Eco-biology of Anopheles superpictus in Iran J Arthropod-Borne Dis, September 2018, 12(3): 196–218 H Vatandoost et al.: Bioecology of … 196 http://jad.tums.ac.ir Published Online: September 30, 2018 Review Article Bioecology of Dominant Malaria Vector, Anopheles superpictus s.l. (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 University 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. was reviewed in Iran in more than half a centu- ry. Different aspects including, distribution, key identification, larval habitats, flight range, seasonal activities, irrita- bility/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 problems worldwide, among them malaria presents a major health problem globally. In 2016, an estimated 216 million cases of ma- laria occurred worldwide, compared with 237 million cases in 2010 and 211 million cases in 2015. Most malaria cases in 2016 were re- ported from the WHO African Region, while the two percent of cases were inhabitants of WHO Eastern Mediterranean Region coun- tries (1). It is one of the important infectious diseases in Iran with an average of about 15000 annual cases in the last decade, while total recorded cases has dropped to less than 100 locally transmitted cases in 2017. Most of indigenous and imported malaria cases in Iran are reported from southern and southeast- ern areas of the country in Sistan and Baluchi- stan, Hormozgan and South of Kerman Prov- inces. The most routes of malaria cases are im- migration from Afghanistan and Pakistan to southern and southeastern areas of the coun- try (Ministry of Health, annual reports). Anopheline mosquitoes (Diptera: Culicidae) are vectors of malaria to humans. Currently there are proven and effective tools to fight against malaria including vector control measures (1). As these tools are scaled up, ma- laria endemic countries need to continually up- date the skills and competence of the health workers engaged in malaria control and elim- ination. All observations indicate that the data re- flect the real situation and that the overwhelm- *Corresponding author: Dr Hassan Vatandoost, E- mail: hvatandoost1@yahoo.com, vatando@tums.ac.ir http://jad.tums.ac.ir/ mailto:hvatandoost1@yahoo.com mailto:vatando@tums.ac.ir J Arthropod-Borne Dis, September 2018, 12(3): 196–218 H Vatandoost et al.: Bioecology of … 197 http://jad.tums.ac.ir Published Online: September 30, 2018 ing majority of cases, which occur, are includ- ed in the national system, although there is room for improvement in the surveillance sys- tem. The spectacular progress can be ascribed to effective implementation of appropriate cu- rative and preventive control interventions through a strong health care infrastructure. Social and economic development allowing better housing, use of air-conditioning etc. has also played a role. There are several activities on different aspects of malaria in the country: including insecticide resistance monitoring (2-12), sib- ling species, molecular study, new record (13- 20), novel methods for vector control (21-26) faunestic study (27, 28), use of plants for lar- val control (29-41) using bednets and long lasting impregnated nets (42-48), morphologi- cal studies (49-51), malaria epidemiology (52- 55), ecology of malaria vectors (56-64), bio- diversity (65, 66), community participation (45, 54), vector control (67), repellent evaluation (68), anthropophilic index of malaria vectors (65, 69), training (70) is designated as malar- ia training center by WHO. There are several reports on different aspects of malaria vec- tors recently different studies have been con- ducted during more than 90 years on malaria (71-96) and its vectors in Iran. Seasonal activity of Anopheline mosqui- toes and their peak of activity vary in different area due to environmental condition. This issue affected the epidemiology of malaria transmis- sion in different regions. Agriculture in Iran remains highly sensitive to climate develop- ments, the country's most important crops are wheat, rice and other grains, sugar beet, fruits, nuts, cotton, and tobacco, which require the use of insecticides. So far different groups of insecticides are using for crops protection in the country. The main governmental use of insecticide in the health sector is their appli- cation for adult mosquito control. The first attempts to control malaria vectors started dur- ing the 1960’s with organochlorines (DDT, dieldrin and BHC), followed by organophos- phates (Malathion and pirimiphos-methyl) for about two decades from 1966. After that dur- ing 1977–1990 propoxur was used by national malaria vector control program. Subsequent- ly, after the introduction of pyroteroids into the market, and given their lower risk for humans and more affordable products, lambdacyhalo- thrin and deltamethrin were used. As the adult mosquitoes control, larval control is also used to reduce the vector abundance. For this pur- pose, Temephos, Reldan® and pirimiphos- methyl was used in past decades. Materials and Methods All the published papers thought the in- ternet and master of sciences and PhD thesis related to An. superpictus s.l. were reviewed and evaluated. Key words for search in scien- tific motor engines were: Anopheles superpic- tus, insecticide resistance, ecology, distribution, identification, anthropophilicity, sporozoite rate, Iran. Results Distribution of Anopheles superpictus s.l. in Iran Faghih' research results showed that this species could be found in areas of 2000 me- ters above sea level (97-99). It has been cap- tured from coastal plains of Persian Gulf in areas with 500 meters height above sea level (in Chelou village in Minab). With the excep- tion of a narrow strip of coastal areas, this species is found in almost all regions of Hor- mozgan Province (100-104) (Fig. 1). Key to the female Anopheles superpictus s.l. Wings with contrasting pale and dark spots, at least on costa (C), radius (R) and radius-one (R1), Hind tarsomeres 3–5 no1 entirely pale, Maxillary palpus dark, or with at most 3 dis- tinct pale bands (pale spots may also be pre- sent): abdominal terga II-VII without dark http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2018, 12(3): 196–218 H Vatandoost et al.: Bioecology of … 198 http://jad.tums.ac.ir Published Online: September 30, 2018 scale-tulips. Although some posterolateral dark scales may be present on distal segments, Hind tarsomere 5 dark, Palpomere 5 entirely pale, Femora and tibiae not spotted: abdominal terga without pale scales, Anal vein with 2 dark spots, distal spot long (104). Key to the Anopheles superpictus s.l. larvae Seta 2- Cephalon inserted at least as far apart as the distance between 2- Cephalon and 3- Cephalon on one side, seta 1- Antenna al- ways simple, seta 5, 6, 7- Cephalon branched (subgenus Cellia), Tergal plates on abdominal segments III-VII smaller, < 0.5 width of seg- ment, and not enclosing median accessory ter- gal plate, Thoracic pleural seta various , Thor- ax with at least long pleural seta 9- Prothorax and 9- Metathorax branched, 9, 10- Mesotho- rax, and 10- Metathorax simple or branched, Thorax with long pleural seta 9- Prothorax and 9, 10- Metathorax branched. Seta 9- Mesothorax branched, 10- Meso- thorax simple, palmate seta 1-III-VII strong, leaflets and filaments various, Seta 3- Cepha- lon simple or with a few short lateral branches, not brush-like in appearance, abdominal pal- mate seta 1- Abdominal segment I non-pal- mate or very weakly palmate, Seta 1, 2- Pro- thorax tubercles separate; seta 3- Metathorax non-palmate or very weakly palmate, Seta 2, 3- Cephalon simple, finely or distinctly frayed, anal papillae normal, abdominal palmate fil- aments  0.5 length of blade, Seta 3, 4- Ceph- alon simple or occasionally bifid, never branched, Seta 2, 3- Cephalon smooth or fine- ly frayed, abdominal seta 1- Abdominal seg- ment II strongly palmate, Seta 3- Cephalon finely frayed, seta 4- Cephalon length > 3- Cephalon, basal tubercle of seta 1- Prothorax weak (Fig. 2) (104). The Anopheles superpictus s.l. species Anopheles superpictus s.l. acts as a main malaria vector (e.g. in Lorestan) or secondary vector (e.g. Sistan and Baluchistan). A survey has been conducted in order to study on dif- ferent morphological and genetic variation of An. superpictus populations in Iran. Mosqui- toes of An. superpictus were collected from the Ardebil, Lorestan, and Sistan and Baluchistan provinces in July-September in 2004 using dif- ferent collection methods. After species iden- tification and morphological study on larvae and adults, the sequence variation of ITS2- rDNA and mtDNA COI-COII fragments were analyzed using PCR-RFLP and PCR-direct se- quencing assays. Results showed that there were significant differences in morphological and genetic characters within and between popu- lations. Digestion of COI-COII fragment us- ing AluI enzyme demonstrated various hap- lotypes indicating intra or inter-species var- iation. Totally 4 haplotypes were observed be- tween specimens/populations in 708bp of COI gene. Totally, the rate of variation among pop- ulations was 12.3%. This rate was 2–5% for within Sistan and Baluchistan populations. Ac- cording to phylogenetic analysis of the COI sequences, An. superpictus populations in Iran constructed 2 main groups including: 1) south- east populations (Sistan and Baluchistan and Kahnooj) and 2) central and northwest popu- lations, each group putatively representing one species. Analysis of ITS2 fragment also re- vealed highly diverged populations represent- ing at least three putative separate species des- ignated as X, Y, and Z (X and Y in Baluchistan and Z in other provinces). The rate of genetic variation in ITS2 was 27% in which respec- tively 0.27%, 0.05% and 26.68% correspond- ed to 5.8S, 28S, and ITS2 regions. Phyloge- netic analysis also revealed two main groups including three branches, each one putatively representing one separate species. In spite of having a high genetic and morphological var- iation among specimens, there were no rela- tionship between phenotypic and genetic var- iations, assuming that other parts of genome is responsible for the variations. The rate of genetic variation in COI and ITS2 regions was far more than that has been seen in other species s.l. (105). http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2018, 12(3): 196–218 H Vatandoost et al.: Bioecology of … 199 http://jad.tums.ac.ir Published Online: September 30, 2018 Flight ranges Flight range of this species was about 2– 2.5 kilometers (observations in Tabas, Birjand). At the beginning of hibernation it reached to 4km (99). Irritability tests The irritability levels of An. superpictus s.l. against diagnostic dose of dichlorodiphe- nyltrichloroethane (DDT) insecticide were measured in a conical exposure chamber ac- cording to WHO methods in Isfahan in 1963. The results of irritability tests showed that DDT had the high irritancy effect against An. superpictus s.l. (106). The time of blood feeding The activity of this species started at about 20pm and reached to peak point at about 21.30pm. The most brutal is in the first half and with low density in the second half of the night and in the morning it was close to zero. The most biting activity in Bazaft, Farsan, Cha- har Mahal Bakhtiari in 1999 was in 22–23pm and 3–5am (110-111). Seasonal activity Researches have been conducted from ear- ly October to April 1953–1955 to determine An. superpictus s.l. seasonal activity. Anoph- eles superpictus s.l. adult population abun- dances for the entire period of August-Sep- tember were high, but during the October, it began to decrease. The last collection was con- ducted in the third week of October. Even though space spray collection using Pyrethrums (PSC), that was applied at homes, very few adult were collected in each station during the months of November–February. Based on in- formation about the larvae collection and dis- sected adults, it has been concluded that this species didn’t enter to hibernation phase in October. It seems that leaving hibernation hap- pened in February, because the females that have been desiccated at this month had high ovarian growth. During the month of May, no larvae were collected. This result showed that although this species ovoposited in Feb- ruary or March, but the eggs were expelled be- cause of abundant rainfall, rapid flow of springs and streams. Changes were not the same dur- ing three winters. Winter 1953–1954 had the coldest winter and 1955–1954 was the modest. The numbers of collected specimens to gen- eralize the reliability results were very low. Alt- hough the temperature in February, was dif- ferent from the temperature in the first three months but the collected females showed the high activity both for the ovarian growth and blood feeding. Even in March that this spe- cies began its activity, the temperature was more than the last 4 months. It has been jus- tified that An. superpictus s.l. entered to hi- bernation phase because of a physiological cy- cle caused by cold weather. In Ilam, An. super- pictus s.l. is the main malaria vector and com- prised almost one hundred percent of the col- lected Anopheles from indoors and outdoors (111). Studies in Kermanshah and Sabzevar in- dicated that the activity of this species depended on the temperature and the onset of its activi- ty was from mid-June and ended in mid-Oc- tober. Maximum activity is in early August to mid- September and with the onset of cold weather that is different in various parts of the plains and mountainous areas; after this time it entered to hibernation. Females entered to hibernation phase in mountainous caves and indoors from mid- September in west with stor- ing fat and from October to next April when the weather was good for mosquito activity (Manoochehri, personal negotiation). In a study in the counties of Pars Abad and Germi in 1997–1998, the activity of this spe- cies has been reported during July-November. The maximum abundances of this species was 10.6 per place in the second half of August and with the least frequency was 0.25 number per location in the first half of December in Dykdash and Qeshlaq Beryan villages. Theis species had one peak of activity in second half of August in (112). http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2018, 12(3): 196–218 H Vatandoost et al.: Bioecology of … 200 http://jad.tums.ac.ir Published Online: September 30, 2018 In human dwellings, the frequency of An. superpictus s.l. in each place was 1.8. In out- doors, An. superpictus s.l. had the highest frequency of 6.2 per place in early of August. In human dwellings, its frequency was 1.8 and in outdoors it was 6.2 per each place with the highest abundance in the early of August. The highest monthly activity of An. superpictus s.l. in Dykdash Village, Germi, was in the eight- eenth of July, 1996. In Dykdash and Agha Mo- hammad Biglou villages its activity began in eighteenth June and ended in third of Decem- ber. In the village of Agha Mohammad Biglou the highest activity was in the second half of August. In Dykdash and Gheshlagh Beryan villages, its activity in indoors has been re- ported during the months of July-November, with the highest frequency of 10.63 mosqui- toes per place in the second half of August and the least abundant numbers per place (0.25) in the first half of December. This species hasn’t been collected from plain of Parsabad (112), but studies of Abai and colleagues in 2002 have been obtained very low abundance in this area. The most abundant of this species in the county of Kahnooj was during September and October (113). Activity of An. superpictus s.l. had one peak point in its curve. This species had incom- plete hibernation. Hibernation starting differed in cool weather in different plains and moun- tainous areas. Based on different studies in the North of Khorasan, Birjand, Kazeroon, it has been concluded that in appropriate thermal conditions and activity of Anopheles, this spe- cies is capable to transmitting Plasmodium vi- vax after the second gonotrophic cycle. Stud- ies conducted in 1996, in the county of Ali- goodarz showed that larvae of this species began its activity in May with the peak activ- ity in September and in October it reached to zero (103, 114). Species composition Fauna and ecology of vectors in the county of Farsan, Bazaft, Chahar Mahal Bakhtiari, in human dwellings, indicated that An. super- pictus s.l. comprised 44.2% of the collected Anopheles populations. In animal habitats it comprised 63.7% of the total collected Anopheles. In outdoors, An. superpictus s.l. comprised 77% of the populations. It has been collected generally in high population densi- ty from outdoors. In Hussain Abad village, of the 243 mosquitoes collected in night bit- ing, 165 of them (67.9%) were An. superpictus s.l. In the village of Mazi, a total number of 356 Anopheles collected with the method of night biting, An. superpictus s.l. comprised 246 (69.1%) of the Anopheles population. In the village of Hussain Abad, of the 254 col- lected Anopheles in pit shelter the number of 180 of them (70.8%) were An. superpictus s.l. (116). The highest biting activity of Anopheles superpictus s.l. in Bazaft, Farsan, Chahar Mahal Bakhtiari in 1999 was occurred in 22–23pm and at 3–5am (115). Anopheles superpictus s.l. was the most important vectors in Siahoo area, Southern Iran. Entomological studies conducted in this dis- trict showed that of the total collected larvae and adults' mosquitoes, the An. dthali, An. ste- phensi, An. superpictus s.l., An. fluviatilis s.l. and other Anopheles populations had the most frequencies of 37%, 55%, 1%, 2% and 5%, respectively. This species has been found in the mountainous region and played an es- sential role in disease transmission (116). In the studies, in Bandar Abbas it has been identified that the most frequency of adult Anophelini were An. stephensi, An. dthali, An. fluviatilis s.l. and with the low density An. culicifacies s.l. and An. superpictus s.l., re- spectively. The last two species were col- lected just in night biting (117). Distribution, anthropophilic index, sporo- zoite rate and behavior of adult Anopheles superpictus s.l. This species had a major role in moun- tainous region. It had a role in malaria trans- mission in Hormozgan Province. Combina- http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2018, 12(3): 196–218 H Vatandoost et al.: Bioecology of … 201 http://jad.tums.ac.ir Published Online: September 30, 2018 tion of malaria vectors in coastal plain and mountainous area of the province was differ- ent. The main vector in the coastal plain was An. stephensi and the secondary vector was An. dthali. In the mountainous region, beside the mentioned species, An. fluviatilis s.l., An. culicifacies s.l., and An. superpictus s.l. had a role in disease transmission. In mountain- ous areas, because of the presence of several outdoor borrows and exophilic behavior of some vectors, vector eradication encountered many problems and was effective only in lowering the population vector (107). Anthropophilic index using ELISA with the blood spot prepared from female An. su- perpictus s.l. showed the Anthropophilic in- dex between 28.5–3.7% and the feeding of cattle and other animals were 19.7%. The night bite on prey animals (cows and calves) in the village of Hussein Abad and Namazi villages indicated that 55.6% and 66.2% of them were An. superpictus s.l. Based on this study it appeared that this species had zoophilic be- havior. In this study An. superpictus s.l. had two peaks of activity, in the early hours of the night and the other in 3–5a.m. and its frequency in first peak was more than the second peak. A similar result has been obtained in previous studies (99, 118). The numbers of 200, An. superpictus s.l. were used to determine parity and age-struc- ture of the An. superpictus s.l. populations. Parous percent in the first period of the sea- sonal activity was observed in 26% and its peak of activity was 44%. This species in the study area naturally preferred outdoors to in- doors. As in some parts of Iran, especially in mountainous areas his species was found in- fected to sporozoites (Sarakhs and Kerman- shah) and is responsible for malaria trans- mission and having anthropophilic index, so it could be a vector (119). About 16% of the total larvae collected in the months of April till November in 1994 in Lenjanat, Isfahan, belonged to this species. Larval activity in its larval habitats began from mid- June and late July with the frequency of 1 larva per ladle. The frequency was constant until the end of August, but its activity de- creased in abundance from this time, so that by the mid-September it has been reduced to zero. This species has been collected in light traps with the frequency of 0.21% and adult activity increased simultaneously with larval activity in mid-July and has reached to its activity with the frequency of 1 mosquito per light trap. Its activity decreased in a way that it reached to zero in late August. This is spe- cies was mainly endophilic in the area and preferred blood feeding from animals to hu- man. Total collection of this species in light traps and night biting methods in March to November 1994 in Lanjanat, Isfahan was very low (120). This species has been collected in indoors of Germi county including villages of Ojagh, Zahra Kandi (Ojaroud), Agha Mohammad Bei- glou, Dykdash, Qeshlagh Beryan (Angoute gharbi), Aq Dash (District of Barzand). In mountainous region of the Germi, Ardabil in- cluding Qeshlagh Beryan and Dykdash, the frequency of An. superpictus was 10.63 mos- quitoes per place and had a wide distribution (112). Two species, An. superpictus s.l. and An. maculipennis s.l., have been distributed in lar- val habitat studied in Mashhad and suburbs. Anopheles superpictus s.l. with the frequency of 94% were more frequent in comparison to An. maculipennis s.l., and were collected from several larval habitats including fresh water, non-polluted and largely stagnant waters with low flows. South of Mashhad, places like ponds, even with non-infected freshwater ponds, Astan Quds Razavi farms and its surroundings, high- ways and Qasem Abad village were places that two species of An. superpictus s.l. and An. maculipennis s.l. were collected (121). Anopheles superpictus s.l. in villages and tribal areas in Bazaft, Farsan, Chahar Mahal Bakhtiari had a wide distribution. Frequency of adults and larvae were 67.2% and 78.9%, http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2018, 12(3): 196–218 H Vatandoost et al.: Bioecology of … 202 http://jad.tums.ac.ir Published Online: September 30, 2018 respectively. In the studied villages, An. su- perpictus s.l. comprised 63% to 100% of col- lected Anopheles. This species was generally the dominant species in the area. The larvae of this species have also been collected from the height of 2500m above sea level (the Sar- tang Sarveh Moorez) while collecting of this species has been reported as high as 2,000 me- ters above sea level. It has been reported that this species had exophilic behavior in the mountainous areas of Sarakhs and Kermanshah. In Farsan, this species had more frequency in outdoor shelters such as mountains' crack, caves or under large rocks, under the bridge and river wall and like the other parts of its distribution it was exophilic. Its seasonal activity began from second half of the July and continued till Oc- tober with the highest frequency in August in outdoors. Adult highest frequency in the study area was 6.2 Anopheles per place and highest frequency of larvae in 10, ladle was 33.7. In the studied area, An. superpictus s.l. was found mainly in cracks of the trees, mountains groove, caves and cracks between the rocks that were used for flat -out accommodation of tribal, pit walls, rivers, canals and springs, under bridges, human dwellings, closets and behind furniture, in dark storage, networking within the outdoor, and shower stalls. Larval habitat of this species was mainly in margins and riverbeds, streams flow in grasslands springs, animal footprints, holes and stagnant water around the road. Hab- itats were more dirt floor in a meadow. The larval habitats were found more in bur- rows in shaded and sunny waters in most places. In a pit shelter study in Hussein Abad village in Farsan, Chahar Mahal Bakhtiari, of the 78.5% of the collection belonged to An. superpictus s.l. that indicate that this species was exophil and most prevalent species in the study areas. With regard to the eradication of this species because of its exophilic property, insecticide repellency, it could not stop disease transmis- sion just using residual spraying and must use environmental improvements, using larvicides and case finding and integrated pest manage- ment (115). In survey that has been conducted in 1971 in this area, results showed that frequency of adult An. superpictus s.l. in Germi County has been increased. This species had a salient ac- tivity with An. sacharovi. Increased abundance of this species that is of main malaria vectors in Iran, is most serious threat to the residents (122-123). Human biting rate In Hussain Abad village, the bites per per- son in a night were 1.1. This figure for each person in Nazi village was 1.4 (115). Blood feeding preferences This species was zoophage, and both en- do-exophilic. Blood feeding preference of hu- man varied depending on geographic location and has been recorded from 5% (124-125). In Iran, the human blood index for this spe- cies has been determined 22.4% and the sed- iment test of fed females collected from caves have shown 4.1% the human Blood Index (119, 125). Blood feeding habits, resting and longev- ity of An. superpictus s.l. in central plateau and south parts of Iran is like An. fluviatilis s.l.. The results of the precipitation test in differ- ent areas of Iran, for anthropophilic index have been reported between 4.8 to 21.4% (124) In a research study in Lorestan Province to determine blood meal type, fed by this species using ELISA, of the 1117 tested blood spots, the number of 128 specimens had pos- itive ELISA for human blood and thus the anthropophilic index of this species in this study has been reported 11.4% (126-130). Anopheles superpictus s.l. fed on animal and human and preferred blood feeding in areas with large groups of hosts than sporad- ic hosts. It preferred large body size hosts to small hosts. This species fed on different hosts, when it got dark or night, even in places both inside and outside areas. The host-seeking be- havior of this species for blood feeding was http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2018, 12(3): 196–218 H Vatandoost et al.: Bioecology of … 203 http://jad.tums.ac.ir Published Online: September 30, 2018 highly active, and could search many build- ings in search of food, and had a high mobil- ity during blood feeding. Results of anthropophily and zoophily tests in Bazaft, Farsan in Chahar Mahal showed that out of the 92 blood samples, 28.4%, 39.1%, 32.6% of the specimens' belonged to human, cattle and other animals, respectively. Inves- tigations in Khorasan showed that human blood feeding on human varied between 65–76%. Studies conducted from May till Novem- ber, between 1997 and 1998 by total catch in three indoor places (human, animal, and barn) and one outdoor place, cave, indicated that this species preferred feeding on domestic rumi- nants and animal than man. The indexes of blood feeding of fed females by ELISA in all places were 1.02%, and in outdoors (Cave), barns, 1.45% and 2.82%., respectively. The hu- man blood index of An. superpictus s.l. has been calculated zero, in human and animal places. The observations in the studied villages showed that most of the people because high tempera- tures at night sleep in open spaces (courtyard of the houses) and some of them slept in nets. Livestock that their numbers were much higher than the number of people in the house that were kept in the open spaces. Unfed mosquitoes after entering the houses preferred feeding on animals than humans. Then they rest followed proper shelter (human indoors, animal, barn or outside shelters). These reasons may explain proper zero coefficient of blood feeding on human in indoors (118). Anthropophilic index for the An. superpictus s.l. in its maximum frequen- cy was very low (9.09%) (131). Longevity of the Anopheles superpictus s.l. populations Various studies (regions of Birjand-North Khorasan, Kazeroon, etc.) has shown that in appropriate temperature conditions, An. super- pictus s.l. after the second gonotrophic cycle is capable of transmitting Plasmodium vivax. In nature there is up to 5 gonotrophic cycles. It has been observed that An. superpictus s.l. for the first laying period was usually required twice blood feeding. Of the 80, An. superpic- tus s.l. (58.7%) were nulliparous, 33 of them were diagnosed parous (41.3%). Result of the dissection of An. superpictus s.l. females, the rate of parous females was found to be 48.5% in 1st gonotrophic cycle, 36.5% in 2nd gono- trophic cycles and 15.1% in 3rd gonotrophic cycles. Basically An. superpictus s.l. in this area is most dangerous age in September. Epidemiological studies showed that in Bir- jand and Kazeroon, An. superpictus s.l. was an unstable vector. Desiccated salivary glands of An. superpictus s.l. in Aligoodarz, showed no sporozoites (103). Sustainability index Epidemiological studies in Birjand and Kazeroon showed that An. superpictus s.l. is an unstable vector (stability index less than 0.5) and the executive observations support this theory. This means that the use of residual in- secticides can easily control this species (ex- cluding the exophil population). Adult shelters In Iran, a significant population of this spe- cies rests in human and animal dwellings in- cluding mud rooms, shed, stack, barns, straw, tents and mud stables, rick, animal sheds, poul- try nests. Some of the population of this spe- cies, especially in the West (Kermanshah) and the East (Kashafroud region) didn’t enter to hu- man habitations and has been collected from outdoors including cave, inside grain storage, cracks in the mountain rock, earth fissures in the walls of the rivers, the aqueducts, under the bridge and artificial pits (99, 132-133). Anopheles superpictus s.l. larvae were col- lected from villages including Hoomeye marka- zi, Roodan, Sandarak, Sirik, Dej Olia River, Dej Sofla River and Bashagard. This species that comprised 1.3% of the total percentage of collected larvae periodically was active dur- ing at least 6 months of the year. This Anoph- eles has been collected from temporary and http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2018, 12(3): 196–218 H Vatandoost et al.: Bioecology of … 204 http://jad.tums.ac.ir Published Online: September 30, 2018 stagnant waters, 62.5% and 100%, respective- ly. It has been collected with low percentages from permanent waters. This species could ovoposite in water nests that the water depth was low, with or without plant, sunny or semi- shade. The larvae of this species prefered lar- val habitat with soil or sandy in their bed along the rivers (to 80%), wetland, grasslands and fresh waters. It chose fresh and clear waters for ovoposition (50%). Anopheles superpictus s.l. larvae have been collected together An. stephensi, An. fluviatilis s.l., An. dtali, An. thurkhudi and An. multicolor in the same lar- val habitat. In some west and south west prov- inces of Iran, An. superpictus s.l. larvae has appeared from temporary and stagnant wa- ters with the frequency of 40% and with low density from permanent waters with or with- out plants. The larvae of this species in Kur- distan began their activity in mid-June and ends in mid-October. The peak activity is from early August to mid-September, and its ac- tivity dependent on temperature. The larvae of this species have been col- lected from the cities of Islamabad-E-Gharb, Paveh, Qasr-e Shirin, Harsin (Bakhtaran) in 1984–1985. In Bakhtaran the maximum abun- dance of larvae were found in July and its ac- tivity were reported from June to November. In Ilam the activity of 3rd and 4th larvae be- gan from June to September, with most ac- tivity and abundances in July. In Khuzistan Province, activities of 3rd and 4th instars lar- vae were from May to October and with its peak of activity in July and August. In Ger- mi and Pars Abad, the larval habitats includ- ed along the Dare Roud River, rice fields, small cavities and holes in the river beds (113). In Bazaft, Farsan, Chahar Mahal Bakhtiyari, of the 6 villages and 4 tribal regions, An. su- perpictus s.l. comprised 44.2% of the Anoph- eles populations in human dwellings. In animal places An. superpictus s.l. comprised 63.7%, of the Anopheles populations and in outdoors it was 77%. Totally, this species has been col- lected from outdoors. In Hussain Abad village, 243 mosquitoes were collected by night-bit- ing method that 165 of them (67.9%) were An. superpictus s.l. In this village in Farsan, of the 254 Anopheles mosquitoes collected in pit shelters, 180 (70.8%) of them were An. superpictus s.l.. Frequency of An. superpic- tus s.l. were 162 (66%) larvae collected from the tribal wattle, 130 (100%) from Shermak, 168 (66.7%) from tribal regions of Labad and in tribal regions of Tashnavi it was 181 (63%) (116). Studies conducted from May till Novem- ber, between 1997 and 1998 by total catch method in three indoors (human, animal, barn) and one outdoor (cave) in the province of Lorestan showed that of 1661 collected Culicidae mosquitoes, the 1632 (98.25%) were Anopheles genus, and among them the total number of 1630 (99.3%) of the collect- ed Anopheles were An. superpictus s.l. 631 (50.8%) collected female An. superpictus s.l. were freshly feeders (119). Malaria transmission potential In some parts of Iran, especially Kashaf roud in Khorasan and Kermanshah it was discovered that despite eradication programs, malaria transmission by this species has not stopped (Mesghali unpublished observation, 1968). Vectorial capacity is a measure of epi- demiology in different geographical regions that is used to determine the malaria transmis- sion risk. Vectorial capacity is affected by three factors including anthropophily, longevity, and mosquito vector population density. In Iran, sporozoite rate has been reported 0.9%. Des- iccation of salivary glands of An. superpictus s.l. in Khorasan, Kermanshah, Kazeroon and Masjed-E-Soleiman showed that almost 1.2% of the desiccated specimens were infected to sporozoite. In Tabas 4.6% of the specimens and in Kazeroon 0.65% of the specimens were infected with sporozoite and 0.7% of them were infected to oocyte. These studies indi- cated that An. superpictus s.l. was of the ma- jor malaria vectors in the central plateau and http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2018, 12(3): 196–218 H Vatandoost et al.: Bioecology of … 205 http://jad.tums.ac.ir Published Online: September 30, 2018 the southern slopes of the Zagros Mountains of Iran (128). Anopheles superpictus s.l. has been iden- tified as a main malaria vector in all regions of central Iranian plateau. In addition, this spe- cies had significant role in maintaining ma- laria as a second or third vector in mountain- ous and foothills of southern Zagros range. In 255 desiccated specimens in Birjand in 1961, the sporozoite index was 4.7% (accidental sam- pling). Desiccation of 411 An. superpictus in the mountainous region of Shapoor (Kazeroon) in 1960, infective index was 0.65%. In Bazaft, Farsan, dissection of 200 An. superpictus to de- termine the number of parous and nulliparous showed that the parous rate were 26%, 46% and 40% in late July, August and September, respectively. A total of 126 Anopheles sali- vary glands and stomach were dissected and none of them was found infective to sporo- zoite and oocyst (116). Larval habitats This species can be found in beds of riv- ers that are drying in hot climate of the sum- mer. This species have been collected from sandy margins of the river (Gamasab and Chamkhal rivers in Kermanshah Province). Captures of 2nd (early instars), 3rd–4th (late instars) instars and pupae have been done for An. superpictus s.l. immature abundances in different agro-ecosystems in Iran. Anopheles superpictus s.l. larvae are associated with gravel or fresh waters of swamplands and marshes, and pebble river and stream beds in shallow, slow-flowing clear water in full sunlight, small rivers or streamlet, holes, pits and natural dams, small pools within or next to river beds and streams, storage tanks, broken pitchers, emp- ty cans, water reservoirs, rice fields and as- sociated irrigation canals, natural grassland, large rivers that makes pools, animal hoof trac- es, tires, small pools within or next to river beds, are suitable as aquatic habitats. Preferred water temperature for ovopositing of this species in day time, usually reached to 35 °C to 38 °C. In 30 °C, the larval period lasted 11 days. However, at temperatures be- tween 19 °C to 20 °C, the larval period has been estimated at 24 days. Frequency of 3rd and 4th instars of An. superpictus s.l. in each ladle from April till November 1994 in Lan- janat, Isfahan in late July, mid-August and late August were 0.1, 0.1 and 0.1, respectively and in the remaining months was zero (122). Ecological characteristics of larval habi- tats of An. superpictus s.l. in 24 larval habi- tats in Lorestan Province showed richness of species composition that is indication of the importance of land use patterns on diversity of larval habitat types that included An. su- perpictus s.l., An. turkhudi, An. stephensi, An. dthali, An. sacharovi, An. claviger and An. martri. Anopheles superpictus s.l. larvae were collected from standing or temporary and es- pecially from still waters. This species was ac- tive in the waters with aquatic vegetation on their surface or outside of them. More than 45% of the specimens were collected from hab- itats without any aquatic vegetation. In 87.5% cases this species oviposit in the sandy and soil beds habitats with fully sunlight. This species prefers clear and fresh waters. Their larval hab- itats were close to rivers (53.2%), lakes, grass- lands, holes, streams, and river beds (46.8%). In man-made larval habitats, 87.5% larval hab- itats were found in rice fields and 12.5% were in cement grooves. Larval peaks of activity have been reported from mid-July till second half of the October. 67.8% of the larval habi- tats were standing and 32.2% of them were temporary. 62.6% of the larval habitats were still waters and rests of them were running waters. In this survey from the 115 larval hab- itats, 88.7% of the specimens were collected from sunny habitats. This species preferred to oviposit in sandy bed larval habitats (55.7%), mud (40.8%) and cement canals (3.5%). These species were mainly found in hab- itats without vegetation (46.9%), vegetation outside of the water (36.5%) and the rests of them in vegetation on the surface or under the http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2018, 12(3): 196–218 H Vatandoost et al.: Bioecology of … 206 http://jad.tums.ac.ir Published Online: September 30, 2018 water. In Lorestan Province, larval habitats were found in agro-villages s.l.es of Pishkouh Zalghi (villages of Baghe lotfian, Kizan Darreh, Kakolestan), Farsash (villages of Farsash, Homa and Ivaj), Barbaroude Shargi (villages of Cham- an Soltan (Shahrake Emam), Ab Barik, Dehnou Khaje), Pache Lake Shargi (villages of Dehe nasir, Sour, Choghatar), Mahrou (villages of Margsar and Chal Ghale). In Bazaft, Farsan, Chahar Mahal Bakhtiari in 1999, in the tribal region, activity of dif- ferent species of Anopheles in ten studied vil- lages were investigated 120 times. A total num- ber of 2543 larvae were collected from dif- ferent larval habitats including river margins, stagnant water, grasslands and springs. In tribal regions a total number of 162 larvae were col- lected that 66.6% of them were An. superpic- tus s.l.. In Labeh of the 168 collected larvae, the frequency of An. superpictus s.l. was 66.7%. In Shermak area of the 130 collected larvae 100% of them were An. superpictus s.l.. In Teshnavy that is a tribal area of the 181 col- lected larvae in 12 times, 63% of them were An. superpictus s.l.. Anopheles superpictus s.l. larvae with the abundance of 33.7% in 10 ladles had the highest density. Adult susceptibility tests The insecticide susceptibility tests on field adults and larvae were performed in 1972–1975 on the An. superpictus s.l. collected from dif- ferent parts of the country including moun- tainous, temperate and desert areas including Isfahan, Kermanshah, Khorasan, Kurdistan, and Ilam provinces. For the adult tests, female An. superpictus s.l. were exposed to discrim- inating doses of OC, OP and PY insecticides including D.D.T. (mortality rate: 99.4%), mal- athion (mortality rate: 100%), lambdacyhalo- thrin (mortality rate: 100%) and dieldrin for 60min. The effects of these pesticides were evaluated in accordance with WHO standards, using mortality rates after 1-hour exposure fol- lowed by monitoring over a 24-hour recovery period. The adult susceptibility tests using WHO criteria (98–100% mortality indicating susceptibility and < 98% mortality indicating resistance), showed that An. superpictus s.l. was susceptible to all the tested insecticides (107-109). In Ilam Province, in 2002, the per- centage of mosquitoes knocked down at 60 minutes were 100%, 99% and 98% for lamb- dacyhalothrin, malathion and DDT, respec- tively (111). Table 1 and Figure 3 show the resistant of species to DDT and susceptible to other insecticides in the country. Fig. 1. Distribution of Anopheles superpictus s.l. in Iran Fig. 2. Morphology of larva of Anopheles superpictus s.l. http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2018, 12(3): 196–218 H Vatandoost et al.: Bioecology of … 207 http://jad.tums.ac.ir Published Online: September 30, 2018 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 Discussion Malaria remains an important parasitic dis- ease in different parts of Iran, despite decades of organized malaria control activities. Malaria is particularly prevalent in tropical provinces including Sistan and Baluchistan. Iran remains highly conducive to vector borne diseases due to geography, and uncontrolled population movement. The Anopheles (Cellia) superpic- tus s.l. is important malaria vectors that have been found in different provinces of Iran. Anopheles superpictus s.l. represent important vectors of malaria throughout the Palearctic Region, including Iran. This s.l. complex contains at least three closely-related sibling species that can be differentiated based on distinctive genetic characters. Current evi- dence shows that climate variability has a direct effect on the epidemiology of vector- borne diseases including malaria). The most influence of climate change on disease trans- mission is likely to be monitored at the ex- tremes of the range of temperatures at which transmission develops. Malaria is of the most dangerous vector-borne diseases in the tropi- cal and subtropical areas. Health risks because of climatic variability will be different among countries that have developed health bases and those that do not (134). Patterns of human settlement in the various areas will affect dis- ease tendency s.l. complex. It has evidenced important anthropogenic ecosystem changes and it contains a great frequency and diversi- ty of mosquito-breeding sites and as a result hosts large mosquito populations, and in areas of endemic malaria. Results indicate that, en- vironmental modifications and changes in the economic, social, and cultural environ- ments can have tough and rapid influences on mosquito populations, climate variability, and drug resistance. These factors influence on http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2018, 12(3): 196–218 H Vatandoost et al.: Bioecology of … 208 http://jad.tums.ac.ir Published Online: September 30, 2018 biting, survival, and reproductive rates of vec- tors (135-143). We recommend new research on different aspects of An. superpictus in the future for decision making. Conclusion Understanding of all bioecology of ma- laria vector will guide the scientist and deci- sion makers for appropriate diseases control. Acknowledgment This research is financially supported by the Ministry of Health and Medical Educa- tion National Institute for Medical Research Development (NIMAD) under code number of 963262. All authors declare that there is no conflict of interest References 1. WHO (2017) World malaria report 2016. WHO Press, Geneva, Switzerland. 2. Vatandoost H, Shahi H, Abai MR, Hanafi- Bojd AA, Oshaghi MA, Zamani G (2004) Larval habitats of main malaria vectors in Hormozgan Province and their sus- ceptibility to different larvicides. South- east Asian J Trop Med Public Health. 35(2): 22–25. 3. Vatandoost H, Mashayekhi M, Abaie MR, Aflatoonian MR, Hanafi-Bojd AA, Shar- ifi I (2005) Monitoring of insecticides resistance in main malaria vectors in a malarious area of Kahnooj district, Ker- man Province, southeastern Iran. 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