Mosquito oviposition deterrents

Environ Sci Pollut Res https://doi.org/10.1007/s11356-017-0408-1

PLANT-BORNE COMPOUNDS AND NANOPARTICLES: CHALLENGES FOR MEDICINE, PARASITOLOGY AND ENTOMOLOGY

Mosquito oviposition deterrents Essam Abdel-Saalam Shaalan 1,2 & Deon Vahid Canyon 3

Received: 9 November 2016 / Accepted: 3 October 2017 # Springer-Verlag GmbH Germany 2017

Abstract Mosquitoes are well-known vectors of disease and threaten the health of millions of people annually. While synthetic insecticides have been relied on to combat these diseases, insecticide resistance and environmental concerns have directed attention towards novel and more targeted mosquitocides derived from botanicals. Research on the activity of botanical derivatives has focused on mosquito larvae and adults with little attention given to their potential as oviposition deterrents against gravid female mosquitoes. This review explores the influence of chemical and biological factors on deterrence and examines issues relating to environmental persistence and non-target effects. With very few discoveries of new insecticide pathways, the answer to effective mosquito control may well reside within other ancient plantbased organisms that have co-resided and evolved with this ubiquitous pest.

Keywords Botanical derivatives . Mosquito control . Mosquito-borne diseases . Plant-based ovideterrents Responsible editor: Philippe Garrigues * Essam Abdel-Saalam Shaalan [email protected]; [email protected] Deon Vahid Canyon [email protected] 1

Biological Sciences Department, College of Science, King Faisal University, P.O. Box 380, Al-Hfouf 31982, Kingdom of Saudi Arabia

2

Zoology Department, Faculty of Science, Aswan University, Aswan 81528, Egypt

3

Daniel K. Inouye Asia-Pacific Center for Security Studies, Honolulu, HI, USA

Introduction Mosquitoes transmit diseases, such as Zika, dengue, malaria, yellow fever, encephalitis, and filariasis, to millions of people annually. The recent spread of Zika virus infections in southern and Central America as well as the Caribbean represents the most recent of Western Hemisphere arbovirus outbreaks after dengue in the 1990s, West Nile virus in 1999, and chikungunya in 2013 (Benelli and Mehlhorn 2016; Benelli and Romano 2017). Mosquito control is the primary strategy for combating diseases for which there are no vaccines (Benelli 2015a; Benelli and Mehlhorn 2016; Benelli et al. 2016b; Benelli and Beier 2017). However, the war on insect pests is becoming untenable because reliance on synthetic insecticides has increasingly led to the development of resistance and there are few new options to continue the battle (Brogdon and McAllister 1998; Perera et al. 2008; Naqqash et al. 2016). Furthermore, the toxic environmental and health impacts of synthetic insecticides have become increasingly unacceptable, which has stimulated the search for new, more efficient and safer bioinsecticides from plants (Nogueira de and Palmerio 2001; Benelli 2015b; Benelli 2016; Pavela and Benelli 2016a). Many natural compounds derived from edible crops, ornamental plants, herbs, grasses, and tropical and subtropical trees have exhibited mosquitocidal activity (Shaalan et al. 2005). Some of these compounds have demonstrated high activity and are potential candidates that may be suitable for use as alternatives to synthetic insecticides in integrated vector control programs (Rajkumar and Jebanesan 2008; Elango et al. 2010). Most of the evidence base concerns adulticidal, larvicidal, and growth-inhibiting activity against different mosquito species (Sukumar et al. 1991; Shaalan et al. 2005), with fewer researchers having studied the oviposition deterrent activity of these compounds, and the number of evaluated plants is fewer than a hundred (Table 1). This latter area is of

Environ Sci Pollut Res

particular interest because synthetic insecticides have been shown to have no significant effect on selection of oviposition sites (Canyon and Muller 2013). The Oviposition Activity Index (OAI), developed by Kramer and Mulla (1979), is used to analyze the behavioral response of gravid mosquitoes to oviposition sites that have been infused with botanical and phytochemical substances. Using the following formula, the OAI corrects for the number of females trapped on the screen in the test (Nt) and control cups (Nc) and then converts the number to a standardized proportion: OAI ¼

Nt−Nc Nt þ Nc

The OAI thus ranges from − 1 (indicating deterrent) to + 1 (indicating attractant), with 0 (indicating a neutral response). This review presents an analysis of available literature on the oviposition deterrent potential of botanical derivatives against mosquitoes, with the aim of evaluating their comparative potential for mosquito control. It covers different plant species that have exhibited ovideterrent activity, factors influencing their effect, field evaluation, challenges, and finally, it recommends future directions.

Phytochemical oviposition deterrent activity The location and selection of an oviposition site is an essential life-cycle behavior for all mosquito species and involves visual, olfactory, and tactile cues (Bentley and Day 1989). Gravid mosquitoes use chemosensory cues to select oviposition sites that are suitable for their offspring before depositing their eggs (Afify and Galizia 2015). Gravid females receive such cues via odor receptors on the antennae, as well as via contact chemoreceptors on tarsi, mouthparts, and antennae (Seenivasagana and Vijayaraghavan 2010). These cues influence oviposition behavior and are exploited by gravid females to detect the presence of eggs, larvae, microbes, infusions, and plant-produced volatiles, which all are indicators of habitat suitability (Afify and Galizia 2015; Seenivasagana and Vijayaraghavan 2010). Such phenomena prompted scientists to look for chemicals that could produce oviposition deterrence as a means of mosquito control. The published literature reveals that derivatives from a large number of plant species exhibit oviposition-deterrent activity against several important mosquito vectors, and some even have the potential for field use (Table 1). Generally speaking, the deterrent activity of any botanical compound is dose dependent and directly proportional to concentration. Several studies have indicated that gravid females deposit fewer eggs or egg rafts, depending on the species, in high doses and vice versa. Botanical essential oils can be highly effective in preventing egg laying due to a variety of

chemical compounds (Prajapati et al. 2005; Waliwitiya et al. 2008; Warikoo et al. 2011; El-Gendy and Shaalan 2012; de Lima et al. 2013; Ramar et al. 2014; Soonwera 2015). However, moving from the laboratory to the field is not always straightforward. Complicating matters is that these oils may degrade rapidly within the oviposition medium, and their secondary metabolites may act independently or synergistically or even antagonistically with other chemicals not found in the laboratory to confuse results on exactly what is inhibiting gravid mosquitoes from laying eggs.

Factors influencing Ovideterrent activity Ovideterrent activity depends on both chemical and biological factors. Laboratory-based factors include the type of solvent used for extracting phytochemicals and fractionation and biological factors include plant species, plant parts, and the growing site as well as mosquito species (Prajapati et al. 2005; Tawatsin et al. 2006). For instance, out of three essential oils screened for ovideterrent activity, Cuminum cyminum Linn. was more effective in preventing oviposition by three mosquito species in order of deterrence: Anopheles stephensi > Aedes aegypti > Culex quinquefasciatus (Prajapati et al. 2005). Furthermore, ovideterrence against Ae. albopictus caused by neem cake hexane, methanol, and ethyl acetate fractions overcame that of other natural plant compounds belonging to the same botanical family, such as the fruit and leaf ethanolic extracts from Melia azedarach Linn., which needed a high dose to achieve substantial oviposition deterrence (Benelli et al. 2015b). The ovideterrent activity of botanical derivatives is derived in part from the particular part of a plant that is used, be it leaves, stems, fruits, rhizomes, seeds, flowers, or roots. Two studies gave account of the influence of plant parts on the efficacy of botanical derivatives as deterrents (Warikoo and Kumar 2014, 2015). For instance, it was found that a petroleum ether root extract of Argemone mexicana Linn. was more potent than the petroleum ether leaf extract (Table 1). Furthermore, the stem essential oil of Achyranthes aspera Linn. exhibited higher oviposition deterrence activity than leaves against Ae. aegypti and Cx. quinquefasciatus at a concentration of 0.1% (Khandagle et al. 2011). In like manner, M. azedarach leaf extract was more potent than the fruit extract (Autran et al. 2009) and essential oils from Piper marginatum Jacq. leaves and stem were more potent against gravid female Ae. aegypti compared to the inflorescences (Coria et al. 2008). Similar to the larvicidal activity of botanical derivatives, metabolites and phytochemicals are often more active ovideterrent than crude extracts. For instance, confertifolin, isolated from Polygonum hydropiper Linn. leaves, exhibited 98.51% ovideterrent activity against Ae. albopictus at the low concentration of 10 ppm (Maheswaran and Ignacimuthu

Rutaceae Rutaceae Asteraceae Asteraceae Asteraceae Asteraceae

Apiaceae Poaceae Lamiaceae Lamiaceae Lamiaceae

Leaves

Leaves

Oils

Leaves

Apium graveolens Linn. C. nardus Mentha piperita Linn. Ocimum basilicum Linn. Rosemarinus officinalis Linn.

Argemone mexicana Linn.

Papaveraceae

Acoraceae Lauraceae Rutaceae Rutaceae Poaceae Myrtaceae Lamiaceae Apiaceae Lamiaceae Poaceae Rutaceae Acanthaceae Acanthaceae Menispermaceae Asteraceae Asteraceae

Commercial oils.

Acorus calamus Linn. Cinnamomum verum J.Presl Citrus sinensis (L.) Osbeck Citrus limon (L.) Burm Cymbopogon nardus (L.) Rendle Myrtus caryophyllus Spreng Ocimum sanctum Linn. Pimpinella anisum Linn. Thymus vulgaris Linn. Vetiveria zizanioides Linn. Aegle marmelos (L.) Corrêa ex Roxb Andrographis lineata Wallich et Nees. Andrographis paniculata (Burm.f.) Wall. ex Nees. Cocculus hirsutus (L.) Diels Eclipta prostrata Linn. Tagetes erecta Linn. A. marmelos Limonia acidissima Linn. Sphaeranthus indicus Linn. Sphaeranthus amaranthoides Linn. Chromolaena odorata (L.) King & H.E. Robins. Ageratum houstonianum Mill.

Leaves

Amaranthaceae Zingiberaceae

Leaves, stem and Rhizome.

Achyranthes aspera Linn. Zingiber officinalis Roscoe

Family

Part

Oviposition deterrent activity of phytochemicals

Species

Plant (s)

Table 1

Reegan et al. (2015)

Tennyson et al. (2012)

Among the different extracts of the five plants screened, the hexane extract (out of three solvents) of L. acidissima showed 100% oviposition deterrent activity at all the tested concentrations against both mosquitoes.

Among hexane, ethyl acetate, and methanol crude leaf extracts, methanol showed an effective deterrent activity against all the three vector species with an oviposition active index of − 0.8, − 0.8, and −0.9, respectively, at 0.1% concentration in laboratory. Field trials on oviposition of Aedes species indicated effective deterrence ranging from 79.0 to 100.0% in indoor and 74.6 to 100.0% in outdoor ovitraps. Addition of 100% pure oil caused complete oviposition deterrence except in A. graveolens (75% effective repellency). The use of 10% oil resulted in 97.5% deterrence as shown by the M. piperita oil while other oils caused 36–97% oviposition deterrence. One percent oil showed decreased deterrent potential with 30–64% effective repellency. The M. piperita oil being exceptional. Reducing concentration to 0.1%, the least effective oil observed was A. graveolens (25% ER). Also, the M. piperita oil showed much reduced activity (40%), while the other oils exhibited 51–58% repellency to oviposition. The deterrence potential gradually increased with increasing concentrations revealing a positive correlation between the two. The maximum oviposition-deterrent potential was pronounced in the petroleum ether extract out of five extracts with 31 and 66%

Ae. aegypti Cx. quinquefasciatus

Ae. aegypti

Ae. aegypti

Ae. aegypti An. stephensi Cx. quinquefasciatus

Warikoo and Kumar (2015)

Warikoo et al. (2011)

Elango et al. (2010)

Ramar et al. (2014)

The oviposition repellency was dose, plant species, and solvent used for extraction dependent. The percentage at 500 ppm was 93.07, 93.95, 98.03, 90.43, 92.63, 81.53, 94.81, 97.50, 97.26, 92.22, 82.85, and 72.77 in hexane and chloroform extracts of plant species respectively.

Cx. quinquefasciatus

An. subpictusi

Khandagle et al. (2011)

References

Stem essential oil of A. aspera exhibited the highest oviposition deterrence activity, 100 and 85.71%, against both mosquitoes respectively, at the concentration of 0.1%. Oviposition activity was dose dependent and clove oil produced the maximum oviposition deterrent activity (100 ± 0.0%).

Deterrent activity

Ae. aegypti Cx. quinquefasciatus

Mosquito vector (s)


A. indica Capsicum frutescens Linn. Momordica charantia Linn. Murraya exotica (L.) Jack A. indica Rhazya stricta Decne. Heliotropium bacciferum Forssk. Syzygeum aromaticum (L.) Merrill & Perry C. sinensis Bryopsis pennata J. V. Lamouroux

Ae. albopictus

Dried seaweed

Seed kernels Peels

Bryopsidaceae

Ae. aegypti Ae. albopictus

Cx. pipiens


Meliaceae Solanaceae Cucurbitaceae Rutaceae Meliaceae Apocynaceae Boraginaceae Myrtaceae Rutaceae

Meliaceae


Leaves

Seeds

Azadirachta indica A. Juss

Amaranthaceae

Ae. aegypti An. sinensis Cx. quinquefasciatus

Ae. aegypti

Ae. albopictus

Seeds

Atriplex canescens (Pursh) Nutt.

Asteraceae

Family

Mosquito vector (s)

Neem Cake

Dry cells

Root

Part

Artemisia annua Linn.

Species

Plant (s)

Table 1 (continued)

Out of four extracts, methanol extract showed the strongest repellent effect against female oviposition and weak toxicity against brine shrimp nauplii as a non-target organism compared to other extracts. Repellency was dose dependent, and all extracts at five concentrations tested were observed to repel mosquitoes from oviposition, except

effective deterrence at 200 and 400 ppm, respectively. The hexane extract was found to be the least effective displayed an ED% range of 61.5 to 2.68%. The petroleum ether root extract was the most efficient extract, with percent effective deterrence of 21% at 40 ppm reaching to 100% at 1000 ppm and 73% at 100 ppm at which other extracts were rendered comparatively ineffective. Other extracts (hexane, benzene, acetone, and ethanol) were not found to be significantly effective at lower concentration but showed a gradual increase in the deterrent potential with increasing concentrations. Results established the efficacy of the non-polar extracts over the polar extracts. The extract showed dose-dependent deterrent activity. At 500 ppm, the percentage effective repellency was > 85% for all the species, with oviposition activity index values of − 0.94, − 0.95, and − 0.78 for the mosquitoes, respectively. Number of ovipositing females decreased significantly from 48.3 to 11.8% at 0–1000 ppm. Oils and ethyl acetate fraction were also able to deter Ae. albopictus oviposition in the field (effective repellence values ranging from 98.55 to 70.10%), while little effectiveness of butanol fraction was found. Seed production site had no influence on ovideterrent activity. Under field experiment, hexane, methanol, and ethyl acetate fractions showed very good effective repellence percentages, even if tested at low dosages (100 ppm: 71.33, 88.59, and 73.49% of effective repellence, respectively). Contrarily, both n-butanol and the aqueous fractions have shown little oviposition repellence rates (100 ppm: 22.72 and 17.06%, respectively). The highest oviposition activity index was achieved by the hexane fraction (− 0.82), followed by the ethyl acetate fraction (− 0.63) and the methanol fraction (− 0.62) while lower oviposition activity index was achieved by the n-butanol fraction (− 0.14) and the aqueous fraction (− 0.09). The different aqueous leaf extracts varied in the anti-ovipositional activities in different concentrations. Highest oviposition-deterrent index (ODI) was found in 0.5% concentration of A. indica, and the lowest one was found in 0.1% concentration of M. charantia. Significant deterrent activity at 0.05 and 0.1% (= 50 and 100 ppm) concentrations of water and methanol extracts, respectively.

Deterrent activity

Yu et al. (2015)

Elhag (1999)

Fatima et al. (2011)

Benelli et al. (2014)

Benelli et al. (2015a)

Ouda et al. (1998)

Cheah et al. (2013)

Warikoo and Kumar (2014)

References


Lauraceae Cupressaceae Apiaceae Lamiaceae Zingiberaceae Rubiaceae

Leaves

Oils

Chenopodium ambrosioides Linn.

Cinnamomum zeylanicum Blume Juniperus macropoda Boiss. P. anisum R. officinalis Z. officinale Coffea canephora Pierre ex A. Froehner

Eugenia jambolana Lam.

Leaves

Leaves

Seeds

Leaves

Myrtaceae

Euphorbiaceae Euphorbiaceae Euphorbiaceae Euphorbiaceae Verbenaceae Apiaceae Ranunculaceae Apiaceae Gleicheniaceae

Chenopodiaceae

Leaves

Croton argyrophylloides Muell Croton nepetaefolius Bail Croton sonderianus Muell Croton zehntneri Pax et Hoffm Lippia sidoides Cham. Cuminum cyminum Linn. Nigella sativa Linn. P. anisum Dicranopteris linearis (Burm.f.) Underw

Annonaceae Poaceae Poaceae Myrtaceae Lamiaceae Myrtaceae Rutaceae Caesalpinnaceae

Essential oils

C. odorata Cymbopogon citratus (DC.) Staph. C. nardus Eucalyptus citriodora Hook. O. basilicum S. aromaticum C. sinensis Cassia obtusifolia Linn.

Dried roasted beans

Annonaceae

Apocynaceae

Leaves

Flowers

Myrtaceae Lamiaceae Fabaceae Asteraceae

Leaves

Cananga odorata (Lamk.) Hook.f. & Thomson

Myrtaceae

Aerial parts

Callistemon lanceolatus (Curtis) Skeels Callistemon viminalis (Sol. ex Gaertn.) G. Don Hyptis suaveolens (L.) Poit. Prosopis juliflora (Sw.) DC. Vernonia cinerea Less. Calotropis procera (Aiton) W. T. Aiton

Family

Part

Species

Plant (s)

Table 1 (continued)

Ae. aegypti

At 100 ppm of fern extract oviposition rates reduced by more than 65% while at 10 ppm of fern-fabricated AgNP, oviposition rates reduced bymore than 70% (OAI were − 0.52 and − 0.55, respectively).

OD95 ranged from 126.7–302.3 μg/mL and influenced by both plant and mosquito species. Ae. aegypti, An. stephensi Cx. quinquefasciatus Ae. aegypti

Ae. aegypti

Oviposition responses were extremely low when highly concentrated extract of coffee were the only oviposition sites, but in dual choices (cups containing coffee extracts and with water), egg deposition occurred at lower rates in those containing coffee than those containing water only. Only L. sidoides, C. zehntneri, and C. argyrophylloides essential oils were able to inhibit the oviposition of female gravid mosquitoes with OD50 values of 35.3, 45.3, and 45.8 μg/mL, respectively.

Oviposition-deterrent activity was concentration dependent. Higher concentration (400 mg/L) showed 92.5% deterrent activity, followed by 300, 200, and 100 mg/L (87.2, 83.0, and 75.5% deterrents, respectively). Egg laying by gravid females reduced from 27.7 to 90.2% at concentrations of 100, 200, 300, and 400 mg/L. Essential oils of C. zeylanicum was found to be highly effective in preventing egg laying by the three mosquito species with an order of deterency, An. stephensi > Ae. aegypti > Cx. quinquefasciatus.

The oviposition activity index (OAI) values of the first six oils indicated that there were more deterrent than the control whereas the last oil acted as oviposition attractant. At higher concentration (10%), Ca. odorata showed the highest percent effective repellency (ER) against oviposition at 99.4, 97.1, and 100% to the three mosquito species, respectively.

Deterrence activity against both mosquitoes at different concentrations was observed with maximal eggs were laid in low concentration of extract particularly in Culex species. Essential oils of Flowers extract at 10% produced 99.4, 97.1, and 100% deterrent activity against the three mosquitoes, respectively.

for the aqueous extract at 50 and 100 μg/mL, hexane extract at 50 μg/mL, and chloroform extract at 50 μg/mL, which exhibited no effect on the oviposition activity. Former mosquito species is slightly more sensitive than the later species. Strong anti-oviposition activity (72–100%) against gravid females was observed. Acetone extract of P. juliflora found to be strong oviposition-deterrent which inhibited > 2-fold egg laying (OAI = − 0.466) at 100 ppm.

Deterrent activity

Ae. albopictus

Ae. aegypti An. sinensis Cx. quinquefasciatus


An. stephensi

Ae. aegypti An. dirus Cx. quinquefasciatus Ae. aegypti An. dirus Cx. quinquefasciatus

An. arabiensis Cx. quinquefasciatus

Ae. albopictus


Mosquito vector (s)

Prathibha et al. (2014)

Rajaganesh et al. (2016)

Prajapati et al. (2005)

de Lima et al. (2013)

Satho et al. (2015)

Rajkumar and Jebanesan (2008) Prajapati et al. (2005)

Rajkumar and Jebanesan (2009)

Phasomkusolsil and Soonwera (2012)

Soonwera (2015)

Elimam et al. (2009)

Yadav et al. (2014)

Mohsen et al. (1990)

References


Lamiaceae Lamiaceae

Leaves

Fruits

Leaves, stems and inflorescences Leaves

Ocimum kilimandscharicum Guerke Ocimum suave Wild

P. anisum

Piper marginatum Jacq.

Solanum nigrum Linn.

R. officinali cineol, citronellal, eugenol, linalool, thymol, pulegone, rosemary oil cymene Sargassum muticum (Yendo) Fensholt

Polygonum hydropiper Linn.

Meliaceae

Fruits and Leaves

Solanaceae

Sargassaceae

Sea weed

Seeds

Lamiaceae

Oils

Polygonaceae

Piperaceae

Apiaceae

Lauraceae Asteraceae Pedaliaceae Simmondsiaceae Zingiberaceae

Seeds Commercial oils

Litsea cubeba Pers. Matricaria recutita Linn. Sesamum indicum Linn. Simmondsia chinensis (Link) C. K. Schneid. Z. officinalis Melia azedarach Linn.

Asteraceae

Convolvulaceae

Leaves

Whole plant

Anacardiaceae Anacardiaceae

Rutaceae Asteraceae Asteraceae

Family

Leaves

Part

Laggera aurita (L. f.) Benth. ex C. B. Clarke

Gluta renghas Linn. Melanochyla fasciculiflora Kochummen Ipomoea cairica Linn.

Euodia ridleyi Hochr. Solidago canadensis Linn. Spilanthes mauritiana (A.Rich. ex Pers.) DC.

Species

Plant (s)

Table 1 (continued)

A. aegypti A. stephensi Cx. quinquefasciatus An. stephensi

Ae. aegypti

Ae. albopictus

Ae. aegypti


An. gambiae

Ae. aegypti

Ae. aegypti Cx. pipiens

An. stephensi

Ae. aegypti Ae. albopictus

Ae. albopictus

An. sinensis Cx. quinquefasciatus

Mosquito vector (s)

Synthesized silver nanoparticles (AgNPs) of the aqueous extract of the seaweed at 10 ppm reduced oviposition rates of more than 70% in the three mosquito species (OAI = − 0.61, − 0.63, and − 0.58, respectively). The concentrations of the hexane extract ranging between 0.03125 and 0.5% showed 27 to 99.5% oviposition deterrence.

Significantly fewer eggs on waters that contained cineol, citronellal, eugenol, linalool, p-cymene, pulegone, rosemary oil, trans-anethole, or thymol compared with their controls.

0.5 g/L of leaf extract and 0.75 g/L of fruit extract reduced laid eggs to about 30% over the control. Significant difference in the number of eggs found in control cups when compared with the number of eggs found in treated cups. Oviposition activity index (OAI) ranged from − 0.19 to − 1% for both plants respectively meaning that first plant is more deterrent. Deterrent activity was dose dependent (84.2, 83.8, and 92.3% for 10, 50, and 100 μL/L, respectively, after 24 h.). At lower doses (10 and 50 μL/L), the activity reduced after 72 h from 84.2 and 83.8 to 39.9 and 43.7%, respectively, for both concentrations but did not affected at the higher dose 100 μL/L. The essential oil and trans-Anethole were toxic for Daphnia magna (90–92% mortality at 50 μL/L) and significantly reduced its fertility at high concentrations (35–50 μL/L) and long exposure (48 h). However, no negative effect on Daphnia mortality or fertility was found at shorter exposure times (6 h) and/or lower concentrations (20 μL/L). Essential oils from leaves and stem reduced number of eggs laid by > 50% at 50 and 100 ppm. 98.51% at 10 ppm of confertifolin which isolated from leaves essential oils.

The extract strongly inhibited oviposition with 100% repellence to Ae. aegypti at lower concentration of 100 ppm, while for Ae. albopictus was at 450 ppm. The oviposition activity index (OAI) values ranged from − 0.69 to − 1. Deterrent activity was dose dependent, and the highest acetone extract concentration (0.5%) reduced egg lying up to 89.18% while the lowest concentration (0.03125%) reduced it up to 21.53%. 80.6% ovideterrent at 0.01%. All oils at three doses (0.5, 5, and 50 ppm) exhibited potent deterrent activity against gravid female mosquitoes with various degrees of repellency (ranging from 48.73–100%) depending on both plant species and applied dose from each plant.

Out of the five concentrations tested (20, 40, 60, 80, and 100 ppm), the concentration of 100 ppm showed a significant egg laying-deterrent capacity. The oviposition activity index value of the four plant species against the three mosquito vectors at 100 ppm were − 0.71, − 0.71, − 0.90, − 0.93, − 0.85, − 0.91, − 1, − 1, − 0.71, − 0.85, − 1, and − 1, respectively. The acetone extract of the second plant was more effective than the first one in displaying oviposition deterrence potential.

Deterrent activity

Singh and Mittal (2013)

Madhiyazhagan et al. (2015)

Maheswaran and Ignacimuthu (2014) Waliwitiya et al. (2008)

Autran et al. (2009)

Pavela (2014)

Kweka et al. (2010)

Coria et al. (2008)

Tawatsin et al. (2006) El-Gendy and Shaalan (2012)

Singh and Mittal (2015)

Ahbirami et al. (2014)

Zuharah et al. (2015)

References


Rajeswary et al. (2017)

Pandey et al. (2009)

Zingiberaceae Oils

An. stephensi An. subpictus Ae. aegypti Ae. albopictus Cx. quinquefasciatus Cx. tritaeniorhynchus

Egg laying by female adults was much significantly reduced when exposed to vapors of thymol compared to the seeds oils. Low doses of Z. cernuum essential oil reduced oviposition rates fin the six mosquito species. Apiaceae Seeds

Trachyspermum ammi (L.) Sprague ex Turrill Zingiber cernuum Dalzell

An. stephensi An. subpictus Ae. aegypti Ae. albopictus Cx. quinquefasciatus Cx. tritaeniorhynchus An. stephensi Myrtaceae Leaves Syzygium lanceolatum (Lam.) Weight & Arn.

Solanaceae Leaves Solanum trilobatum Linn.

Plant (s)

Table 1 (continued)

Family Part Species

An. stephensi

Mosquito vector (s)

Deterrent activity

Egg laying by gravid females reduced from 18 to 99% at range of 0.01, 0.025, 0.05, 0.075, and 0.1% from the extract. S. lanceolatum essential oils was effective as oviposition deterrent against the six tested mosquito species. The OAI were − 0.83, − 0.81, − 0.84, − 0.83, − 0.84, and − 0.86, respectively.

References

Rajkumar and Jebanesan (2005) Benelli et al. (2016a)


2014). In like manner, oviposition was significantly reduced when gravid female An. stephensi were exposed to vapors of thymol compared to seed oil of Trachyspermum ammi (L.) Sprague et Turril (Pandey et al. 2009). It has been determined that the production or growing site of Azadirachta indica A. Juss significantly influenced the quantity of active phytochemicals produced, which had a direct relationship on larvicidal activity. However, no association has yet been found between this factor and ovideterrent activity (Benelli et al. 2015a), which does not necessarily mean that it does not exist. In general, both aedenines and anophelines are easier to deter than culicines (Benelli et al. 2015b), but sometimes, the former genera exhibit the same degree of deterrent response. Although aedenines are typically more easily deterred than anophelines, a few studies have indicated the contrary. For instance, An. stephensi were deterred slightly more easily than Ae. aegypti (OAI = − 0.63 and − 0.61, respectively) when gravid females were subjected to 10 ppm Sargassum muticum (Yendo) Fensholt synthesized with silver nanoparticles of the aqueous extract (Madhiyazhagan et al. 2015). Among aedines, Ae. aegypti is typically more sensitive than Ae. albopictus, but culicines are occasionally more sensitive than both these genera (Ahbirami et al. 2014; Yu et al. 2015). The type of solvent used for extracting phytochemicals significantly influenced oviposition deterrent activity. Solvents can be broadly classified into two categories: polar (such as ethyl acetate, acetone, ethanol, methanol, and water) and nonpolar (such as pentane, hexane, chloroform, and diethyl ether). Results for polarity are inconsistent and indicate that non-polar solvents occasionally positively influenced the activity of the deterrent activity of phytochemicals compared to polar ones, and at other times, polar solvents were better than non-polar ones (Table 1). For instance, studies on A. mexicana extract revealed that non-polar solvents, especially petroleum extracts of leaves and roots, were more potent than the polar solvents (Warikoo and Kumar 2014, 2015). Similarly, hexane extracts of five plants were superior to ethyl acetate and methanol extracts at all the tested concentrations against both Ae. aegypti and Cx. quinquefasciatus mosquitoes (Reegan et al. 2015). Contrarily, a methanol extract of the sea weed Bryopsis pennata J. V. Lamouroux showed the strongest ovideterrent effect against both Ae. aegypti and Ae. albopictus females when compared to the polar solvents chloroform and hexane (Yu et al. 2015). In addition, a methanol extract showed effective deterrent activity against Ae. aegypti, An. stephensi, and Cx. quinquefasciatus vector species compared to both hexane and ethyl acetate extracts (Tennyson et al. 2012). As explained above, the different results obtained for the many varieties of ovideterrents listed in Table 1 were due to variations in concentration and type of active ingredients as well as the biological and physiological characteristics in botanicals and mosquitoes.


Field evaluation Only three field studies on ovideterrence were identified from the literature. In the first, field trials were conducted to determine the efficacy of an Ageratum houstonianum Mill. extract treatment in outdoor ovitraps against oviposition by gravid Ae. aegypti females (Tennyson et al. 2012). The level of effective deterrence ranged from 74.6 to 100.0% in outdoor ovitraps. In the second and third studies, both neem seed oil and neem cake were very effective at deterring oviposition by Ae. albopictus under experimental field conditions (Benelli et al. 2014, 2015a). Although it is generally assumed that natural substances will rapidly breakdown in field environments, data in Table 1 show that little is actually known about the persistence of ovideterrent phytochemicals in the environment and their potential long-term effects on both target and non-target organisms. Furthermore, the residual capacity of botanical oviposition deterrents against gravid mosquitoes is a crucial factor in mosquito control that has received little attention from researchers. Only one 3-day study evaluated the effects of a Pimpinella anisum Linn. fruit extract against Cx. quinquefasciatus gravid females (Pavela 2014). The ovideterrent activity of this extract was dose and time dependent since it reduced at lower doses (10 and 50 μL/L) and after 72 h from 84.2 and 83.8 to 39.9 and 43.7% respectively, but the efficacy of a higher dose (100 μL/L) was not affected by this timeframe. Phytotoxicity of botanicals requires serious attention when formulating products for market because they produce a wide variety of insect toxins, many of which are dangerous to mammals as well as insects (D’Mello 1997, Lindberg et al. 2000). Assuming that phytochemicals are completely safe can lead to dangerous assumptions. The most prominent example is photodegradation that produces products such as peroxides, epoxides, and doperoxides (Hausen et al. 1999). The aforementioned studies and information highlight the need of further field studies particularly against both malaria and filarial vectors because they breed in large open-breeding sites compared to the dengue vector which is a container breeding mosquito.

Impacts on non-target organisms Four studies on toxicity against other non-target aquatic organisms were identified. Three found that botanical deterrents were non-toxic to the other aquatic organisms including mosquito predators. The first found that a methanol extract of the seaweed B. pennata showed weak toxicity against thenon-target organism brine shrimp nauplii (Yu et al. 2015). Similarly, the toxicity of essential oils extracted from Syzygium lanceolatum (Lam.) Wight & Arn. leaves against several biological control agents of mosquitoes (the water bugs Anisops bouvieri and

Diplonychus indicus and fishes Gambusia affinis and Poecilia reticulata) was extremely low, with LC50 ranging between 4148 and 15,762 μg/mL (Benelli et al. 2016a). The essential oil of Zingiber cernuum Dalzell also showed very low toxicity against four mosquito predators with LC50s ranging from 3119 to 11,233 μg/mL (Rajeswary et al. 2017). In contrast, the essential oil and trans-Anethole of P. anisum fruits were found to be toxic for the water flea Daphnia magna (90–92% mortality at 50 μL/L) and significantly reduced its fertility at high concentrations (35– 50 μL/L) and long exposure (48 h), while no negative effect on Daphnia mortality or fertilitywasfound at shorterexposuretimes (6 h) and/or lower concentrations, 20 μL/L (Pavela 2014). The scarcity of studies on phytochemical toxicity against non-target aquatic organisms is noteworthy since some promising phytochemical candidates have emerged, and they merit more research (Shaalan et al. 2005).

Formulation and commercialization Unlike mosquito repellents, further studies are required to correctly formulate oviposition-deterrent ingredients for commercial production. Phytochemicals that possess dual action, larvicidal activity in addition to oviposition deterrent activity, would be the most interesting and promising ones for formulation, control of mosquitoes, and commercialization. Although botanical ovideterrents may be suitable for formulation and commercial production as ecofriendly compounds because of their repellency, low mammalian toxicity, and biodegradability, they still require scientific validation to test their activity, efficacy, and safety before commercialization. Chemical standardization, quality control, and difficulties in registration are the main barriers to the commercialization of such materials. In addition to physical, chemical, and biological factors influencing the formulation process of botanical deterrents, the mode of application is another critical issue since they do not all persist in the aquatic habitat. Since most ovideterrents are essential oils, formulations that involve controlled release and encapsulation are recommended, particularly if they are to be applied in aquatic habitats. The first method allows smaller quantities to be used, which are highly effective over a given period of time (Kydonieus 1980). The second method is a suitable and efficient stabilizing method for entrapping essential oils of very different chemical compositions (Pavela and Benelli 2016b). This method reduces loss of active principles, leading to high loaded microparticles that offer protection against environmental agents (Moretti et al. 2002). Furthermore, encapsulation methods may extend the efficacy period while gradually releasing the active substances as well as offering excellent prospects for the development of new botanicals which are safe for the environment and health (Pavela 2016).


Some American companies have brought commercial essential oil-based pesticides to market (Tripathi et al. 2009). These products are based on cinnamon oil, with cinnamaldehyde (30% in EC formulations) as the active ingredient. Another firm aims to become a world leader in essential oil-based pesticides and currently produces aerosol and dust formulations containing mixtures of essential oil compounds, including eugenol and 2-phenethyl propionate aimed at controlling domestic pests (cockroaches, ants, fleas, flies, wasps, etc.).

Acknowledgements The authors wish to express their sincere appreciation to Dr. Giovanni Benelli for inviting them to write this paper, reading the full manuscript, enhancing its accuracy and clarity and providing valuable criticism. The views expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Daniel K. Inouye Asia Pacific Center for Security Studies, the Department of Defense, or the US Government. Compliance with ethical standards Conflict of interest The authors declare that they have no conflict of interest.

Conclusions and future challenges References This review presented the results of available studies on botanical extracts that exhibited oviposition-deterrent activity against common, globally distributed, mosquito vectors of disease. Only 78 plants have been evaluated for ovipositiondeterrent activity, which is a tenth of the number evaluated for larvicidal activity. Since chemical and biological factors influence deterrent potential, identifying residual capacity under field conditions and their effects on non-target organisms remains important future work. The field remains wide open for investigation and full of potential. Not all mosquitoes lay eggs in human waste products as conveniently as Ae. aegypti, and not all oviposition sites are easily removed or overturned. With Zika virus on the move and continual outbreaks involving other mosquito species, ovideterrents provide a potentially effective and ecofriendly solution for the problem of treating hard-to-reach or hard-to-remove mosquito breeding sites. The studies mentioned in this paper only touch the surface of this topic, and much remains unknown about the ovideterrent potential of botanical extracts and phytochemicals. The following areas require further investigation: & & &

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Chemical characterization and identification of primary effective compounds Influence of phytochemical blends on gravid females compared to individual phytochemicals Influence of physical and chemical factors (such as sunlight, aquatic bodies temperature, water salinity, organic matter content, oxygen content, total dissolved solids, and pH) on capacity Influence of extraction methodology Field evaluation of botanical products Field application methods Toxicity of botanicals against aquatic organisms sharing the same ecological niche as mosquitoes Synthesized phytochemicals and nanoparticles from botanical extracts which could reduce the dose required to produce an oviposition-deterrent effect Persistence of ovideterrent phytochemicals in the environment and their long-term effects on mosquitoes

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