J Arthropod-Borne Dis, March 2018, 12(1): 1–15 Z Saeidi and H Vatandoost: Aquatic Insect …

Review Article Aquatic Insect from for Possible Use of Biological Control of Main Vector-Borne Disease of Malaria and Water Indicator of Contamination

Zahra Saeidi 1, *Hassan Vatandoost 1, 2

1Department of Medical Entomology and Vector Control, School of Public Health, University of Medical Sciences, Tehran, Iran 2Department of Environmental Chemical Pollutants and Pesticides, Institute for Environmental Research, Tehran University of Medical Sciences, Tehran, Iran

(Received 16 Oct 2017; accepted 12 Mar 2018)

Abstract Iran has a wide variety of zoogeographical regions and different seasons. Here are some important mosquito-borne diseases. Mosquitoes normally live in waters. Its aquatic insect fauna is highly unexplored. To being resolved this faunal gap, a variety of literature records from previous century in different parts of Iran was reviewed. In some southern and southeastern foci in Iran, Malaria is still a main endemic disease which is unstable with two seasonal spring and autumn peaks even though Iran is lunching Malaria elimination. This review article showed the wide vari- ety of aquatic insects throughout the country. Researchers can discuss water pollutant and its quality by using aquatic insect fauna as well as biological control for vectors. Types of aquatic insects and macroinvertebrates sampling can be useful for water quality monitoring as indicators. Looking at aquatic insects’ life in water could be one of the most cost-effective and the easiest method to assess the water contaminations by different pollutants and will provide a guideline for scientific communities and environmental agencies for decision making.

Keywords: aquatic insects, Arthropod-borne diseases, Iran, water quality

Introduction

There are some important arthropod-borne as one of the most important parasitic infec- diseases in Iran including Malaria, Cutaneous tious diseases. Locally transmitted cases have leishmaniasis, Visceral leishmaniasis, Crimean- dropped to 500 recorded cases in 2013. Three Congo hemorrhagic fever, tick relapsing fever, most prevalence provinces in Iran are Sistan- Furthermore scorpions are one of the risk fac- Baluchestan, Hormozgan and Kerman which tors for life in some parts, while other arthro- located in south and southeastern part of the pod-related diseases such as myiasis exist more country. The rifest route of transmission is im- or less across the country. Some probable Ar- migration from Afghanistan and Pakistan to thropod-borne disease in the future may be: this area (Ministry of Health, annual report). Q-fever, Papatasi fever, Tularemia, Rift val- You can find a considerable decline of ma- ley fever, Dengue fever, Yellow fever, West laria burden in Iran during last 20 years. The Nile viruses, Lactodictism (spider bite), Plague, disease cases have been reduced from about scabies, Nuisance insects of horseflies and Cu- 100000 cases in 1991 to 246 autochthonous licidae mosquitoes, Cockroach-borne diseases, cases in 2014. Most of the transmitted cases damages by fire ants, blister beetles and bee are reported from the south-eastern part of the stings. country that is related to population traffic In Iran with about 15000 annual cases of across Pakistan border beyond the difficulties the disease in recent years, malaria is known in malaria control. Recent malaria number

*Corresponding author: Dr Hassan Vatandoost, E- mail: [email protected], [email protected] 1 http://jad.tums.ac.ir Published Online: March 18, 2018

J Arthropod-Borne Dis, March 2018, 12(1): 1–15 Z Saeidi and H Vatandoost: Aquatic Insect …

reported is 42 cases all over the country in- Gueorguiev recorded Methles rectus from Iran, cluding 23 local malaria patients, 12 imported but he did not publish the exact location (88). cases and seven relapsed ones before August Afterwards, in 1976 some researcher from an- 2016. Majority of researchers have worked on other field such as environment researchers who various aspects of malaria such as insecticide surveyed on mayfly and stonefly to determine resistance monitoring (1-10) new records, sib- the acute metal toxicity of some heavy metals ling species and molecular studies (11-18). such as lead, copper, zinc, and silver. They were Some researchers have worked on vector con- found more tolerant than most fish to heavy trol using novel methods (19-24), faunestic metals. This study indicated that aquatic insect study (25-26), Larval control using various can help us as effective biological monitors of plants (3, 27-38), using bed nets and long last- heavy metals pollution (91). Subsequently a sur- ing impregnated nets (39-46), Study on mor- vey was conducted on water beetles of South- phology (47-49), Malaria epidemiology (50- western Iran and reported Haliplidae (two gen- 54) Malaria vector ecology (18, 39, 52, 55-60), era, two species), Dytiscidae (16 genera, 24 spe- Biodiversity (53, 61), Community participation cies), and Gyrinidae (two genera, two species). (62), Vector control (63), Repellent evaluation Hydrophilidae (10 genera, 34 mostly uniden- (31, 64), susceptibility against insecticide (65- tified species) (92). A researcher from a uni- 67), Anthropophilic index of malaria vectors versity of Shiraz focused on life history, mor- (68-69) Training (70) is nominated as malaria phology and behaviour of the immature stag- training center by WHO researchers also can es of a coleopteran, Hydrophilidae in laborato- find several reports on different aspects of ma- ry condition (93). After about 20 years of water laria vectors done in recent years (21, 71-87). beetle collecting from a wide range of area, Although Iran has a vast geographical area habitat and provinces in Iran founded a small with a wide range of diversity in climate and number of M. rectus sharp in a few places in animal including insects, its aquatic insect’s Guilan Province in a collection made in 1976, fauna remains largely unexplored for years. 1993 and 1995 in Southern part of Caspian With a total area about 1.65 million Km2, Sea, northern Iran (94). around 7% covered with water- Iran is one of the large countries ranked eighteenth in the Current century world (88-89). The aquatic insect has a crit- During 2000–2002 a study on aquatic bee- ical role in biomonitoring of water safety or tle of Tabriz region, East Azarbaijan, North- water contamination. It is inevitable to use western Iran was conducted and four species such kind of insect to evaluate water quality out of five species of the family Hydraenidae as a biological indicator and can help us as reported a new record (95). During 2001–2005 water resource management. Aquatic insects some specimen collected by Vafaei et al. (96) a vital role in energy flow in fresh water and in Markazi Province central Iran and they es- they are important in food web between aquatic tablished the presence of 24 species of aquat- animals. ic beetles (Coleoptera: Polyphaga) belonging to 13 genera and five families. In other pub- lication, they claim that they found 33 species Historical overview of Aquatic Insects of diving beetles belonging to 18 genera dur- from Iran ing same time and same places (97). In 2005 another team worked on a descriptive study of Past century aquatic insects’ fauna in Kashan, central Iran. Iran aquatic insects have been studied since During nine rounds of sampling from four mat- 1965 by a hand full of researchers. Vassil uration artificial ponds they reported as fol-

2 http://jad.tums.ac.ir Published Online: March 18, 2018

J Arthropod-Borne Dis, March 2018, 12(1): 1–15 Z Saeidi and H Vatandoost: Aquatic Insect …

lowed: Diptera order (52%), including Chi- the species Nabis pseudoferus, Notonecta vi- ronomidae and Culicidae families, Hemiptera ridis, Anthocoris nemorum, Velia affinis, Hy- (24%) Corixidae, Notonectidae, Copepodae and drometra stagnorum and Gerris maculates were Copepodidae families, Ciclopodidae (12%), predators. The most abundant species belong- Hydroacarina (9.5%), Coleptera (0.77%), Ara- ing to Pentatomidae. They reported 32 species nida (0.67%), Hymenoptera (0.58%), Odona- as new records for the studied area. Newly in- ta (0.48%) (98). In another publication, 31 dif- troduced species, Stinctopleurus crassicornis ferent Plecoptera reported from different fam- and Stinctopleurus punctatonervosus, registered ilies and two families of Ephemeroptera (99). for Iran insect fauna (104). During 2006 and 2007 39 species have In another study that carried out in East been found belonging to 16 families in Zan- Azarbaijan Province on Heteroptera, they found janrud, Zanjan Province. Three specimens be- 28 species from 12 families and Polymerus long to Lygaeidae, Scutelleridae and Reduvi- brevirostris Knight, 1925 was a new record idae were identified at the genus level. Among (105). In Ardabil East Azarbaijan Province them, there are some predators’ species such Northwestern Iran. Two species of aquatic as Anthocoris nemorum, Nabis pseudoferus, beetles belonging to two genera that did not Notonecta viridis, Velia affinis, Gerris macu- study before from two sampling site during lates, Hydrometra stagnorum. The most fre- 2000–2008. They faced Peltodytes Regimbart, quent Species belonged to Pentatomidae. All 1878 and Haliplus Latreille, 1802 (106). A species were first records from the Zanjan species Haliplus heydeni Wehncke, 1875 was Province (100). a new record of Iran. In another teamwork in Some families of Coleoptera such as Dy- Neka County, the Mazandaran Province, North- tiscidae, Gyrinidae, Helophoridae and Hydro- ern Iran five species of four genera were found philidae with a new record and notes on the in tree holes during 2009. They reported Anoph- rare species Coleostoma transcaspicum Reit- eles plumbeus, Culisetaannulata, Culex pipiens, ter, 1906 from North part of and Ochlerotatus geniculatus by larval col- was reported (101). Work on Odonata as ef- lection, Ochlerotatus pulcritarsisby adult col- fective predators in the rice field and other lection and Oc.geniculatus, 55.87%, Ochlero- sites in Mazandaran Province North of Iran tatus echinus 1.33%, Oc. pulcritarsis 8.8%, (2003–2006). They found 30 species from 19 Cx. pipiens 33.8%, and An. plumbeus 0.2% genera and eight families of Odonata (Anisop- of bait net collection. They found some Cs. tera and Zygoptera suborder. In Anisoptera sub- Annulata larvae in low abundance in cavities order, Aeshnidae, five species, one species of of trees for the first time (61). During 2008– Corduliidae, two species of Gomphidae, 13 2009 İncekara et al. (107) collected 42 species species of Libellulidae. In Zygoptera suborder, of aquatic beetle (Coleoptera: Hydrophiloidea) one species of Calopterygidae, six species of belonging to 13 genera and three families (Hel- Coenagrionidae, one species of Euphaeidae, ophoridae, Hydrochidae and Hydrophilidae) one species of Platycnemididae (102). A sur- in Tehran, Mazandaran, Guilan, Qazvin, and vey in Zayande Rud River in Esfahan Prov- Sanandaj in Kordestan Provinces in Iran. They ince, central Iran during one year and in eight reported 11 new species from Iran in this sur-

stations who found that the water quality can vey. During 2009–2011 on the work on the have an effective impact on diversity and rich- aquatic insect of River, Ahvaz, Khu- ness of benthic macroinvertebrate (103) rec- zestan Province, Southwestern Iran revealed orded total of 47 species belonging to17 Fam- Damselflies and Dragonflies nymphs of Odona- ilies of Heteroptera in Ghara Dagh forest, East ta order, five genera from four families and all Azarbayjan, Northwestern Iran: Among them, of them were the new records from this area.

3 http://jad.tums.ac.ir Published Online: March 18, 2018

J Arthropod-Borne Dis, March 2018, 12(1): 1–15 Z Saeidi and H Vatandoost: Aquatic Insect …

Recent years

These days we are able to find some more Anopheles larvae from Indian Remote Sens- articles about Iran aquatic insects that worked in ing Satellite (IRS) image and digital elevation a wide range of natural areas (Fig. 1). It seems model of the area using GIS by monthly sam- more researchers know the importance of aquat- pling from Surface water bodies during 2009– ic insects as biological control and water in- 10 for anopheline larvae carried out. The lowest dicator and they are interested in investigat- and highest frequencies were in February and ing on them. In 2011 Salavatian et al. who April, respectively. Anopheles culicifacies was worked on feeding behavior of Brown trout, Dominant species (53). In a study conducted in Salmo trutta fario, published a paper that shows Gahar Lake, Lorestan Province in three differ- us this fish fed on 32 animal groups including ent seasons they found most and least variety some insects such as Chironomidae (88.6%), and abundance in spring and autumn respec- Simulidae (60%), Baetidae (51.4%) and Tip- tively. Maximum density belonged to Simu- ulidae (50%) that they were most frequent food lidae and Chironomidae (113). in its gut. They showed that the proportion of Ghahari collected, identified and published consumed food by Brown trout was Diptera about 19 species from nine genera (Micronecta, 91.5% (Chironomidae pupa and larvae 85.8%), Corixa, Sigara, Aquarius, Gerris, Hydrometra, Coleoptera 6.4% and others 2.1% (109). Other Anisops, Chartoscirta, Saldula) of aquatic and team surveyed aquatic insects’ fauna of Karun semiaquatic Heteroptera from the families Co- River, Ahvaz City, Khuzestan Province, South- rixidae, Gerridae, Hydrometridae, Notonecti- west of Iran. They reported 57 species belong- dae, Saldidae from southern areas of Caspian ing to seven orders and 22 families, Collem- Sea, Northern Iran (114). From 16 different bola (1 species), Ephemeroptera (4 species), sites in Iran, 23 nominal species are now iden- Odonata (6 species), Hemiptera (9 species), Col- tified, including some new records for Simu- eoptera (34 species), Diptera (2 species) and lium crassicaulum (Rubtsov) and Simulium ala- Trichoptera (1 species). The most abundant spe- jense Rubtsov, and the southernmost world cies in this study was the beetle Hydroglyphus record for Simulium transcaspicum Enderlein signatellus Klug, 1834 (Coleoptera: Dytiscidae) in Iran. Multiple cytoforms of the Simulium (110). An Ecological Risk Assessment (ERA) aureum group, Simulium bezzii complex, and for Shadegan wetland, Khuzestan Province, Simulium ornatum group were found (115). Southwest of Iran to assess the risk to zoo- Shaverdo et al. reported 21 species of div- plankton, phytoplankton, invertebrate, insect ing beetles Dytiscidae from Ahvaz, Khuzestan larvae, and fish affected by Five pesticides, Province, southwest Iran. Cybister lateralim DDT, Aldrin, Dieldrin, Lindane and Ametryn. arginalisponticus, 1882, Hydroporus inscitus Insect larvae (Chironomus sp) like other crea- 1882, and Laccophilus sordidus 1882 are ture are highly at risk of harmful pesticide were reported from Iran for the first time (116). conducted (111). Study on Tajan river macroin- Shayeghi et al. reported a variety of aquatic vertebrate communities’ distribution in Ma- orders, two families of Hemiptera (Gerridae zandaran Province, Northern Iran and south and Notonectidae) Odonata (Coenagrionidae), part of . They realized that the dis- Coleoptera (Carabidae), and pro stigmata from solved oxygen, turbidity, water temperature, the family of Hydrachindae in Zayanderood, pH and TSS were the most critical physico- Esfahan Province, Central Iran during 2011 chemical factors to affect the distribution of (117). In another study in the same area and them (112). the same year, they collected 741 specimens Work on the potential aquatic habitats for of aquatic insects including seven families

4 http://jad.tums.ac.ir Published Online: March 18, 2018

J Arthropod-Borne Dis, March 2018, 12(1): 1–15 Z Saeidi and H Vatandoost: Aquatic Insect …

and 12 genera of two orders. The order of vealed 5270 specimens belonging to four gen- Diptera (92.31%) including Culicidae, Syr- era and 14 species in Northern Iran. They re- phidae and Chironomidae and Coleoptera ported one dominant species, two dominant (7.69%) including Gyrinidae, Dytiscidae, Hal- species, two subdominant species, two rare spe- iplidae, Hydrophilidae families (76). cies and eight sub rare species by using Hey- Maleki-Ravasan et al. (118) conducted a demann classification (123). Southwest of Iran, bi-seasonal study in Lavasan River, North- Bashagard district is one of the most important eastern Tehran, the most abundant species be- areas because of Malaria transmission collect- tween 14 families and 62 Trichoptera species ed research conducted revealed totally 5150 belonged to the Hydropsychidae. They reported larvae from 36 different larval habitats. They the presence of Annulipalpian Hydropsyche recorded six species: An. culicifacies (29.36%), sciligra H Malicky, 1977 in that district. Habitat An. moghulensis (25.20%), An. dthali (18.02%), water quality of this species reported resem- An. superpictus (17.24%), An.turkhudi (5.17%) ble human drinking water and presence of Phy- and An. stephensi (5.01%). They investigated sa acuta (snail) and Capoeta buhsei (fish) in the water quality and they stated abundant Anophe- sampling area indicated inferior quality. Daril- lin larvae existed in permanent and full sun- maz et al. listed 27 species and subspecies of light habitat with no vegetation and algae. 17 genera of the families Dytiscidae, Halipli- Larval density had the correlation with water dae, Noteridae and Gyrinidae (Coleoptera: temperature. Some factors also had the spe- Adephaga) from , Gilan, Mazandaran, cific impact on larval abundance and distri- Qazvin, and Tehran Provinces northern Iran bution such as conductivity, total alkalinity, (119). A total of 9 families in Shapoor River chloride and sulphate. Knowing of this data in Bushehr region during 2012 (120). and correlation between them can be consid- Researchers evaluated aquatic insects’ fau- ered for sufficient planning and implement- na in Golestan Province, North of Iran in dif- ing Malaria elimination program (124). In Ba- ferent sites during 2011–2012. They published shagard area epidemiological and entomolog- different stages of Diptera 64.54% (Culicidae, ical aspects to determine malaria situation, spe- Chironomidae, Tabanidae, Simulidae, Sci- cies composition of anopheline mosquitoes and omyzidae families), Heteroptera 11.03%, susceptibility status of main vectors to insec- Ephemeroptera 9.53% (Heptagenidae, Bae- ticides/ larvicides during 2002–2010 were con- tidae), Trichoptera 7.07% (Limnephilidae), ducted. They have reported An. culicifacies, An. Odonata 4.82% (Aeshnidae, Gomphidae, Li- dthali, An. stephensi, An. superpictus, An. flu- bellulidae) and Coleoptera 2.99% (Dytiscidae, viatilis, An. moghulensis, An. turkhudi and An. Gyrinidae) in this study. They reported some apoci with two peak in April and October. water surface insects such as Gerridae, Co- They have found resistance against DDT in rixidae, Hydrometridae, Nepidae families (121). An. stephensi and tolerance against Deltame- A study in River, North of Iran. 211 thrin and Bendiocarb.Their larvae found sus- samples of three orders; Plecoptera, Trichop- ceptible against all larvicides except for An. tera and Ephemeroptera and seven genera (Per- stephensi with tolerance against Fenthion (125). la, Isoperla, Hydropsyche, Cheumatopsyche, In summer 2014 Shayeghi et al. carried out a Baetis, Heptagenia and Maccafferium) from study in Sabalan mountainous river, in differ- five families (Perlidae, Perlodidae, Hydropsy- ent sites around Meshginshahr, Ardabil Prov- chidae, Batidae, Heptagenidae) were found. Or- ince, Northwestern Iran. They reported six or- der of Plecoptera was the most predominant ders (Coleoptera, Ephemeroptera, Hemiptera, order then Trichoptera (122). Investigated bio- Diptera, Plecoptera and Trichoptera) includ- diversity of culicid mosquitoes from Keka re- ing 12 families (Helmidae, Leptophlebiidae,

5 http://jad.tums.ac.ir Published Online: March 18, 2018

J Arthropod-Borne Dis, March 2018, 12(1): 1–15 Z Saeidi and H Vatandoost: Aquatic Insect …

Ecdyonuridae, Corixidae, Culicidae, Simuli- dant families were Culicidae (61.55%) and a idae, Perlidae, Leptoceridae, Hydropsychidae, few number of Plecoptera: Perlodidae (0.5%) Chironomidae, Caenidae and Baetidae) among (126). 262 specimens. They wrote that most abun-

Fig. 3. Map of Iran showing some main rivers and natural events

Conclusion Monitoring of insecticide resistance in Anopheles sacharovi (Favre, 1903) This review article will provide a clue for in borderline of Iran, Armenia, Naxci- management of vector control as well as in- van and Turkey, 2001. Iran J Public dicators for water classification. Health. 31(3–4): 96–99. 2. Enayati AA, Vatandoost H, Ladonni H, Townson H, Hemingway J (2003) Mo- Acknowledgements lecular evidence for a kdr-like pyre- throid resistance mechanism in the ma- The authors like to appreciate very much laria vector mosquito Anopheles ste- for kind collaboration of all staff of Depart- phensi. Med Vet Entomol. 17(2): 138– ment of Medical Entomology and Vector Con- 144. trol as well as Institute for Environmental Re- 3. Vatandoost H, Vaziri VM (2004a) Larvi- search, Tehran University of Medical Scienc- cidal activity of a neem tree extract es, Iran. (Neemarin) against mosquito larvae in the Islamic Republic of Iran. East References Mediterr Health J. 10(4–5): 573–581. 4. Vatandoost H, Mashayekhi M, Abaie MR, 1. Salari Lak S, Vatandoost H, Entezarmahdi Aflatoonian MR, Hanafi-Bojd AA, M, Ashraf H, Abai M, Nazari M (2002) Sharifi I (2005) Monitoring of insec-

6 http://jad.tums.ac.ir Published Online: March 18, 2018

J Arthropod-Borne Dis, March 2018, 12(1): 1–15 Z Saeidi and H Vatandoost: Aquatic Insect …

ticides resistance in main malaria vec- reaction assay for identification of sib- tors in a malarious area of Kahnooj ling species of Anopheles fluviatilis in District, Kerman Province, southeast- Iran. Southeast Asian J Trop Med Pub- ern Iran. J Vector Borne Dis. 42(3): lic Health. 34 Suppl 2: 56–60. 100–108. 12. Naddaf SR, Oshaghi MA, Vatandoost H, 5. Hanafi-Bojd AA, Vatandoost H, Jafari R Assmar M (2003) Molecular charac- (2006) Susceptibility status of Anoph- terization of Anopheles fluviatilis spe- eles dthali and Anopheles fluviatilis to cies complex in the Islamic Republic commonly used larvicides in an en- of Iran. East Mediterr Health J. 9(3): demic focus of malaria, southern Iran. 257–265. J Vector Borne Dis. 43(1): 34–38. 13. Naddaf SR, Oshaghi MA, Vatandoost H 6. Davari B, Vatandoost H, Ladonni H, Shaeghi (2012) Confirmation of Two Sibling M, Oshaghi M, Basseri H (2006) Com- Species among Anopheles fluviatilis parative Efficacy of Different Imagi- Mosquitoes in South and Southeastern cides Against Different Strains of Iran by Analysis of Cytochrome Oxi- Anopheles stephensi in the Malarious dase I Gene. J Arthropod borne Dis. 6 Areas of Iran, 2004–2005. Pak J Biol (2): 144–150. Sci. 9(5): 885–892. 14. Oshaghi MA, Sedaghat MM, Vatandoost 7. Davari B, Vatandoost H, Oshaghi M, La- H (2003 b) Molecular characterization donni H, Enayati A, Shaeghi M (2007) of the Anopheles maculipennis com- Selection of Anopheles stephensi with plex in the Islamic Republic of Iran. DDT and dieldrin and cross-resistance East Mediterr Health J. 9(4): 659–666. spectrum to pyrethroids and fipronil. 15. Oshaghi MA, Shemshad K, Yaghobi-Er- Pestic Biochem Physiol. 89(2): 97–103. shadi MR, Pedram M, Vatandoost H, 8. Abai MR, Mehravaran A, Vatandoost H, Abaie MR (2007) Genetic structure of Oshaghi MA, Javadian E, Mashayekhi the malaria vector Anopheles super- M (2008) Comparative performance of pictus in Iran using mitochondrial cy-

imagicides on Anopheles stephensi, tochrome oxidase (COI and COII) and main malaria vector in a malarious area, morphologic markers: a new species southern Iran. J Vector Borne Dis. 45 complex. Acta Trop. 101(3): 241–248. (4): 307–312. 16. Sedaghat MM, Linton YM, Oshaghi MA, 9. Vatandoost H, Hanafi-Bojd AA (2012) In- Vatandoost H, Harbach RE (2003) The dication of pyrethroid resistance in the Anopheles maculipennis complex (Dip- main malaria vector, Anopheles ste- tera: Culicidae) in Iran: molecular char- phensi from Iran. Asian Pac J Trop acterization and recognition of a new Med. 5(9): 722–726. species. Bull Entomol Res. 93(6): 527– 10. Soltani A, Vatandoost H, Oshaghi MA, 535. Enayati AA, Raeisi A, Eshraghian MR 17. Azari-Hamidian S, Abai MR, Ladonni H, (2013) Baseline Susceptibility of Dif- Vatandoost H, Akbarzadeh K (2006) ferent Geographical Strains of Anoph- Anopheles peditaeniatus (Leicester) new eles stephensi (Diptera: Culicidae) to to the Iranian mosquito fauna with notes Temephos in Malarious Areas of Iran. on Anopheles hyrcanus group in Iran. J Arthropod Borne Dis. 7(1): 56–65. J Am Mosq Control Assoc. 22(1): 144– 11. Dezfouli SR, Oshaghi MA, Vatandoost H, 146. Assmar M (2003) rDNA-ITS2 based 18. Mehravaran A, Oshaghi MA, Vatandoost species-diagnostic polymerase chain H, Abai MR, Ebrahimzadeh A, Roodi

7 http://jad.tums.ac.ir Published Online: March 18, 2018

J Arthropod-Borne Dis, March 2018, 12(1): 1–15 Z Saeidi and H Vatandoost: Aquatic Insect …

AM (2011) First report on Anopheles 25. Moosa-Kazemi S, Vatandoost H, Nikookar fluviatilis U in southeastern Iran. Ac- H, Fathian M (2009) Culicinae (Dip- ta Trop. 117(2): 76–81. tera: culicidae) mosquitoes in Chaba- 19. Soltani A, Vatandoost H, Jabbari H, Mes- har County, Sistan and Baluchistan daghinia A, Mahvi A, Younesian M Province, Southeastern Iran. Iran J Ar- (2008) Use of expanded polystyrene thropod Borne Dis. 3(1): 29–35. (EPS) and shredded waste polystyrene 26. Oshaghi MA, Vatandoost H, Gorouhi A, (SWAP) beads for control of mosqui- Abai MR, Madjidpour A, Arshi S toes. J Arthropod Borne Dis. 2(2): 12– (2011) Anopheline species composi- 20. tion in borderline of Iran-Azerbaijan. 20. Soltani A, Vatandoost H, Jabbari H, Mes- Acta Trop. 119(1): 44–49. daghinia AR, Mahvi AH, Younesian M 27. Hadjiakhoondi A, Aghel N, Zamanizadeh- (2012) Field efficacy of expanded pol- Nadgar N, Vatandoost H (2000) Chem- ystyrene and shredded waste polysty- ical and biological study of Mentha spi- rene beads for mosquito control in ar- catal essential oil from Iran. DARU J tificial pools and field trials, Islamic Pharmaceutical Sci. 8(1–2): 19–21. Republic of Iran. East Mediterr Health 28. Hadjiakhoondi A, Vatandoost H, Jamshidi J. 18(10): 1042–1048. A, Amiri EB (2003) Chemical Con- 21. Omrani SM, Vatandoost H, Oshaghi MA, stituents of Efficacy of Cymbopogon Shokri F, Guerin PM, Yaghoobi Er- Olivieri (Boiss) Bar Essential Oil shadi MR (2010a) Fabrication of an ol- Against Malaria Vector, Anopheles factometer for mosquito behavioral stepensi. DARU J Pharmaceutical Sci. studies. J Vector Borne Dis. 47(1): 17– 11(3): 125–128. 25. 29. Hadjiakhoondi A, Vatandoost H, Khanavi 22. Omrani SM, Vatandoost H, Oshaghi M, M, Abai MR, Karami M (2005) Bio- Shokri F, Yaghoobi-Ershadi M, Rassi chemical investigation of different ex- Y (2010b) Differential Responses of tracts and larvicidal activity of Taget- Anopheles stephensi (Diptera: Cu- es minuta L. on Anopheles stephensi licidae) to Skin Emanations of a Man, larvae. Iran J Pharmaceutical Sci. 1(2): a Cow, and a Guinea Pig in the Olfac- 81–84. tometer. Iran J Arthropod Borne Dis. 30. Hadjiakhoondi A, Vatandoost H, Kha- 4(1): 1–16. navi M, Sadeghipour Roodsari HR, 23. Omrani SM, Vatandoost H, Oshaghi MA, Vosoughi M, Kazemi M (2006) Fat- Rahimi A (2012) Up wind responses ty acid composition and toxicity of of Anopheles stephensi to carbon di- Melia azedarach L. fruits against ma- oxide and L-lactic acid: an olfactom- laria vector Anopheles stephensi. Iran eter study. East Mediterr Health J. 18 J Pharmaceutical Sci. 2(2): 97–102. (11): 1134–1142. 31. Oshaghi M, Ghalandari R, Vatandoost H, 24. Chavshin AR, Oshaghi MA, Vatandoost Shayeghi M, Kamali-Nejad M, Toura- H, Pourmand MR, Raeisi A, Enayati bi-Khaledi H (2003a) Repellent effect AA (2012) Identification of bacterial of extracts and essential oils of Citrus microflora in the midgut of the larvae limon (Rutaceae) and Melissa offici- and adult of wild-caught Anopheles nalis (Labiatae) against main malaria stephensi: a step toward finding suit- vector, Anopheles stephensi (Diptera: able paratransgenesis candidates. Ac- Culicidae). Iran J Pub Health. 32(4): ta Trop. 121(2): 129–134. 47–52.

8 http://jad.tums.ac.ir Published Online: March 18, 2018

J Arthropod-Borne Dis, March 2018, 12(1): 1–15 Z Saeidi and H Vatandoost: Aquatic Insect …

32. Sadat Ebrahimi S, Hadjiakhoondi A, Re- stituents and larvicidal activity of Kelus- zazadeh S, Fereidunian N, Vatandoost sia odoratissima essential oil against H, Abaee M (2005) The components two mosquito vectors Anopheles ste- of Tagetes minuta L. and its biologi- phensi and Culex pipiens (Diptera: Cu- cal activities against malaria vector, licidae). Exp Parasitol. 132(4): 470–474. Anopheles stephensi in Iran. J Medic- 39. Vatandoost H, Oshaghi MA, Abaie MR, inal Plants. 4(16): 43–47. Shahi M, Yaaghoobi F, Baghaii M 33. Shahi M, Hanafi-Bojd AA, Iranshahi M, (2006a) Bionomics of Anopheles ste- Vatandoost H (2010) Larvicidal effi- phensi Liston in the malarious area of cacy of latex and extract of Calotropis Hormozgan Province, southern Iran, procera (Gentianales: Asclepiadaceae) 2002. Acta Trop. 97(2): 196–203. against Culex quinquefasciatus and 40. Vatandoost H, Ramin E, Rassi Y, Abai M Anopheles stephensi (Diptera: Cu- (2009) Stability and wash resistance of licidae). J Vector Borne Dis. 47(3): local made mosquito bednets and deter- 185–188. gents treated with pyrethroids against 34. Khanavi M, Toulabi PB, Abai MR, Sa- susceptible strain of malaria vector dati N, Hadjiakhoondi F, Hadjiakhoon- Anopheles stephensi. Iran J Arthropod di A (2011) Larvicidal activity of ma- Borne Dis. 3(1): 19–28. rine algae, Sargassum swartzii and 41. Vatandoost H, Mamivandpoor H, Abai MR, Chondria dasyphylla, against malaria Shayeghi M, Rafi F, Raeisi A (2013) vector Anopheles stephensi. J Vector Wash resistance and bioefficacy of al- Borne Dis. 48(4): 241–244. pha-cypermethrin long lasting impreg- 35. Khanavi M, Vatandoost H, Khosravi nated nets (LLIN-Interceptor (R) against Dehaghi N, Sanei Dehkordi A, Seda- Anopheles stephensi using Tunnel Test. ghat MM, Hadjiakhoondi A (2013) Lar- J Arthropod Borne Dis. 7(1): 31–45. vicidal activities of some Iranian na- 42. Moosa-Kazemi SH, Vatandoost H, Raeisi tive plants against the main malaria vec- A, Akbarzadeh K (2007) Deltamethrin tor, Anopheles stephensi. Acta Med Iran. impregnated bed nets in a malaria con- 51(3): 141–147. trol program in Chabahar, Southeast 36. Sedaghat M, Dehkordi AS, Abai M, Kha- Baluchistan, Iran. J ArthropodBorne navi M, Mohtarami F, Abadi YS (2011) Dis. 1(1): 43–51. Larvicidal activity of essential oils of 43. Rafinejad J, Vatandoost H, Nikpoor F, Abai Apiaceae plants against malaria vec- MR, Shaeghi M, Duchen S (2008) Ef- tor, Anopheles stephensi. Iran J Ar- fect of washing on the bioefficacy of thropod Borne Dis. 5(2): 51–59. insecticide-treated nets (ITNs) and long- 37. Sedaghat MM, Dehkordi AS, Khanavi M, lasting insecticidal nets (LLINs) against Abai, MR, Mohtarami F, Vatandoost main malaria vector Anopheles stephen- H (2011) Chemical composition and si by three bioassay methods. J Vec- larvicidal activity of essential oil of Cu- tor Borne Dis. 45(2): 143–150. pressus arizonica E.L. Greene against 44. Soleimani-Ahmadi M, Vatandoost H, malaria vector Anopheles stephensi Lis- Shaeghi M, Raeisi A, Abedi F, ton (Diptera: Culicidae). Pharmacog- Eshraghian MR (2012) Effects of ed- nosy Res. 3(2): 135–139. ucational intervention on long-lasting 38. Vatandoost H, Sanei Dehkordi A, Sadeghi insecticidal nets use in a malarious ar- SM, Davari B, Karimian F, Abai MR ea, southeast Iran. Acta Med Iran. 50 (2012) Identification of chemical con- (4): 279–287.

9 http://jad.tums.ac.ir Published Online: March 18, 2018

J Arthropod-Borne Dis, March 2018, 12(1): 1–15 Z Saeidi and H Vatandoost: Aquatic Insect …

45. Soleimani-Ahmadi M, Vatandoost H, 52. Hanafi-Bojd AA, Azari-Hamidian S, Vatan- Shaeghi M, Raeisi A, Abedi F, doost H, Charrahy Z (2011) Spatio- Eshraghian MR (2012) Field evalua- temporal distribution of malaria vectors tion of permethrin long-lasting insec- (Diptera: Culicidae) across different cli- ticide-treated nets (Olyset R) for ma- matic zones of Iran. Asian Pac J Trop laria control in an endemic area, south- Med. 4(6): 498–504. east of Iran. Acta Trop. 123(3): 146– 53. Hanafi-Bojd AA, Vatandoost H, Oshaghi 153. MA, Charrahy Z, Haghdoost AA, Sed- 46. Soleimani-Ahmadi M, Vatandoost H, Zare aghat MM (2012) Larval habitats and M (2014) Characterization of larval biodiversity of anopheline mosquitoes habitat for anopheline mosquitoes in (Diptera: Culicidae) in a malarious ar- a malarious area under elimination pro- ea of southern Iran. J Vector Borne Dis. gram in the Southeast of Iran. Asian 49(2): 91–100. Pac J Trop Biomed. 4(1): S73–S80. 54. Hemami MR, Sari AA, Raeisi A, Vatan- 47. Doosti S, Azari-Hamidian S, Vatandoost doost H, Majdzadeh R (2013) Malar- H, Hosseini MOM (2006) Taxonom- ia elimination in Iran, importance and ic differentiation of Anopheles sacha- challenges. Int J Prev Med. 4(1): 88–94. rovi and An. maculipennis Sl (Dip- 55. Vatandoost H, Dehakia M, Djavadian E, tera: Culicidae) larvae by seta 2 (an- Abai MR, Duchson S (2006) Compar- tepalmate hair). Acta Med Iran. 44(1): ative study on the efficacy of lambda- 21–27. cyhalothrin and bifenthrin on torn nets 48. Doosti S, Vatandoost H, Oshaghi M, Hos- against the malaria vector, Anopheles seini M, Sedaghat M (2007) Applying stephensi as assessed by tunnel test morphometric variation of seta 2 (An- method. J Vector Borne Dis. 43(3): tepalmate Hair) among the larvae of the 133–135. members of the Maculipennis Subgroup 56. Vatandoost H, Shahi M, Hanafi-Bojd AA, (Diptera: Culicidae) in Iran. J Arthro- Abai M, Oshaghi M, Rafii F (2007) pod Borne Dis. 1(1): 28–37. Ecology of Anopheles dthali Patton in 49. Emami SN, Vatandoost H, Oshaghi MA, Bandar Abbas District, Hormozgan Mohtarami F, Javadian E, Raeisi A Province, southern Iran. Iran J Ar- (2007) Morphological method for sex- thropod Borne Dis. 1(1): 21–27. ing anopheline larvae. J Vector Borne 57. Vatandoost H, Emami SN, Oshaghi MA, Dis. 44(4): 245–249. Abai MR, Raeisi A, Piazzak N (2011) 50. Vatandoost H, Ashraf H, Lak SH, Mahdi Ecology of malaria vector Anopheles RE, Abai MR, Nazari M (2003) Fac- culicifacies in a malarious area of Sis- tors involved in the re-emergence of tan va Baluchestan Province, south-east malaria in borderline of Iran, Armenia, Islamic Republic of Iran. East Medi- Azerbaijan and Turkey. The Southeast terr Health J. 17(5): 439–445. Asian J Trop Med Public Health. 34 58. Soleimani-Ahmadi M, Vatandoost H,

(Suppl 2): 6–14. Shaeghi M, Raeisi A, Abedi F, 51. Hanafi-Bojd AA, Vatandoost H, Philip E, Eshraghian MR (2012) Vector ecolo- Stepanova E, Abdi A, Safari R (2010) gy and susceptibility in a malaria-en- Malaria situation analysis and stratifi- demic focus in southern Islamic Re- cation in Bandar Abbas county, south- public of Iran. East Mediterr Health ern Iran, 2004–2008. Iran J Arthropod- J. 18(10): 1034–1041. Borne Dis. 4(1): 31–41. 59. Soleimani-Ahmadi M, Vatandoost H, Hanafi-

10 http://jad.tums.ac.ir Published Online: March 18, 2018

J Arthropod-Borne Dis, March 2018, 12(1): 1–15 Z Saeidi and H Vatandoost: Aquatic Insect …

Bojd AA, Zare M, Safari R, Mojahe- 66. Vatandoost H, Zahirnia AH (2010) Respon- di A (2013) Environmental character- siveness of Anopheles maculipennis to istics of anopheline mosquito larval different imagicides during resurgent habitats in a malaria endemic area in malaria. Asian Pac J Trop Med. 3(5): Iran. Asian Pac J Trop Med. 6(7): 510– 360–363. 515. 67. Abai MR, Hanafi-Bojd AA, Vatandoost H 60. Vatandoost H, Shahi H, Abai MR, Hanafi- (2016) Laboratory evaluation of Bojd AA, Oshaghi MA, Zamani G temephos against Anopheles stephen- (2004) Larval habitats of main malar- si and Culex pipiens Larvae in Iran. J ia vectors in Hormozgan Province and Arthropod Borne Dis. 10(4): 510–518. their susceptibility to different larvi- 68. Oshaghi MA, Chavshin AR, Vatandoost cides. Southeast Asian J Trop Med Pub- H (2006) Analysis of mosquito blood lic Health. 35(2): 22–25. meals using RFLP markers. Exp Par- 61. Nikookar S, Moosa-Kazemi SH, Oshaghi asitol. 114(4): 259–264. MA, Yaghoobi-Ershadi MR, Vatan- 69. Oshaghi MA, Chavshin AR, Vatandoost doost H, Kianinasab A (2010) Spe- H, Yaaghoobi F, Mohtarami F, Noor- cies composition and diversity of mos- jah N (2006) Effects of post-ingestion quitoes in Neka County, Mazandaran and physical conditions on PCR am- Province, Northern Iran. Iran J Arthro- plification of host blood meal DNA pod Borne Dis. 4(2): 26–34. in mosquitoes. Exp parasitol. 112(4): 62. Hanafi-Bojd AA, Vatandoost H, Oshaghi 232–236. MA, Eshraghian MR, Haghdoost AA, 70. Vatandoost H, Mesdaghinia AR, Zamani Abedi F (2011) Knowledge, attitudes G, Madjdzadeh R, Holakouie K, and practices regarding malaria control Sadrizadeh B (2004) Development of in an endemic area of southern Iran. the regional malaria training center in Southeast Asian J Trop Med Public Bandar Abbas, Islamic Republic of Health. 42(3): 491–501. Iran. East Mediterr Health J. 10(1–2): 63. Vatandoost H, Abai MR, Abbasi M, Shaeghi 215–224. M, Abtahi M, Rafie F (2009) Design- 71. Chavshin AR, Oshaghi MA, Vatandoost ing of a laboratory model for evalua- H, Yakhchali B, Zarenejad F, Terenius tion of the residual effects of deltame- O (2015) Malpighian tubules are im- thrin (K-othrine WP 5%) on different portant determinants of Pseudomonas surfaces against malaria vector, Anoph- transstadial transmission and longtime eles stephensi (Diptera: Culicidae). J persistence in Anopheles stephensi. Par- Vector Borne Dis. 46(4): 261–267. asites Vectors. 8: 36–42. 64. Vatandoost H, Hanafi-Bojd AA (2008) 72. Anjomruz M, Oshaghi MA, Pourfatollah Laboratory evaluation of 3 repellents AA, Sedaghat MM, Raeisi A, Vatan- against Anopheles stephensi in the Is- doost H (2014) Preferential feeding suc- lamic Republic of Iran. East Mediterr cess of laboratory reared Anopheles Health J. 14(2): 260–267. stephensi mosquitoes according to ABO 65. Chavshin AR, Dabiri F, Vatandoost H, blood group status. Acta Trop. 140: Bavani MM (2015a) Susceptibility of 118–123. Anopheles maculipennis to different 73. Anjomruz M, Oshaghi MA, Sedaghat MM, classes of insecticides in West Azarbai- Pourfatollah AA, Raeisi A, Vatandoost jan Province, Northwestern Iran. Asian H (2014) ABO blood groups of resi- Pac J Trop Biomed. 5(5): 403–406. dents and the ABO host choice of ma-

11 http://jad.tums.ac.ir Published Online: March 18, 2018

J Arthropod-Borne Dis, March 2018, 12(1): 1–15 Z Saeidi and H Vatandoost: Aquatic Insect …

laria vectors in southern Iran. Exp Par- 80. Fathian M, Vatandoost H, Moosa-Kazemi asitol. 136: 63–67. SH, Raeisi A, Yaghoobi-Ershadi MR, 74. Khoshdel-Nezamiha F, Vatandoost H, Oshaghi MA (2015) Susceptibility of Azari-Hamidian S, Bavani MM, Dabiri Culicidae Mosquitoes to Some Insec- F, Entezar-Mahdi R (2014) Fauna and ticides Recommended by WHO in a larval habitats of mosquitoes (Diptera: Malaria Endemic Area of Southeastern Culicidae) of West Azerbaijan Prov- Iran. J Arthropod Borne Dis. 9(1): 22–34. ince, Northwestern Iran. J Arthropod 81. Ataie A, Moosa-Kazemi SH, Vatandoost Borne Dis. 8(2): 163–173. H, Yaghoobi-Ershadi MR, Bakhshi H, 75. Khoshdel-Nezamiha F, Vatandoost H, Anjomruz M (2015) Assessing the sus- Oshaghi MA, Azari-Hamidian S, Mi- ceptibility status of mosquitoes (Dip- anroodi RA, Dabiri F (2016) Molecu- tera: Culicidae) in a Dirofilariasis Fo- lar characterization of mosquitoes (Dip- cus, Northwestern Iran. J Arthropod tera: Culicidae) in Northwestern Iran Borne Dis. 9(1): 7–21. by using rDNA-ITS2. Jpn J Infect Dis. 82. Soltani A, Vatandoost H, Oshaghi MA, 69(4): 319–322. Ravasan NM, Enayati AA, Asgarian 76. Shayeghi M, Vatandoost H, Gorouhi A, F (2015) Resistance Mechanisms of Sanei-Dehkordi AR, Salim-Abadi Y, Anopheles stephensi (Diptera: Cu- Karami M, Jalil-Navaz MR, Akhavan licidae) to Temephos. J Arthropod AA, Shiekh Z, Vatandoost S, Arandian Borne Dis. 9(1): 71–83. MH (2014) Biodiversity of aquatic in- 83. Golfakhrabadi F, Khanavi M, Ostad SN, sects of Zayandeh Roud river and its Saeidnia S, Vatandoost H, Abai MR branches, Isfahan Province, Iran. J Ar- (2015) Biological activities and com- thropod Borne Dis. 8(2): 197–203. position of Ferulago carduchorum es- 77. Ghezelbash Z, Vatandoost H, Abai MR, sential oil. J Arthropod Borne Dis. 9 Raeisi A, Rassi Y, Hanafi-Bojd AA (1): 104–115. (2014) Laboratory and field evalua- 84. Tavassoli M, Shayeghi M, Vatandoost H, tion of two formulations of Bacillus Abai MR, Khoobdel M, Bakhshi H, thuringiensis M-H-14 against mos- Rafie F (2015) Repellency effect of quito larvae in the Islamic Republic of Picaridin and DDT against Anopheles Iran, 2012. East Mediterr Health J. 20 stephensi on human volunteers. J En- (4): 229–235. tomo Zool Studies. 3(2): 343–347. 78. Karimian F, Oshaghi MA, Sedaghat MM, 85. Pirmohammadi M, Shayeghi M, Vatan- Waterhouse RM, Vatandoost H, Hanafi- doost H, Abaei MR, Mohammadi A, Bojd AA (2014) Phylogenetic analysis Bagheri A (2016) Chemical composi- of the oriental Palearctic Afrotropical tion and repellent activity of Achillea members of Anopheles (Culicidae: Dip- vermiculata and Satureja hortensis tera) based on nuclear rDNA and mi- against Anopheles stephensi. J Ar- tochondrial DNA characteristics. Jpn thropod Borne Dis. 10(2): 201–210. J Infect Dis. 67(5): 361–367. 86. Gorouhi MA, Vatandoost H, Oshaghi MA, 79. Soleimani-Ahmadi M, Vatandoost H, Zare Raeisi A, Enayati AA, Mirhendi H M, Turki H, Alizadeh A (2015) Topo- (2016) Current susceptibility status of graphical distribution of anopheline Anopheles stephensi (Diptera: Cu- mosquitoes in an area under elimina- licidae) to different imagicides in a ma- tion programme in the south of Iran. larious area, southeastern Iran. J Ar- Malar J. 14: 262–268. thropod Borne Dis. 10(4): 493–500.

12 http://jad.tums.ac.ir Published Online: March 18, 2018

J Arthropod-Borne Dis, March 2018, 12(1): 1–15 Z Saeidi and H Vatandoost: Aquatic Insect …

87. Sanei-Dehkordi A, Vatandoost H, Abaei 59(3): 239–242. MR, Davari B, Sedaghat MM (2016) 97. Vafei R, Ostovan H, Incekara Ü, Pesic V Chemical composition and larvicidal (2008) A faunistic study on the div- activity of Bunium persicum essential ing beetles (Coleoptera: Dytiscidae) of oil against two important mosquitoes Markazi Province (Central Iran) with vectors. J Essential Oil Bearing Plants. the new records. Mun Ent Zool. 3(1): 19(2): 349–357. 165–170. 88. World Wildlife Federation (2013) Ecore- 98. Dehghani R, Miranzadeh MB, Yosef Za- gions: Earth’s most special places. deh M, Zamani S (2007) Fauna aquatic Available at: insects in swage maturation ponds of http://wwf.panda.org/about_our_earth Kashan University of medical sciences. /ecoregions/ (Accessed 1 March 2013) Pak J Biol Sci. 10(6): 928–931. 89. World Wildlife Federation (2013) Wild- 99. Mohammadian HH (2008) Aquatic insects finder. Available at: of Iran, First volume, Ephemeroptera. http://worldwildlife.org/science/wildf shabpare publication, Iran, p. 184. inder/ (Accessed 23 April 2013) 100. Askari O, FarshbafPourabad R, Khaganin- 90. Gueorguiev V (1965) Sur la fauna des ia S (2009) Faunistic study of Heter- coleopteres Hydrocantharesd’Iran (Re- optera of Zanjanroud region in Zanjan sume). Acad. Bulg. Sci. 19: 116–117. Province of Iran. Mun Entomol Zool. 91. Nehring RB (1976) Aquatic insects as 4(2): 560–563. biological monitors of heavy metal 101. Vafaei R, Darilmaz MJ, Nazari E, Incekara pollution. Bull Environ Contam Tox- U, Piazak N (2009) Contributions to icol. 15: 147-154. the knowledge of Iranian aquatic Col- 92. Gentilil E, Ostovan H, Ghahari H, Ko- eoptera fauna (Dytiscidae, Gyrinidae, marek A (2018) Annotated checklist Helophoridae and Hydrophilidae) with of Iranian Hydrophilidae (Coleoptera: new records and notes on the rare spe- Polyphaga: Hydrophiloidea). Aquatic cies Coleostoma transcaspicum Reit- Insect. 1: 12–18. ter-1906. Acta Entomol Serbica. 14(1): 93. Hosseinie SO (1995) Life history, behav- 101–107. ior and morphology of the immature 102. Ghahari H, Tabari M, Sakenin H, Ostovan stages of Enochrus quadripunctatus H, Imani S (2009) Odonata (Insecta) herbest in the laboratory (Coleoptera: from Northern Iran, with comments Hydrophilidae) II. Morphology J Sci. on their presence in rice fields. Mun 6(4): 195–206. Entomol Zool. 4(1): 148–154. 94. Hosseinia S, Hosseinpour H (1996) Meth- 103. Nemati Varnosfaderany M, Ebrahimi E, les rectus sharp confirm for Iran. La- Mirghaffary N, Safyanian A (2010) tissmus. 7: 18–28. Biological assessment of the Zayandeh 95. Atamehr A, Kamali K, Ostovan H (2004) Rud River, Iran, using benthic macroin- Report on aquatic beetles of the fami- vertebrates. Limnologica. 40: 226–232. ly Hydraenidae (Coleoptera) in Tabriz 104. Khaghaninia S, Askari O, Farshbaf Pour region. J Agricultural Sci. 10(3): 13–29. Abad R, Shahim K (2010) Some ad- 96. Vafaei R, Ostovan H, Incekara Ü, Pešic ditional notes about Heteroptera fau- V (2007) Faunistic study of the aquatic na of Qaradag forests-Iran. Mun En- beetles (Coleoptera: Polyphaga) of tomol Zool. 5(2): 513–518. Markazi Province (Central Iran) with 105. Sadeghi R, Farshbaf Pourabad R, Kazemi new records. Arch Biol Sci. Belgrade. MH, Hassanzadeh M (2009) Introduc-

13 http://jad.tums.ac.ir Published Online: March 18, 2018

J Arthropod-Borne Dis, March 2018, 12(1): 1–15 Z Saeidi and H Vatandoost: Aquatic Insect …

tion of some Heteroptera of Qurigol Iran. World J Zool. 8(3): 285–291. (Iran). Mun Entomol Zool. 4(2): 498– 114. Ghahari H (2013) A study on aquatic and 500. semiaquatic bugs (Hemiptera: Heter- 106. Atamehr A, Alaei M (2010) Two aquat- optera) from northern Iran. Biolo- ic beetles reported (Haliplidae: Cole- giezentrum Linz/Austria. 45(2): 1991– optera) from Azerbaijan, Iran. World 1996. Applied Sci J. 11(8): 918–923. 115. Khazeni A, Adler PH, Telmadareiiy Z, 107. İncekara Ü, Darilmaz M, Vafaei R, Po- Oshaghi MA, Vatandoost H, Abtahi lat A (2013) Contributions to the SM, Lotfi A (2013) The Black Flies knowledge of Iranian aquatic polypha- (Diptera: Simuliidae) of Iran. Zootaxa. ga (Coleoptera) fauna. Turk J Ento- 3694(1): 67–74. mol. 37(1): 49–56. 116. Shaverdo HV, Esfandiari M, Khadempur 108. Esfandiari M, Sadeghi S, Khadempour A A, Nasserzadeh H, Ghodrati A (2013) (2014) First record of Odonata nymphs Diving beetles of Ahvaz City, Khu- from Karun River, south-west Iran. zestan Province, Iran (Coleoptera: Dy- Iran J Animal Biosys. 10(2): 205–208. tiscidae). Koleopt Rdsch. 83: 17–22. 109. Salavatian M, Gholiev Z, Aliev A, Abassi 117. Shayeghi M, Doosti S, Bazrafkan S, Hos- K (2011) Feeding behaviour of brown seini-Vasoukolaei N, Vatandoost H, trout, Salmo truttafario, during spawn- Akhavan AA, Vatandoost S, Arandi- ing season in four rivers of Lar Na- an MH (2013) Prevalence of aquatic tional Park, Iran Caspian. J Environ entomofauna, the predators of mos- Sci. 9(2): 223– 233. quitoes, in the Zayandeh River of Cen- 110. Khadempoor A, Esfandiari M, Jam- tral Iran. Asian Pac J Trop Dis. 4(1): shidniya A (2011) Aquatic insects of S240–S245. Karun River at Ahvaz City, SW Iran. 118. Malekei-Ravasan N, Bahrami A, Shayeghi Annual Zoological Congress of “Grigo- M, Oshaghi MA, Malek M, Man- reAntipa” Museum, Nov 2011, Nation- soorian AB, Vatandoost H (2013) al Museum of Natural History, Bu- Notes on the Iran Caddisflies and role charest, Romania. P. 200. of Annulipalpian hydropsychid Cad- 111. Karimi F, Moattar F, Farshchi P, Savari disflies as a bio-monitoring agent. J A, Parham H (2012) ERA: Suitable Arthropod Borne Dis. 7(1): 71–82. method for estimation of ecological 119. Darilmaz MC, Incekara Ü, Vafaei R effects of pesticide contamination on (2013) Contributions to the knowledge aquatic species. J (Ma- of Iranian aquatic Adephaga (Cole- rine Science). 3(8): 67–73. optera). Spixiana. 36(1): 149–152. 112. Sharifinia M, Imanpour Namin J, Bo- 120. Pourbehi H, Zare Khormizi M, Biran- zorgi Makrani A (2012) Benthic Ma- vand A (2013) Estimation of field biotic croinvertebrate distribution in Tajan index and water quality of Shapoor River using canonical correspondence River in autumn season using aquatic analysis. Caspian J Env Sci. 10(2): insect’s fauna. Int J Agric Crop Sci. 181–194. 6(11): 766–768. 113. Gorjian Arabi MH, Shapoori M, Hosse- 121. Eyidozehi K, Narouyi Y, Mehraban A, inzadeh MA, Erfanifar E, Abedi K, Vazirimehr MR, Rigi K (2014) Eval- Erfanifar E (2013) Effectiveness of uation of aquatic insect fauna such as macro invertebrate based biotic indexes Heteroptera, Ephemeroptera, Diptera, in assessing lake water quality in Gahar, Trichoptera, Coleoptera, Odonata and

14 http://jad.tums.ac.ir Published Online: March 18, 2018

J Arthropod-Borne Dis, March 2018, 12(1): 1–15 Z Saeidi and H Vatandoost: Aquatic Insect …

so on in east of Golestan Province. J Bio Env Sci. 5(1): 508–513. 122. Shayeghi M, Nejati J, Shirani-Bidabadi L, Koosha M, Badakhshan M, Moham- madi Bavani M, Arzamani K, Choubdar N, Bagheri F, Saghafipour A, Veysi A, Karimian F, Akhavan AA, Vatandoost H (2014) Assessing the fauna of aquat- ic insects for possible use for malaria vector control in large river, central Iran. Acta Med Iran. 53(9): 523–532. 123. Nikookar SH, Moosa-Kazemi SH, Oshaghi MA, Vatandoost H, Yaghoobi-Ershadi MR, Enayati AA, Motevali-Haghi F, Ziapour SP, Fazeli-Dinan M (2015) Biodiversity of culicid mosquitoes in rural Neka township of Mazandaran Province, Northern Iran. J Vector Borne Dis. 52(1): 63–72. 124. Soleimani-Ahmadi M, Vatandoost H, Zare M, Alizadeh A, Salehi M (2014) Community knowledge and practices regarding malaria and long-lasting in- secticidal nets during malaria elimina- tion programme in an endemic area in Iran. Malaria J. 13: 511–521. 125. Hanafi-Bojd AA, Vatandoost H, Oshaghi MA, Haghdoost AA, Shahi M, Sed- aghat MM (2012b) Entomological and epidemiological attributes for malaria transmission and implementation of vector control in southern Iran. Acta Trop. 121(2): 85–92. 126. Shayeghi M, Moradi Asl E, Saeidi Z, Mozafari E, Poudat A, Salimi M, Vatan- doost H (2016) Aquatic insects fauna of Meshkin Shahr, Ardabil Province, Northwestern Iran, 2014. J Marine Sci Res Dev. 6: 206–211.

15 http://jad.tums.ac.ir Published Online: March 18, 2018