Revista Brasileira de Entomologia Revista Brasileira de Entomologia
Rev Bras Entomol 2017;61:101-6 - Vol. 61 Núm.2 DOI: 10.1016/j.rbe.2017.03.005
Review
Host–parasite interaction and impact of mite infection on mosquito population
Atwa A. Atwaa, Anwar L. Bilgramia,, , , Ahmad I.M. Al-Saggafb
a King Abdulaziz University, Deanship of Scientific Research, Jeddah, Saudi Arabia
b King Abdulaziz University, Faculty of Sciences, Department of Biological Sciences, Jeddah, Saudi Arabia
Recebido 11 Janeiro 2017, Aceitaram 16 Março 2017
Abstract

During the present study, the host–parasite relationship between mosquitoes and parasitic mites was investigated. The 8954 individuals of male and female mosquitoes belonging to 26 genera: seven each of Aedes and Culex, six of Anopheles and one each of Toxorhynchites, Coquillettidia and Uranotaenia were collected from 200 sites. The male and female mosquitoes were collected from the State of Uttar Pradesh, located at 26.8500°N, 80.9100°E in North India by deploying Carbon dioxide-baited and gravid traps. The intensity of mite's infection, type and number of mites attached to mosquitoes, mite's preference for body parts and host sexes were the parameters used to determine host–parasite relationship. Eight species of mites: Arrenurus acuminatus, Ar. gibberifrons, Ar. danbyensis, Ar. madaraszi, Ar. kenki, Parathyas barbigera, Leptus sp., and Anystis sp., parasitized mosquitoes. Parasitic mites preferred host's thorax for attachment as compared to the head, pre-abdomen or appendages. The present study suggests phoretic relationship between parasitic mites and mosquitoes. Wide occurrence, intensity of infection, parasitic load, and attachment preferences of the mites suggested their positive role in biological control of adult mosquitoes. The present study will set the path of future studies on host–parasite relationships of mites and mosquitoes and define the role of parasitic mites in the biological control of mosquitoes.

Keywords
Mosquito, Mites, Host, Parasite, Infection, Biocontrol
Introduction

Aedes, Anopheles and Culex species of mosquitoes transmit diseases to humans and animals. They are most prevalent in developing and under developed countries, and spread diseases like malaria, dengue, chikungunya, yellow fever, filaria (Esteva et al., 2007). Despite decreasing incidence of human mortality, mosquito borne diseases are still the cause of serious health issues to over 214 million people (WHO, 2015) in developing and under developed countries.

Parasitic mites are ubiquitous and prevalent in the fresh-water habitats, their population density reaches up to 500 individuals with more than 50 species within 1m2 (Di Sabatinol et al., 2010). They parasitize insects, including mosquitoes and predate upon them. Larval mites of Arrenuridae, Thyasidae, Anystidae, Hydryphantidae (Mullen, 1975; Smith, 1983) are obligate parasites, which ingest hemolymph by piercing exoskeleton of the host (Smith et al., 2009; Gerson et al., 2003). Attached to mosquito pupae as parasite, the larval stages of mites transform to adults upon ecdysis (Smith and McLever, 1984). In contrast, Parathyas larvae attach to their hosts, when host returns to oviposit at the surface of the water (Mullen, 1997). Studies made by Lanciani and Boyt (1977), Lanciani and McLaughlin (1989), Rajendran and Prasad (1992), Nelson (1998), Sarkar et al. (1990), Mathieu et al. (2006), Esteva et al. (2007), Kirkhoff et al. (2013), and Worthen and Turner (2015) have generated significant interest in parasitic mites and their possible role in biological control of insects.

The biphasic (parasitic and predation) life cycle of parasitic mites consists of egg, pre-larva, larva, three nymphal stages and adult stage (Smith, 1988; Esteva et al., 2006). Parasitic mites hatch in the water, and attach to the host during emergence as a phoretic partner (Worthen and Turner, 2015). After completing parasitic phase, larval mites transform into deutonymph and adults, becoming predatory in nature and feeding upon insects and mosquitoes alike. Mites grasp and puncture prey-using chelicerae, secrete stylostome to feed on digested tissues (Smith, 1988) much like plant-parasitic nematodes, which make feeding-plugs to suck host contents (Bilgrami and Gaugler, 2004). Mites can also attach to previously uninfected adults through transfers during mating (Hussell et al., 2010). The larval development completes upon dropping of mites by insects, which return to water bodies, leaving scars as indicators of parasitism (Rolff et al., 2000). Mites grow in size (80–90 times) during feeding and up to 47 mite's infected one mosquito individual at a time (Mitchell, 1967; Kirkhoff et al., 2013), significantly enough to affect and reduce host diversity and mosquito population in the area.

The contacts between the mosquito and mite are co-incidental, except in some cases where chemical or other cues play a role (Mullen, 1997). The larval stages of terrestrial mites (e.g. Erthraeidae and Trombellidae) affect mosquito populations (Welbourn and Young, 1988; Southcolt, 1992), whereas others e.g. Charletonia and Leptus parasitize adult mosquitoes during inactive and resting phases (Wohltmann and Wendt, 1966).

The use of chemical pesticides impacts mosquito populations but alongside, it leaves toxic and adverse effects on human and animal populations. Parasitism (Mullen, 1975; Williams and Proctor, 1991; Gerson et al., 2003) and predation (Bilgrami and Tahseen, 1992; Bilgrami, 1994; Bilgrami, 1997a,b) are ecological interactions that may act alone or concomitantly during biological control process of the pests and vectors. Such is the relationship between mosquitoes and aquatic mites (Acari: Hydrachnidia) (Esteva et al., 2006).

A few options such as Bacillus thuringiensis, B. sphericus, and Gambusia affinis are available to biologically control mosquito larvae but none is available to use against adult mosquitoes. The parasitic mites possessing biological control potentials, few studies made on their biology and behavior, and the need of an effective biological control agent to control adult mosquitoes have led us to carry out this study.

The present study was made on the collected individuals of 23 species of mosquitoes in order to determine prevalence, parasitic load, host preference, attachment site preference, host–parasite relationships, and biological control potential of mites against adult mosquitoes.

Materials and methodsCollection of mosquitoes

The Carbon dioxide-baited and Gravid Traps were used to collect male and female mosquitoes from more than 200 sites in the State of Uttar Pradesh, located at 26.8500°N, 80.9100°E in North India. Each trap was set from dusk to dawn, once a week between May 1st and October 30th 2014. The following morning, mosquitoes were collected and mite infested mosquitoes were sorted out based on mosquito species and parasitic mites. Mosquito individuals infected by the mites were stored at −80°C for further analysis. No animal specimens were exported out of the country for any purpose. During present study, Toxorhynchites splendens, Uranotaenia compestris and Coquillettidia sp., are referred to as “others”, since they were not available in sufficient numbers. They are included in this study for comparison purposes.

Collection of parasitic mites

The parasitic mites carefully separated from mosquitoes, and preserved in the Alcohol-Glycerin-Acetic Acid solution (AGA) (Gibb and Oseto, 2006) for identification. Five to seven mites were mounted in AGA solution on a glass slide, under 12mm circular cover slip, in such a way that the legs of the mite stayed separated (Smith et al., 2009). Mites were identified by using taxonomic keys provided by Prasad and Cook (1972), Mullen (1974, 1975) and Pesic et al. (2010).

Analysis of host–parasite relationship

The infested mosquito individuals were examined for the intensity of mite infection, type and species of mites, number of mites attached, and preference for host species, sex and body parts. Mosquito–mite relationship was determined in terms of infection intensity (defined as the number of aquatic mites on a host individual) and the mean infection intensity (defined as the total number of parasitic mites divided by total number of parasitized hosts) (Margolis et al., 1982). Preference of mites for male or female mosquitoes was determined on the basis of the number of individuals parasitized. The attachment sites were grouped into five categories: head, thorax, pre-abdomen (between metathoracic and first abdominal segment), abdomen and appendages (legs and wings) (Kirkhoff et al., 2013).

Statistical analysis

Statistical analysis of the data was performed by using Ky-Plot version 2 (Yoshioga, 2002). Student's ‘t-test’ and Tukey's multiple range test were applied to determine significant differences at p0.05.

Results

A total number of 8954 individuals belonging to six mosquito genera and 23 species i.e., seven species each of Aedes and Culex, six of Anopheles and one each of Toxorhynchites, Coquillettidia and Uranotaenia were collected (Tables 1–4). From the collection, 43.73% mosquito individuals were parasitized by eight species of parasitic mites i.e., Arrenurus acuminatus, Ar. gibberifrons, Ar. kenki, Ar. danbyensis, Ar. madaraszi, Parathyas barbigera, Leptus sp., and Anystis sp. Fig. 1 shows Aedes sp., infected with Ar. danbyensis, Cx. pipiens infected with Ar. danbyensis, and Coquillettidia sp. with Leptus sp.

Table 1.

Aedes mosquitoes parasitized by mites.

Mosquito speciesa  Aedes albopictus  Aedes aegypti  Aedes pallidostriatus  Aedes pipersalatus  Aedes novalbopictus  Aedes vittatus  Aedes ramachandarai 
Number of mosquitoes collected  436  987  543  654  203  565  156 
Number of parasitized host  124  523  145  163  41  218  53 
Number of mites attached  533  2928  580  340  234  324  109 
Mean infection intensity  4.29  5.59  4.0  2.08  5.7  1.48  2.05 
Parasitic load  1–9  1–21  1–6  1–3  1–10  1–2  1–3 
Arrenurus acuminatus  113  85 
Arrenurus gibberifrons  63 
Arrenurus kenki  86  63 
Parathyas barbigera  533  2928  381  192  171  324  109 
a

Arrenurus danbayensis, A. madaraszi, Leptus sp. and Anystis sp. did not parasitize any mosquito species, hence not included in the table.

Table 2.

Anopheles mosquitoes parasitized by mites.

Mosquito speciesa  Anopheles barbarostris  Anopheles thomsoni  Anopheles minimus  Anopheles stephensi  Anopheles quinque-fasciatis  Anopheles culicifacies 
Number of mosquitoes collected  98  768  298  1267  432  165 
Number of parasitized host  14  226  161  543  121  51 
Number of mites attached  47  678  916  3974  454  213 
Mean infection intensity  3.35  3.0  5.68  7.31  3.75  4.17 
Parasitic load  1–4  1–6  1–9  1–12  1–16  1–6 
Arrenurus acuminatus  17  46  1697  244  164 
Arrenurus kenki  678  23 
Parathyas barbigera  30  870  2277  187  49 
a

Arrenurus danbayensis, A. gibberifrons, A. madaraszi, Leptus sp. and Anystis sp. did not parasitize any mosquito species, hence not included in the table.

Table 3.

Culex mosquitoes parasitized by mites.

Mosquito speciesa  Culex vishnui  Culex infula  Culex nigropuntatus  Culex pipiens fatigans  Culex malayi  Culex tritaenio-rhynchus  Culex bitritaeni-orhynchus 
Number of mosquitoes collected  301  431  308  786  109  213  64 
Number of parasitized host  213  321  175  543  34  106  29 
Number of mites attached  468  2562  987  1574  98  371  45 
Mean infection intensity  2.19  7.98  5.64  2.89  2.88  3.50  1.55 
Parasitic load  1–3  1–27  1–6  1–10  1–6  1–6  1–2 
Arrenurus acuminatus  987  347  18 
Arrenurus danbyensis  1824 
Arrenurus madaraszi  326 
Arrenurus kenki  468  517  64  371 
Parathyas barbigera  412  391  24  27 
Leptus sp.  67 
Anystis sp.  252 
a

Arrenurus gibberifrons did not parasitize any mosquito species, hence not included in the table.

Table 4.

Other species of mosquitoes parasitized by mites.

Mosquito speciesa  Toxorhynchitis splendens  Uranotaenia compestris  Coquillettidia Spp. 
Number of mosquitoes collected  23  65  82 
Number of parasitized host  19  29  64 
Number of mites attached  45  19  368 
Mean infection intensity  1.0  1.6  5.6 
Parasitic load  1–2  1–2  1–43 
Parathyas barbigera  45  19  368 
a

Arrenurus acuminatus, A. danbayensis, A. gibberifrons, A. madaraszi, A. kenki, Leptus sp. and Anystis sp., did not parasitize any mosquito species, hence not included in the table.

Fig. 1.
(0.54MB).

(A) Culex pipiens fatigans infected by Arrenurus danbyensis; (B and C) Coquillettidia sp. infected with Leptus sp.; (D) Aedes sp., infected with Arrenurus danbyensis.

Aedes parasitized by parasitic mites

Parathyas barbigera parasitized all species of Aedes. Arrenurus acuminatus and Ar. kenki parasitized Ae. pallidostriatus and Ae. pipersalatus whereas, Ar. gibberifrons infected Ae. novalbopictus (Table 1). Arrrenurus danbyensis, Ar. madaraszi, Leptus sp., and Anystis sp., did not parasitize any individual of Aedes.

Parathyas barbigera parasitized maximum number of Ae. aegypti (63.13%) with mean infection intensity of 5.59 (p0.05) and parasitic load of 1–21 (Table 1). Mites parasitized fewer individuals of Ae. albopictus (11.49%) but the mean infection intensity (4.29) and parasitic load (1–9) was significantly higher than other Aedes species. The other Aedes species were parasitized between 2.35 and 8.21% of the collected population, with mean infection rate and parasitic load ranging between 1.48–5.7 and 1–10 respectively (Table 1).

Anopheles parasitized by parasitic mites

Arrenurus acuminatus and Pr. barbigera parasitized all species of Anopheles mosquitoes except An. thompsoni (Table 2). The 67.30% of An. stephensi were parasitized with mean infection intensity of 7.30 and parasitic load of 1–12 (Table 2). In terms of parasitized individuals, An. thomsoni was the second most preferred mosquito species (20.00%) (p0.05), which carried less parasitic load (1–6) and mean infection intensity (3.0) as compared to other species of Anopheles. Arrenurus kenki was parasitic on An. thomsoni and An. quinquefasciatus. Anopheles barbarostris was least preferred with only 1.25% of it's population parasitized at the mean infection intensity of 3.35 and parasitic load of 1–4 (Table 2).

Culex parasitized by parasitic mites

Mites preferred Culex species more than others. Seven species of mites parasitized 64.24% of collected individuals of mosquitoes. Arrenurus kenki and Pr. barbigera, each was parasitic on four species of Culex. Arrenurus acuminatus, Ar. danbyensis, Ar. madaraszi and Anystis sp., each parasitized one species of Culex mosquito. Leptus sp., infected two species of Culex, whereas, Cx. pipiens was parasitized by four species of mites i.e., Ar. acuminatus, Pr. barbigera, Leptus sp. and Anystis sp., (Table 3). Culex infula was parasitized maximally (74.0%). The mean infection intensity on Cx. pipiens was second to Cx. nigropunctatus, where it was highest (7.98) (p0.05) with parasitic load ranging between 1 and 27. Mites preferred individuals of Cx. tritaeniorhynchus the least in terms of the number of host individuals parasitized (31.19%), mean infection rate (1.55) and parasitic load (1–2) (Table 3).

Other mosquitoes parasitized by parasitic mites

Parathyas barbigera parasitized 82.0% of Tx. splendens, 44.61% of Ur. compestris and 78.04% of Coquillettidia sp. (Table 1). The mean infection intensity (5.6) and parasitic load (1–43) was the highest for Coquillettidia sp., in this group (Table 4).

Preference for mosquito species

Mites parasitized Culex (64.02%) in greater numbers than Aedes (35.75%), Anopheles (36.45%) or Uranotaenia (44.0%) (p0.05) (Fig. 2). Mites also infected Toxorhynchites (82.0%) at higher numbers (p0.05) (Fig. 2), which may not be true representative of host preference behavior, since observations were based on fewer specimens. They are included in the study for comparison purposes.

Fig. 2.
(0.09MB).

Mosquitoes parasitized by mites. Tukey's multiple comparison tests were applied at 95% confidence to compare differences. Bars (±SE) with different letters show significant differences at p0.05. Bars without SE=no variations.

Preference of mites for attachment sites

Parasitic mites showed preferential rates of attachment to the host body parts. All species of mites attached maximally to the thorax (41.3–79.8%), as compared to the head (3.9–18.0%), pre-abdomen (4.3–28.6%) or appendages (0.9–4.8) (Fig. 3). The rate of attachment also varied with the species of mites. Anystis sp., attached to the thorax (79.8%) maximally as compared to other species of mites (p0.05) (Fig. 3).

Fig. 3.
(0.16MB).

Attachment preferences of mites for mosquito body parts. Bars show±SE, comparisons are made at 95% confidence using ANOVA. Bars without SE=no variations.

Sexual preference for attachment

All species of mites preferred female mosquitoes as the host (Fig. 4). Fewer than 6.5% of males were parasitized by various species of parasitic mites. No males, but all female individuals of Tx. splendens, Ur. compestris and Coquillettidia sp. were parasitized.

Fig. 4.
(0.07MB).

Attachment preference of mites for mosquito sexes. Bars show±SE, comparisons are made at 95% confidence using ANOVA. Bars without SE=no variations.

Discussion

To the best of our knowledge, this study presents the largest mosquito collection in order to study host–parasite relationships between mosquitoes and parasitic mites after Kirkhoff et al. (2013). It is also the first detailed study made on the host–parasite relationships of parasitic mites with mosquitoes in Asia.

Effective biological control agents possess several attributes of successful biological control agents (Spurrier, 1998; Bilgrami et al., 2005). Parasitic mites also possess beneficial traits such as wide spread occurrence, effective dispersal capability, moderate host preference, host body part preference for attachment, and significant parasitic load to make differences in mosquito populations as biological control agents.

The parasitic mites prefer to stay in the still or slow moving fresh water streams, as indicated by their association with 23 species of mosquito. Seven species each of Aedes and Anopheles, six of Culex and one each of Toxorhynchites, Uranotaenia and Coquillettidia were parasitized by different species of mites. The present study showed that five species of Arrenurus and one each of Parathyas, Leptus and Anystis were parasitic on Aedes, Anopheles, Culex, Toxorhynchites and Uranotaenia.

The density of mites depended upon the rain, available food, mosquito species and abundance of mosquito individuals. With one peak in the early mosquito season, density of mites remained high and plateau for some time before declining toward the end of the mosquito season (end of November, when low temperatures bring down populations of mites and mosquitoes), a phenomenon that was also observed by Spurrier (1998).

The mosquito life cycle i.e. univoltine or multivoltine may have played a role in host selection by the mites (Milne et al., 2008). In all likelihood, the rate of attachment of mites to emerging multivoltine mosquitoes with higher rates of fecundity should also be high. Mosquito females would return to oviposition sites multiple times in a single season, resulting in the increase of mosquito density many folds as compared to univoltine or other multivoltine species, which have low rates of fecundity. Therefore, mosquito density made differences in the host selection, parasitism and rate of attachment of mites. Host preference by parasitic mites depended upon host species, number of parasitized individuals, mean infection intensity and parasitic load of mites as evident during the present study. Such preferences explain adaptive mechanisms that allow larval mites to co-evolve successfully and parallel to their mosquito hosts (Martins, 2004). Anystis sp., terrestrial in nature, was found attached to the individuals of Cx. pipiens and Cx. malayi, and possibly transferred by males to females during mating (Hussell et al., 2010).

Parasitic mites hatch in water, float at the surface, climb and attach to the pupae (Worthen and Turner, 2015), they wait until pupae hatch and young adult mosquito emerges. The mites use their pedipalps to attach to mosquito individuals at the time of later's emergence. During or shortly after emergence, mosquito individuals have short spans of inactivity, sufficient for parasitic mites to attach to the host. Parasitic mites use chelicerae to cut host cuticle, whereas, some species of Arrenurus secrete adhesive secretions to construct a feeding tube (Martins, 2004).

Thorax, that emerges immediately after the head provides mites the maximum opportunity to attach (Smith, 1988; Kirkhoff et al., 2013). Should the sequence of emerging mosquito body parts play any role in preference of host body parts then the head should have the highest number of mites attached, nonetheless mites preferred mosquito thorax over other body parts. This has resulted due to prolonged exposure of thorax at the time of mosquito emergence at the water surface that has provided extended time to mites to attach. Similar to other organisms, physio-chemical factors such as texture of attachment site or chemicals eliciting mite's responses toward specific body parts also play an important role in differential rates of attachments. As is the case with other insects (Mitchell, 1967), timing of larval mite attachment to the adult host also play a significant role in determining where mite should attach to the host. Our findings are comparable to those of Sharma and Prasad (1998), who have observed 85% of parasitic mites preferring thorax, Milne et al. (2008), however, reported mite's preference for the host abdomen.

The parasitic load of mites varied from1.0 to 47/individual and the infection intensity from 1 to 7.98. In the present study, some mosquito species with moderate to heavy parasitic loads suggest that attached mites could hinder flight and dispersal of mosquitoes due to their weight, allowing mites to feed on the host and cause mortality. During the present study, no specific factor other than increased chances of contact between mite and host appeared to have played any role in the attachment process. Female mosquito individuals returning to habitat multiple times to oviposit have increased chances of mites to attach to female individuals, resulting in the attachment ratio of females to male as 95:5.

Arrenurus danbyensis could be a potential candidate of biological control, which have shown detrimental effects on Cq. perturbans and Aedes spp. (Smith and McLever, 1984). Our study also showed similar phenomenon, where Aedes, Culex and Anopheles species were parasitized by different species of mites. Arrenurus species have extreme detrimental effects in terms of its diversity, density and wide geographical presence as compared to other species of mites, Parathyas barbigera also showed similar promise, when it comes to the rates of infection intensity and parasitic loads at which they were attached.

In conclusion, parasitic mites i.e., Arrenurus, Parathyas, Anystis, and Leptus showing beneficial traits of biological control agent e.g. wide host range, population abundance, high rates of attachment, infection and infection intensities, suggest that they may play a significant role in mosquito biological control (Mitchell, 1967; Smith and McLever, 1984). How effective parasitic mites be in the adult mosquito depends on future studies investigating detrimental effects of mites, and studies on population dynamics, reproductive rates, dispersal capabilities, host specificity and distribution of mites with particular reference to adult mosquito population.

Conflicts of interest

The authors declare no conflict of interest.

Acknowledgements

The work was supported by the Deanship of Scientific Research (DSR), King Abdulaziz University, Jeddah, under grant No. (305-803-D1435). The authors, therefore, gratefully acknowledge the DSR technical and financial support.

References
Bilgrami, 1994
A.L. Bilgrami
Predatory behaviour of a nematode feeding mite Tyrophagus putrescentiae (Sarcoptiformes: Acridae)
Fundam. Appl. Nematol., 17 (1994), pp. 293-297
Bilgrami, 1997a
A.L. Bilgrami
Evaluation of the predation abilities of a nematode feeding mite, Hypoaspis calcuttaensis on plant and soil nematodes
Fundam. Appl. Nematol., 20 (1997), pp. 96-98
Bilgrami, 1997b
A.L. Bilgrami
Prey catching and feeding mechanisms of nematode feeding mites Hypoaspis calcuttaensis and Tyrophagus putrescentiae
Ann. Plant Protect. Sci., 5 (1997), pp. 90-93
Bilgrami and Gaugler, 2004
A.L. Bilgrami,R. Gaugler
Feeding behavior
Nematode Behaviour, pp. 91-126
Bilgrami et al., 2005
A.L. Bilgrami,R. Gaugler,C. Brey
Prey preference and feeding behavior of a diplogasterid predator Mononchoides gaugleri (Nematoda: Diplogasteridae)
Nematology, 7 (2005), pp. 333-342
Bilgrami and Tahseen, 1992
A.L. Bilgrami,Q. Tahseen
A nematode Feeding mite, Tyrophagus putrescentiae (Sarcoptiformis: Acaridae)
Fundam. Appl. Nematol., l5 (1992), pp. 477-478
Di Sabatinol et al., 2010
A.R. Di Sabatinol,R. Gerecke,R. Gledhill,T.H. Smit
The taxonomic status of the water mite genera Todothyas Cook and Parathyas Lundblad. Supplement to Di Sabatino et al. (2009)
Zootaxa, 2361 (2010), pp. 68
Esteva et al., 2006
L. Esteva,G. Rivas,H.M. Yang
Modelling parasitism and predation of mosquitoes by water mites
J. Math. Biol., 53 (2006), pp. 540-555 http://dx.doi.org/10.1007/s00285-006-0020-3
Esteva et al., 2007
L. Esteva,G. Rivas,H.M. Yang
Assessing the effects of parasitism and predation by water mites on the mosquitoes
TEMA, 8 (2007), pp. 63-72
Gibb and Oseto, 2006
T.J. Gibb,C.Y. Oseto
Arthropod Collection and Identification, Field and Laboratory Techniques
Academic Press, (2006)pp. 321
Gerson et al., 2003
U. Gerson,R.L. Smiley,R. Ochoa
Mites (Acari) for Pest Control
Wiley-Blackwell, (2003)pp. 560
Hussell et al., 2010
C. Hussell,C.D. Lowe,I.F. Harvey,P.C. Watts,D.J. Thompson
Phenology determines seasonal variation in ecto-parasitic loads in natural insect population
Ecol. Entomol., 35 (2010), pp. 514-522
Kirkhoff et al., 2013
C.J. Kirkhoff,T.W. Simmons,M. Hutchinson
Adult mosquitoes parasitized by larval water mites in Pennsylvania
J. Parasitol., 99 (2013), pp. 31-39 http://dx.doi.org/10.1645/GE-3105.1
Lanciani and Boyt, 1977
C.A. Lanciani,A.D. Boyt
The effect of parasitic water mite, Arrenurus pseudotenuicollis (Acari: Hydrochnellae) on the survival and reproduction of the mosquito Anopheles crucians (Diptera: Culicidae)
J. Med. Entomol., 14 (1977), pp. 10-15
Lanciani and McLaughlin, 1989
C.A. Lanciani,R.E. McLaughlin
Parasitism of Coquillettidia perturbans by two water mite species (Acari: Arrenuridae) in Florida
J. Am. Mosq. Control Assoc., 5 (1989), pp. 428-431
Margolis et al., 1982
L. Margolis,R.C. Anderson,J.C. Holmes
Recommended usage of selected terms in ecological and epidemiological parasitology
Can. Soc. Zool. Bull., 13 (1982), pp. 14
Martins, 2004
P. Martins
Specificity of attachment sites of larval water mites (Hydrachnidia, Acari) on their insect hosts (Chironomidae-Diptera) evidences from some streaming living species
Exp. Appl. Acarol., 34 (2004), pp. 95-112
Mathieu et al., 2006
B. Mathieu,L. Bertrand,V. Peyrusse,F. Scaffner,M. Bertrand
Culicidae and water mites: parasitism under Mediterranean climatic conditions
Acarologia, 47 (2006), pp. 55-61
Mitchell, 1967
R. Mitchell
Host exploitation of two closely related water mites
Evolution, 21 (1967), pp. 9-75
Milne et al., 2008
M.A. Milne,V.J. Townsend,P. Smelser,B.E. Felgenhauer,M.K. Moore,F.J. Smyth
Larval aquatic and terrestrial mites infesting a temperate assemblage of mosquitoes
Exp. Appl. Acarol., 47 (2008), pp. 19-33 http://dx.doi.org/10.1007/s10493-008-9194-2
Mullen, 1974
G.R. Mullen
Acrine parasites and mosquitoes. I. Illustrated larval key to the families and genera of mites reportedly found on mosquitoes
Mosq. News, 34 (1974), pp. 183-195
Mullen, 1975
G.R. Mullen
Acrine parasites and mosquitoes. II. A critical review of all known records of mosquitoes parasitized by mites
J. Med. Entomol., 12 (1975), pp. 27-36
Mullen, 1997
G.R. Mullen
Acarine parasites of mosquitoes IV. Taxonomy, life history and behavior of Thyas barbigera and Thyasides sphagnorum (Hydrachnelle: Thyasidae)
J. Med. Entomol., 13 (1997), pp. 475-485
Nelson, 1998
B.O. Nelson
The water mites Thyas barbigera (Hydrachnellae: Thyasidae) parasitizing mosquitoes
Eur. Mosq. Bull., 2 (1998), pp. 10-12
Pesic et al., 2010
V. Pesic,T. Chatterjee,S. Bordoiloi
A checklist of the water mites (Acari: Hydrachnidia) of India with new records and description of one new species
Zootaxa, 2617 (2010), pp. 1-54
Prasad and Cook, 1972
V. Prasad,D.R. Cook
The taxonomy of water mite larvae
Mem. Am. Entomol. Inst., 18 (1972), pp. 1-326
Rajendran and Prasad, 1992
R. Rajendran,R.S. Prasad
Influence of mite infestation on the longevity and fecundity of the mosquito Mansonia uniformis (Diptera: Insecta) under laboratory conditions
J. Biosci., 17 (1992), pp. 35-40
Rolff et al., 2000
J. Rolff,H. Aantvogel,I. Schrimpf
No correlation between parasitism and male mating success in a damselfly: why parasite behavior matters
J. Insect Behav., 13 (2000), pp. 563-571
Sarkar et al., 1990
P.K. Sarkar,D.R. Nath,P.P. Talikdar,P.R. Malhotra
Seasonal incidence of water mites (Arrenurus sp.) parasitizing mosquito vectors at Tezpur, Assam, India
Ind. J. Malariol., 27 (1990), pp. 121-126
Sharma and Prasad, 1998
S.N. Sharma,R.N. Prasad
Water mite (Arrenurus sp.) parasitizing mosquitoes in district Shahjahanpur, UP
Ind. J. Malariol., 29 (1998), pp. 255-258
Smith, 1983
B.P. Smith
The potential of mites as biological control agents of mosquitoes
Research Needs for Development of Biological Control of Pests of Mites, pp. 79-85
Smith, 1988
B.P. Smith
Host–parasite interaction and impact of larval water mites on insects
Ann. Rev. Entomol., 33 (1988), pp. 487-507
Smith et al., 2009
I.M. Smith,D.R. Cook,B.P. Smith
Water Mites (Hydrachnida) and Other Arachnids in Ecology and Classification of North American Freshwater Invertebrates, pp. 659
Smith and McLever, 1984
B.P. Smith,S.B. McLever
The impact of Arrenurus danbyensis Mullen (Acari: Prostigmata; Arrenuridae) on a population of Coquillettidia perturbans Walker (Diptera: Culicidae)
Can. J. Zool., 62 (1984), pp. 1121-1134
Southcolt, 1992
R.V. Southcolt
Revision of the larva of Leptus (Acrina: Trombidiidae) of Europe and North America, with descriptions of post-larval instars
Zool. J. Linn. Soc., 105 (1992), pp. 1-153
Spurrier, 1998
M.F. Spurrier
Mite parasitism of mosquitoes in central Wyoming
Gt. Basin Nat., 58 (1998), pp. 184-187
Welbourn and Young, 1988
C.R. Welbourn,O.P. Young
Mites parasitic on spiders with a description of a new species of Eutrombidium (Acari: Eutrombiidae)
J. Arachnol., 16 (1988), pp. 373-385
Williams and Proctor, 1991
C.R. Williams,F.E. Proctor
Parasitism of mosquitoes (Diptera: Culicidae) by larval mites (Acari: Parasitengona) in Adelaid Australia
Aus. J. Entomol., 41 (1991), pp. 161-163
Wohltmann and Wendt, 1966
A. Wohltmann,F.E. Wendt
Observations on the biology of two hygrobiotic trombidioid (Acari: Prostigmata: Parasitengonae), with special regard to host recognition and parasitism tactics
Acarologia, 37 (1966), pp. 31-44
WHO, 2015
World Health Organization
Malaria
(2015)
Available at: http://www.who.int/malaria/en/ (accessed 20.07.16)
Worthen and Turner, 2015
W.B. Worthen,L. Turner
The effects of odonate species abundance and diversity on parasitism by water mites (Arrenurus spp.): testing the dilution effect
Int. J. Odontol., 18 (2015), pp. 233-248
Yoshioga, 2002
Yoshioga, K. (2002). Available at http://link.springer.com/chapter/10.1007%2F978-3-642-57489-4_4#close (accessed on 20.07.16). DOI: 10.1007/978-3-642-57489-4_4.
Corresponding author. (Anwar L. Bilgrami alegman@kau.edu.sa)
Copyright © 2017. Sociedade Brasileira de Entomologia
Rev Bras Entomol 2017;61:101-6 - Vol. 61 Núm.2 DOI: 10.1016/j.rbe.2017.03.005