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. 2016 Jan 5;10(2):252–257.

Odonate Nymphs: Generalist Predators and Their Potential in the Management of Dengue Mosquito, Aedes aegypti (Diptera: Culicidae)

Waseem Akram 1, Hafiz Azhar Ali-Khan 2,*
PMCID: PMC4906764  PMID: 27308283

Abstract

Background:

Dengue is amongst the most serious mosquito-borne infectious disease with hot spots in tropical and subtropical parts of the world. Unfortunately, no licensed vaccine for the disease is currently available in medicine markets. The only option available is the management of dengue vector mosquito, Aedes aegypti (Diptera: Culicidae).

Method:

Predatory potential of five odonate nymphs namely Anax parthenope, Bradinopyga geminate, Ischnura forcipata, Rhinocypha quadrimaculata, and Orthetrum sabina were evaluated against the 4th instar larvae of the dengue vector mosquito, Aedes aegypti, under laboratory conditions. The consumption of the mosquito larvae was evaluated at three water volume levels viz., 1 liter, 2 liter and 3 liter.

Results:

The number of Ae. aegypti larvae consumed varied significantly among the five species, and at different levels of water volume (P< 0.01). However, the interaction between odonate nymphs and the water volumes was statistically non-significant (P> 0.05). Ischnura forcipata consumed the highest number of Ae. aegypti larvae (n=56) followed by A. parthenope (n=47) and B. geminate (n=46). The number of larvae consumed was decreased with increasing search area or water volume, and the highest predation was observed at 1-liter water volume.

Conclusion:

The odonate nymphs could be a good source of biological agents for the management of the mosquitoes at larval stages.

Keywords: Biological control, Dragonflies, Damselflies, Mosquitoes, Dengue vectors

Introduction

Dengue is amongst the most serious mosquito-borne infectious disease with hot spots in tropical and subtropical parts of the world. Unfortunately, no licensed vaccine for the disease is currently available in medicine markets (Kovendan et al. 2012). The only option available is the management of the mosquito, Aedes aegypti (Diptera: Culicidae), which is a vector of deadly diseases like dengue fever, chikungunya and yellow fever (Khan and Akram 2013). Different chemical measures such as indoor residual sprays, larviciding, insecticide treated bed nets and fogging are prioritized for the management of dengue mosquitoes worldwide (Zia et al. 2012), however, these measures are linked with serious environmental concerns like the development of insecticide resistance and environmental pollution (Bilal et al. 2012). Moreover, recent reports on the development of insecticide resistance in different mosquito species including dengue vector mosquitoes (Khan et al. 2011, Rathore et al. 2013) stress the need to explore alternate measures. Naturally, occurring aquatic predators have been assumed a significant ecological factor in regulating different mosquito species. For example, the predators such as amphibians (Ohba et al. 2010), copepods (Marten and Reid 2007), crustaceans (Su and Mulla 2002), odonates (Mandal et al. 2008), water bugs (Aditya et al. 2004), wolf spiders (Futami et al. 2008) and backswimmers (Rodriguez-Castro et al. 2006) have shown their tendency to feed on and regulate different mosquito species in aquatic habitats like ponds and paddy fields (Kweka et al. 2011).

Of these stated predators, odonates (Insecta: Odonata) have been explored less for their predatory potential both in the Asian and world perspective (Mandal et al. 2008). To the best of authors’ knowledge, aquatic predators, particularly odonate nymphs have not been explored to much extent against mosquitoes in Pakistan. The odonate nymphs usually co-exist with many mosquito species immatures, and their long nymphal stage (1 year or more) and competitive predatory ability (Corbet 1980), offer a good opportunity to use them as biological agents.

Therefore, the present study focused on the comparative evaluation of predatory potential of the different odonate nymphs against the larvae of Ae. aegypti. The results presented provide a baseline for the field experiments, and possibility to include these predators in environment friendly management plans for the mosquito control.

Materials and Methods

A field collected population of Ae. aegypti from Lahore (31° 32′ 59 N; 74° 20′ 37 E) was reared under laboratory conditions (25± 2°C, 65± 5% RH) as described previously (Khan et al. 2011). Briefly, the mosquito larvae and adults were collected from artificial containers and natural habitats and reared in the laboratory by standard rearing procedures. The larvae were reared in steel trays approximately 3 inch deep and fed on Tetramin (artificial diet) until the adults emerged. Early-instar naiads/nymphs of five odonate species (Insecta: Odonata) namely Anax parthenope (Family Aeshnidae), Bradinopyga geminate (Libellulidae), Ischnura forcipata (Coenagrionidae), Rhinocypha quadrimaculata (Chlorocyphidae), and Orthetrum sabina (Libellulidae) were collected from ponds and rice fields by using aquatic dip nets. The nymphs were identified by following Fraser (1933), Anjum (1997) and Nesemann et al. (2011), and were kept in distilled water under the laboratory conditions. Before predation experiments, the nymphs were provided Chironomid larvae for feeding.

A feeding bioassay was performed by following the methodology of Mandal et al. (2008) with some modifications. Before starting the experiment, the nymphs were starved for a period of 6 hours. A single nymph of each odonate species was introduced into water bowl (4-liter capacity) containing distilled water and one hundred 4th instar larvae of Ae. aegypti. The consumption rate of the nymphs was evaluated at three different water levels viz., 1 liter, 2 liter and 3 liter, and the number of mosquito larvae consumed was noted after 24 h of the introduction of the nymphs into the bowl. The experiment was replicated at six different times, using the new nymphs and mosquito larvae.

All the data on consumption rate by the odonate nymphs at three different water levels were analyzed by 2-way analysis of variance using the software Statistix 8.1v (Analytical software 2005) and means were compared with the least significant difference test. P< 0.005 was considered signifant.

Results

The number of Ae. aegypti larvae consumed varied significantly among the five species of odonate nymphs (F= 144.30, df= 4, 75, P<0.001), and at different levels of water volume (F= 18.32, df= 2, 75, P< 0.001). However, the interaction between odonate nymphs and the water volumes was statistically non-significant (F= 0.32, df= 8, 75, P= 0.96). Ischnura forcipata consumed the highest amount of Ae. aegypti larvae (55.89) followed by A. parthenope (47.22) and B. geminate (46.06) (Fig. 1). The number of larvae consumed by different odonate species was decreased with increasing search area or water volume. The highest consumption of the larvae was observed at 1 liter water volume (46.90) followed by 2 liter (44.56) and 3 liter (42.27) volumes (Fig. 2).

Fig. 1.

Fig. 1.

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Rate of consumption of 4th instar Aedes aegypti larvae by different odonate nymphs

Fig. 2.

Fig. 2.

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Cumulative effect of different different water volumes on the consumption rate of 4th instar Aedes aegypti larvae by different odonate nymphs

Discussion

In the present study, predatory potential of five different odonate nymphs has been evaluated. The predator-prey relationship could have a significant impact in an ecosystem by affecting population dynamics and energy flow through food webs. Predators could affect prey populations directly through prey consumption (Khan et al. 2012). The only mosquito species, which have been investigated in the present study, is Ae. aegypti.

Recently this species along with Ae. albopictus played havoc in different parts of Pakistan. To manage these pests different measures have been adopted with the major focus on chemical control. Resultantly, occurrence of field evolved resistance in mosquitoes and other public health pests have been reported which stressed the need to explore alternate management tools (Khan et al. 2011, Khan et al. 2013).

In the present study, predatory potential of five different odonate nymphs has been evaluated. The results showed that the nymphs were able to consume Ae. aegypti voraciously, however, increasing the volume of water had a negative effect on the consumption rate, perhaps due to the evasion tactics of the mosquito larvae (Bhattacharjee et al. 2009). Since Ae. aegypti mosquitoes usually lay eggs and complete immature stages in small water volumes (Vezzani et al. 2005), the findings of the study are of worth importance. Previously, some researchers have evaluated the potential of odonate species against different mosquito species (Mandal et al. 2008, Kweka et al. 2011) but such studies are rare in Pakistan. Our results are in agreement with those of Mandal et al. (2008) who evaluated different species of odonates against Cx. quinquefasciatus and found that I. forcipata was the most voracious feeder of the mosquito larvae. They further reported that the volume of the water had a negative impact on predation efficiency.

The negative effect of increasing water volume has also observed with hemipteran bug species (Saha et al. 2008) and larvivorous fish species (Ghosh et al. 2005, Bhattacharjee et al. 2009). With increasing water volume, the aquatic predators possibly required more time to search, capture and ultimately consume the mosquito larvae (Ghosh et al. 2006). In Myanmar (Sebastian et al. 1990) and India (Mandal et al. 2008) the augmentative releases of different odonate species have regulated Ae. aegypti and Cx. quinquefasciatus mosquitoes, respectively. The lengthened developmental time of odonate nymphs (i.e. 1 year or more from egg to adult) and predation ability (Corbet 1980) provide an opportunity to use these predators in the management plans designed for Ae. aygypti.

Conclusion

Keeping in view the high consumption rate of the larvae per 24 h, these predators could be assumed to feed on a good number of Ae. aegypti larvae during their long nymphal stage. Although the species used in the present study varied in their consumption rate, all of the species could be considered for inclusion in the management plan. However, there is a need to explore the predatory potential of the species in the field and in different ecological zones.

Acknowledgements

The authors declare that there is no conflict of interests.

References

  1. Aditya G, Bhattacharyya S, Kundu N, Saha GK, Raut SK. (2004) Predatory efficiency of the water bug Sphaerodema annulatum on mosquito larvae (Culex quinquefasciatus) and its effect on the adult emergence. Bioresour Technol. 95: 169– 172. [DOI] [PubMed] [Google Scholar]
  2. Analytical Software , Statistix version 8.1: User’s manual. Analytical Software, Tallahassee, Florida, 2005. [Google Scholar]
  3. Anjum SA. (1997) Biosystematics of Odonata naiads of the Punjab by rearing technique. [M.Sc. thesis]. University of Agriculture, Faisalabad, Pakistan. [Google Scholar]
  4. Bhattacharjee I, Aditya G, Chandra G. (2009) Laboratory and field assessment of the potential of larvivorous, air-breathing fishes as predators of culicine mosquitoes. Biol Control. 49: 126– 133. [Google Scholar]
  5. Bilal H, Akram W, Khan HAA, Hassan SA, Khan IA. (2012) Toxicity of selected indigenous plant extracts against Aedes albopictus (Diptera: Culicidae). A potential dengue vector in dengue positive areas. Pak J Zool. 43: 371– 375. [Google Scholar]
  6. Corbet PS. (1980) Biology of odonata. Annu Rev Entomol. 25: 189– 218. [Google Scholar]
  7. Fraser FC. (1933) Fauna of British India including Ceylon and Burma, vol. 1–3 Odonata Taylor and Francis, London. [Google Scholar]
  8. Futami K, Sonye G, Akweywa P, Kaneko S, Minakawa N. (2008) Diving behavior in Anopheles gambiae (Diptera: Culicidae): avoidance of a predacious wolf spider (Araneae: Lycosidae) in relation to life stage and water depth. J Med Entomol. 45: 1050– 1056. [DOI] [PubMed] [Google Scholar]
  9. Ghosh A, Mondal S, Bhattacharjee I, Chandra G. (2005) Biological control of vector mosquitoes by some common exotic fish predators. Turk J Biol. 29: 167– 171. [Google Scholar]
  10. Ghosh A, Bhattacharjee I, Chandra G. (2006) Biocontrol efficacy by Oreochromis niloticus niloticus. J Appl Zool Res. 17: 114– 116. [Google Scholar]
  11. Jeffery JAL, Clements ACA, Nguyen YT, Nguyen LH, Tran SH, Le NT, Vu NS, Ryan PA, Kay PH. (2012) Water Level Flux in Household Containers in Vietnam-A Key Determinant of Aedes aegypti Population Dynamics. PLoS ONE. 7: e39067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Khan HAA, Akram W, Shehzad K, Shaalan EAS. (2011) First report of field evolved resistance to agrochemicals in dengue mosquito, Aedes albopictus (Diptera: Culicidae), from Pakistan. Parasit Vectors. 4: 146. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Khan HAA, Sayyed AH, Akram W, Raza S, Ali M. (2012) Predatory potential of Chrysoperla carnea and Cryptolaemus montrouzieri larvae on different stages of the mealybug, Phenacoccus solenopsis: A threat to cotton in South Asia. J Insect Sci. 12: 1– 12. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Khan HAA, Akram W. (2013) Citrus-based essential oils could be used for dengue vector mosquitoes control. Asian Pac J Trop Med. 6: 504. [DOI] [PubMed] [Google Scholar]
  15. Khan HAA, Shad SA, Akram W. (2013) Resistance to new chemical insecticides in the house fly, Musca domestica L., from dairies in Punjab, Pakistan. Parasitol Res. 112: 2049– 2054. [DOI] [PubMed] [Google Scholar]
  16. Kovendan K, Murugan K, Vincent S. (2012) Evaluation of larvicidal activity of Acalypha alnifolia Klein ex Willd. (Euphorbiaceae) leaf extract against the malarial vector, Anopheles stephensi, dengue vector, Aedes aegypti and Bancroftian filariasis vector, Culex quinquefasciatus (Diptera: Culicidae). Parasitol Res. 110: 571– 581. [DOI] [PubMed] [Google Scholar]
  17. Kweka EJ, Zhou G, Gilbreath TM, Afrane Y, Nyindo M, Githeko AK, Yan G. (2011) Predation efficiency of Anopheles gambiae larvae by aquatic predators in western Kenya highlands. Parasit Vectors. 4: 128. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Mandal SK, Ghosh A, Bhattacharjee I, Chandra G. (2008) Biocontrol efficiency of odonate nymphs against larvae of the mosquito, Culex quinqu-efasciatus Say, 1823. Acta Trop. 106: 109– 114. [DOI] [PubMed] [Google Scholar]
  19. Marten GG, Reid JW. (2007) Cyclopoid copepods. J Am Mosq Control Assoc. 23: 65– 92. [DOI] [PubMed] [Google Scholar]
  20. Nesemann H, Shah RDT, Shah DN. (2011) Key to the larval stages of common Odonata of Hindu Kush Himalaya, with short notes on habitats and ecology. J Threat Taxa 3: 2045– 2060. [Google Scholar]
  21. Ohba SY, Kawada H, Dida GO, Juma D, Sonye G, Minakawa N, T M. (2010) Predators of Anopheles gambiae sensu lato (Diptera: Culicidae) larvae in wetlands, western Kenya: confirmation by polymerase chain reaction method. J Med Entomol. 47: 783– 787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Rathore HR, Nadeem G, Khan IA. (2013) Pesticide susceptibility status of Anopheles mosquitoes in four flood-affected districts of South Punjab, Pakistan. Vector Borne Zoonotic Dis. 13: 60– 66. [DOI] [PubMed] [Google Scholar]
  23. Rodriguez-Castro VA, Quiroz-Martinez H, Solis-Rojas H, Tejada LO. (2006) Mass rearing and egg release of Buenoa scimitra Bare as biocontrol of larval Culex quinquefasciatus. J Am Mosq Control Assoc. 22: 123– 125. [DOI] [PubMed] [Google Scholar]
  24. Saha N, Aditya G, Bal A, Saha GK. (2008) Influence of light and habitat on predation of Culex quinquefasciatus (Diptera: Culicidae) larvae by the waterbugs (Hemiptera: Heteroptera). Insect Sci. 15: 461– 469. [Google Scholar]
  25. Sebastian A, Sein MM, Thu MM, Corbet PS. (1990) Suppression of Aedes aegypti (Diptera: Culicidae) using augmentative release of dragonfly larvae (Odonata: Libellulidae) with community participation in Yangon, Myanmar. Bull Entomol Res. 80: 223– 232. [Google Scholar]
  26. Su T, Mulla MS. (2002) Spatial occurrence and hatch of field eggs of the tadpole shrimp Triops newberryi (Notostraca: Triopsidae), a potential biological control agent of immature mosquitoes. J Vector Ecol. 27: 128– 137. [PubMed] [Google Scholar]
  27. Vezzani D, Rubioa A, Velazquez SM, Schweigmanna N, Wiegand T. (2005) Detailed assessment of microhabitat suitability for Aedes aegypti (Diptera: Culicidae) in Buenos Aires, Argentina. Acta Trop. 95: 123– 131. [DOI] [PubMed] [Google Scholar]
  28. Zia K, Hafeez F, Ashfaq M, Akram W, Khan HAA. (2012) Larvicidal action of four indigenous plant extracts against dengue vector Aedes aegypti. Pak Entomol. 31: 93– 97. [Google Scholar]

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