatic factors on the distribution of sand flies, Singh (1999) found that the preferred temperature range for P. papatasi was from 28 to 34° C and for P. sergenti from 31 to 33° C. Previous studies show that P. papatasi usually prefers arid and semi-arid areas where temperatures are high and relative humidity is moderate and it can be found in a variety of habitats such as deserts, steppes or the Mediterranean basin (Lane et al. 1988, Guernaoui et al. 2006, Benkova and Volf 2007). Wasserberg et al. (2003) revealed that P. papatasi prefers also humid areas with relatively low temperatures rather than arid ones. In the Cukurova Basin, this species occurred during the entire active season, reaching peak values in May (rainy period) and later again in August (dry period). On the other hand, P. sergenti, P. syriacus/neglectus, and S. dentata appeared to peak only in June with very low densities compared to P. tobbi as the dominant species.

Although altitude alone is not a selective factor, biotic and abiotic properties of the environment are highly correlated with altitudinal gradients (Karan et al. 2000). Temperature is known to vary linearly, with altitude dropping on average 0.6° C per 100 m. In this study, sand fly abundance was not strongly and significantly influenced by altitude but there were significant differences between altitude gradients in terms of population abundances. In their large scaled study (0–1600 m) in southern Anatolia including the Cukurova Region, Simsek et al. (2007) collected the majority of their specimens at between 0–199 m. The same study also revealed that the diversity of sand flies was highest in the Adana and Hatay provinces which are situated in the Cukurova Basin. Similar to Jordan (Kamhawi et al. 2000), this diversity may reflect the rocky nature and warm, humid conditions of these provinces combined with the influence of both the Mediterranean and subtropical southeastern elements.

When the distribution and abundance of sand fly species are evaluated according to different altitudinal intervals, it appeared that all the widely distributed species in the Cukurova Region were aggregated between altitudes of 100–199 m and 200–299 m. Eighty-one percent of all collected samples came from the four villages situated within this narrow altitudinal belt Tepecikoren (150 m), Camili (180 m), Zerdali (275 m) and Aydın (279 m) (Figure 1). These villages are also in the CL focus of the Cukurova Basin (Svobodova et al. 2009). Temperature and humidity of these villages were not significantly different from nearby areas, and therefore the relative abundance of species within this region cannot be attributed to climatic properties. High relative abundances can, however, be correlated with the percent slope of the area since these villages are situated close to Taurus Mountain hillsides. Likewise Ostfeld et al. (2004) observed that their capture success of Lutzomyia vexator (Coquillet, 1907) was greater with the higher slopes and greater topography, suggesting that slope can be a good predictor of sand fly abundance.

P. tobbi was the most prevalent species at all altitudinal gradients together with P. syriacus / neglectus and S. dentata. On the other hand, the dominancy of P. perfiliewi / galilaeus, the second most abundant species, seemed restricted to between 100–299 m. Most of the specimens of this species were sampled in only one village through the study area (Camili, 1,255 specimens; 65%) . The abundance of P. tobbi was highest between altitudes of 100–199 m (Camili, 2,730 specimens; 45%) . This species is found to be scarcest in mountainous areas (Sayedi-Rashdi and Nadim 1992). Previous studies carried out in Anatolia showed that the frequency of this species decreases with altitude (Simsek et al. 2007, Yaman and Özbel 2004, Houin et al. 1971). Swalha et al. (2003) reported that the abundance of P. tobbi was highest from sea level up to 400 m in Palestine. Together with P. tobbi, the abundance of P. papatasi also decreased with altitude. No specimen of this species was sampled between 300–399 m and only five specimens were found between altitudes of 500–599 m in the Cukurova Basin. Guernaoui et al. (2006) explained the high occurrence of this species in the lowlands of Marrakech and its low frequency in mountainous areas by its preference for arid and per arid habitats. In contrast to these two species, P. sergenti is defined as a “mountainous” species and usually sampled between 500–700 m above sea level (Sayedi-Rashdi and Nadim 1992). In the study of altitudinal structuring of sand flies in the Atlas Mountains, Guernaoui at al. (2006) reported that P. sergenti was widespread and more abundant between 800 and 999 m. Moin-Vaziri et al. (2007) collected P. sergenti specimens from the hills and mountainous areas of Iran, but they also indicated that no specimens could be found above 2,500 m. However, in the Mediterranean basin this species usually sampled in larger numbers between 0–200 m (Simsek et al. 2007, Yaman and Özbel 2004). Similarly, in this current study, the highest number of P. sergenti was sampled between 200–299 m and no specimens were found between 500–599 m.

In conclusion, the Cukurova Region was found to have favorable climatic and topographic conditions capable of supporting large populations of sand flies. Our findings showed the study area to have the richest sand fly fauna within southern Anatolia and to harbor important vector species. Svobodova et al (2009) identified L. infantum as the etiological agent of CL in the study area which is transmitted by P. tobbi. P. tobbi was also found to be the most abundant species within the entire study area. The abundance of this species was highest in the Camili-Tepecikören villages where the number of CL cases reached its peak. Therefore, there is a high correlation between the abundance of the vector and prevalence of the disease. The Cukurova basin is the largest agricultural area within Turkey and is also a major route between eastern and western Anatolia. Thus, migration into the region is relatively high. This high migration activity and high population densities of proven vectors throughout the active season pose important risks for transmission of L. infantum. Therefore, we suggest that further studies should be conducted detailing the probable transmission of CL via P. tobbi and other vector species, and monitoring studies should be set up to establish necessary counter measures to prevent CL outbreaks.

Acknowledgments

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

This work was funded by the Scientific and Technological Research Council of Turkey (TBAG 105 T 205) and Hacettepe University Scientific Research Unit (05.01.601.005). This study is a part of a PhD thesis submitted to Hacettepe University.

REFERENCES CITED

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED
  • Alexander, B. 2000. Sampling methods for Phlebotomus sand flies. Med. Vet. Entomol. 14: 109122.
  • Alten, B., S.S. Çağlar, S. Kaynas, and F.M. Simsek. 2003. Evaluation of protective efficacy of K-OTAB impregnated bed nets for CL control in Southeast Anatolia-Turkey. J. Vector Ecol. 28: 5364.
  • Belen, A., B. Alten, and A.M. Aytekin. 2004. Altitudinal variation in morphometric and molecular characteristics of Phlebotomus (Phlebotomus) papatasi populations. Med. Vet. Entomol. 15: 18.
  • Belen, A. and B. Alten. 2006. Variation in life table characteristics among populations of Phlebotomus papatasi at different altitudes. J. Vector Ecol. 31: 3544.
  • Benkova, I. and P. Volf. 2007. Effect of temperature on metabolism of Phlebotomus papatasi (Diptera: Psychodidae). J. Med. Entomol. 44: 150154.
  • Erisoz Kasap, O. and B. Alten. 2005. Laboratory estimation of degree-day developmental requirements of Phlebotomus papatasi (Diptera: Psychodidae). J. Vector Ecol. 30: 328333.
  • Erisoz Kasap, O., A. Belen, S. Kaynas, F.M. Simsek, L. Biler, N. Ata., and B. Alten. 2009. Activity patterns of sand fly species (Diptera: Psychodidae) and comparative performance of different traps in an endemic CL focus in Cukurova Plain, Southern Anatolia. Acta Vet. Brno. 78: 327335.
  • Guernaoui, S., A. Boumezzough, and A. Laamrani. 2006. Altitudinal structuring of sand flies (Diptera: Psychodidae) in the High – Atlas Mountains (Morocco) and its relation to the risk of leishmaniasis transmission. Acta Trop. 97: 346351.
  • Hammer, Ø., D.A.T. Harper, and P.D. Ryan. 2001. PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontol. Electron. 4: 9 pp. http://palaeo-electronica.org/2001_1/past/issue1_01.htm.
  • Houin, R., E. Abonnenc, and M. Deniau. 1971. Phlébotomes du sud de la Turquie. Ann. Parasitol. Human Complic. 46: 663652.
  • Kamhawi, S., G.B. Modi, P.F.P. Pimenta, E. Rowton, and D.L. Sacks. 2000. The vectorial competence of Phlebotomus sergenti is specific for Leishmania tropica and is controlled by species – specific, lipophosphoglycan – mediated midgut attachment. Parasitol. 121: 2533.
  • Karan, D., S. Dubey, B. Moretau, R. Parkash, and J.R. David, 2000. Geographical clines for quantitative traits in natural populations of a tropical drosophilid: Zaprionus indianus. Genetica 108: 91100.
  • Killick-Kendrick, R. 1990. Phlebotomine vectors of the leishmaniases: a review. Med. Vet. Entomol. 4: 124.
  • Killick-Kendrick, R., Y. Tang, M. Killick-Kendrick, D.K. Sang, M.K. Sirdar, L. Ke, R.W. Ashford, J. Schorscher, and R.H. Johnson. 1991. The identification of female sandflies of the subgenus Larroussius by the morphology of the spermathecal ducts. Parasitologia 33 (Suppl.): 337347.
  • Lane, R.P., S. Abdel-Hafez, and S. Kamhawi. 1988. The distribution of phlebotomine sandflies in the principal ecological zones of Jordan. Med. Vet. Entomol. 2: 237246.
  • Lewis, D.J. 1982. A taxonomic review of the genus Phlebotomus (Diptera:Psychodidae). Bull. Brit. Mus. Nat. Hist. (Ent.) 45: 121209.
  • Moin-Vaziri, V., J. Depaquit, M-R. Yaghoobi-Ershadi, M-A. Oshagi, P. Derakhshandeh-Peykar, H. Ferte, M. Kaltenbach, M.D. Bargues, N. Leger, and A. Nadim. 2007. Intraspecific variation within Phlebotomus sergenti Parrot (1917) (Diptera: Psychodidae) based on mtDNA sequences in Islamic Republic of Iran. Acta Trop. 102: 2937.
  • Ok, Ü.Z., İ.C. Balcıoğlu, A. Taylan Özkan, S. Özensoy, and Y. Özbel, 2002. Leishmaniasis in Turkey. Acta Trop. 84: 4348.
  • Ostfeld, R.S., P. Roy, W. Haumaier, L. Canter, F. Keesing, and E.D. Rowton. 2004. Sand fly (Lutzomyia vaxator) (Diptera: Psychodidae) populations in Upstate New York: Abundance, microhabitat and phenology. J. Med. Entomol. 41: 774778.
  • Ozbel, Y, N. Turgay, S. Ozensoy, A. Ozbilgin, M.Z. Alkan, M.A. Ozcel., C.L. Jaffe, L. Schnur, and L. Oscam. 1995. Epidemiology, diagnosis and control of leishmaniasis in Mediterrenean Region. Ann. Trop. Med. Parasitol. 89: 8993.
  • Seyedi-Rashdi, M.A. and A. Nadim. 1992. The genus Phlebotomus (Diptera: Psychodidae: Phlebotominae) of the countries of the eastern Mediterranean Region. Iran. J. Publ. Hlth. 21: 1150.
  • Simsek, F.M., B. Alten, S.S. Çaglar, Y. Ozbel, A.M. Aytekin, S. Kaynas, A. Belen, O.E. Kasap, M. Yaman, and S. Rastgeldi. 2007. Distribution and altitudinal structuring of phlebotomine sand flies (Diptera:Psychodidae) in southern Anatolia, Turkey: their relation to human CL. J. Vector Ecol. 32: 269279.
  • Singh, K.V. 1999. Studies on the role of climatic factors in the distribution of phlebotomine sandflies (Diptera: Psychodidae) in semi-arid areas of Rajasthan, India. J. Arid Environ. 42: 4348.
  • Svobodova, M., B. Alten, L. Zidkova, V. Dvorak, J. Hlavackova, J. Myskova, V. Seblova, Ö.E. Kasap, A. Belen, J. Votypka, and P. Volf. 2009. CL caused by Leishmania infantum and transmitted by Phlebotomus tobbi. Int. J. Parasitol. 39: 251256.
  • Swalha, S.S., M.S. Shtayeh, H.M. Khanfar, A. Warburg, and Z.A. Abdeen. 2003. Phlebotomine sand flies (Diptera: Psychodidae) of the Palestinian West Bank: Potential vectors of leishmaniasis J. Med. Entomol. 40: 321328.
  • Theodor, O. 1958. Psychodidae – Phlebotominae. In: E.Lindner (ed.). Die fliegen der Palearktischen Region. pp. 155. E. Schweizerbartsche Verlags Stuttgart Germany .
  • Toprak, S. and N. Ozer. 2005. Sand fly species of Sanliurfa province in Turkey. Med. Vet. Entomol. 19: 107110.
  • Volf, P., Y. Ozbel, F. Akkafa, M. Svoboava, J. Votypka, and K.P. Chang 2002. Sandflies (Diptera:Psychodidae) in Sanlıurfa Turkey: Relationship of Ph. sergenti with the epidemic of anthroponotic CL. J. Med. Entomol. 39: 1215.
  • Wasserberg, G., I. Yarom, and A. Warburg. 2003. Seasonal abundance patterns of the sandfly P. papatasi in climatically distinct foci of cutaneous leishmaniasis in Israeli deserts. Med. Vet. Entomol. 17: 452456.
  • Yaman, M. and Y. Özbel. 2004. The sandflies (Diptera: Psychodidae) in the Turkish province of Hatay: some possible vectors of the parasites causing human CL. Ann. Trop. Med. Parasitol. 98: 741750.
  • Yaman, M. and B. Dik. 2006. An inventory of the phlebotomine sandflies (Diptera: Psychodidae) found in the Turkhish province Konya. Ann. Trop. Med. Parasitol. 100: 265275.