Mosquitoes have had a major impact on human life throughout the history. They are especially problematic in tropics and subtropics. They are a huge nuisance in many areas and can transmit some important human and animal diseases such as malaria, yellow fever, dengue fever and filariasis. Even when they don’t transmit diseases, they can be very irritating because of their blood-sucking behavior. When in very high numbers, they can even cause death in cattle by sucking a high amount of blood out of the body of their victims and (Howard, 1988).
Many different control methods have been and are still being used throughout the world to suppress the population of mosquitoes. These include reducing the breeding sites, using insecticides in aquatic environments to kill their larvae and using natural enemies.
Biological control agents:
Mosquito fish (Gambusia affinis & G. holbrooki) are members of the family Poeciliidae and are believed to be native to Eastern United States. Identification of these two species can be difficult as the taxonomic characters are not easy to identify. They are adaptable to a wide range of habitats, have a high reproductive rate and have been introduced to many countries around the world to control the population of mosquitoes; therefore, they can be found in all continents except Antartica. Mosquitoes are one of the components of their diet and laboratory studies have shown that these fish would feed on mosquito larvae (Pyke, 2008). Other components of their diet may include cladocerans, crustaceans(shrimps, copepods) rotifers, insects (chironomid larvae, backswimmers,water boatmen), mollusks, plant material, small fish, diatoms and even tadpoles (Mansfield, 1998; Pyke, 2005; 2008). It has been observed that when Gambusia is added to ponds with high number of mosquito larvae, they will greatly reduce the larval abundance (Pyke, 2008). Therefore, Gambusia has been considered as an important predator of mosquito larvae and has been widely used as a biocontrol agent in different parts of the world. In fact, Gambusia affinis and G. holbrooki are among the most studied fish species in the world. (Pyke, 2008).
In contrast to general accepted belief, however, there are not many scientific evidences on the reducing effect of mosquito fish on the abundance of mosquito larvae. Many of the experiments are believed not to be accurate and some of them show no change or even increase in the mosquito population after the introduction of Gambusia spp. (Pyke, 2008). For example, it has been reported that in some areas, the introduction of G. affinis has led to algal growth which is a result of mosquito fish predation on phytoplankton-eating invertebrates. Consequently, mosquito fish and other fish species died and caused even more mosquito problems (van Emden & Service, 2004). Another study by Hoy et al. (1972) revealed higher mosquito density in ponds with G. affinis when the fish was stocked at low rates. In contrast, when the fish stocked at high levels, there was more mosquito predation. Their explanation was that mosquito fish ate backswimmers (Notonectidae) preferably over mosquito larvae and therefore ignoring mosquitoes at low stocking rate. However, when the stocking rate was high, they ate both backswimmers and mosquitoes (as cited in Pyke, 2008) presumably due to inadequate backswimmers to support the fish population in the pond.
There are also some other problems associated with the using of mosquito fish which should be taken into account. One of these factors is the vegetation density; there is a negative correlation between vegetation density and feeding rate of mosquito fish. In medium to high vegetation densities, mosquito larvae tend to distribute themselves in the vegetated area and rarely occur in open water. This behavior reduces the probability of the larvae being predated by mosquito fish; (Willems et al., 2005); therefore, it is believed that Gambusia spp. are unlikely to be effective in areas with dense vegetation. Another factor to be considered is the contribution of mosquito larvae to the average daily food intake of mosquito fish. For example in one study, depending on the availability of food, mosquito larvae comprised 50-92% and an average of ~75% of total volume of daily food eaten by G. affinis in a salt marsh in Florida. This study determined G. affinis as a diverse feeder of many animals and also plant material (Harrington & Harrington, 1961). Therefore, as mentioned before, mosquito larvae may not be the dominant food for Gambusia spp. depending on the aquatic fauna in any specific environment (Pyke, 2008).
It is believed that the introduced Gambusia species may have detrimental effect on local amphibians and fish species. G. affinis for example, eats anuran eggs especially the eggs of those species which breed in temporal water bodies as they lack the mechanical and chemical defenses developed in permanent water egg-laying species (Grubb, 1972). G. holbrooki has been observed attacking and killing tadpoles of several species of frogs in the laboratory but generally preferring invertebrate food over tadpoles (Reynolds, 2009). Similar negative effect of G. affinis has been reported on endangered fire salamander in northern Israel in which the fish threatens the salamander by damaging its appendages especially the tailfin (Segev et al., 2009). G. affinis has been reported preying on or showing aggression toward other fish species and therefore reducing their population or expelling them from the micro-habitat that they are best adapted to (Ayala et al., 2007).
There are more than 300 larvivorous fish species worldwide in 32 genera. Most of them are in the family Cypridontidae with 15 genera and 300 larvivorous species and in other families in order from high to low: Cyprinidae, Hemirhamphidae, Anabantidae, Chilidae, Goodeidae and Poeciliidae (Ghosh & Dash, 2007).
There has been allegations on mosquito control potential of some birds, bats, frogs and lizard species. However, there are not enough evidences showing their effectiveness or even any sign indicating their mosquito eating behavior. Therefore, their mosquitoes control effect efficacy is believed to be anecdotal.
For example, there have been some allegations that purple martin can eat up to 2,000 mosquitoes per day implying that this bird can be used as a biological control agent. Although some stomach content studies were able to show some to many mosquitoes present their stomach at specific times, many others failed to show any mosquitoes in their stomach and even those which were positive in having mosquitoes failed to show a similar content on later studies in the same area. In addition, no observation has been made on any active mosquito feeding behavior by purple martins. Therefore, it is believed that mosquitoes don’t comprise any significant portion of purple martin’s diet. In fact, it is believed that for most part of the day mosquitoes and purple martins do not occur at the same time (Kale, 1990).
Genus: Toxorhynchites spp. (Diptera: Culicidae)
Toxorhynchites spp. are members of the subfamily (Toxorhynchitinae) within the mosquito family (Culicidae). There are about 69 species worldwide. Their larva is aquatic and adults are active fliers. Eggs are dropped by female mosquito from a distance into the water body. This is believed to be advantageous for enabling the female to lay eggs in places which are partially covered or inaccessible otherwise. They are unusual members of the family Culicidae in respect to two aspects of their biology: 1) adult females do not feed on blood (non-haematophagous) 2) larvae are predatory. Adult females feed on nectar and other sugary sources from plants (Steffan & Evenhuis, 1981) whereas larvae prey on different types of aquatic invertebrates such as larvae of blood-sucking mosquitoes, other families of flies (Chironomidae, Tipulidae, Psychodidae, Ceratopogonidae, Ephydridae, Syrphidae, Corethrellidae), beetles (Scirtidae), Acari, Cladocera, Copepoda, Ostracoda, Olichaeta, Rotifera, Protozoa (Campos & Lounibos, 2000), dragonfly naiads, and even small tadpoles (as cited in Steffan & Evenhuis, 1981). Toxorhynchites spp. also get attracted to and attack surface trapped insect nearby (Breland, 1949). In fact, larvae of Toxorhynchites are cannibalistic and will easily prey on each other in smaller environment. This is indicated by single larva surviving per container when the size of container is small (Steffan & Evenhuis, 1981). Two species, namely, T. brevipalpis and T. amboinensis have shown to have “prepupal killing behavior” in which the larvae kills many mosquito larvae around without consuming them before going into the pupal stage. This is believed to be advantageous to the predatory larvae as it reduced the chance of being predated by other predators during its vulnerable pupal stage (Campos & Lounibos, 2000; Steffan & Evenhuis, 1981).
Introduction of Toxorhynchites spp. has been done in Hawaii, Fiji, Java, India, Malaysia, Thailand & USA but has not been successful all the times. In Hawaii for example, T. brevipalpis, T. theobaldi & T. amboinensis were introduced to control filiriasis but had little success. It turned out that despite being established, T. amboinensis was not effective in controlling Aedes albopictus. A success story was recorded in American Samoa Island in which T. amboinensis and T. brevipalpis were introduced to control Aedes polynesiensis; T. amboinensis was established and found to be effective against the vector. Another success has been the introduction of T. amboinensis to Fiji for controlling A. polynesiensis. However, the former introductions of T. splendens & T. inornatus were both unsuccessful (as cited in Collins & Blackwell, 2000)
One problem which arises in the introduction of Toxorhychites spp. is the mismatch between the oviposition sites of the vector and the predator. For example, in one study in Lousiana in an attempt to control Aedes aegypti, T. rutilus rutilus was released into the habitat with low success. In fact, T. rutilus rutilus got established but instead of ovipositing into the artificial containers where A. aegypti larvae mostly occur, they mostly laid their eggs in tree holes and therefore didn’t have any significant effect on the vector population. In another study in New Orleans, however, the population of A. aegypti and C. quinquefasciatus were reduced by 74% after the introduction of the same species (T. rutilus rutilus) into the urban area. In addition, it is believed that the introduction of Toxorhynchites as larvae generally results in a better control of the vector than releasing adults (as cited in Collins & Blackwell, 2000).
There are some other insect predators reported feeding on mosquito larvae. There are several predators in the culicidae family in the genera Anopheles, Culex, Bezzia, Corethrella and Culicoides. For example, Anopheles barberi has been found to prey on tree-hole mosquito larvae and Culex fuscanus preys on Aedes egypti, Anopheles stephani and Culex quinquefasciatus. Other dipterans worth mentioning are: Dolichopus gratus (Dolichopodidae), Mochlonyx culiciformis (Chaoboridae), Monohelea maya (Ceratopogonidae), Ochthera chalybesceens (Ephydridae) (as cited in Shaalan & Canyon, 2009).
Beetles (Order:Coleoptera) have some representative mosquito predators in families Dytiscidae and Hydrophilidae. Some of the dytiscid species which have been studied in mosquito control are: Acilius sulcatus, Agabus erichsoni, Agabus opacus, Colymbetes paykulli, Ilybius ater, Ilybius fuliginosus, Dytiscus marginicolis, Lacconectus punctipennis,Rhantus sikkimensis (as cited in Shaalan & Canyon, 2009)
Order Hemiptera contains several water dwelling species in the familes Notonectidae, Nepidae & Belostomatidae which feed on mosquito larvae. Backswimmers (Notonectidae) are especially important and have been studied more than the other two families. Among notonectids, Anisops spp. and Notonecta spp. have received more attention by scientists. For example, Anisops assimilis was found to be effective in reducing mosquito larvae in New Zealand and Notonecta hoffmani strongly affected mosquito population in Santa Barbara, California (as cited in Shaalan & Canyon, 2009).
Dragonfly naiads are known to prey on mosquito larvae especially on bottom feeding mosquitoes such as Aedes. In contrast, there is a report showing that damselfly immatures prey less often on mosquito larvae (as cited in Shaalan & Canyon, 2009).
This genus is a member of the family Cyclopidae in the suborder Copepoda (Crustacea). Members of this genus feed on the larvae of different species of mosquitoes.
One of the first scientific publications on the predatory behavior of Mesocyclops goes back to 1981 in which scientists observed that Mesocyclops leuckarti shows predatory behavior on larvae of Aedes aegypti (Rivière & Thirel., 1981). Later, similar predatory behavior was found in Mesocyclops venezolanus and a few other Mesocyclops spp. feeding on Anopheles albimanus in Colombia. It was found that A. albimanus larvae were not present in ponds containing M. venezolanus whereas being numerous in adjacent ponds lacking this copepod. Mesocyclops spp. usually feed on the first-instar larvae of mosquitoes and can detect the prey when they come in close contact with the larvae by detecting mechanical disturbance in water. They attack the larvae from any direction and chew the whole body except the head capsule. The feeding process takes about 2-3 minutes (Marten et al., 1989).
Although Mesocyclops spp. feed on mosquito larvae at high rates, the presence of alternative food can highly reduce their efficacy in feeding on mosquito larvae. For example, it is known that in the laboratory conditions, M. theromocyclopoides eats considerably lower number of Culex quinquefasciatus in the presence of other planktons as a food source.
In contrast, there was no significant difference between the average larvae of Aedes aegypti consumed in experiments with or without alternate food (Mittal et al., 1997). In a similar study it was found the Mesocyclopsannulatus feeds on Aedes aegypti and Culex pipiens larvae in laboratory conditions but the mortality of both mosquito larvae was significantly lower in the presence of alternate food (algal-protozoan suspension). In addition, it was found that M. annulatus prefers larvae of A. aegypti over the larvae of C. pipiens when present together in the same container (Micieli et al., 2002).
Some genera other than Mesocyclops in the family Cyclopidae (Copepoda: Crustacea) have been identified as predators of mosquito larvae. Some of these include: Macrocyclops, Megacyclops and Acanthocyclops (Micieli et al., 2002).
A few members of the Mirmithidae family have been known as a biological control agent of mosquitoes.
One species, Romanomermis culicivorax, has been extensively studied for this purpose by different scientists (Paily & Balaraman, 2000). It is an obligate parasite of the larvae of many mosquito species. The parasitic phase lasts 6-10 days and during this time the parasite feeds on the host haemolymph. Then, it exits the host, molt and begins its reproduction by mating and laying eggs. The host usually remains alive until shortly after the parasite leaving the host (Giblin & Platzer, 1985).
There are some other species which have been reported attacking mosquito larvae: Romanomermis iyengari, R. kiktoreac, R. hermaphrodites, Epidomermis cozii, Agomermis pachysoma, Culicimermis schakhovii (Paily & Balaraman, 2000; Petersen, 1980). The infective stage (preparasite) of these nematodes attacks the larvae of mosquitoes in aquatic environments. The preparasite of M. culicivorax finds the second-instar larvae of mosquito and starts to secrete an adhesive material from the anterior parts of the body which is believed to be useful in attachment to host. Then, it seeks an appropriate penetration site and starts to probe by its odentostyle. This causes partial paralysis of mosquito larvae and believed to be caused by esophageal secretions (Shamseldean & Platzer, 1989).
Mosquito infecting nematodes can be quite effective depending on the nematode and mosquito species. For example in one study, the rate of lethal infection caused by Romanomermis iyengari in Culex sitiens was 95%, Culex quinquefasciatus (90%), Aedes aegypti (79%), Anopheles culicifacies (36%) (Paily & Balaraman, 2000).
Romanomermis culicivorax is generally very infectious and lethal to mosquitoes. This means that in high densities, the nematodes will kill all of their hosts and will soon die themselves; therefore, they need to be reintroduced to the area. Also, they can become very aggregated but show little dispersal between aquatic environments. In other words, they should be introduced to every single aquatic environment even when they are close to each other (van Emden & Service, 2004).
Ayala J, Rader R, Belk M & Schaalje G (2007) Ground-truthing the impact of invasive species: spatio-temporal overlap between native least chub and introduced western mosquitofish. Biological Invasions 9: 857-869. doi:10.1007/s10530-006-9087-4.
Breland OP (1949) The biology and the inmature stages of tho mosquito, Megarhinus septentrionalis Dyar & Knab. Annals of the Entomological Society of America 42: pp. 38-47.
Campos RE & Lounibos LP (2000) Natural Prey and Digestion Times of Toxorhynchites rutilus (Diptera: Culicidae) in Southern Florida. Annals of the Entomological Society of America 93: 1280-1287. doi:10.1603/0013-8746(2000)093[1280:npadto]2.0.co;2.
Chang K-H, Nagata T & Hanazato T (2004) Direct and indirect impacts of predation by fish on the zooplankton community: an experimental analysis using tanks. Limnology 5: 121-124. doi:10.1007/s10201-004-0116-7.
Collins LE & Blackwell A (2000) The biology of Toxorhynchites mosquitoes and their potential as biocontrol agents. Biocontrol News and Information 21: 105N-115N.
Frisch D & Green AJ (2007) Copepods come in first: rapid colonization of new temporary ponds. Fundamental and Applied Limnology 168: 289-297. doi:10.1127/1863-9135/2007/0168-0289.
Ghosh SK & Dash AP (2007) Larvivorous fish against malaria vectors: a new outlook. Transactions of the Royal Society of Tropical Medicine and Hygiene 101: 1063-1064. doi:10.1016/j.trstmh.2007.07.008.
Giblin RM & Platzer EG (1985) Romanomermis culicivorax parasitism and the development, growth, and feeding rates of two mosquito species. Journal of Invertebrate Pathology 46: 11-19. doi:10.1016/0022-2011(85)90124-7.
Grubb JC (1972) Differential Predation by Gambusia affinis on the Eggs of Seven Species of Anuran Amphibians. American Midland Naturalist 88: 102-108.
Harrington RW, Jr. & Harrington ES (1961) Food Selection among Fishes Invading a High Subtropical Salt Marsh: From Onset of Flooding through the Progress of a Mosquito Brood. Ecology 42: 646-666.
Howard S (1988) Mosquitoes kill cows in Florida: Anchorage Daily News (ed., p. A6.
Kale HW (1990) The Relationship of Purple Martins to Mosquito Control.
Mansfield S (1998) Dietary composition of (Family Poeciliidae) populations in the northern Waikato region of New Zealand. New Zealand journal of marine and freshwater research 32: 375-383. doi:10.1080/00288330.1998.9516832.
Marten GG, Astaiza R, Suarez MF, Monje C & Reid JW (1989) Natural control of larval Anopheles albimanus (Diptera: Culicidae) by the predator Mesocyclops (Copepoda: Cyclopoida). Journal of Medical Entomology 26: 624-627.
Micieli MV, Marti G & García JJ (2002) Laboratory evaluation of Mesocyclops annulatus (Wierzejski, 1892) (Copepoda: Cyclopidea) as a predator of container-breeding mosquitoes in Argentina. Memórias do Instituto Oswaldo Cruz 97: 835-838.
Mittal PK, Dhiman RC, Adak T & Sharma VP (1997) Laboratory evaluation of the biocontrol potential of Mesocyclops thermocylopoides thermocyclopoides (Copepoda: Cyclopidae) against mosquito larvae. Southeast Asian Journal of Tropical Medicine and Public Health 28: 857-861.
Paily KP & Balaraman K (2000) Susceptibility of ten species of mosquito larvae to the parasitic nematode Romanomermis iyengari and its development. Medical and Veterinary Entomology 14: 426-429. doi:10.1046/j.1365-2915.2000.00263.x.
Petersen JJ (1980) Nematode pathogens of Culicidae (mosquitos). Bulletin of the World Health Organization 58 Suppl: 85-97.
Pyke GH (2005) A Review of the Biology of Gambusia affinis and G-holbrooki. Reviews in Fish Biology and Fisheries 15: 339-365. doi:10.1007/s11160-006-6394-x.
Pyke GH (2008) Plague Minnow or Mosquito Fish? A Review of the Biology and Impacts of Introduced Gambusia Species, Vol. 39: Annual Review of Ecology Evolution and Systematics (ed., pp. 171-191.
Reynolds SJ (2009) Impact of the Introduced Poeciliid Gambusia holbrooki on Amphibians in Southwestern Australia. Copeia 2009: 296-302. doi:10.1643/ch-08-101.
Rivière F & Thirel. R (1981) La prédation du co-pepode Mesocyclops leuckarti pilosa (Crustacea) sur les larves de Aedes (Stegomyia) aegypti et de Ae. (St.) polynesiensis (Dip.: Culicidae). Essais prélimi-naires d’utilisation comme agent de lutte biologique. Entomophaga 26: 427-439.
Segev O, Mangel M & Blaustein L (2009) Deleterious effects by mosquitofish (Gambusia affinis) on the endangered fire salamander (Salamandra infraimmaculata). Animal Conservation 12: 29-37. doi:10.1111/j.1469-1795.2008.00217.x.
Shaalan EA-S & Canyon DV (2009) Aquatic insect predators and mosquito control. Tropical Biomedicine 26: 223-261.
Shamseldean MM & Platzer EG (1989) Romanomermis culicivorax: Penetration of larval mosquitoes. Journal of Invertebrate Pathology 54: 191-199. doi:10.1016/0022-2011(89)90028-1.
Steffan WA & Evenhuis NL (1981) BIOLOGY OF TOXORHYNCHITES. Annual Review of Entomology 26: 159-181. doi:10.1146/annurev.en.26.010181.001111.
van Emden HF & Service MW (2004) Pest and vector control. Cambridge University Press.
Willems KJ, Webb CE & Russell RC (2005) A comparison of mosquito predation by the fish Pseudomugil signifier Kner and Gambusia holbrooki (Girard) in laboratory trials. Journal of vector ecology 30: 87-90.