J Arthropod-Borne Dis, June 2021, 15(2): 162–170 P Faraji-Fard et al.: Species Variety of … 162 http://jad.tums.ac.ir Published Online: June 30, 2021 Original Article Species Variety of the Calf and Human-Attracted Mosquitoes in Southwest Iran Parvaneh Faraji-Fard1; Kambiz Ahmadi-Angali2; *Abdolamir Behbahani1,3 1Infectious and Tropical Diseases Research Center, Health Research Institute, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran 2Department of Biostatistics, Faculty of Public Health, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran 3Department of Medical Entomology, Faculty of Public Health, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran *Corresponding Author: Dr Abdolamir Behbahani, Email: behbahani-a@ajums.ac.ir (Received 21 Oct 2017; accepted 14 Apr 2021) Abstract Background: Any mosquito control methods requires precise information about population dynamics, variety, biology and mosquito habitat. This research assessed Culicid mosquitoes' attraction to a human host and a calf to better under- stand their behavior. Methods: Adult mosquitoes were sampled in 22 weeks in southwestern Iran's Nur Ali Village from May to October 2015. The mosquitoes were drawn to the person and calf as bait, while the unbaited trap was also used. A substantial statistical difference between attracted mosquitoes to the hosts was determined in the T-test. Results: Within 22 weeks, 29821 mosquitoes were captured. Only 9% were collected from the human baited net trap, 89.1% from the calf baited net trap, and 1.9% from the unbaited net trap. The number of collected female mosquitoes was statistically significantly higher using the calf baited net trap of the total mosquitoes, 916 were randomly identified at the species level by local identification keys. Of these, 63 were Anopheles stephensi (human: 16%, calf: 75% and unbaited: 9%), 83 An. pulcherrimus (human: 27%, calf: 60% and unbaited: 13%), 118 Aedes caspius (human: 24%, calf: 69% and unbaited: 7%), 493 Culex tritaeniorhynchus (human: 52%, calf: 37% and unbaited: 11%), 153 Cx. quin- quefasciatus (human: 44%, calf: 47% and unbaited: 9%), and 6 Cx. theileri (human: 33%, calf: 50% and unbaited: 17%). Conclusion: The obtained results here provide useful insights into the mosquito population and the possibility of using this information as an essential part of integrated vector management regarding the reemergence of malaria or other mosquito-borne. Keywords: Mosquitoes; Diversity; Iran Introduction Blood feeding of female mosquitoes (Dip- tera: Culicidae) plays an essential role in trans- mitting diseases by mosquitoes, for instance, Rift Valley fever, yellow fever, West Nile, den- gue and malaria. The above plus other trans- mitted diseases by vectors cause about one bil- lion people infected and more than one million deaths worldwide every year (1). Parasitic and arboviral mosquito-borne diseases have been reported from Iran for a long time. Despite con- siderable progress recently in eliminating ma- laria in Iran, 799 reported malaria (632 cases were imported) were registered in 2015 (2). The records of other mosquito-borne diseases in Iran, including dengue, West Nile fever, diro- filariasis and sinbis, were reported in the litera- ture (3-9). Based on a retrospective cross-sec- tional study, 541 cases of malaria were reported in Khuzestan Province in the southwest of Iran between 2001 and 2014. The most prevalent malaria species was Plasmodium vivax with 478 (88.35%) cases compared with P. falciparum Copyright © 2021 The Authors. Published by Tehran University of Medical Sciences. This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International license (https://creativecommons.org/licenses/by- nc/4.0/). Non-commercial uses of the work are permitted, provided the original work is properly cited. http://jad.tums.ac.ir/ https://creativecommons.org/licenses/by-nc/4.0/ https://creativecommons.org/licenses/by-nc/4.0/ J Arthropod-Borne Dis, June 2021, 15(2): 162–170 P Faraji-Fard et al.: Species Variety of … 163 http://jad.tums.ac.ir Published Online: June 30, 2021 with 63 (11.65%) cases (10). The Culicidae has 41 or 113 genera (depending on the classifica- tion of the tribe Aedini), which are classified in the number of 3583 mosquito species. These 41 (113) genera are divided into the following two subfamilies: Anophelinae and Culicinae (11). Based on the most recent Iranian mos- quito studies, 70 species were reported in 8 to 12 genera in Iran (12-15). Several species of culicid mosquitoes are recorded in Khuzestan Province, including An. stephensi, An. fluviati- lis s.l., An. dthali, An. Superpictus, An. pulcher- rimus, An. culicifacies, An. hyrcanus, An. sa- charovi, Culex pipiens, Cx. perexiguus, Cx. si- naiticus, Cx. modestus, Cx. tritaeniorhynchus, Cx. theileri, Cx. pusillus, Cx. quinquefasciatus, Aedes caspius, Uranotaenia unguiculata and a Culiseta species (14-21). Insecticide-treated nets and indoor residual spraying were used as the primary control activities of malaria vectors in the country (2). The explanation behind the progress made against malaria by Iran and other countries was that governments were us- ing Insecticide-treated nets and indoor residual spraying to avoid malaria in significant transmission areas. It will aid little in manag- ing malaria and zoonotic diseases with zoo- philic vectors (22, 23). Due to indoor residual spraying and treated mosquito nets by many societies, mosquitoes have adapted to remain alive by being more likely to feed on animal blood than ever. Hence, appropriate manage- ment steps will be required to eliminate ma- laria or other vector-borne diseases in some regions of the world where it is caused by zo- ophilic disease vectors that are difficult to control (22, 24-26). The natural tendency of mosquitoes to feed from domestic animals, especially cattle reduces bites to nearby hu- mans. Therefore, the possibility of diversion of mosquitoes to animals was proposed as a ma- laria control method (27-29). The above con- cept application has been presented as a part of the integrated vector management, such as applying insecticides on cattle in the areas un- der specific conditions (30). After insecticide resistance and the harmful effects of certain in- secticides in the environment were noted, this approach seemed like the best option. It is in- expensive, effective, and easy to encourage peo- ple to participate and contribute to disease vec- tors' control (31, 32). This research attempts to determine and compare the number of col- lected female mosquitoes in human baited, calf baited, and unbaited net traps to explain the obtained mosquito population's assortment traps toward providing information about the available potential control methods. Besides, it provided some basic knowledge into the vec- tor population to help the health authorities make the right decisions in case of any mos- quito-borne disease in the area. Materials and Methods Study area This research was carried out in Nour Ali Village (31o 57' 17" N, 48o 55' 42"E, and 41M above sea level) within the central district in Shoushtar County, Khuzestan Province in the southwest of Iran (Fig. 1). With 16 families, the village has 79 and an average of 4.9 persons per household. The village, situated along with one of the Karoun River branches called Gargar, is plain and flat. For several aquaculture farms in and around the village, this river supplies vital water, people farming crops, herds cows, sheep, goats, and ostrich. Adult sampling The sampling of adult mosquitoes was con- ducted for 22 weeks period from May to Oc- tober 2015. Mosquitoes were collected using three types of net traps: first, a big standing rectangle is 2m by 1.5m by 1.5m as a human baited (a volunteer female in her fifties, who weighs 65kg) net trap. A steel frame sur- rounded an open area with a mosquito net all around. Second, a calf baited (four months with an average of 60kg calf) net trap (3m by 3m by http://jad.tums.ac.ir/ J Arthropod-Borne Dis, June 2021, 15(2): 162–170 P Faraji-Fard et al.: Species Variety of … 164 http://jad.tums.ac.ir Published Online: June 30, 2021 3m). The calf was held in the center of the net trap inside a steel frame. The third was the un- baited net trap (2 by one by 1.6m). Our exper- iment's unbaited net trap was used to describe and relate the findings to only a human and a calf to attract the mosquitoes. The netting sides were raised approximately 30 centimeters above the ground to enable host-seeking mosquitoes to enter the net trap inside (33). Traps were placed at the end of the day and stayed in po- sition until dawn. The next morning, before en- tering the net trap to catch mosquitoes trapped overnight, the net trap sides were lowered to the floor. Mosquitoes were captured by an as- pirator from the internal walls and roof of the net trap and placed into labeled paper cups for later identification (33). Field identification of mosquitoes All female mosquitoes were sorted. For eve- ry night trapping, if sufficient samples were available, 20 specimens were randomly cho- sen and identified from each baited net trap and five specimens from unbaited net trap to spe- cies level according to the local keys available (34, 35). Statistics The collected data during 22 weeks from all types of net traps were considered for anal- ysis. The collected data were entered in Ms- Excel 2010 version. The calculations were done using the SPSS version 25.00. The means of collected mosquitoes in the net traps were com- pared using a T-test. Results Of the total collected female mosquitoes, 9 percent were trapped by human baited, 89.1 percent by calf baited and 1.9 percent by un- baited net trap (Fig. 2). This research showed that statistically, less- er Culicid mosquitoes (25.73±6.57) were at- tracted by Unbaited net trap relative to human baited net trap (122.36±39.44), t (22.16)= 2.42, p< 0.05. This analysis showed that the calf baited net trap was statistically stronger at at- tracting mosquitoes (1207.41±264.46) than the Unbaited baited net (25.73±6.57) t(21.03)= 4.47, p< 0.05. This analysis showed that human bait- ed net trap, relative to calf baited net trap (1207.41±264.46), t(21.93)= 4.05, p< 0.05, at- tracted fewer Culicid mosquitoes (122.36± 39.44) statistically (Fig. 2). Of the total 916 identified female mosqui- toes, they were 42.3% (n= 388) from human baited net trap, 47.3% (n= 433) from calf baited net trap and 10.4% (n= 95) from unbaited net trap. The results of the species identification showed out of 916 identified female mosqui- toes were 6.9% (n= 63) Anopheles stephensi, 9.1% (n= 83) An. pulcherrimus, 12.9% (n= 118) Aedes caspius, 53.8% (n= 493) Culex tri- taeniorhynchus, 16.7% (n= 153) Cx. quinque- fasciatus, and 0.6% (n= 6) Cx. Theileri. Table 1. The mosquito's comparison in the trap with human bait against the trap containing a calf baited in Iran's southwest in 2015 Species Mean±Std. Deviation calf baited Mean ±Std. Deviation human baited F P Ae. caspius 81(3.68 ± 4.05) 28(1.27 ± 1.42) 6.95 0.01 Cx. tritaeniorhynchus 180(8.18 ± 3.96) 258(11.73 ± 5.17) 8.03 0.00 Cx. quinquefasciatus 72(3.27 ± 2.51) 68(3.09 ± 2.38) 0.06 0.80 Cx. theileri 3(0.14 ± 0.46) 2(0.09 ± 0.29) 0.16 0.68 An. stephensi 47(2.14 ± 2.94) 10(0.45 ± 0.80) 7.47 0.00 An. pulcherrimus 50(2.27 ± 2.51) 22(1.00 ± 1.41) 5.17 0.02 http://jad.tums.ac.ir/ J Arthropod-Borne Dis, June 2021, 15(2): 162–170 P Faraji-Fard et al.: Species Variety of … 165 http://jad.tums.ac.ir Published Online: June 30, 2021 Fig. 1. The area of this research is Shoushtar County (Khuzestan Province) in Iran's southwest 2015 Fig. 2. The comparison of human baited, calf baited and an unbaited net trap to collect mosquitoes in 22 weeks from May to October 2015 in southwestern Iran Discussion The factors that control the distribution of diseases transmitted by vectors are still poorly known in many areas. The arrival of humans into new areas as part of their migration pat- tern increases exposure to vector and pathogen vectors. Determining the significance of mos- quitoes as disease vectors requires knowledge of their biology and ecology (36). This research's observations have shown that collected mosquitoes were An. stephensi, An. pulcherrimus, Ae. caspius, Cx. tritaeniorhyn- chus, Cx. quinquefasciatus and Cx. theileri. Anopheles stephensi was believed to be the primary malaria vector in the south (37, 38), in similar ways, it was found that blood-feed- ing females stayed substantially in animal shel- http://jad.tums.ac.ir/ J Arthropod-Borne Dis, June 2021, 15(2): 162–170 P Faraji-Fard et al.: Species Variety of … 166 http://jad.tums.ac.ir Published Online: June 30, 2021 ters following blood-feeding (17). Anopheles pulcherrimus was recorded as a potential ma- laria vector in southeastern Iran (14). The pri- mary Rift Valley fever vector in Saudi Arabia has been identified as Cx. tritaeniorhynchus, despite positive reports in Iran, potential vec- tors were not established (15, 39-40). Never- theless, the ability to transmit the vector-borne diseases regarding these species' blood-feeding is considered nuisance and annoyance pests for inhabitants in the area. The findings of this anal- ysis revealed that Cx. tritaeniorhynchus from Culicinae and An. pulcherrimus from Anophe- linae had the most significant number of spec- imens among the collected samples (Table 1). While Cx. theileri was scarce in the traps. Due to the abundance of aquaculture farm-related breeding sites in the region, variations between the densities of collected species will occur due to some species' favor to these locations than others. Also, the difference in the attractiveness of the hosts for different species may cause different collection densities. The propensity of mosquitoes to have a particular host relies on genetic variations between their various popu- lations. However, regardless of genetic traits, it depends on the environmental conditions, the hosts' presence, density and the interaction be- tween the vector and the disease microorgan- isms (41). A strong positive relationship (p˂ 0.05) was statistically demonstrated between the collected mosquitoes' densities in the net traps. The differences between the hosts' at- tractiveness in the current study may refer to the number of odors of different hosts and the olfaction, making the mosquitoes search for their hosts (42). The collected mosquitoes' sig- nificant results (1207.41±264.46) were observed in the calf baited net trap against the human baited and unbaited net trap. The higher mean of mosquito density showed significantly in the human baited net trap (122.36±39.44) com- pared to the unbaited net trap (25.73±6.57). The baited traps' host attraction has been veri- fied by the lowest number of trapped mosqui- toes without bait in the trap (p< 0.05). Factors affecting the host preference for hematophagy include accessibility of hosts, their protective actions, and the suitability composites of their blood (43). Our data indicate that the calf body's relatively large size compared to the exposed human body parts can lead to a calf releasing higher carbon dioxide, attracting more hungry mosquitoes (44–46). As shown in Ta- ble 1, our results indicate that An. pulcherrimus and An. stephensi were particularly capable of feeding on the calf. This result was close to previous studies (25, 44). However, only the small number of specimens described may be biased as related. The Culex spp reported were Cx. quinquefasciatus, Cx. theileri and Cx. tri- taeniorhynchus, which are considered effec- tive vectors ((15). Many Culex mosquitoes have been affiliated with human populations that prepare an optimal environment for mosquito larvae, such as standing water (47). Our stud- ies found no statistically important change in the attraction of Cx. quinquefasciatus and Cx. theileri to the calf or human. These results agree that previous studies that reported Cx. quinquefasciatus have different preferences, from 100 percent on humans to a high bird- likeness degree (41, 48). The vast range of hosts that Cx. quinquefasciatus can feed blood un- der many distinct conditions seems to have chosen the most prevalent host type (41). Our observation concerning Cx. theileri did not follow previous studies that considered much of animals' blood meals than humans (49, 50). In contrast (Table 1), Cx. tritaeniorhynchus was markedly attracted to humans than the calf. Previous experiments have proven this spe- cies to be zoophilic, although only a limited number of species reported here could be bi- ased (51). Aedes caspius, as a potential vector of some vector-borne diseases (15), was drawn significantly to the calf. More mosquito stud- ies are recommended to better understand and evaluate mosquito tendencies in the field, as a subset of collected mosquitoes has been iden- tified. As Figure 2 shows, keeping a calf has been shown to attract ten times as many mos- http://jad.tums.ac.ir/ J Arthropod-Borne Dis, June 2021, 15(2): 162–170 P Faraji-Fard et al.: Species Variety of … 167 http://jad.tums.ac.ir Published Online: June 30, 2021 quitoes as we would expect the man to have. This protection can improve when implement- ed as an integrated control measure. Never- theless, some reports have demonstrated that, when animals are kept near humans, it could lead to the person being attacked by mosqui- toes (32, 52). Therefore, the number of zoo- philic mosquitoes that can transmit mosquito vector-borne diseases to humans is increased by keeping an animal within a human settle- ment in rural areas (53). However, maintain- ing the different sheds outside the human res- idences helps eliminate the area's associated vector-borne disease (31, 53). Consequently, lo- cal studies are critical before the control meth- od is applied. Some key factors, such as spe- cies variety of mosquitoes, the assortment of hosts, distance between animal shelters and res- idential areas, socio-economic factors, and host preferences, should be considered (32, 54). Conclusion The obtained results here provide useful in- sights into the mosquito population regarding keeping animals in the right and a safe dis- tance from their dwellings in the area and the possibility of using integrated vector manage- ment in case of the reemergence of malaria or other transmitted diseases by vectors in the southwest of Iran. Acknowledgements This project was performed by Mrs Par- vaneh Faraji-Fard (Grant No. 94178) in the MSc thesis of Medical Entomology. The mon- ey for this thesis was obtained from the Re- search Deputy of Ahvaz Jundishapur Univer- sity of Medical Sciences. The authors declare that they have no competing interests. References 1. World Health Organization (2014) A global brief on vector-borne diseases. 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