J -Borne Dis, September 2018, 12(3): 196–218 H Vatandoost et al.: Bioecology of … DOI: 10.18502/jad.v12i3.73

Review Article Bioecology of Dominant Malaria Vector, superpictus s.l. Grassi (Diptera: Culicidae) In Iran

*Hassan Vatandoost 1, 2, Ahmad Ali Hanafi-Bojd 1, 2, Ahmad Raeisi 2, 3, Mohammad Reza Abai 1, 2, Fatemeh Nikpour 1, 2

1Department of Medical Entomology and Vector Control, School of Public Heath, Tehran University of Medical Sciences, Tehran, Iran 2Department of Chemical Pollutants and Pesticides, Institute for Environmental Research, Tehran Univer- sity of Medical Sciences, Tehran, Iran 3Ministry of Health and Medical Education, Tehran, Iran

(Received 8 July 2018; accepted 29 Sep 2018)

Abstract Background: Malaria continues to be a main vector-borne public health problem in Iran. The endemic foci of the disease are mainly located in south-eastern part of the country. Iran is now launching the elimination of malaria. Studies on the bioecology and susceptibility of malaria vectors to insecticide are essential in this phase. Methods: The literature on bio-ecology of Anopheles superpictus s.l. Grassi was reviewed in Iran in more than half a century. Different aspects including, distribution, key identification, larval habitats, flight range, seasonal activities, irritability/susceptibility to insecticides, and anthropophilicity index were identified. Results: The adult females of An. superpictus s.l. were susceptible to all WHO-recommended imagicides except DDT. Distribution, morphology, sibling species, larval habitat, flight range, Irritability tests, sustainability index, blood feeding preference and related factors were discussed in details Conclusion: Results of the evaluating will help for decision making of authorities for vector control.

Keywords: Anopheles superpictus s.l., Ecology, Biology, Insecticide resistance, Iran

Introduction

Mosquito-borne diseases are the major ern areas of the country in Sistan and Baluchi- problems worldwide, among them malaria stan, Hormozgan and South of Kerman Prov- presents a major health problem globally. In inces. The most routes of malaria cases are im- 2016, an estimated 216 million cases of ma- migration from Afghanistan and Pakistan to laria occurred worldwide, compared with 237 southern and southeastern areas of the coun- million cases in 2010 and 211 million cases try (Ministry of Health, annual reports). in 2015. Most malaria cases in 2016 were re- Anopheline mosquitoes (Diptera: Culicidae) ported from the WHO African Region, while are vectors of malaria to humans. Currently the two percent of cases were inhabitants of there are proven and effective tools to fight WHO Eastern Mediterranean Region coun- against malaria including vector control tries (1). It is one of the important infectious measures (1). As these tools are scaled up, ma- diseases in Iran with an average of about laria endemic countries need to continually up- 15000 annual cases in the last decade, while date the skills and competence of the health total recorded cases has dropped to less than workers engaged in malaria control and elim- 100 locally transmitted cases in 2017. Most ination. of indigenous and imported malaria cases in All observations indicate that the data re- Iran are reported from southern and southeast- flect the real situation and that the overwhelm- 196 *Corresponding authors: Dr Hassan Vatandoost, E- http://jad.tums.ac.ir mail: [email protected], [email protected] Published Online: September 30, 2018

J Arthropod-Borne Dis, September 2018, 12(3): 196–218 H Vatandoost et al.: Bioecology of … DOI: 10.18502/jad.v12i3.73

ing majority of cases, which occur, are includ- phates (Malathion and pirimiphos-methyl) for ed in the national system, although there is about two decades from 1966. After that dur- room for improvement in the surveillance sys- ing 1977–1990 propoxur was used by national tem. The spectacular progress can be ascribed malaria vector control program. to effective implementation of appropriate cu- Subsequently, after the introduction of rative and preventive control interventions pyroteroids into the market, and given their through a strong health care infrastructure. lower risk for humans and more affordable Social and economic development allowing products, lambdacyhalothrin and deltamethrin better housing, use of air-conditioning etc. were used. As the adult mosquitoes control, has also played a role. larval control is also used to reduce the vector There are several activities on different abundance. For this purpose, Temephos, aspects of malaria in the country: including Reldan® and pirimiphos-methyl was used in insecticide resistance monitoring (2-12), sib- past decades. ling species, molecular study, new record (13- 20), novel methods for vector control (21-26) Materials and Methods faunestic study (27, 28), use of plants for lar- val control (29-41) using bednets and long All the published papers thought the in- lasting impregnated nets (42-48), morphologi- ternet and master of sciences and Ph.D thesis cal studies (49-51), malaria epidemiology (52- related to An. superpictus s.l. were reviewed 55), ecology of malaria vectors (56-64), bio- and evaluated. Key words for search in scien- diversity (65, 66), community participation (45, tific motor engines were: Anopheles superpic- 54), vector control (67), repellent evaluation tus, insecticide resistance, ecology, distribution, (68), anthropophilic index of malaria vectors identification, anthropophilicity, sporozoite rate, (65, 69), training (70) is designated as malar- Iran. Also master of sciences and Ph.D thesis ia training center by WHO. There are several related to An. superpictus s.l. were collected reports on different aspects of malaria vec- from the academic libraries in Iran. All col- tors recently different studies have been con- lected resources were reviewed and evaluated. ducted during more than 90 years on malaria (71-96) and its vectors in Iran. Seasonal activity of Anopheline mosqui- Results toes and their peak of activity vary in different area due to environmental condition. This issue Distribution of Anopheles superpictus s.l. affected the epidemiology of malaria transmis- in Iran sion in different regions. Agriculture in Iran Faghih' research results showed that this remains highly sensitive to climate develop- species could be found in areas of 2000 me- ments, the country's most important crops are ters above sea level (97-99). It has been cap- wheat, rice and other grains, sugar beet, fruits, tured from coastal plains of Persian Gulf in nuts, cotton, and tobacco, which require the areas with 500 meters height above sea level use of insecticides. So far different groups of (in Chelou village in Minab). With the excep- insecticides are using for crops protection in tion of a narrow strip of coastal areas, this the country. The main governmental use of species is found in almost all regions of Hor- insecticide in the health sector is their appli- mozgan Province (100-104) (Fig. 1). cation for adult control. The first attempts to control malaria vectors started dur- Key to the female Anopheles superpictus s.l. ing the 1960’s with organochlorines (DDT, Wings with contrasting pale and dark spots, dieldrin and BHC), followed by organophos- at least on costa (C), radius (R) and radius-one 197 http://jad.tums.ac.ir Published Online: September 30, 2018

J Arthropod-Borne Dis, September 2018, 12(3): 196–218 H Vatandoost et al.: Bioecology of … DOI: 10.18502/jad.v12i3.73

(R1), Hind tarsomeres 3–5 no1 entirely pale, Anopheles superpictus s.l. acts as a main Maxillary palpus dark, or with at most 3 dis- malaria vector (e.g. in Lorestan) or secondary tinct pale bands (pale spots may also be pre- vector (e.g. Sistan and Baluchistan). A survey sent): abdominal terga II-VII without dark has been conducted in order to study on dif- scale-tulips. Although some posterolateral dark ferent morphological and genetic variation of scales may be present on distal segments, Hind An. superpictus populations in Iran. Mosqui- tarsomere 5 dark, Palpomere 5 entirely pale, toes of An. superpictus were collected from the Femora and tibiae not spotted: abdominal terga Ardebil, Lorestan, and Sistan and Baluchistan without pale scales, Anal vein with 2 dark spots, provinces in July-September in 2004 using dif- distal spot long (104). ferent collection methods. After species iden- tification and morphological study on larvae Key to the Anopheles superpictus S.l. larvae and adults, the sequence variation of ITS2- Seta 2- Cephalon inserted at least as far rDNA and mtDNA COI-COII fragments were apart as the distance between 2- Cephalon and analyzed using PCR-RFLP and PCR-direct se- 3- Cephalon on one side, seta 1- Antenna al- quencing assays. Results showed that there were ways simple, seta 5, 6, 7- Cephalon branched significant differences in morphological and (subgenus Cellia), Tergal plates on abdominal genetic characters within and between popu- segments III-VII smaller, < 0.5 width of seg- lations. Digestion of COI-COII fragment us- ment, and not enclosing median accessory ter- ing AluI enzyme demonstrated various hap- gal plate, Thoracic pleural seta various , Thor- lotypes indicating intra or inter-species var- ax with at least long pleural seta 9- Prothorax iation. Totally 4 haplotypes were observed be- and 9- Metathorax branched, 9, 10- Mesotho- tween specimens/populations in 708bp of COI rax, and 10- Metathorax simple or branched, gene. Totally, the rate of variation among pop- Thorax with long pleural seta 9- Prothorax ulations was 12.3%. This rate was 2–5% for and 9, 10- Metathorax branched. within Sistan and Baluchistan populations. Ac- Seta 9- Mesothorax branched, 10- Meso- cording to phylogenetic analysis of the COI thorax simple, palmate seta 1-III-VII strong, sequences, An. superpictus populations in Iran leaflets and filaments various, Seta 3- Cepha- constructed 2 main groups including: 1) south- lon simple or with a few short lateral branches, east populations (Sistan and Baluchistan and not brush-like in appearance, abdominal pal- Kahnooj) and 2) central and northwest popu- mate seta 1- Abdominal segment I non-pal- lations, each group putatively representing one mate or very weakly palmate, Seta 1, 2- Pro- species. Analysis of ITS2 fragment also re- thorax tubercles separate; seta 3- Metathorax vealed highly diverged populations represent- non-palmate or very weakly palmate, Seta 2, ing at least three putative separate species des- 3- Cephalon simple, finely or distinctly frayed, ignated as X, Y, and Z (X and Y in Baluchistan anal papillae normal, abdominal palmate fil- and Z in other provinces). The rate of genetic aments £ 0.5 length of blade, Seta 3, 4- Ceph- variation in ITS2 was 27% in which respec- alon simple or occasionally bifid, never tively 0.27%, 0.05% and 26.68% correspond- branched, Seta 2, 3- Cephalon smooth or fine- ed to 5.8S, 28S, and ITS2 regions. Phyloge- ly frayed, abdominal seta 1- Abdominal seg- netic analysis also revealed two main groups ment II strongly palmate, Seta 3- Cephalon including three branches, each one putatively finely frayed, seta 4- Cephalon length > 3- representing one separate species. In spite of Cephalon, basal tubercle of seta 1- Prothorax having a high genetic and morphological var- weak (Fig. 2) (104). iation among specimens, there were no rela- tionship between phenotypic and genetic var- The Anopheles superpictus s.l. species iations, assuming that other parts of genome 198 http://jad.tums.ac.ir Published Online: September 30, 2018

J Arthropod-Borne Dis, September 2018, 12(3): 196–218 H Vatandoost et al.: Bioecology of … DOI: 10.18502/jad.v12i3.73

is responsible for the variations. The rate of species didn’t enter to hibernation phase in genetic variation in COI and ITS2 regions October. It seems that leaving hibernation hap- was far more than that has been seen in other pened in February, because the females that species s.l.es (105). have been desiccated at this month had high ovarian growth. During the month of May, Flight Ranges no larvae were collected. This result showed Flight range of this species was about 2– that although this species ovoposited in 2.5 kilometers (observations in Tabas, Birjand). February or March, but the eggs were expelled At the beginning of hibernation it reached to because of abundant rainfall, rapid flow of 4km (99). springs and streams. Changes were not the same during three winters. Winter 1953– Irritability tests 1954 had the coldest winter and 1955–1954 The irritability levels of An. superpictus was the modest. The numbers of collected S.l. against diagnostic dose of dichlorodiphe- specimens to generalize the reliability results nyltrichloroethane (DDT) insecticide were were very low. Although the temperature in measured in a conical exposure chamber ac- February, was different from the temperature cording to WHO methods in Isfahan in 1963. in the first three months but the collected The results of irritability tests showed that females showed the high activity both for the DDT had the high irritancy effect against An. ovarian growth and blood feeding. Even in superpictus S.l. (106). March that this species began its activity; the temperature was more than the last 4 months. The time of Blood feeding It has been justified that An. superpictus s.l. The activity of this species started at about entered to hibernation phase because of a 20p.m. and reached to peak point at about physiological cycle caused by cold weather. In 21.30p.m. The most brutal is in the first half Ilam, An. superpictus s.l. is the main malaria and with low density in the second half of the vector and comprised almost one hundred night and in the morning it was close to zero. percent of the collected Anopheles from The most biting activity in Bazaft, Farsan, Cha- indoors and outdoors (111). har Mahal Bakhtiari in 1999 was in 22–23p.m. Studies in Kermanshah and Sabzevar in- and 3–5a.m. (111). dicated that the activity of this species depended on the temperature and the onset of its Seasonal activity activity was from mid-June and ended in Researches have been conducted from ear- mid-October. Maximum activity is in early ly October to April 1953–1955 to determine August to mid- September and with the onset An. superpictus s.l. seasonal activity. Anoph- of cold weather that is different in various eles superpictus s.l. adult population parts of the plains and mountainous areas; abundances for the entire period of August- after this time it entered to hibernation. September were high, but during the October, Females entered to hibernation phase in it began to decrease. The last collection was mountainous caves and indoors from mid- conducted in the third week of October. Even September in west with storing fat and from though space spray collection using Pyrethrums October to next April when the weather was (PSC), that was applied at homes, very few good for mosquito activity (Manoochehri, adult were collected in each station during the personal negotiation). months of November–February. Based on in- In a study in the counties of Pars Abad and formation about the larvae collection and dis- Germi in 1997–1998, the activity of this sected adults, it has been concluded that this species has been reported during July-No- 199 http://jad.tums.ac.ir Published Online: September 30, 2018

J Arthropod-Borne Dis, September 2018, 12(3): 196–218 H Vatandoost et al.: Bioecology of … DOI: 10.18502/jad.v12i3.73

vember. The maximum abundances of this of this species began its activity in May with species was 10.6 per place in the second half the peak activity in September and in of August and with the least frequency was October it reached to 0.25 number per location in the first half of zero (103, 114). December in Dykdash and Qeshlaq Beryan villages. Theis species had one peak of activ- Species composition ity in second half of August in (112). Fauna and ecology of vectors in the county In human dwellings, the frequency of An. of Farsan, Bazaft, Chahar Mahal Bakhtiari, in superpictus s.l. in each place was 1.8. In out- human dwellings, indicated that An. super- doors, An. superpictus s.l. had the highest pictus s.l.s.l. comprised 44.2% of the collect- frequency of 6.2 per place in early of August. ed Anopheles populations. In habitats In human dwellings, its frequency was 1.8 and it comprised 63.7% of the total collected in outdoors it was 6.2 per each place with the Anopheles. In outdoors, An. superpictus s.l. highest abundance in the early of August. The comprised 77% of the populations. It has been highest monthly activity of An. superpictus in collected generally in high population s.l. Dykdash Village, Germi, was in the eight- density from outdoors. In Hussain Abad eenth of July, 1996. In Dykdash and Agha Mo- village, of the 243 mosquitoes collected in hammad Biglou villages its activity began in night biting, 165 of them (67.9%) were An. eighteenth June and ended in third of Decem- superpictus s.l.s.l. In the village of Mazi, a ber. In the village of Agha Mohammad Biglou total number of 356 Anopheles collected the highest activity was in the second half of with the method of night biting, An. August. In Dykdash and Gheshlagh Beryan superpictus s.l.s.l. comprised 246 (69.1%) of villages, its activity in indoors has been the Anopheles population. In the village of reported during the months of July- Hussain Abad, of the 254 collected Anopheles November, with the highest frequency of in pit shelter the number of 180 of them 10.63 mosquitoes per place in the second half (70.8%) were An. superpictus s.l.s.l. (116). of August and the least abundant numbers per The highest biting activity of Anopheles place (0.25) in the first half of December. This superpictus s.l.s.l. in Bazaft, Farsan, Chahar species hasn’t been collected from plain of Mahal Bakhtiari in 1999 was occurred in 22– Parsabad (112), but studies of Abai and 23p.m. and at 3–5a.m. (115). colleagues in 2002 have been obtained very Anopheles superpictus s.l.s.l. was the most low abundance in this area. The most abundant important vectors in Siahoo area, Southern Iran. of this species in the county of Kahnooj was Entomological studies conducted in this during September and October (113). district showed that of the total collected lar- Activity of An. superpictus s.l.s.l. had one vae and adults' mosquitoes, the An. dthali, An. peak point in its curve. This species had incom- stephensi, An. superpictus s.l.s.l., An. plete hibernation. Hibernation starting differed fluviatilis s.l. and other Anopheles in cool weather in different plains and populations had the most frequencies of 37%, mountainous areas. Based on different studies 55%, 1%, 2% and 5%, respectively. This in the North of Khorasan, Birjand, Kazeroon, species has been found in the mountainous it has been concluded that in appropriate region and played an essential role in disease thermal conditions and activity of Anopheles, transmission (116). this species is capable to transmitting In the studies, in Bandar Abbas it has been Plasmodium vivax after the second gono- identified that the most frequency of adult trophic cycle. Studies conducted in 1996, in Anophelini were An. stephensi, An. dthali, An. the county of Aligoodarz showed that larvae fluviatilis s.l. and with the low density An. 200 http://jad.tums.ac.ir Published Online: September 30, 2018

J Arthropod-Borne Dis, September 2018, 12(3): 196–218 H Vatandoost et al.: Bioecology of … DOI: 10.18502/jad.v12i3.73

culicifacies s.l. and An. superpictus s.l., s.l. doors. As in some parts of Iran, especially in respectively. The last two species were col- mountainous areas his species was found in- lected just in night biting (117). fected to sporozoites (Sarakhs and Kerman- shah) and is responsible for malaria trans- Distribution, Anthropophilic index, sporo- mission and having anthropophilic index, so zoite rate and behavior of adult Anopheles it could be a vector (119). superpictus s.l.s.l. About 16% of the total larvae collected This species had a major role in moun- in the months of April till November in 1994 tainous region. It had a role in malaria trans- in Lenjanat, Isfahan, belonged to this species. mission in Hormozgan Province. Combina- Larval activity in its larval habitats began from tion of malaria vectors in coastal plain and mid- June and late July with the frequency of mountainous area of the province was differ- 1 larva per ladle. The frequency was constant ent. The main vector in the coastal plain was until the end of August, but its activity de- An. stephensi and the secondary vector was creased in abundance from this time, so that An. dthali. In the mountainous region, beside by the mid-September it has been reduced to the mentioned species, An. fluviatilis s.l., An. zero. This species has been collected in light culicifacies s.l., and An. superpictus s.l. had traps with the frequency of 0.21% and adult a role in disease transmission. In mountain- activity increased simultaneously with larval ous areas, because of the presence of several activity in mid-July and has reached to its outdoor borrows and exophilic behavior of activity with the frequency of 1 mosquito per some vectors, vector eradication encountered light trap. Its activity decreased in a way that many problems and was effective only in it reached to zero in late August. This is lowering the population vector (107). species was mainly endophilic in the area Anthropophilic index using ELISA with and preferred blood feeding from to the blood spot prepared from female An. su- human. Total collection of this species in perpictus s.l.s.l. showed the Anthropophilic light traps and night biting methods in index between 28.5–3.7% and the feeding of March to November 1994 in Lanjanat, Isfahan cattle and other animals were 19.7%. The night was very low (120). bite on prey animals (cows and calves) in the This species has been collected in indoors village of Hussein Abad and Namazi villages of Germi county including villages of Ojagh, indicated that 55.6% and 66.2% of them were Zahra Kandi (Ojaroud), Agha Mohammad Bei- An. superpictus s.l.s.l. Based on this study it glou, Dykdash, Qeshlagh Beryan (Angoute appeared that this species had zoophilic be- gharbi), Aq Dash (District of Barzand). In havior. In this study An. superpictus s.l.s.l. had mountainous region of the Germi, Ardabil in- two peaks of activity, in the early hours of the cluding Qeshlagh Beryan and Dykdash, the night and the other in 3–5a.m. and its frequency frequency of An. superpictus was 10.63 mos- in first peak was more than the second peak. quitoes per place and had a wide distribution A similar result has been obtained in previous (112). studies (99, 118). Two species, An. superpictus s.l. and An. The numbers of 200, An. superpictus s.l. maculipennis s.l., have been distributed in lar- were used to determine parity and age-struc- val habitat studied in Mashhad and suburbs. ture of the An. superpictus s.l. populations. Anopheles superpictus s.l. with the frequency Parous percent in the first period of the sea- of 94% were more frequent in comparison to sonal activity was observed in 26% and its An. maculipennis s.l., and were collected from peak of activity was 44%. This species in the several larval habitats including fresh water, study area naturally preferred outdoors to in- non-polluted and largely stagnant waters with 201 http://jad.tums.ac.ir Published Online: September 30, 2018

J Arthropod-Borne Dis, September 2018, 12(3): 196–218 H Vatandoost et al.: Bioecology of … DOI: 10.18502/jad.v12i3.73

low flows. South of Mashhad, places like ponds, In a pit shelter study in Hussein Abad village in even with non-infected freshwater ponds, Astan Farsan, Chahar Mahal Bakhtiari, of the 78.5% Quds Razavi farms and its surroundings, high- of the collection belonged to An. superpictus ways and Qasem Abad village were places that s.l. that indicate that this species was exophil two species of An. superpictus s.l. and An. and most prevalent species in the study areas. maculipennis s.l. were collected (121). With regard to the eradication of this species Anopheles superpictus s.l. in villages and because of its exophilic property, insecticide tribal areas in Bazaft, Farsan, Chahar Mahal repellency, it could not stop disease transmis- Bakhtiari had a wide distribution. Frequency sion just using residual spraying and must use of adults and larvae were 67.2% and 78.9%, environmental improvements, using larvicides respectively. In the studied villages, An. su- and case finding and integrated pest manage- perpictus s.l. comprised 63% to 100% of col- ment (115) . lected Anopheles. This species was generally In survey that has been conducted in 1971 the dominant species in the area. The larvae in this area, results showed that frequency of of this species have also been collected from adult An. superpictus s.l. in Germi County has the height of 2500m above sea level (the Sar- been increased. This species had a salient ac- tang Sarveh Moorez) while collecting of this tivity with An. sacharovi. Increased abundance species has been reported as high as 2,000 me- of this species that is of main malaria vectors ters above sea level. It has been reported that in Iran, is most serious threat to the residents this species had exophilic behavior in the (122-123). mountainous areas of Sarakhs and Kermanshah. In Farsan, this species had more frequency in Human biting rate outdoor shelters such as mountains' crack, caves In Hussain Abad village, the bites per per- or under large rocks, under the bridge and river son in a night were 1.1. This figure for each wall and like the other parts of its distribution it person in Nazi village was 1.4 (115). was exophilic. Its seasonal activity began from second half of the July and continued till Blood feeding preferences October with the highest frequency in August This species was zoophage, and both en- in outdoors. Adult highest frequency in the do-exophilic. Blood feeding preference of hu- study area was 6.2 Anopheles per place and man varied depending on geographic location highest frequency of larvae in 10, ladle was and has been recorded from 5% (124-125). 33.7. In the studied area, An. superpictus s.l. In Iran, the human blood index for this was found mainly in cracks of the trees, species has been determined 22.4% and the mountains groove, caves and cracks between sediment test of fed females collected from the rocks that were used for flat -out caves have shown 4.1% the human Blood In- accommodation of tribal, pit walls, rivers, dex (119, 125). canals and springs, under bridges, human Blood feeding habits, resting and dwellings, closets and behind furniture, in dark longevity of An. superpictus s.l. in central storage, networking within the outdoor, and plateau and south parts of Iran is like An. shower stalls. Larval habitat of this species was fluviatilis s.l.. The results of the precipitation mainly in margins and riverbeds, streams flow test in different areas of Iran, for in grasslands springs, animal footprints, anthropophilic index have been reported holes and stagnant water around the road. Hab- between 4.8 to 21.4% (124) itats were more dirt floor in a meadow. In a research study in Lorestan Province The larval habitats were found more in bur- to determine blood meal type, fed by this rows in shaded and sunny waters in most places. species using ELISA, of the 1117 tested blood 202 http://jad.tums.ac.ir Published Online: September 30, 2018

J Arthropod-Borne Dis, September 2018, 12(3): 196–218 H Vatandoost et al.: Bioecology of … DOI: 10.18502/jad.v12i3.73

spots, the number of 128 specimens had reasons may explain proper zero coefficient positive ELISA for human blood and thus of blood feeding on human in indoors (118). the anthropophilic index of this species in Anthropophilic index for the An. superpictus this study has been reported 11.4% (126- s.l. in its maximum frequency was very low 130). (9.09%) (131). Anopheles superpictus s.l. fed on animal and human and preferred blood feeding in Longevity of the Anopheles superpictus S.l. areas with large groups of hosts than populations sporadic hosts. It preferred large body size Various studies (regions of Birjand-North hosts to small hosts. This species fed on Khorasan, Kazeroon, etc.) has shown that in different hosts, when it got dark or night, appropriate temperature conditions, An. super- even in places both inside and outside areas. pictus s.l. after the second gonotrophic cycle The host-seeking behavior of this species for is capable of transmitting Plasmodium vivax. blood feeding was highly active, and could In nature there is up to 5 gonotrophic cycles. search many buildings in search of food, and It has been observed that An. superpictus s.l. had a high mobility during blood feeding. for the first laying period was usually required Results of anthropophily and zoophily tests twice blood feeding. Of the 80, An. in Bazaft, Farsan in Chahar Mahal showed that superpictus s.l. (58.7%) were nulliparous, 33 out of the 92 blood samples, 28.4%, 39.1%, of them were diagnosed parous (41.3%). Re- 32.6% of the specimens' belonged to human, sult of the dissection of An. superpictus s.l. cattle and other animals, respectively. females, the rate of parous females was found Investigations in Khorasan showed that human to be 48.5% in 1st gonotrophic cycle, 36.5% blood feeding on human varied between 65– in 2nd gonotrophic cycles and 15.1% in 3rd 76%. gonotrophic cycles. Basically An. Studies conducted from May till Novem- superpictus s.l. in this area is most ber, between 1997 and 1998 by total catch in dangerous age in September. three indoor places (human, animal, and barn) Epidemiological studies showed that in and one outdoor place, cave, indicated that this Birjand and Kazeroon, An. superpictus s.l. species preferred feeding on domestic was an unstable vector. Desiccated salivary ruminants and animal than man. The indexes glands of An. superpictus s.l. in Aligoodarz, of blood feeding of fed females by ELISA in showed no sporozoites (103). all places were 1.02%, and in outdoors (Cave), barns, 1.45% and 2.82%., respectively. Sustainability index The human blood index of An. superpictus s.l. Epidemiological studies in Birjand and has been calculated zero, in human and Kazeroon showed that An. superpictus s.l. is animal places. The observations in the studied an unstable vector (stability index less than 0.5) villages showed that most of the people because and the executive observations support this high temperatures at night sleep in open spaces theory. This means that the use of residual in- (courtyard of the houses) and some of them secticides can easily control this species (ex- slept in nets. Livestock that their numbers were cluding the exophil population). much higher than the number of people in the house that were kept in the open spaces. Unfed Adult shelters mosquitoes after entering the houses preferred In Iran, a significant population of this spe- feeding on animals than humans. Then they cies rests in human and animal dwellings rest followed proper shelter (human indoors, including mud rooms, shed, stack, barns, animal, barn or outside shelters). These straw, tents and mud stables, rick, animal sheds, 203 http://jad.tums.ac.ir Published Online: September 30, 2018

J Arthropod-Borne Dis, September 2018, 12(3): 196–218 H Vatandoost et al.: Bioecology of … DOI: 10.18502/jad.v12i3.73

poultry nests. Some of the population of this tivity were reported from June to November. species, especially in the West (Kermanshah) In Ilam the activity of 3rd and 4th larvae and the East (Kashafroud region) didn’t enter to began from June to September, with most human habitations and has been collected activity and abundances in July. In from outdoors including cave, inside grain Khuzistan Province, activities of 3rd and 4th storage, cracks in the mountain rock, earth instars larvae were from May to October and fissures in the walls of the rivers, the with its peak of activity in July and August. aqueducts, under the bridge and artificial pits In Germi and Pars Abad, the larval habitats (99, 132-133). included along the Dare Roud River, rice fields, Anopheles superpictus s.l. larvae were col- small cavities and holes in the river beds lected from villages including Hoomeye marka- (113). zi, Roodan, Sandarak, Sirik, Dej Olia River, In Bazaft, Farsan, Chahar Mahal Bakhtiyari, Dej Sofla River and Bashagard. This species of the 6 villages and 4 tribal regions, An. that comprised 1.3% of the total percentage of superpictus s.l. comprised 44.2% of the Anoph- collected larvae periodically was active eles populations in human dwellings. In animal during at least 6 months of the year. This places An. superpictus s.l. comprised 63.7%, Anopheles has been collected from temporary of the Anopheles populations and in outdoors and stagnant waters, 62.5% and 100%, it was 77%. Totally, this species has been col- respectively. It has been collected with low lected from outdoors. In Hussain Abad village, percentages from permanent waters. This 243 mosquitoes were collected by night-bit- species could ovoposite in water nests that ing method that 165 of them (67.9%) were the water depth was low, with or without plant, An. superpictus s.l.. In this village in Farsan, sunny or semi-shade. The larvae of this species of the 254 Anopheles mosquitoes collected prefered larval habitat with soil or sandy in in pit shelters, 180 (70.8%) of them were An. their bed along the rivers (to 80%), wetland, superpictus s.l.. Frequency of An. grasslands and fresh waters. It chose fresh superpictus s.l. were 162 (66%) larvae and clear waters for ovoposition (50%). collected from the tribal wattle, 130 (100%) Anopheles superpictus s.l. larvae have been from Shermak, 168 (66.7%) from tribal re- collected together An. stephensi, An. gions of Labad and in tribal regions of Tash- fluviatilis s.l., An. dtali, An. thurkhudi and navi it was 181 (63%) (116). An. multicolor in the same larval habitat. In Studies conducted from May till Novem- some west and south west provinces of Iran, ber, between 1997 and 1998 by total catch An. superpictus s.l. larvae has appeared from method in three indoors (human, animal, temporary and stagnant waters with the barn) and one outdoor (cave) in the province frequency of 40% and with low density from of Lorestan showed that of 1661 collected permanent waters with or without plants. Culicidae mosquitoes, the 1632 (98.25%) The larvae of this species in Kurdistan began were Anopheles genus, and among them the their activity in mid-June and ends in mid- total number of 1630 (99.3%) of the October. The peak activity is from early collected Anopheles were An. superpictus s.l. August to mid-September, and its activity 631 (50.8%) collected female An. dependent on temperature. superpictus s.l. were freshly feeders (119). The larvae of this species have been col- lected from the cities of Islamabad-E-Gharb, Malaria transmission potential Paveh, Qasr-e Shirin, Harsin (Bakhtaran) in In some parts of Iran, especially Kashaf 1984–1985. In Bakhtaran the maximum abun- roud in Khorasan and Kermanshah it was dance of larvae were found in July and its ac- discovered that despite eradication programs, 204 http://jad.tums.ac.ir Published Online: September 30, 2018

J Arthropod-Borne Dis, September 2018, 12(3): 196–218 H Vatandoost et al.: Bioecology of … DOI: 10.18502/jad.v12i3.73

malaria transmission by this species has not from sandy margins of the river (Gamasab stopped (Mesghali unpublished observation, and Chamkhal rivers in Kermanshah Prov- 1968). Vectorial capacity is a measure of epi- ince). demiology in different geographical regions Captures of 2nd (early instars), 3rd–4th (late that is used to determine the malaria transmis- instars) instars and pupae have been done for sion risk. Vectorial capacity is affected by three An. superpictus s.l. immature abundances in factors including anthropophily, longevity, and different agro-ecosystems in Iran. Anopheles mosquito vector population density. In Iran, superpictus s.l. larvae are associated with gravel sporozoite rate has been reported 0.9%. or fresh waters of swamplands and marshes, Desiccation of salivary glands of An. and pebble river and stream beds in shallow, superpictus s.l. in Khorasan, Kermanshah, slow-flowing clear water in full sunlight, small Kazeroon and Masjed-E-Soleiman showed rivers or streamlet, holes, pits and natural dams, that almost 1.2% of the desiccated specimens small pools within or next to river beds and were infected to sporozoite. In Tabas 4.6% streams, storage tanks, broken pitchers, of the specimens and in Kazeroon 0.65% of empty cans, water reservoirs, rice fields and the specimens were infected with sporozoite associated irrigation canals, natural grass- and 0.7% of them were infected to oocyte. land, large rivers that makes pools, animal These studies indicated that An. superpictus hoof traces, tires, small pools within or next s.l. was of the major malaria vectors in the to river beds, are suitable as aquatic habitats. central plateau and the southern slopes of the Preferred water temperature for ovopositing Zagros Mountains of Iran (128). of this species in day time, usually reached Anopheles superpictus s.l. has been to 35 °C to 38 °C. In 30 °C, the larval period identified as a main malaria vector in all lasted 11 days. However, at temperatures be- regions of central Iranian plateau. In addition, tween 19 °C to 20 °C, the larval period has this species had significant role in been estimated at 24 days. Frequency of 3rd maintaining malaria as a second or third and 4th instars of An. superpictus s.l. in each vector in mountainous and foothills of ladle from April till November 1994 in southern Zagros range. In 255 desiccated Lanjanat, Isfahan in late July, mid-August and specimens in Birjand in 1961, the sporozoite late August were 0.1, 0.1 and 0.1, respectively index was 4.7% (accidental sampling). and in the remaining months was zero (122). Desiccation of 411 An. superpictus in the Ecological characteristics of larval habi- mountainous region of Shapoor (Kazeroon) in tats of An. superpictus s.l. in 24 larval habi- 1960, infective index was 0.65%. In Bazaft, tats in Lorestan Province showed richness of Farsan, dissection of 200 An. superpictus to de- species composition that is indication of the termine the number of parous and nulliparous importance of land use patterns on diversity showed that the parous rate were 26%, 46% of larval habitat types that included An. su- and 40% in late July, August and September, perpictus s.l., An. turkhudi, An. stephensi, An. respectively. A total of 126 Anopheles dthali, An. sacharovi, An. claviger and An. salivary glands and stomach were dissected martri. Anopheles superpictus s.l. larvae were and none of them was found infective to collected from standing or temporary and es- sporozoite and oocyst (116). pecially from still waters. This species was ac- tive in the waters with aquatic vegetation on Larval habitats their surface or outside of them. More than This species can be found in beds of 45% of the specimens were collected from hab- rivers that are drying in hot climate of the itats without any aquatic vegetation. In 87.5% summer. This species have been collected cases this species oviposit in the sandy and soil 205 http://jad.tums.ac.ir Published Online: September 30, 2018

J Arthropod-Borne Dis, September 2018, 12(3): 196–218 H Vatandoost et al.: Bioecology of … DOI: 10.18502/jad.v12i3.73

beds habitats with fully sunlight. This species perpictus s.l. larvae with the abundance of prefers clear and fresh waters. Their larval hab- 33.7% in 10 itats were close to rivers (53.2%), lakes, grass- ladles had the highest density. lands, holes, streams, and river beds (46.8%). In man-made larval habitats, 87.5% larval hab- Adult susceptibility tests itats were found in rice fields and 12.5% were The insecticide susceptibility tests on field in cement grooves. Larval peaks of activity adults and larvae were performed in 1972–1975 have been reported from mid-July till second on the An. superpictus s.l. collected from dif- half of the October. 67.8% of the larval habi- ferent parts of the country including moun- tats were standing and 32.2% of them were tainous, temperate and desert areas including temporary. 62.6% of the larval habitats were Isfahan, Kermanshah, Khorasan, Kurdistan, still waters and rests of them were running and Ilam provinces. For the adult tests, female waters. In this survey from the 115 larval hab- An. superpictus s.l. were exposed to discrim- itats, 88.7% of the specimens were collected inating doses of OC, OP and PY insecticides from sunny habitats. This species preferred to including D.D.T. (mortality rate: 99.4%), mal- oviposit in sandy bed larval habitats (55.7%), athion (mortality rate: 100%), lambdacyhalo- mud (40.8%) and cement canals (3.5%). thrin (mortality rate: 100%) and dieldrin for These species were mainly found in hab- 60min. The effects of these pesticides were itats without vegetation (46.9%), vegetation evaluated in accordance with WHO standards, outside of the water (36.5%) and the rests of using mortality rates after 1-hour exposure fol- them in vegetation on the surface or under the lowed by monitoring over a 24-hour recovery water. In Lorestan Province, larval habitats were period. The adult susceptibility tests using found in agro-villages s.l.es of Pishkouh Zalghi WHO criteria (98–100% mortality indicating (villages of Baghe lotfian, Kizan Darreh, susceptibility and < 98% mortality indicating Kakolestan), Farsash (villages of Farsash, Homa resistance), showed that An. superpictus s.l. and Ivaj), Barbaroude Shargi (villages of Cham- was susceptible to all the tested insecticides an Soltan (Shahrake Emam), Ab Barik, Dehnou (107-109). In Ilam Province, in 2002, the per- Khaje), Pache Lake Shargi (villages of Dehe centage of mosquitoes knocked down at 60 nasir, Sour, Choghatar), Mahrou (villages of minutes were 100%, 99% and 98% for lamb- Margsar and Chal Ghale). dacyhalothrin, malathion and DDT, respec- In Bazaft, Farsan, Chahar Mahal Bakhtiari tively (111)). Table 1 and Figure 3 show the in 1999, in the tribal region, activity of resistant of species to DDT and susceptible different species of Anopheles in ten studied vil- to other insecticides in the country. lages were investigated 120 times. A total num- ber of 2543 larvae were collected from different larval habitats including river margins, stagnant water, grasslands and springs. In tribal regions a total number of 162 larvae were collected that 66.6% of them were An. superpictus s.l.. In Labeh of the 168 collect- ed larvae, the frequency of An. superpictus s.l. was 66.7%. In Shermak area of the 130 col- lected larvae 100% of them were An. super- pictus s.l.. In Teshnavy that is a tribal area of Fig. 1. Distribution of Anopheles superpictus s.l. in the 181 collected larvae in 12 times, 63% of Iran them were An. superpictus s.l.. Anopheles su- 206 http://jad.tums.ac.ir Published Online: September 30, 2018

J Arthropod-Borne Dis, September 2018, 12(3): 196–218 H Vatandoost et al.: Bioecology of … DOI: 10.18502/jad.v12i3.73

Fig. 2. Morphology of larva of Anopheles superpictus s.l. Table 1. Status of insecticide resistance in Anopheles superpictus from Iran, 1957–2016

Insecticide Anopheles superpictus DDT 4% R Dieldrin 0.4–4% S Malathion 5% S Lambdacyhalothrin 0.025–0.1% S

S= Susceptible R= resistant

Fig. 3. Mapping status of Anopheles superpictus to DDT in Iran of organized malaria control activities. Malaria Discussion is particularly prevalent in tropical provinces including Sistan and Baluchistan. Iran remains

highly conducive to vector borne diseases due Malaria remains an important parasitic dis- to geography, and uncontrolled population ease in different parts of Iran, despite decades 207 http://jad.tums.ac.ir Published Online: September 30, 2018

J Arthropod-Borne Dis, September 2018, 12(3): 196–218 H Vatandoost et al.: Bioecology of … DOI: 10.18502/jad.v12i3.73

movement. The Anopheles (Cellia) superpic- Understanding of all bioecology of ma- tus s.l. is important malaria vectors that have laria vector will guide the scientist and deci- been found in different provinces of Iran. sion makers for appropriate diseases control. Anopheles superpictus s.l. represent important vectors of malaria throughout the Palearctic Acknowledgment Region, including Iran. This s.l. contains at least three closely-related sibling species that This research is financially supported by can be differentiated based on distinctive ge- the Ministry of Health and Medical Educa- netic characters. Current evidence shows that tion National Institute for Medical Research climate variability has a direct effect on the Development (NIMAD) under code number epidemiology of vector-borne diseases in- of 963262. All authors declare that there is cluding malaria). The most influence of cli no conflict of interest

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