Hindawi

BioMed Research International

Volume 2020, Article ID 4065315, 11 pages
https://doi.org/10.1155/2020/4065315

Review Article
Naturally Occurring Microbiota Associated with Mosquito
Breeding Habitats and Their Effects on Mosquito Larvae

H. A. K. Ranasinghe and L. D. Amarasinghe

Department of Zoology and Environmental Management, Faculty of Science, University of Kelaniya, Dalugama, Kelaniya, Sri Lanka
GQ 11600

Correspondence should be addressed to L. D. Amarasinghe; deepika@kln.ac.lk

Received 22 March 2020; Revised 12 July 2020; Accepted 4 August 2020; Published 15 December 2020

Academic Editor: Mansour El-Matbouli

Copyright © 2020 H. A. K. Ranasinghe and L. D. Amarasinghe. This is an open access article distributed under the Creative
Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the
original work is properly cited.

Immature mosquitoes are aquatic, and their distribution, abundance, and individual fitness in a particular breeding habitat are
known to be dependent on mainly three factors: biotic factors, abiotic factors, and their interaction between each other and with
other associated taxa. Mosquito breeding habitats harbor a diversified naturally occurring microbiota assemblage, and the biota
have different types of interactions with mosquito larvae in those habitats. Those interactions may include parasitism,
pathogenism, predation, and competition which cause the mortality of larvae, natural reduction of larval abundance, or
alterations in their growth. Many microbiota species serve as food items for mosquito larvae, and there are also some
indigestible or toxic phytoplanktons to larvae. However, when there is coexistence or mutualism of different mosquito species
along with associated microbiota, they form a community sharing the habitat requirements. With the available literature, it is
evident that the abundance of mosquito larvae is related to the densities of associated microbiota and their composition in that
particular breeding habitat. Potential antagonist microbiota which are naturally occurring in mosquito breeding habitats could
be used in integrated vector control approaches, and this method rises as an ecofriendly approach in controlling larvae in
natural habitats themselves. To date, this aspect has received less attention; only a limited number of species of microbiota
inhabiting mosquito breeding habitats have been recorded, and detailed studies on microbiota assemblage in relation to diverse
vector mosquito breeding habitats and their association with mosquito larvae are few. Therefore, future studies on this
important ecological aspect are encouraged. Such studies may help to identify field characteristic agents that can serve as
mosquito controlling candidates in their natural habitats themselves.

1. Introduction competition. When there is coexistence or mutualism of dif-

ferent mosquito species along with other biotic organisms,
Due to the importance of mosquitoes as vectors for diseases they form a community sharing habitat requirements [9].
in terms of public health, studying their ecological and envi- Larval density in a breeding habitat is affected by different
ronmental conditions influencing the abundance of these abiotic characteristics of the breeding site such as vegetation,
species is a vital necessity [1]. Determining the larval densi- temperature, turbidity, pH, the concentration of ammonia,
ties, proliferation, and species assemblage, mosquito habitat salinity, nitrite and nitrate, sulfate, phosphate, chloride, cal-
ecology plays an important role [2]. Immature mosquitoes cium, and water hardness [10, 11]. Further, larval densities
are aquatic, and the distribution, abundance, and individual are controlled by hydrology, light/shade, and nutrient avail-
fitness of mosquitoes in a particular breeding habitat are ability also [12]. However, among biotic factors associated
known to be dependent on mainly three factors: biotic factors with mosquito breeding habitats, several species of bacteria,
[3, 4], abiotic factors [5, 6], and their interaction between fungi, unicellular organisms such as protists [13], entomo-
each other and with other associated taxa [7, 8]. Those inter- pathogenic nematodes [14], and filamentous fungi [15] are
actions included parasitism, pathogenism, predation, and recorded for the infection to mosquito larvae.
2 BioMed Research International

There is a diversified naturally occurring microbiota parameters for exclusion. Studies related to screening on
assemblage in mosquito breeding habitats. Microbiota are macrofauna in the mosquito breeding habitats including
partly potential food organisms, competitors, and/or poten- freshwater fish; macrocrustaceans; larvae of dragonflies/-
tial mosquito predators. However, among them, there may damselflies, mollusks, coleopteran, and hemipteran larvae;
be parasitic or pathogenic microbiota species to mosquito and hydrophytes or macrophytes were excluded as they did
larvae as well. So, some of the microbiota in the habitat act not fall into the category of the microbiota.
as natural biocontrol agents against mosquito larvae. Micro- The full text of each article was reviewed to determine its
biota communities associated with mosquito breeding habi- eligibility for our study according to the inclusion and exclu-
tats often vary in composition as there are species that are sion criteria. After concluding this process, all papers/studies
highly sensitive for the changes in nutrient cycling and vari- and abstracts which met the inclusion criteria were included
able environmental conditions including temperature [16]. into our study. Information was extracted, organized, and
Excreta of some animals can be influenced on the structure sorted according to key themes and issues: pathogenic, para-
and functioning of plankton communities as the excreta sitic, predatory microbiota, microbiota as competitors and
could act as a significant source of nitrogen and phosphorus. food items, bacteria as microbiota in mosquito breeding hab-
Mosquito larvae were provided with diverse resources to prey itats, and other microbiota recorded from global studies.
on, by the interactions of microinvertebrates [17]. Information was managed under those subcategories. Find-
Although vector control strategies have traditionally ings were reported using a combination of tables with
focused on killing mosquitoes using a variety of synthetic descriptions according to our themes, in a way that the infor-
chemical insecticides, the development of insecticide resis- mation clearly links to the extent of the literature and to iden-
tance has declined the efficiency of killing mosquitoes. Also, tify gaps.
the financial burden of insecticide-based vector control pro-
grams is prohibited by the widespread usage of larvicides 3. Results
and adulticides in many countries where mosquito-borne
diseases remain endemic [13]. Thus, information on micro- 3.1. Parasitic and Pathogenic Effects of Microbiota on
biota associated with mosquito breeding habitats and their Mosquito Larvae. Endoparasitic ciliates (Protista: Cilio-
effects on mosquito larvae is worth investigating with regard phora) have been known to infect mosquito larvae since
to their potential usage in integrated vector control 1921. The first record was by Lamborn, from a sample col-
approaches to be used. However, there are only a very limited lected from an earthen pot in Kuala Lumpur reporting the
number of studies and scattered information focused on this occurrence of Lambornella stegomyiae infection in the larvae
aspect; only a limited number of such potential parasitic or of Aedes albopictus [19].
pathogenic species have been recorded from those studies. After about a 74-year gap, the transformation of Lambor-
nella stegomyiae trophonts to theronts, the distribution of
2. Methodology invasion cysts on larval Aedes albopictus cuticle, and the vir-
ulence of L. stegomyiae to Ae. albopictus and Aedes aegypti
Reviewing was performed with the use of the six-step meth- under laboratory conditions were studied by Arshad and
odological approach defined by Arksey and O’Malley [18]. Sulaiman [20]. The survival of the parasitic agents (ciliates)
The microbiota association in mosquito breeding habitats is under dry conditions; thus, the encystation of these ciliates
and their effects on developing larvae, either as positive or is a possible way for the time lap. After excystation, free-
negative influences, were established as the research question swimming stages of these ciliates could be increased easily
to review. Relevant studies were comprehensively searched when the optimum environmental conditions reoccurred.
using a general internet Google search and several electronic Cysts and the processes of encystation and excystation have
databases, including Google Scholar and ResearchGate, been described for many such ciliate species associated with
meeting abstracts and dissertations. We also searched the mosquito breeding habitats. Arshad and Sulaiman [20] have
Science Citation Index for papers that our initial searches found out the transformation of trophonts of the parasitic
may have missed. A very broad comprehensive search was agent into theronts was induced by a morphogenic agent
conducted to gather information as recommended by Arksey released from a larval Ae. albopictus homogenate. Further,
and O’Malley [18]. Once the relevant literature was identi- the first transformation was observed 4 hrs after exposure
fied, the exclusion and inclusion criteria that were established to the larval mosquito homogenate, but most transforma-
were applied to the papers. tions occurred between 12 and 16 hrs. Distribution of inva-
Inclusion parameters were established; studies on micro- sion cysts on the cuticle of mosquito larvae was not
scopic invertebrate animals such as ciliates, rotifers, and uniform, and most cysts were formed on their abdomen
freshwater microcrustaceans and their juvenile stages, mainly and head. L. stegomyiae was highly infective and virulent to
comprised of members in the groups of ostracod, copepod, Ae. albopictus (mortality rate: 99.53%) and Ae. aegypti (mor-
and cladocerans associated with mosquito breeding habitats, tality rate: 90.83%) larvae [20].
were selected. Further, studies on microflora associated with After a gap of fifty years of identifying the first parasitic
mosquito breeding habitats which mainly included plank- ciliate on mosquito larvae, the second species of Lambornella
tonic algae (e.g., green algae, brown algae, and diatoms) (L. clarki) (Ciliophora: Tetrahymenidae) was isolated from
and cyanobacteria (blue-green algae) species associated with newly flooded tree hole-breeding mosquito larvae, Aedes sir-
mosquito breeding habitats were selected. We carefully set ensis [21]. After twelve years of recording the parasitism of L.
BioMed Research International 3

clarki, Washburn and Mercer [22] have studied the parasit- were less (14.13%) susceptible to Chilodonella infection than
ism of newly hatched Aedes sierrensis (Diptera: Culicidae) Culicine larvae (75.21%). Thousands of motile endoparasitic
larvae by L. clarki following the habitat flooding. As early as stage of the ciliate were found packed in body cavities of dead
24 hrs after flooding, ciliates initiated the first parasite cycle and transparent larvae while numerous cuticular cysts were
by forming cuticular cysts on first instar larvae, and by observed on the cadaver of larvae and pupae [28].
64 hrs, cysts were observed on larvae. Further, the same study However, a study conducted by Patil et al. [29] revealed
mentioned that among tree-hole populations, the proportion inhibition of larval growth, development, and adult emer-
of larvae with L. clarki cysts ranged from 2 to 100% at 48 hrs. gence of An. stephensi larvae due to infection of Vorticella
Ciliates began entering mosquito larval hosts from 48 to sp. The same study further reported that Vorticella sp. has
72 hrs after flooding, but some larvae were able to escape the first preference to Anopheles, but it could attack other
from parasitization by molting to the second instar before cil- mosquito species like Aedes aegypti. Far back in 1950, Micks
iates penetrate the cuticle [22]. [30, 31] reported the lethal effect of the ciliate, V. microstoma,
In 1986, Egerter et al. found that the L. clarki is dispersed on An. quadrimaculatus. Both the above previous studies
by infected adult mosquitoes. Invasion of the ovaries induces suggest that the growth, development, and emergence of
parasitically castrated females to exhibit oviposition behavior mosquito larvae are inhibited by Vorticella, resulting in death
and thereby actively disperse ciliates through deposition into although the precise reason for that is still unknown. From
water. Adults of both sexes also passively disperse ciliates by the microbiota species identified from mosquito breeding
dying on water surfaces. However, infected adults were more habitats in Sri Lanka, Vorticella microstoma and Chilodonella
likely to die on the water than uninfected adults. Ciliates are sp. were found to be effective negatively on Culex spp. mos-
dispersed by infected adults who can infect larvae and form quito larvae and Zoothamnium sp. found as an epibiont on
desiccation-resistant cysts. Parasitism of L. clarki indicated Culex spp. mosquito larvae. The trophont stages of V. micro-
a significant biological control potential against container- stoma and Zoothamnium sp. were found attached to the cuti-
breeding mosquitoes due to their parasite-induced dispersal cle of mosquito larvae [32, 33].
by hosts, desiccation-resistant cysts, an active host-seeking
infective stage, and high infection and mortality rates [23].
Washburn et al. [24] indicated that induced free-living tro- 3.2. Predatory Effects of Microbiota on Mosquito Larvae. The
phonts of L. clarki undergo an asynchronous response in term “predators” of mosquito larvae refers to macro-/micro-
which cells divide and transform into parasitic cells (ther- invertebrates that feed upon mosquito larvae [34, 35]. Natu-
onts) that encyst on larval predators. Parasitic ciliates pene- rally occurring Cyclopoids (Subphylum: Crustacea, Sub-
trate the cuticle, enter the hemocoel, and ultimately kill class: Copepoda) are able to prey on mosquito larvae [36–
their predator-host then. However, Anopheline larvae 40]. The first field trial was carried out with Mesocyclops
(Anopheles barbirostris, An. hyrcanus group, and An. philip- aspericornis against the larvae of Aedes polynesiensis Riviere
pinensis) breeding in peridomestic ditches was found et al. [36] and revealed that they reduce the Aedes polynesien-
infected with a Lambornella sp. in Northeast India [25]. sis and/or Aedes aegypti by 91-99% in burrows, tree holes,
A ciliate species belonging to another genus, Tetrahy- drums, wells, and tires in French Polynesia. But M. aspericor-
mena pyriformis, was observed in the body cavity and anal nis could not effectively reduce the larval population of Culex
gills of mosquito larvae of bamboo-breeding species Armi- particularly Cx. roseni and Cx. quinquefasciatus. Thereafter,
geres dolichocephalus, Ar. dentatus, and Ar. digitatus col- many field and laboratory trials were conducted with many
lected from a bamboo forest near Kuala Lumpur by Corliss microbiota species as predators of mosquito larvae, and they
[26]. The parasitism of Tetrahymena to mosquito larvae are summarized in Table 1.
becomes fatal in heavy infestations which make the larvae Determinants of the efficiency of mosquito larval preda-
transparent, whitish, or opaque. These facultative parasites tion are the predator’s ability to consume prey from early lar-
probably enter via the oral route and invade the hemocoel vae onwards, high attacking rate, and its preference for target
through the gut wall of mosquito larvae [26]. High concen- prey instead of other prey types. Additionally, it depends on
trations of Tetrahymena pyriformis have resulted in high the predator’s preference for advanced instars, as it avoids the
mortalities of Culex tarsalis larvae where the concentration compensatory effect of the reduction in competitive interac-
is fairly less to achieve the same result for Aedes aegypti in tions among the surviving prey [47, 48].
the United States [27]. Besides, Udayanga et al. [46] found that the predatory
Das [28] has reported that another endoparasitic ciliate, efficiencies varied significantly among the copepod species;
Chilodonella uncinata, has been isolated from the infected Mesocyclops leuckarti showed the highest predatory effi-
larval head capsule, antennae, body cavity, anal gills and ciency for Ae. aegypti and Ae. albopictus larvae [46]. Mesocy-
siphons of Culicine larvae, and Anopheline larvae breed in clops aspericornis was the most effective predator of Aedes
paddy fields, irrigation channels, marshy areas, wells, ponds, mosquitoes while Mesocyclops darwini was less efficient
and pools in North India. The natural infestation of Chilodo- [43]. Rey et al. [44] revealed that cyclopoid copepods were
nella uncinata has resulted in high mortalities in Culex tritae- most effective on 1-4-day-old Aedes larvae, and further,
niorhynchus and Culex pseudovishnui larvae collected from Chansang et al. [45] found that Mesocyclops thermocyclo-
paddy fields. C. uncinata was found to cause chronic and poides copepods alone were able to produce mortality of
fatal infection in the natural population of mosquitoes in 98-100% in the 1st instar larvae of Ae. aegypti when the cope-
and around Delhi, North India, while Anopheline larvae pod : larvae ratios are ranging from 1 : 1 to 1 : 4.
4 BioMed Research International

Table 1: Recorded predatory cyclopoid species associated with mosquito breeding habitats.

Microbiota species Mosquito species tested against References

Aedes aegypti and Aedes Lardeux et al.
Mesocyclops aspericornis
polynesiensis [36]
Mesocyclops spp. Anopheles albimanus Marten [41]
Anopheles spp. and Culex
Mesocyclops longisetus and Macrocyclops albidus Marten et al. [37]
quinquefasciatus
Mesocyclops longisetus Aedes aegypti Marten et al. [37]
Anopheles spp. and Culex
Mesocyclops longisetus and Mesocyclops albidus Marten et al. [37]
quinquefasciatus
Mesocyclops longisetus Aedes aegypti Marten et al. [37]
Mesocyclops leuckarti pilosa Aedes albopictus Marten [42]
Mesocyclops aspericornis, Mesocyclops australiensis, Mesocyclops darwini, and
Aedes spp. Brown et al. [43]
Mesocyclops notius
Macrocyclops albidus Aedes spp. Rey et al. [44]
Chansang et al.
Mesocyclops thermocyclopoides Ae. aegypti
[45]
Udayanga et al.
Mesocyclops leuckarti and Mesocyclops scrassus Aedes aegypti and Aedes albopictus
[46]

3.3. Microbiota as Competitors of Mosquito Larvae. The com- metamorphosis. Further, they caused a small survival reduc-
petitors also can reduce the survival of mosquitoes by com- tion (21.9%) in Culex longiareolata, while not affecting time
peting for the same food resources. The term “competitors” to, or size at, pupation [57].
in relation to mosquitoes refers to invertebrate species who Ostracoda was identified as both predator and food com-
feed upon the same functional food like algae, bacteria, detri- petitor for mosquito larvae, and it shows a strong negative
tus, and protists, as mosquito larvae [49]. These competitors impact on larval development [54, 55, 58, 59]. The effects of
include mainly the species under Subphylum Crustacea, such ciliate protists and rotifers on lower trophic level microbial
as cladocerans (Phyllopoda), calanoids (Copepoda), harpac- food resources, such as bacteria, small flagellates, and organic
ticoids (Copepoda), and ostracods (Ostracoda) [50–52]; particles, in the water column, and on Cx. nigripalpus larval
and cause a negative impact on mosquito larval populations. development and adult production were studied in the recent
Naturally occurring microcrustaceans are potentially effec- past [60]. The authors indicated that ciliates and rotifers, sin-
tive competitors against mosquito larvae because many spe- gly or in combination, altered other microbial populations in
cies show similar biotope preferences with mosquito larvae mosquito breeding habitat and thereby inhibited Cx. nigri-
[53], and polyphagous activities of mosquito larvae and asso- palpus mosquito growth suggesting that instead of serving
ciated major competitors explain the abundance and coinha- as food resources, they competed with early instar mosquito
bitation of mosquito larvae in breeding habitats [17]. larvae for getting food items.
Kroeger et al. [54] highlighted that the larvae of Cx.
pipiens were found to be spatially associated with competing 3.4. Microbiota as Food Items for Developing Mosquito
Cladocera, and they prevent the Cx. pipiens colonization. The Larvae. Microbiota that inhabit aquatic habitats serve as food
same study showed Ostracods as abundant microcrustaceans organisms to developing mosquito larvae. Many undergo a
associated with ponds, and their dominance has inhibited the similar trend of surviving the ephemeral nature of the micro-
colonization of mosquito larvae in ponds. Nonmosquito habitats and eventually, when the conditions become favor-
competitors such as larvae of Chironomidae and cladocerans able, serve as competitors sometimes or food organisms to
were found to limit the abundance of An. quadrimaculatus mosquito larvae. Depending on the larval species, food items
and Cx. pipiens to a great extent in temporary ponds of include many microbiota species such as bacteria, fungi, and
Northwest Pennsylvania in the USA by Chase and Knight protists, diatoms, microcrustaceans, cyanobacteria, and uni-
[8]. cellular or filamentous algae [61, 62]. Protozoans and rotifers
The potential of cladocerans as controphic competitors are relatively smaller in their size in which 50-250 μm in
of the mosquito Cx. pipiens was studied [55] and revealed length coincides with the waterborne particles ingested by
that the oviposition of mosquitoes was fully inhibited under mosquito larvae while filter-feeding [63].
high densities of a cladoceran, Daphnia magna, and there The availability of sufficient food sources determines the
were consequently no mosquito larvae. Mosquito larvae in proliferation of mosquitoes, affecting them positively most of
the presence of cladocerans took two more days to emerge the time and negatively sometimes. Larval immature survi-
than where predators and competitions were absent [56]. vorship and their developmental rate depend on the quality
Daphnia magna did not significantly affect survival to the and quantity of their food. The mosquito adult emergence,
pupation of Cx. pipiens, but competing for food resources, body size, response to repellents and insecticides, survival,
it increased the time for metamorphosis and reduced size at sexual maturity, fecundity, egg production, and longevity of
BioMed Research International 5

the adult female and more importantly vector competence live cells/mL, respectively. However, larval production could
are also influenced by the availability of the food resources be reduced in the absence of some algal species as well. Bond
for larval development [64]. et al. [75] at Chiapas, Mexico, reported that An. pseudopunc-
There are at least 200 species of phytoplankton associated tipennis breeding was reduced by removing a filamentous
with mosquito breeding habitats, and larvae extensively feed chlorophyte green alga, Spirogyra, from their breeding sites.
upon them [65, 66]. Cyanobacteria have an important role in The extraction of this alga brought about a striking decline
the diet of mosquito larvae. Kaufman et al. [67] indicated the in the density of An. pseudopunctipennis larvae sustained
importance of algal biomass on the growth and development for about six weeks and thus a concurrent reduction in the
of An. gambiae larvae. Although most of the algal species are adult population.
nutritious food for many species of mosquito larvae, some Cyanobacteria, numerous unicellular and filamentous
species are able to kill the larvae if ingested in large quantities. algae, zooflagellates, and other protozoans, rotifers, crusta-
Sometimes, it is possible that they die due to starvation by ceans, organic debris, unspecified inorganic materials, spores,
feeding on indigestible algae. The vector mosquitoes have and insect scales were identified by the dissected guts of sev-
not developed resistance to these algal toxins. eral mosquito species belonging to five genera [76]. Dissec-
In particular, Cyanobacteria, the blue-green algae, are tions of the larvae of A. punctipennis, A. quadrimaculatus,
able to effect on larval mortality by virtue of toxicity, and and A. crucians showed that all three species were indiscrim-
some species of green algae (Order Chlorococcales) are able inate feeders and that none has a characteristic plankton food
to kill larvae by being indigestible. Microcystis sp. showed a in their guts, and the places in which A. punctipennis breeds
significant negative effect on developing mosquito larvae, throughout the season were identified as always deficient in
where the larvae grown in the presence of alga were signifi- plankton in which alimentary tracts of some contained only
cantly smaller. Further, species such as Kirchneriella, Scene- particles of clay and silica [77]. However, Kaufman et al.
desmus, Coelastrum, Selenastrum, Dactylococcus, and [67] indicated the importance of algal biomass to the growth
Tetrallantos were found virtually indigestible by Culex, and development of Anopheles gambiae larvae.
Aedes, and Anopheles mosquito larvae, thus reducing their
existence and failure to develop successfully in the water 3.5. Bacteria as Microbiota Associated with Mosquito
where certain species of closely related green algae in the Breeding Habitats. The bacteria in mosquito breeding waters
order Chlorococcales are the main source of food [42, 68]. can affect ovipositing mosquitoes, have effects on larval
Further, the green alga Kirchneriella irregularis could kill development, and can modify larval and adult mosquito gut
Ae. albopictus larvae in container breeding habitats in Hawaii bacterial composition [78]. Mosquitoes are exposed to a vari-
due to starvation as they were unable to digest Kirchneriella. ety of bacterial species in their habitats. Bacteria inhabiting in
In order to kill the larvae, there is no need for the Kirchner- larval habitats have been considered as the most important
iella to be highly abundant but abundant enough to predom- that comprise the food of mosquito larvae by previous studies
inate in larval guts to the exclusion of other food [42]. Marten carried out [61, 79, 80]. Bacteria act as the most abundant
[69] has reported that many species of Scenedesmus were microbiota present in mosquito larval diets and sometimes
found to kill the larvae. However, in a recent study done in can even be the major nutritional source for their growth
2017, Scenedesmus species were encountered from both lar- and development. Mosquito larval growth is possible in cul-
val gut and in larval habitats; its larvicidal property is yet to tures of bacteria alone [62].
be confirmed there [70]. Rozeboom [81] found that Aedes aegypti larvae could not
Rejmankova et al. [71] found that An. albimanus larval develop in bacteria-filtered water, revealing that bacteria are
densities in cyanobacteria (blue-green algae) mats were rela- indispensable for the mosquito larval development.
tively high in both wet and dry seasons, concluding that these Further, higher larval mortalities were observed in water
cyanobacteria mats provide suitable habitats for mosquito treated with antibiotics [82]. Besides, many bacteria have
larvae. The number of cyanobacterial cells ingested and been shown to either attract [83, 84] or repel (Juan [85])
digested by mosquito larvae was dependent on the cyanobac- gravid mosquitoes to potential breeding sites. Mosquitoes
terial strain and varied with the mosquito species associated preferred to oviposit on unmodified substrates from natural
[72]. Cyanobacteria species associated with Anopheles albi- larval habitats containing live microorganisms and microbial
manus larvae from southern Chiapas, Mexico, were studied populations in breeding sites. They were found to produce
and revealed the presence of Phormidium sp., Oscillatoria volatiles, specific bacteria-associated carboxylic acids and
sp., Aphanocapsa littoralis, P. animalis, Lyngbya lutea, and methyl esters that serve as potent oviposition stimulants for
Anabaena spiroides. However, Aphanocapsa littoralis were gravid Ae. aegypti [84]. However, oviposition was signifi-
associated with habitats of relatively lower larval abundance, cantly reduced when the bacterial colonies of Stenotropho-
and higher cyanobacteria abundance was observed from monas maltophilia was present and oviposition was neither
estuaries, irrigation canals, river margins, and mangrove reduced nor enhanced with the presence of bacterial species,
lagoons [73]. Pseudomonas putida or Pseudomonas alcaligenes (Juan [85]).
From a study carried out in Finland, Cyanobacterium Bacterial species that are present in mosquito larval hab-
Oscillatoria agardhii and Anabaena circinalis were found as itats are acquired from the aquatic larval stage, and they are
highly toxic to Aedes aegypti larvae [74]. Further, the toxin established in the midgut of mosquito larvae, exhibiting dif-
was found to be water-soluble, and fourth and second instar ferent functional tasks and retaining in the gut as symbiotic
larvae of A. aegypti showed 24 h LC50 values as 8.7 and 6.1 μg species. Many recent studies have used culture-dependent
6 BioMed Research International

Table 2: Other global records on microbiota associated with mosquito breeding habitats.

Identified microbiota species and effects on mosquito

Description on study References
larvae
(i) Protists: Paramecium caudatum, Pleurotricha sp.,
and Chlamydomonas reinhardtii
(ii) Rotifers: Brachionus plicatilis and Philodina sp.
(iii) Microcrustaceans: Ephemeroporous barroisi,
Microinvertebrates coinhabited with mosquito larvae
Bosmina longirostris, Daphnia pulex, Diaphanosoma
of Ae. vittatus, An. gambiae, Cx. macfiei, Cx.
birgei, Diaphanosoma brachyurum, Laptonopsis
perfidiosus, Cx. pipiens, and Cx. simpsoni were Obi et al. [17]
occidentalis, Macrothrix pulex, Macrothrix rosea,
identified from patchy rock pools on inselbergs within
Moinodaphnia macleayi, Moina macrocopa, Sida
Kaduna state, Nigeria
crystallina, Bradleystrandesia reticulata, Candona
intermedia, Candona parallela, Cypria obesa,
Heterocypris incongruens, Potamocypris hyboforma,
Cyclops sp., and Macrocyclops sp.
(i) Ciliates, rotifers, microcrustaceans (Cladocera,
Copepoda, and Ostracoda), isopods (Asellus)
(ii) Microcrustaceans were identified as the most
abundant and most frequently encountered
invertebrates
The associated invertebrate taxa with mosquito larvae (iii) The abundance of Aedes spp. was affected by the
were studied in temporary ponds of wetland areas in presence of Ceriodaphnia spp., Chydorus spp., Elono et al. [114]
Germany Daphnia spp., Simocephalus spp., Calanoida, and
larvae of Chironomidae as they competed efficiently
with mosquito larvae for food resources
(iv) Cyclopoida act as antagonists while Zygoptera
and Dytiscidae which were known as strict predators
exerted the smallest influence
Prevalence of microfauna associated with different (i) Coleps hirtus, Zoothamnium sp., Vorticella sp.,
Amarasinghe and
mosquito breeding habitats in Mawanella area in Sri Chaetonotus sp., Ichthydium sp., Lecane sp., and
Rathnayaka [115]
Lanka Rotaria sp.
(i) Three main taxa of algae were found,
Bacillariophyceae, Chlorophyceae, and
Cyanobacteria. The diversity of Bacillariophyceae was
higher in the larval habitats, and only Cyanobacteria
were positively related to the abundance of immature
stage of Ae. aegypti
Ecological characterization of Ae. aegypti larval
(ii) Oscillatoria, Dactylococcopsis, Nostoc, Synedra,
habitats in artificial water containers in Girardot, Garcia-Sánchez et al. [70]
Scenedesmus, Pinnularia, Cymbella, Meridium,
Colombia
Navicula, and Dictyosphaerium were identified as the
most abundant algal genera
(iii) Oscillatoria, which belonged to Cyanobacteria,
had the greatest abundance
(iv) The only zooplankton found were some rotifers,
in very small numbers, and in only a few samples
(i) Main variables associated with the presence of An.
Biotic factors associated with the presence of
arabiensis larvae in habitats were green algae and the
Anopheles arabiensis immatures and their abundance
Cyperaceae plant family Gouagna et al. [116]
in naturally occurring and manmade aquatic habitats
(ii) An. arabiensis larvae were associated with
at low altitudes in remote areas in Reunion Island
approximately 13 species of macroinvertebrates
Microbiota associated with irrigated rice fields in Sri (i) Identified 94 species of invertebrates belonged to
Bambaradeniya et al. [117]
Lanka 10 phyla
(i) Forty-five microbiota species/taxa from Gampaha
district and 44 microbiota species/taxa from
Ranasinghe and
Microbiota associated with a variety of mosquito Kurunegala district were identified which belonged to
Amarasinghe [33] and
breeding habitats in Kurunegala and Gampaha Amoebozoa, Arthropoda, Bacillariophyta,
Amarasinghe and
districts, Sri Lanka Ciliophora, Charophyta, Chlorophyta, Sarcodina,
Ranasinghe [32]
Cyanobacteria/Cyanophyta, Euglenozoa,
Ochrophyta/Heterokontophyta, and Rotifera
Charles et al. [118]
BioMed Research International 7

Table 2: Continued.

Identified microbiota species and effects on mosquito

Description on study References
larvae
(i) Had a greater proposition of species belonged to
the phylum Bacillariophyceae compared to other
species in the phyla of Chlorophyceae, Cyanophyceae,
Desmidaceae, and Euglenophyceae
Microbiota associated with mosquito larvae collected (ii) An. stephensi mosquito larvae were associated
from different larval habitats in Mysore with the filamentous chlorophyte green algae,
Spirogyra spp., which was served as food for them
(iii) Filamentous cyanobacterium, Oscillatoria
species, was encountered in breeding sources of Cx.
quinquefasciatus
Algae species associated with mosquito breeding (i) Anopheline larvae were strongly associated with
Wallace and Merritt [119]
habitats in Michigan state naturally occurring algae in their habitats

and culture-independent approaches to characterize the species that belonged to phylum Proteobacteria and Firmi-
microbial communities in different mosquito species includ- cutes [78]. In Thailand and Laos, a higher abundance of
ing Aedes, Culex, Anopheles, and Mansonia mosquitoes. The Escherichia coli in breeding waters was strongly correlated
members of Enterobacteriaceae (e.g., Enterobacter), Erwinia- to the presence of Ae. aegypti mosquitoes [113].
ceae (e.g., Pantoea), and Bacillaceae (e.g., Bacillus) have been
identified as the most frequently described bacteria from the 3.6. Other Records on Microbiota Associated with Mosquito
gut of adult Aedes spp. [86–90]. Several studies were con- Breeding Habitats. Many other microbiota species/taxa were
ducted on symbiotic bacteria in Anopheles mosquitoes and recorded from a variety of breeding habitats globally. They
species belonging to several genera; Pseudomonas, Alcali- have been summarized in Table 2.
genes, Bordetella, Myroides, Aeromonas, Acinetobacter, Bacil-
lus, Chryseobacterium, Delftia, Exiguobacterium, Kurthia, 4. Conclusion
Microbacterium, Staphylococcus, Thorsellia, and Variovorax
have been identified [91]. Besides, few studies about the bac- Potential biocontrol of mosquito larvae with naturally
teria species in vector mosquitoes have been conducted [92– occurring microbiota associated as predators/pathogens
95]. Extensive dispersal and evolutionary success of mosqui- and other biocontrol agents would be a more effective and
toes are widely motivated by these symbiotic relationships ecofriendly approach. Therefore, with the available litera-
with microbes and mosquito larval stages. Adult mosquitoes ture, it is evident that the abundance of mosquito larvae is
have been shown to contain gut bacteria found in their breed- inversely related to the densities of associated microbiota
ing waters [96, 97]. that are potential antagonists. Mosquito indigestible or toxic
These microbial communities and their roles in mosquito phytoplanktons could serve as a field characteristic agent
biology have been more broadly studied, and midgut micro- against mosquito larval control. To date, only a small num-
biota of mosquitoes were proven to play various important ber of species of the microbiota that inhabit in mosquito
roles in immunity, food digestion, fertility, and fecundity, breeding habitats have been recorded, and detailed studies
thereby affecting larval growth, adult fitness, vector popula- on microbiota assemblage in relation to diverse vector mos-
tions, and disease prevalence [98]. In addition, studies have quito breeding habitats and their association with mosquito
summarized the positive and negative effects of these gut larvae are few. Therefore, future studies on this ecological
microbial communities on vector competency through inter- aspect are encouraged. Such studies may help health
action with hosts and parasites [88, 99]. The resident bacteria researchers, entomologists, policy makers, and practitioners
were shown to promote or assist the gut infection of incom- for developing strategies for the management of vector mos-
ing pathogens of mosquitoes or augment the immune quito larvae.
responses of the mosquito [93, 100–107] or impair pathogen
infection through competition for resources [108]. Conflicts of Interest
Bacteria species associated with waters in a variety of
There are no conflicts of interests.
mosquito breeding habitats have been investigated from pre-
vious studies [97, 109–112]. Characterization of bacterial
communities in breeding waters of Anopheles darlingi in
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