ABSTRACT

Objective:

Aedes cretinus, a white and black stripped Aedes species, shares morphological similarities with Aedes albopictus and Aedes aegypti which are among the most important vectors and invasive species in the world. Due to its limited distribution and low population density, information on the biology and ecology of the species has been limited so far. This study aimed to determine distribution of Ae. cretinus in Türkiye.

Methods:

Field works have been carried out in the Mediterranean, Aegean and Marmara Regions of Türkiye. Larval samples were collected by larval dippers while adult mosquito catches were performed using the human landing catch method and CDC-light traps.

Results:

A total of 44 different Ae. cretinus populations were identified in the Mediterranean, Aegean and Marmara Regions of Türkiye. The larval specimen collected from small containers, tires, tree holes and natural small habitats. A plane (Platanus orientalis), walnut (Juglans regia), Türkiye oak (Quercus cerris), chestnut (Castenea sativa) and cedar (Cedrus libani) tree holes are the main larval habitats in which the specimen collected. In some localities, larvae were found together with Anopheles plumbeus, Anopheles claviger and Aedes geniculatus larvae in tree holes. Human landing catch method captured a greater number of females than CDC-light traps.

Conclusion:

This study determined the distribution of Ae. cretinus in Türkiye for the first time. Information on respective geographic distribution of Ae. cretinus is fundamental for effective control programmes. Further studies are needed to understand the biology and ecology of these species.

Keywords: Aedes cretinus, distribution, Mediterranean, Aegean, Marmara

INTRODUCTION

Mosquito-borne diseases are an increasing global health challenge, threatening over 40% of the world’s population (1). Approximately 40% of the world’s population are at risk of dengue transmission, with an estimated 400 million infections per year resulting in 50-100 million clinical cases and 3.6 million hospitalisations (2,3).

The subgenus Stegomyia which is classified under the genus Aedes contains important human disease vector species such as Aedes (Stegomyia) aegypti (Linnaeus, 1762), Aedes (Stegomyia) albopictus (Skuse, 1895) and Aedes (Stegomyia) cretinus (Edwards 1921) (4). There are some microscobic differentiations related to scaling patterns of the scutum. The scutum is lyre-shaped marking of white scales and also clypeus are with scales in Ae. aegypti. Ae. cretinus has submedian narrow lines of pale scales extending from posterior of the scutal angle to the scutum with a lateral line of pale scales while Ae. albopictus has not got this lateral line. (5). The remarkable morphological features and bio-ecological resemblance of Ae. cretinus, Ae. aegypti and Ae. albopictus may sometimes cause confusions among public (Figure 1) (6).

Figure 1

Ae. cretinus is described as an anthropophilic and aggressive day time biter causing serious irritation to humans when it is around the people (7). The larvae may be found in natural habitats such as tree holes or even man-made containers such as used tyres (8,9). The distribution of Ae. cretinus is limited in the Mediterranean and has low population density (6). The first record of the Mediterranean representatives of “Ae. albopictus” in the words of Edwards (1921) was reported from Greece in 1921 (6,10,11). In the following years, Ae. cretinus was reported from Cyprus (12), Türkiye (Antalya) (13,14), Crete, Macedonia and some parts of Attica (7,10,15), Lebanon (16), South Ukraine, Russia (8) and Georgia (12). As it is understood from its limited distribution and low population density of Ae. cretinus, little is known about the bio-ecological characteristics of the species and vectorial capacity of the species is even still unknown (17). However, in the regions where it spreads, its aggressive behaviour causes discomfort and concern among the people due to its close morphological similarity to Asian tiger mosquito Ae. albopictus. As a result, understanding the current distribution of Ae. cretinus populations in Türkiye could be of importance. Understanding the distribution of the species and conducting studies on its bio-ecological characteristics have become especially important as the entry and rapid invasions of Ae. albopictus in to Türkiye continues in recent years. After the first detection of Ae. albopictus in Edirne in 2011, its distribution spread larger areas in the Marmara Region (18,19), Black Sea Region (20) and finally Aegean Region (21). However, studies on the distribution of Ae. cretinus have not been reported in Türkiye after it was reported in Antalya (13,14). In this study, we, for the first time, reported the distribution of Ae. cretinus populations in Türkiye. We believe that the information gathered by this study, is fundamental for the goal of reducing the impact of vector-borne diseases in Türkiye and managing vector control studies.

METHODS

Field works have been performed in the Mediterranean (Adana, Mersin, Antalya, Burdur, Isparta, Osmaniye, Kahramanmaraş, Hatay), Aegean (Aydın, İzmir, Manisa, Denizli, Uşak, Muğla) and Marmara (Balıkesir, Bursa, Birecik, Çanakkale) Regions of Türkiye between May-October in 2012-2021 (Figure 2). Every possible natural (tree holes, puddles) and artificial containers (human-made plastic cups, ceramic pots, used tyres) water habitats have been checked for the presence of larval samples. Larval dippers have been used for the collection of larval samples and transferred to plastic bottles. Adult specimens were caught in outdoor and indoor areas (animal stables) with CDC light traps and Human Landing Catch Method (HLCM). Collected samples were brought to vector insects laboratory of Biology Department in Aydın Adnan Menderes University. Larval samples were reared to adults under standard conditions at 26-28 °C, 12:12 h photoperiod and 70-80% relative humidity in an insectarium. Morphological identifications have been performed under stereomicroscope using an identification key (11,22).

Figure 2

Statistical Analysis

Statistical analysis has not been performed for this study.

RESULTS

As a result of long-term sampling studies in the Mediterranean, Aegean and Marmara Regions, Ae. cretinus larvae were obtained from a total of 43 localities and adult samples were collected from 31 localities (Table 1). The larvae were sampled in four different breeding habitats: Small containers, tires, tree holes and natural small habitats (Figure 3). Results obtained from the larvae sampling do not show the habitat preference of the species since the research is based on the presence/absence detection of Ae. cretinus. However, it has been determined that small containers and tires in urban areas, tree holes and natural small habitats in rural areas are frequently used as breeding habitats. The tree hole larvae of Ae. cretinus were sampled from tree holes on plane (Platanus orientalis), walnut (Juglans regia), Türkiye oak (Quercus cerris), chestnut (Castenea sativa) and cedar (Cedrus libani) trees. Of the 22 tree holes sampled, 13 were detected in plane, 4 in walnut (Akçatekir, Ödemiş, Yiğitali, Ayvacık), 2 in cedar (Hisarçandır, Ovacık), 2 in Turkish oak (Honaz, Uzunyurt) and 1 in chestnut tree (Tire). While Ae. cretinus larvae were sampled alone in all of the small container and tire habitats, they were found together with other mosquito larvae in some tree holes and small natural habitats. Ae. cretinus larvae were found together with Anopheles plumbeus larvae in tree holes in Gazipaşa, Darıpınarı, Ekincik (Plane) and Akçatekir (Walnut); It has been sampled together with Anopheles claviger larvae in small natural habitats in Kadriye, Pınarbaşı, Gözne and Darıpınarı and with Aedes geniculatus larvae in cedar tree hollows in Ovacık.

Figure 3

Only female Ae. cretinus specimens were caught by outdoor and indoor CDC light traps and HLCM applied in different localities in the study area. A total of 127 females were caught with HLCM while 89 females were caught by CDC light traps. Totally 69 females were caught by CDC light traps in outdoor while 20 females were caught by the traps deployed indoor. It can be stated that the species exhibits exophilic and anthropophilic tendencies based on the results. Although Ae. cretinus female specimens were caught with HLCM in 28 localities in the study area, it was determined that the females caught in all localities did not show aggressive biting behaviour.

DISCUSSION

Information on respective geographic distribution of mosquito species is so precious for planning effective mosquito control strategies (23). This study determined the distribution of Ae. cretinus in the Mediterranean, Aegean and Marmara Regions of Türkiye. The first report of Ae. cretinus population in Türkiye was determined in Antalya by Şahin (13). In the following years, Alten et al. (14) also reported the distribution of the Ae. cretinus populations in the same area in Antalya in 2000. The incidence of Ae. cretinus was calculated as 9% of mosquito fauna of İstanbul between 2019-2020 (24). Since then, this study is the first report of distribution of Ae. cretinus populations in the Mediterranean, Aegean and Marmara Regions of Türkiye. Larval samples were collected from both tree holes, natural small habitats, small containers and tires in the study. Similarly, larvae were collected from tree holes in the South Ukraine and Russia (8) and Cyprus (12,25). Other possible breeding sites were reported as forests, open areas, potholes and small hollows in forests as well as tree holes (14) and containers such as tyres (9). In addition to tree holes and tyres in those studies, small containers were also containing Ae. cretinus larvae in this study. This result demonstrates that Ae. cretinus is not only well adapted to natural habitats but also spreads in domesticated environment. This situation refers to ability of Ae. cretinus to colonize habitats where it occurs (15). Interestingly, larvae were found in tree holes together with Ae. geniculatus in Ovacık; with An. plumbeus in Gazipaşa, Darıpınarı, Ekincik and Akçatekir; with An. claviger in Kadriye, Pınarbaşı, Gözne and Darıpınarı. This is similar to the fact that Ae. cretinus larvae was found in tree holes with Ae. geniculatus. They were also found together with Anopheles plumbeus and Orthopodomyia pulcripalpis in the South of Ukraine and Russia (8).

In the study, larvae were collected from the tree holes of plane (Platanus orientalis), walnut (Juglans regia), Türkiye oak (Quercus cerris), chestnut (Castenea sativa) and cedar (Cedrus libani) trees. Although, there have been no relationship between larval habitat preference and tree species in the literature, bamboo grove has been reported to be related with larval development by Gutsevich et al. (8). In addition to that, it was stated that the study area where Ae. cretinus was rediscovered after 66 years in Cyprus, was dominated by old and high plane trees (Platanus orientalis) (25). The HLCM and CDC-light traps were used to detect adult mosquitoes in this study. While few females obtained from light traps, a greater number of females were caught by HLCM. It was reported that CO₂ and New Jersey light traps were also useful to catch exophilic Ae. cretinus in Antalya (26). Standard New Jersey light trap, Heavy duty EVS, CO₂ Mosquito traps caught adult Ae. cretinus specimen at very low density in outdoors and indoors and accounted for 0.07% of the catches in monitored houses in Lebanon (16).

In this study specimen collection were carried out in a 10-year period including 2012-2021 and between May and September. Caglar et al. (26) reported that population growth was rapid during May and June but disappearance was rapid during July and Ae. cretinus were not found after July in Belek (Antalya). However, both larvae and adults were sampled from May to September in many localities in this study. For instance, the Sarıseki population were collected in the end of September in 2021.

Today, Ae. albopictus pose a great risk because it threatens public health with mainly dengue and other viral factors that it carries and it is known to invade our country rapidly (21). Ae. cretinus and Ae. albopictus shares some morphological characters in their developmental stages (11). These characteristics might be distinguished by skilled and experienced taxonomists when the specimens are not damaged and collected properly. Another way to differentiate the species is molecular techniques using reliable molecular markers such as internal transcribed spacer 2 of nuclear genome or mitochondrial cytochrome oxidase I fragments (4). The morphological resemblance between Ae. cretinus and Ae. albopictus might cause undue anxiety and concern among the public if the species distinction is not made properly based on either morphological characters or molecular techniques. Thus, this situation caused undue panic among Greek people (6).

This study is the first to reveal the distribution of Ae. cretinus populations in Türkiye. The study both shows the populations of Ae. cretinus and serves as a warning not to cause unnecessary anxiety since it can be confused with Ae. albopictus. Information on geographic distribution of mosquito species is an important component of controlling vector species. This study also highlights the importance of surveys and the need for mosquito identification. Further studies are needed to determine bio-ecological features of Ae. cretinus populations since detailed information are crucial in order to run a successful management mosquito control programmes.

CONCLUSION

This study is a clear proof of that Ae. cretinus rapidly invades Türkiye. As it is known, intense human mobility, passenger transportation, airports, ships, port routes, trade ships are the primary factors in the transportation of mosquito species to areas where it has not been spread before. It is also very clear that once Ae. cretinus enters in a new area, it will facilitate the distribution of the species due to the very favorable climatic conditions in Türkiye as well as its adaptability to man-made containers as we determined some larvae from man-made containers. We also proved the existence of the species in Osmaniye, Kahramanmaraş, Adana, Hatay, Mersin, Antalya, Burdur, Isparta, Muğla, Denizli, Aydın, İzmir, Manisa, Uşak, Bilecik, Bursa, Balıkesir and Çanakkale. It is very important to carry out field studies at regular intervals in many risky regions in other regions of Türkiye to prevent the invasion of this species. In a conclusion, it should be clearly emphasized that it is of the utmost importance to continue Aedes surveillance for early detection of new Aedes-borne disease outbreaks and prevent the invasion of the invasive species. Additionally, further studies on Aedes behaviour and possible role in the transmission of dengue and other Aedes-borne disease are needed.

Ethics

Ethics Committee Approval: This article does not contain any studies with animals performed by any of the authors.

Informed Consent: This article does not contain any studies with animals performed by any of the authors.

Peer-review: Externally peer-reviewed.

Authorship Contributions

Concept: F.M.Ş., Design: F.M.Ş., Data Collection or Processing: F.M.Ş., Analysis or Interpretation: S.İ.Y., Literature Search: S.İ.Y., Writing: S.İ.Y.

Conflict of Interest: No conflict of interest was declared by the authors.

Financial Disclosure: The authors declared that this study received no financial support.

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Distribution of Aedes (Stegomyia) cretinus in Türkiye