Anyaele Okorie & Obembe Abiodun

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J Vector Borne Dis 47, September 2010, pp. 181–184Laboratory evaluation of the biocontrol potential of Aphyosemiongularis against Anopheles larvaeAnyaele Okorie & Obembe AbiodunDepartment of Zoology, University of Ibadan, Oyo State, NigeriaKey words Anopheles; Aphyosemion gularis; biological control; larvivorous fish; malariaLarvivorous fish have been employed as biocontrolagents of mosquito larvae in several countries acrossthe world including Iran1, Argentina2, Australia3,Turkey4 and India5,6. Despite the fact that this vectorcontrol strategy is simple, relatively inexpensive andtherefore, particularly suitable for the Africansituation, information concerning its application inNigeria is scarcely available. The genus Aphyosemionbelongs to the family Cyprinodontidae and iscommonly called toothed carp, or topminnow. TheAphyosemion gularis (Synonyms: Aphyosemionsjoestedti, Fundulopanchax sjoestedti) otherwisecalled blue gularis belongs to the group of fishregarded as killifish and is indigenous to tropicaland sub-tropical Africa. Although World HealthOrganization7,  mentioned Aphyosemion as one ofthe annual killifishes noted to have drought resistanteggs, recent work classified them as semi-annualbecause they can be water incubated and live longerthan the annuals in areas which sometimes dry out tomoist mud, but at other times retain water throughoutthe dry season8.Three species, namely Aphyosemion gardneri, A.arnoldi and A. gularis have been described as part ofthe freshwater fishes in Nigeria. According to Umeh9,the three species have similar dietary and ecologicalcharacteristics, and are commonly found during thedry season at the surface of small bodies of stagnantwater of rain forest pools, ponds and streams wheredead leaves are abundant at the bottom. Umeh9 alsoclassified them as larvivorous, with their diet includingmosquito larvae and pupae, detritus and other smallterrestrial insects that fall on water surface. A. gularisare substrate spawners which could sometimes spawnon aquatic weeds and the eggs can hatch in 16–18days after they are laid10. Having drought resistanteggs that can be water incubated and the ability tosurvive for longer periods compared to the annuals arefeatures that can make them survive in both temporaryand permanent pools where mosquitoes easily breed.However, their larvivorous potential against noxiousinsects like mosquitoes have not been assessed. Inorder to complement the existing control measures inthe country, this work was undertaken to evaluate thebiocontrol potential of this native Nigerian fishspecies, against Anopheles mosquito larvae.Anopheles mosquito larvae were collected fromshallow pools and depressions within Ibadanmetropolis with a dipper. Only the III and IV instarlarvae were selected for the feeding experiments.A. gularis found naturally in some canals and pondswere collected with a mesh aquatic net at Ojoo(3o54’44.23" E and 7o27’38.83" N) and Beere(3o54’00.68" E and 7o22’32.92" N) in Ibadan,Nigeria. The fish identification was based on thetaxonomic keys of Umeh9. All the fish wereacclimatized under laboratory conditions over a threemonth period before the experiment and were fedwith commercially available fish feed and mosquitolarvae occasionally. Prior to the experiments, the totallength and weight measurements were taken  andbased on these two measurements, the fish wereseparated into two main groups, namely large (3.5–4.5 cm, 0.47 ± 0.18 g) and small (1.5–2.5 cm, 0.04 ±0.02 g). After the three months acclimatizationperiod, the experiments were carried out in glass J  VECTOR  BORNE  DIS  47, JUNE 2010 182Fig. 1: Percentage predation of Anopheles larvae by thelarge and small fish groups in the 12 h light period.aquaria (22×16×16 cm) containing de-chlorinatedwater (temperature 26–31oC and pH 6.48–6.94). Theprocedures of Ungureanu et al11 were adopted forthe laboratory feeding experiments. Five fish of thesame size group were placed in separate glass aquariacontaining 2 L of de-chlorinated water, 24 h prior tothe start of the experiment. In order to standardizetheir hunger level, the fish were not fed during thisperiod. Each group of five size-matched fish wasoffered III and IV instar of Anopheles larvae at threeseparate densities of 50, 150 and 250. Each preydensity had four replicates and the number of larvaeconsumed by each fish group was recorded separatelyat 3 h interval after which the number of larvaeconsumed was replenished in each of the aquariumto maintain the prey density for another interval. Theobservations of prey consumption were categorizedinto 12 h light and dark periods each comprising of 4intervals. Student’s t-test was used to compare thevarious result obtained.The total percentage predation of the three differentdensities of Anopheles larvae by the large and smallfish groups in the 12 h light and 12 h dark periodsare summarized respectively in Figs. 1 and 2. At thelarval density of 50, where a total of 200 Anopheleslarvae were presented to the two fish groupsthroughout the 12 h light period, 100±0% larvalconsumption was observed for the large fish group,while the small group consumed 86±3.63% (Fig. 1).However, at the larval density of 150, where a totalof 600 Anopheles larvae were presented, the largefish group still showed 100 ± 0.57% Anopheles larvalconsumption while the larval consumption by thesmall fish group decreased to 37 ± 23.29%. At 250larval density, where a total of 1000 Anopheles larvaewere presented, the total percentage of larvaeconsumed by the large and small fish groups  was79±14.03 and 13±8.03% respectively (Fig. 1).On the other hand, during the 12 h dark period, atthe larval density of 50 where  a total of 200Anopheles larvae were presented separately to eachgroup, the large fish group consumed 100±0% ofthe Anopheles larvae  while the small fish groupconsumed only 43±15.23% (Fig. 2). At the larvaldensity of 150, where a total of 600 Anopheles larvaewere presented to each group, the large fish groupstill consumed 100±0.57% of the Anopheles larvaewhile the small fish group consumed 30±17.12%.Whereas, at 250 larval density, where a total of 1000Anopheles larvae were presented to each group, thetotal consumption by the large and small fish groupswere 74±25.61 and 11±14.34% respectively (Fig. 2).The results indicate that the number of larvae con-sumed by the large fish at a larval density of 50 were1.16 and 2.33 times higher compared to that of thesmall fish in the light and dark periods respectively.At 150 larval density, larval consumption of the largeFig. 2: Percentage predation of Anopheles larvae by the largeand small fish groups in the 12 h dark period. 183 OKORIE & ABIODUN : BIOCONTROL POTENTIAL OF A. GULARISfish were respectively 2.68 and 3.31 times highercompared to that of the small fish group in the lightand dark periods. Whereas at 250 larval density, thelarge fish respectively consumed 6.01 and 6.88 timeshigher than that of small fish group in the light anddark periods. Statistically, at all larval densities, ex-cept 50, the difference between the number of larvaeconsumed by the large and small fish groups werefound to be significant (p<0.05). This exception couldhave resulted from the innate predatory ability of thefish species against Anopheles mosquito larvae mak-ing even the small sized group to feed effectively ona considerable number of the late stages (III and IVinstars) of the larvae. These small sized fish grouphowever became overwhelmed at the larval densityof 150 and 250 because they could only consumeand digest a limited number of larvae per time. Atthe larval density of 150 where the small fish groupwere overwhelmed, the large fish group on the otherhand, consumed all the larvae presented to them per-haps because they have larger stomach storage cham-ber and can digest more per unit time. The small fishgroup therefore tends to get filled easily after con-suming relatively less number of larvae. It impliesthat all adult males which are normally smaller thanthe mature females will feed on less number of lar-vae. This suggests that mature adult female fish aremore voracious and have higher biocontrol potentialcompared to the males and other juveniles.Keeping in mind that a single vector is capable oftransmitting the malaria disease, it is necessary toensure that none of the vector escapes. Therefore,the implication of these results for Anopheles mos-quito control is that in a situation where only thesmall fish are present, then a larger population ofthis group would be required to achieve total con-trol of a considerably high Anopheles larval popula-tion density in practical field applications.In accordance with the findings of Yildirim andKaracuha4 and Manna et al6, the results of this worktherefore indicate that the larval consumption in-creased in relation to the fish size. Moreover, thenumbers of Anopheles larvae consumed by the fishhere is greater when compared with those observedin other laboratory experiments where fishes of thesame size range such as Danio rerio and Gambusiaaffinis were used as reported respectively by Sharmaand Ghosh12 and Chatterjee and Chandra13.  Fur-thermore, in comparison with the adult sizes of othercommonly known larvivorous fish species such asOsphronemus gorami, which is up to 80 cm inlength14 and Pseudotropheus tropheops, which isabout 20 cm in length15, A. gularis is smaller in size,making them to have a very reduced food value andhence unattractive to the general public for nutri-tional and/or economic purposes. In addition, thisfish is native to West Africa where malaria is en-demic and is therefore not likely to cause any ad-verse ecological consequences when introduced tothe waters in the region.  According to WHO7, thenative Aphyosemion species also produce droughtresistant eggs. These qualities, thus, confer on it anadvantage as a biological control agent of mosquitolarvae compared to the other ones mentioned aboveespecially in temporary mosquito breeding sites.The study also revealed that larval consumption in-creased with increase in larval density until satiationlevel is reached when the fish became overwhelmed.This finding is in consonance with the work ofWillems et al3 who reported that the consumptionof Culex larvae by Pseudomugil signifer and G.holbrooki increased with increased density until theybecame overwhelmed at highest larval density of 200.The implication of this to field application is that inbreeding sites of high larval population densities,commensurate number of fish is required to achievetotal control. This is because any larva that is allowedto escape into adult cause considerable harm as adisease vector.The work also revealed that larval consumption washigher in the light than in the dark period suggestingthat the fish relies more on visual stimuli in locatingtheir preys. This result agrees with the works ofGhosh et al5 and Pamplona et al16. The implicationof this is that in turbid waters with reduced visibility,the voracity of the fish may be low compared to clean J  VECTOR  BORNE  DIS  47, JUNE 2010 184waters. The results from these experiments indicatethat A. gularis have mosquito biocontrol potentiali-ties. Considering the limitations of other malaria con-trol measures, there is the need to exploit this rela-tively less expensive, environmentally compatiblealternative in order to complement other efforts incombating the malaria scourge. It could be consid-ered sustainable especially when adopted on a localcommunity basis. In addition, this fish is native toand readily available in Nigeria and therefore wouldmost likely not cause any side-effects as attributedto G. affinis17. Therefore, we are of the opinion thatthe potential of this native killifish in reducing ma-laria burden in endemic zone will not be in doubt ifproper and far reaching introductions are made.Malaria endemic sub-Saharan Africa needs relativelyinexpensive, efficient and sustainable methods ofcontrolling the mosquito vectors in order to amelio-rate the distress of the people especially the ruralpoor. The field introduction of this fish vis-à-vis re-duction in malaria transmission in selected areas iscurrently being assessed.References1. Tabibzadeh GB, Nakhai R. Use of Gambusia fish in theMalaria Eradication Programme of Iran. Geneva: WHO1970 (Unpublished document WHO/VBC/70.198).2. Marti GA, Azpelicueta MDM, Tranchida MC, PelizzaSA, Garcia JJ. Predation efficiency of indigeneouslarvivorous species on Culex pipiens larvae (Diptera:Culicidae) in drainage ditches in Argentina. J Vector Ecol2005; 31(1): 102–6.3. Willems KJ, Webb CE, Rusell RC. A comparison of mos-quito predation by the fish Pseudomugil signifer and Gam-busia holbrooki (Girard) in laboratory trials. J Vector Ecol2005; 30(1): 87–90.4. Yildirim O, Karacuha A. A preliminary study on deter-mination of Aphanius chantrei feeding behaviour on mos-quito larvae. Acta Tropica 2007; 102 (3): 172–5.5. Ghosh SK, Tiwari SN, Sathyanarayan TS, Sampath TR,Sharma VP, Nanda N. Larvivorous fishes in wells targetthe malaria vector siblings species of the Anophelesculicifacies complex in villages in Karnataka, India.Trans R Soc Trop Med Hyg 2005;  99: 101–5.6. Manna B, Aditya G, Banerjee S. Vulnerability of themosquito larvae to the guppies (Poecilia reticulata) in thepresence of alternative preys. J Vector Borne Dis 2008;45: 200–6.7. Data sheet on Nothobranchius spp, WHO unpublisheddocument 1981; WHO/VBC/81.829; available on requestfrom the Division of Control of Tropical Disease, WorldHealth Organization, Geneva, Switzerland.8. Killifish. Available from: http://www.killifishbreeders.com.9. Umeh GI. Freshwater fishes of Nigeria: taxonomy, eco-logical notes, diet and utilization. Benin City, Nigeria:Idodo Umeh Publishers 2003; p. 159–60.10. Breeding the blue gularis, Aphyosemion sjoestedt. Avail-able from: http://www.aquaticcommunity.com.11. Ungureanu E, Pull JH, Pal R. Detailed study design forfield studies regarding the evaluation of the efficacy of thelarvivorous fish for the control of malaria. WHO/VBC/81.816.12. Larvivorous fishes of inland ecosystems. In:  Sharma VP,Ghosh A, editors.  Proceedings of the MRC-CICFRIWorkshop 1989; Delhi: Malaria Research Centre (ICMR)1989.13. Chatterjee SN, Chandra G. Laboratory trials on the feed-ing pattern of Anopheles subpictus,  Culex quinque-fasciatus and Armigeres subalbatus larvae by Gambusiaaffinis. Sci Cult 1997; 63: 51–2.14. Osphronemus gorami Lacepede 1802. Available from:http://www.aquaworld.com.15. McBirney C. Tropheops species “Red Cheek”. Availablefrom: http://www.animalworld.com.16. Pamplona LGC, Jose RSP, Claudia AFR, Jose FP. Jr, LinsRF, Primos ES, et al.  Efficacy of fish as predators of Aedesaegypti larvae, under laboratory conditions. Rev SaudePublica 2007; 41(4): 638–44.17. Rupp HR. Adverse assessments of  Gambusia affinis: Analternative view for mosquito control practitioners. J AmMosq Control Assoc 1996; 12: 155–66.Corresponding author: Dr O.O. Anyaele, Department of Zoology, Faculty of Science, University of Ibadan, Oyo State,Nigeria.E-mail: oo.anyaele@mail.ui.edu.ng; okorieanyaele@gmail.comReceived: 18 March 2010 Accepted in revised form: 8 July  2010

Laboratory evaluation of the biocontrol potential of Aphyosemion gularis against Anopheles larvae

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