Pesticidal plants as a possible alternative to synthetic acaricides in tick control: A systematic review and meta-analysis

Elsevier Industrial Crops and Products Available online 27 July 2018 In Press, Corrected ProofWhat are Corrected Proof articles? Industrial Crops and Products Author links open overlay panelOlubukola TolulopeAdenubiadAroke ShahidAhmedaFolorunso OludayoFasinabLyndy JoyMcGawaJacobus NicolaasEloffaVinnyNaidooac a Phytomedicine Programme, Department of Paraclinical Sciences, Faculty of Veterinary Sciences, University of Pretoria, Onderstepoort, 0110, South Africa b Department of Veterinary Tropical Diseases, Faculty of Veterinary Sciences, University of Pretoria, Onderstepoort, 0110, South Africa c Biomedical Research Centre, Faculty of Veterinary Sciences, University of Pretoria, Onderstepoort, 0110, South Africa d Department of Veterinary Physiology and Pharmacology, College of Veterinary Medicine, Federal University of Agriculture, PMB 2240, Alabata, Abeokuta, Ogun State, Nigeria Received 10 August 2017, Revised 20 May 2018, Accepted 22 June 2018, Available online 27 July 2018. https://doi.org/10.1016/j.indcrop.2018.06.075 Get rights and content Highlights • Ticks cause enormous stock losses globally and transmit human and animal diseases. • Chemical acaricides are expensive and many ticks are increasingly resistant. • Rural farmers have been using plant extracts to control ticks for many centuries. • One of the most useful chemical acaricide classes, pyrethroids discovered from plant. • We summarize work reported in international databases in this meta-analyis. Abstract Ticks are a large group of parasitic arthropods which transmit pathogens to animals and humans, causing great economic losses. Chemical-based antitick measures include the use of pyrethroids, carbamates, organophosphates, formamidines and macrocyclic lactones, which all have associated costs, resistance-development and environmental hazards. Some plant-based alternatives may have good efficacy, low toxicity and reduced environmental impacts. A review of published scientific articles was conducted for medicinal plants with in vitro tick repellent or acaricidal activities against immature and adult stages of ticks. Veterinary databases (All Databases, CAB Abstracts and Global Health, PubMed, Web of Science, BIOSIS Citation Index, Science Direct, Current Content Connect and Google Scholar) were used. The search words were “acaricidal”, “tick repellent”, “medicinal plants”, “phytochemical constituents” and “antitick assays”. To investigate correlations, meta-analysis was conducted using the Fixed-effect model in an Excel programme.The different plant parts, extractants used and their efficacies, where available are listed. Extracts of some species including Azadirachta indica, Gynandropsis gynandra, Lavandula angustifolia, Pelargonium roseum and Cymbopogon species have good acaricidal and larvicidal effects with 90–100% efficacy, comparable to those of currently used synthetic acaricides. Bioassays used in the determination of repellent, acaricidal, larvicidal, inhibition of oviposition and hatchability include tick climbing repellency, Petri dish, larval packet and immersion tests amongst others. Using a total of 1 428, 1 924, 574, 281 and 68 events, the median efficiency value for acaricidal, larvicidal, egg hatching inhibition, inhibition of oviposition, repellency, acaricidal effects of the Lamiaceae and Asteraceae families were 80.12 (CI95%: 79.20–81.04), 86.05 (CI95%: 85.13–86.97), 83.39 (CI95%: 82.47–84.31), 53.01 (CI95%: 52.08–53.93), 92.00 (CI95%: 91.08–92.93), 80.79 (CI95%: 79.87–81.71) and 48.34% (CI95%: 47.42–49.26) respectively. Among the 26 isolated active compounds identified, some such as azadirachtin, carvacrol, linalool, geraniol and citronellal and their potential uses are discussed. While plant species used in ethnoveterinary medicine hold vast potential as parasiticides, the variations in testing methodologies and assay conditions make comparison among studies very problematic. The standardization of components, extraction techniques and experimental design is urgently required to fully explore their potential. Abbreviations Cl-Chloride CNSCentral Nervous System ConcConcentration DDTDichlorodiphenyltrichloroethane DEETN,N-Diethyl-meta-toluamide ECEffective concentration FigFigure GABAγ- Aminobutyric acid GluClGlutamate-gated chloride LCLethal concentration LDLethal dose MEVMedian efficiency value NDNot determined Picaridin1-Piperidinecarboxylic acid 2-(2-hydroxyethyl)-1-methylpropylester PMDPara-menthane-3,8-diol SS2201S,2S-2-Methylpiperidinyl-3-cyclohexene-1-carboxamide Keywords Antitick Acaricide Tick repellent Phytochemical Livestock Plant extract 1. Introduction Ticks are a diverse group of haematophagous arthropods, with at least 898 recognized species, distributed among three families: Argasidae (194 species), Ixodidae (703 species) and Nuttalliellidae (1 species) (Norval et al., 2004). They parasitize a wide range of hosts, and are ranked closely with mosquitoes in their capacity to transmit disease agents of importance (protozoa, bacteria, rickettsia and viruses) to livestock, domestic animals and humans (Sonenshine et al., 2002). Ticks are the most economically important ectoparasites and the most widespread species include Amblyomma testudinarium, Dermacentor auratus, Haemaphysalis bispinosa, Rhipicephalus (Boophilus) microplus, Ixodes acutitarsus, Ixodes ovatus, Nosomma monstrosum, Rhipicephalus haemaphysaloides, Rhipicephalus sanguineus and Rhipicephalus turanicus (Mans and Neitz, 2004). Economic loss caused by ticks and tick-borne diseases in cattle is estimated to be more than 7 billion USD worldwide (Zahir et al., 2010). Tick control programmes are largely based on the use of commercially available ectoparasiticides such as the organochlorines, organophosphates, pyrethroids and more recently, the insect growth regulators and isoxazolines on or in the animals or in the environment (de Oliveira et al., 2012; McTier et al., 2016) (Table 1). Limiting exposure to tick-infested areas and the use of repellents is also considered effective in preventing ticks and tick-borne diseases in companion animals and humans (Cisak et al., 2012). At present, the most commonly used repellents include N, N-diethyl-meta-toluamide (DEET) and 1-piperidinecarboxylic acid 2-(2-hydroxyethyl)-1-methylpropylester (picaridin) (Table 2). Table 1. Classes of acaricides and their mechanisms of action. Class of acaricide and examples Site and mechanism of action Chemical Structure LC50 (mg/ml) References Arsenicals: arsenic trioxide, potassium arsenite, dihydro-1, 3, 2,-dithiarsenol-2ylmercapto-acetic acid In the citric acid cycle, they inhibit pyruvate dehydrogenase and by competing with phosphate, uncouple oxidative phosphorylation, thus inhibiting energy-linked reduction of nicotinamide adenine dinucleotide, mitochondrial respiration and adenosine triphosphate synthesis leading to death Arsenic trioxide – Klaassen and Watkins (2003)a Organochlorines: benzenehexachloride, dichlorodiphenyltrichloroethane (DDT), lindane, aldrin, dieldrin, toxaphene, endosulphan, methoxychlor, hexachlorocyclohexane Binding at the picrotoxinin site in the gamma aminobutyric acid (GABA) chloride (Cl−) ionophore complex which inhibits Cl- flux into the nerve causing hyperexcitation and death DDT 36.8 Lawrence and Casida (1984)a, Camerino (2015)b Organophosphates: coumaphos, chlorfenvinphos, diazinon, parathion, malathion, diaxanthion, oxinothiophos Act at the synapse of nerve junctions and inhibit the activity of acetylcholinesterase irreversibly. Acetylcholinesterase breaks down the neurotransmitter acetylcholine, which carries impulses across the synapse from one nerve cell to another. Cholinesterase inhibition results in continuous nerve discharges leading to paralysis and death Coumaphos 0.39 Barthold and Schier (2005)a, Singh et al. (2014)b Carbamates: carbaryl, aldicarb, carbofuran, ethienocarb, fenobuacrb, oxamyl, propoxur Reversibly inhibits the activity of acetylcholinesterase. Cholinesterase inhibition results in continuous nerve discharges leading to paralysis and death Propoxur 0.039 Barthold and Schier (2005)a, Camerino (2015)b Formamidines: amitraz, chlordimeform, clenpyrin, chloromethiuron Competes with octopamine for its receptor site, guanosine diphosphate is replaced with guanosine triphosphate, inducing the production of cyclic adenosine monophosphate leading to inhibition of attachment and ultimately blood feeding with eventual death Amitraz 0.001 Beugnet and Franc (2012)a, Malan (2015)b Pyrethroids: cypermethrin, permethrin, deltamethrin They block sodium ion movement along the axon of the nerve fibre. This stimulates repetitive nerve discharges that lead to paralysis and death Cypermethrin 0.005 Shafer et al. (2005)a, Singh et al. (2014)b Macrocyclic lactones: avermectins (ivermectin, eprinomectin, selamectin, doramectin, abamectin) milbemycins Bind to GABA and glutamate-gated chloride channels (GluCl) thereby opening chloride channels in nerves, resulting in disruption of activity and loss of function in these cells leading to paralysis and death Ivermectin 0.61 Raymond and Sattelle (2002)a, Rodriguez-Vivas et al. (2017)b Phenylpyrazoles: fipronil, pyriprole Binds to the allosteric sites of GABAA and GluCl channels of the parasites as an antagonist (non-competitive inhibition). This prevents the opening of Cl− channels normally encouraged by GABA, reducing the Cl− ability to lower the neuron’s membrane potential. This results in an overabundance of neurons reaching action potential, CNS toxicity via over-stimulation and eventual death Fipronil 0.00053 Cole et al. (1993)a, Ravindran et al. (2014)b Spinosyns: Spinosad (mixture of spinosyn A and D), spinetoram Primarily targets binding sites on nicotinic acetylcholine receptors of the parasite’s nervous system leading to disruption of neurotransmission, paralysis and death Spinosyn A, R=H Spinosyn D, R = CH3 Spinosad 0.11 Bacci et al. (2016)a, Kovendan et al. (2012)b *Insect growth regulators: azadirachtin, methoprene, diflubenzuron, fluazuron Bears a structural resemblance to the moulting hormone, 20-hydroxyecdsyone, thus interrupting moulting, metamorphosis and development of the female reproductive system. Ticks which survive are unable to produce a progeny Azadirachtin 5 Beckage et al. (2000)a, Al‐Rajhy et al. (2003)b Isoxazolines: afoxolaner, fluralaner, sarolaner, lotilaner, CPD I Non-competitive GABA receptor antagonists, bind to Cl− channels in nerve and muscle cells blocking the transmission of neuronal channels, paralysis and death Fluralaner 0.28 McTier et al. (2016)a Williams et al. (2015)b a Reference for synthetic acaricide and mechanism of action. b Reference for LC50; LC50-Lethal concentration killing 50% of the population. * Demonstrates tick growth regulator activity. Table 2. Insect/Tick repellents and their mechanisms of action. Tick repellent Site and mechanism of action Chemical Structure References N, N-diethyl-meta-toluamide (DEET) Blocks the olfactory receptors for 1-octen-3-ol, a volatile constituent of sweat and breath. A protein, ionotropic receptor 40a, has also been identified as a putative DEET receptor Kain et al. (2013) 1-piperidinecarboxylic acid 2-(2-hydroxyethyl)-1-methylpropylester (Picaridin) The receptors, CquiOR136•CquiOrco and odorant binding protein 1 have been identified Drakou et al. (2017) Para-menthane-3,8-diol (PMD) ND Van Langenhove and Paul (2014) Ethyl butylactyloaminopropionate (IR3535) Has a dual effect on olfactory receptors, both inhibiting (antagonism) and activating them (agonism), thus, the arthropod can no longer detect attractant cues from a host Bohbot and Dickens (2012) 1S,2S-2-methylpiperidinyl-3-cyclohexene-1-carboxamide (SS220) Modality for repellent activity is olfactory Carroll et al. (2005) Racemic 2-methylpiperidinyl-3-cyclohexene-1-carboxamide (AI3-37220) Ionotropic receptor 40a could be a putative receptor Kain et al. (2013) The sale and procurement of ectoparasiticides accounted for 22% of the annual veterinary market of 872 million ZAR (73 million USD) in 2003 in South Africa (Peter et al., 2005). In other countries such as Kenya, Zambia, Zimbabwe, Nigeria, Tanzania and Uganda, the annual cost of importing ectoparasiticides had been estimated at 16 million, 10 million, 9.3 million, 30 million, 26 million and 26 million USD respectively (Kaaya and Hassan, 2000). The global parasiticide market was valued at 6 509.1 million USD in 2013. This is expected to reach 8 918.1 million USD by 2019 growing at a rate of 5.4% (www.marketsandmarkets.com). Commercial repellents and/or acaricidal agents are available for use on companion animals, livestock and humans, in different formulations, including tablets, sprays, soaps, shampoos, powders, impregnated collars, dip solutions, pour-on and spot-on applications (Gassel et al., 2014). Appropriate use of these chemicals is beneficial in controlling ticks, but improper application and misuse may lead to poisoning of humans and animals, emergence of resistant strains, issues of drug residues in animal food products (meat and milk) as well as environmental hazards (Babar et al., 2012). To overcome these obstacles, the development of an effective and environmentally friendly alternative of low toxicity to replace the synthetic agents is required. Research and Development orientated towards alternative methods of tick control that are consistent with the principles of sustainable agriculture, includes the use of tick antigens as vaccines (Shahein et al., 2013), entomopathogenic fungi (Nana et al., 2015, 2016) and plant-based alternatives (Benelli et al., 2017a,b). Plants have long provided mankind with a source of medicinal agents, with natural products once serving as the major provider of all therapeutic drugs (Balandrin et al., 1993). Many plant secondary metabolites are synthesized to provide protection against pathogens, predators and pests. These agents act in one or more of the following ways: counteraction of growth regulatory hormones, anti-feeding effects, inhibition of egg development, disruption of mating and sexual communication, inhibition of chitin formation and repellent action (Benelli et al., 2016b). It should be kept in mind that plant-produced chemicals that deter invertebrates and vertebrates primarily target herbivores and not blood feeders, such as ticks. Probably because of their shared arthropod lineage with herbivorous insects, ticks are also susceptible to some plant-produced deterrents. For example, the pyrethrins, which are a class of organic compounds derived from the dried flower heads of Chrysanthemum cinerariifolium (Trev.) Vis, have been used for centuries for their acaricidal and tick repellent properties (Dhang and Sanjayan, 2014). They also provide a structural backbone for the synthetic pyrethroids which are components of many household, agricultural and industrial insecticides (Dhang and Sanjayan, 2014). In some countries, plant-based ectoparasitic formulations are commercially available (Freitag and Kells, 2013). MyggA® Natural (Bioglan, Lund, Sweden), contains 30% of Corymbia citriodora (Hook.) oil with a minimum of 50% para-menthane-3,8-diol (PMD); Citriodiol®, manufactured by Citrefine International Limited, UK contains 64% PMD; Economist®, a natural alternative to permethrin, which contains pyrethrins and d-limonene, obtained from Citrus species is available in South Africa; BioUD®, with the active ingredient 7.75% 2-undecanone, originally derived from Lycopersicon hirsutum subsp glabratum C.H. Mull (wild tomato plants), registered by the United States Environmental Protection Agency in 2007 and TT-4302 (Guardian®Wilderness; Tyratech, Inc. Morrisville, NC, U.S.A) containing 5% geraniol (Bissinger et al., 2009, 2016). In an attempt to find safe and efficient compound(s) with tick repellent and/or acaricidal properties, research on plant extracts used traditionally in tick control has grown in recent years as seen in many reviews (Atanasov et al., 2015; Adenubi et al., 2016; Benelli et al., 2016b; Pavela et al., 2016; Katz and Baltz, 2016; Benelli and Lukehart, 2017; Benelli et al., 2017a,b). Renewed interest in natural compounds derived from plants and microorganisms to develop non-synthetic medications for the veterinary industry using newer methodologies such as combinatorial chemistry, computational biology and high throughput screening, could yield new repellents/acaricides (Sparks et al., 2016). Tick repellents or acaricides with mechanisms of action targeting previously unexplored metabolic pathways can be developed that may overcome multi-acaricide resistant populations. The market for plant-based tick repellents and acaricides is extremely promising considering the high level of synthetic acaricide consumption (Borges et al., 2011). Plant-based products could be useful for organic livestock production as well as providing alternatives for controlling resistant strains. As prevention of contamination of food and the environment is one of the sustainable development goals to transform our world, it is essential to invest in developing a pharmaceutical phytotherapy industry, with interdisciplinary approaches towards finding solutions to the menace caused by ticks and tick-borne diseases. In this review, we provide information from selected studies that include plant species used in traditional veterinary medicine globally for tick infestation as repellents or acaricides, including those with antifeedant and growth-inhibition properties. Plant species cited are reviewed for efficacy, bioactive constituents and possible mechanism of action to validate their traditional use in animal health. We have summarized and harmonized the most important results of the tests of plant extract efficacy against different tick species and life stages (eggs, larvae, nymphs or adults), To investigate correlations, meta-analysis was conducted. Plant species and compounds therein showing very good efficacy are highlighted. Bioactive products based on plant extracts or isolated compounds may constitute prototypes for the development of promising alternatives to chemical acaricides. 2. Materials and methods The keywords used to collect relevant literature for the review were: “tick repellent”, “acaricidal”, “medicinal plants”, “isolated compounds” and “antitick assays”. Veterinary databases (All Databases, CAB Abstracts and Global Health, PubMed, Web of Science, BIOSIS Citation Index, Science Direct, Current Content Connect and Google Scholar) were searched. Specifically, the plant species tested, the effective concentrations and concentration killing 50% of the population (LC50), extractants, possible mechanism of action, species and life stage of ticks targeted, type of bioassay used and compounds isolated were considered. 2.1. Selection criteria applied to published results The selected papers focusing on in vitro tick repellent and/or acaricidal efficacy of plant extracts as listed in the Web of Science database, complied with at least one of the four criteria listed below: (1) Efficacy for the evaluation of larvae, nymph and adult mortalities and/or tick repellency higher than 60%. (2) Efficacy for the evaluation of growth inhibition estimated. (3) The LC50 (acaricidal) and/or EC50 (repellency) estimated. (4) Compounds isolated from the plant extracts. 2.2. Meta-analysis applied to published results Data for plant extracts with tick repellent and/or acaricidal properties was extracted and compiled from peer reviewed journals obtained from the databases mentioned above. The data was quality-checked through data filtration to remove duplicates and harmonized into a single Microsoft Excel® spreadsheet. All concentrations (including LC50/EC50) were harmonized and expressed as mg/ml. Filtered data was coded for use in a Microsoft Excel® programme, including: the plant name, part(s) of the plants used and family; acaricidal activity, larvicidal activity, inhibition of oviposition, egg hatching inhibition and repellency effects; assay type employed and further in vivo studies (if any). The number of events, sample sizes and outcomes were calculated based on the data. Data was analysed using fixed-effect model (precision-based estimates) in the Meta-analyses software on Excel and comparison between individual studies was calculated in WinPepi v11.24 (Neyeloff et al., 2012). Outputs were generated as percentage of acaricidal, larvicidal, inhibition of oviposition, egg hatching inhibition and repellency effects of the plants or of specific families with 95% confidence intervals. Cumulative events with measures of central tendencies were also produced in forest plots. 3. Results 3.1. Plant species with repellent potential In total, 27 plant species from 18 families were represented (Table 3). The family with the highest frequency was: Asteraceae (15%), followed by Lamiaceae (11%). The Cleomaceae, Poaceae, Rutaceae and Verbenaceae had 7% representation each while the other families were represented by 1 plant species (4%) each (Table 3). Most of the studies used essential oils from the aerial parts of the plants (63%). This was followed by ethanol extracts (22%), methanol and hexane extracts (7%). The leaf was the most used part, followed by the aerial parts, fruits, flowers and drupes in one study. About 56% of the studies used nymphs to test for repellency, 37% used adults while 7% used larvae. Tick climbing repellency, fingertip repellency, vertical filter paper and Petri dish repellency assays were commonly employed. Duration of repellency ranged from 1 h to 35 h (Lavandula angustifolia Mill.) and active phytochemicals include eugenol, β-caryophyllene, linalool, carvacrol, 1, 8-cineole, myrcene and geraniol (Table 3, Table 6). Only 1 study progressed to in vivo validation of in vitro studies. Table 3. Plant species evaluated for repellent activity and their possible bioactives. Plant family and species Common name Plant part/ Extractant Tick repellent bioassay, tick species and life stage studied Conc. (mg/ml) Effect (%) EC50 (mg/ml) Some active isolated compounds References Asparagaceae Convallaria majalis L. Lily of the valley L (EO) PDR using nymphal I. ricinus 100 67 ND Convallamaroside Nartowska et al. (2004)b, Thorsell et al. (2006)a Asteraceae Ageratum conyzoides (L.) L Billy-goat weed L (EtOH) FR using nymphal A. cajennense 1.1 85 0.21 Stigmasterol, β-sitosterol, precocene II, ageratochromene Soares et al. (2010)a, Kumar et al. (2016)b Artemisia abrotanum L. Southern wormwood L (EO) PDR using adult I. ricinus 100 69.1 ND Coumarin, thujyl alcohol, cinnamyl aldehyde, α-copaene, eugenol, eucalyptol Tunón et al. (2006)a, b Artemisia absinthium L. Absinthe wormwood L (EO) FVR using nymphal I. ricinus 100 78.1 ND Sabinene, thujenol, linalool, geranyl acetate Sabinene, thujenol, linalool, geranyl acetate Jaenson et al. (2005)a, b Tagetes minuta L. Southern marigold AP (EO) TCR using adult H. marginatum rufipes – – 0.07 Cis-ocimene, β-ocimene, 3-methyl-2-(-2-methyl-2-butenyl)-furan, 2-butanone, dihydrotagetone, cis-tagetone Nchu et al. (2012) Makang’a (2012)b Bignoniaceae Kigelia africana (Lam.) Benth Sausage tree Fr (MeOH) FR using larvae R. appendiculatus 0.25 76 ND Kiglin, 6-methoxymellein, stigmasterol, lapachol Gabriel and Olubunmi (2009)b, Opiro et al. (2013)a Burseraceae Commiphora holtziana Engl. Myrrh Re (HX) PDR using larvae R. (B.) microplus 10 80 ND Germacrene-D, δ-elemene, β-bourbonene β-selinene, β-elemene, γ-elemene, α-cubebene Birkett et al. (2008)a, b Caryophyllaceae Dianthus caryophyllus L. Carnation Fl (EO) PDR using nymphal I. ricinus 100 100 ND 2-Phenyl-ethanol, eugenol, geraniol, coumarin, α-pinene, β-citronellol Tunón et al. (2006)a, b Chenopodiaceae Dysphania ambrosioides (L.) Mosyakin & Clemants (formerly Chenopodium ambrosioides L.) Wormseed L (EtOH) FR using nymphal A. cajennense 2.2 100 0.51 Ascaridole, 2-carene, ρ-cymene, isoascaridole, α-terpinene Soares et al. (2010)a, Chu et al. (2011)b Cleomaceae (previously Capparaceae) Cleome gynandra L. (syn. Gynandropsis gynandra (L.) Briq.) Cat’s whiskers AP (EO) TCR using adult R. appendiculatus 0.1 98.9 ND Carvacrol, transphytol, linalool, trans-2-methylcyclopentanol, β-caryophyllene Lwande et al. (1999)a, b Cleome monophylla L. Single-leaved cleome AP (EO) TCR using adult R. appendiculatus 0.1 89.9 ND Terpenolene, 1-α-terpeneol, 2-dodecanone, α-humulene, β-humulene, n-Pentacosane Ndungu et al. (1995)a, b Cupressaceae Chamaecyparis nootkatensis (D. Don) Spach (formerly Cupressus nootkatensis D. Don) Alaska yellow cedar AP (EO) FVR using nymphal I. scapularis – – 0.48 Nootkatone, valencene-13-ol, nootkatone 1, 10- epoxide, carvacrol Dietrich et al. (2006)a, b Ericaceae Rhododendron tomentosum (Stokes) H. Harmaja (formerly Ledum palustre L.) Rhododendron tomentosum Harmaja Marsh Labrador tea L (EO) FVR using nymphal I. ricinus 100 95.1 ND Myrcene, palustrol, 2,6-dimethyl-1,5,7-octatriene-3-ol, 2-methyl-6-methylene-1,7-octadiene-3-one (myrcenone), alloaromadendrene, ledol, p-cymene, β-caryophyllene Jaenson et al. (2005)a, b Fabaceae Senna (Cassia) didymobotrya (Fresen.) Irwin & Barneby African senna AP (MeOH) FR using larval R. appendiculatus 0.25 87.6 ND Anthraquinones, terpenoids, flavonoids, phenolic compounds, tannins Opiro et al. (2013)a, Alemayehu et al. (2015)b Geraniaceae Pelargonium graveolens L'Her Rose geranium L (EO) VFP using nymphal A. americanum 0.10 90 ND Citronellol, geraniol, 10-epi-γ-eudesmol Tabanca et al. (2013)a, b Lamiaceae Lavandula angustifolia Mill. (syn. L. officinalis Chaix ex Vill.) English lavender AP (EO) TCR using adult H. marginatum rupifes 200 100 ND Linalool, borneol, camphor, eucalyptol Mkolo and Magano (2007)a, Fadia et al. (2015)b Mentha pulegium L. Squaw mint AP (EtOH) FR using nymphal A. cajennense 1.1 85 0.45 1α, 6βdimethyl-5β-hydroxy-4β-(prop-1-en-2-yl)-decahydronaphthalen-2-one, 1-(O-β-D-glucopyranosyl)-2,7-dimethyloct-5-en-3-one Soares et al. (2010)a, Ibrahim (2013)b Ocimum suave (Wild) Wild basil L (EO) TCR using adult R. appendiculatus – – 0.24 1,8-cineole, linalool, pinene, eugenol, camphor, methyl chavicol, ocimene, terpinene, limonene Mwangi et al. (1995)a, b, Pandey et al. (2014)b Lauraceae Lindera melissifolia (Walter) Blume Pondberry D (EO) TCR using nymphal A. americanum 0.83 74 0.67 β-caryophyllene, α-humulene, germacrene D, β-elemene Oh et al. (2012)a, b Meliaceae Melia azedarach L. Chinaberry tree Fr (HX) FR using nymphal A. cajennense – – 2.22 3,7,11,15- tetramethyl-2-hexadecen-1-ol, carotene, rhodoxanthin, meliatoxin, melianone, meliantriol, nimbolidin A, nimbolidin B Soares et al. (2010)a, Krishnaiah and Prashanth (2014)b Myrtaceae Syzygium aromaticum (L.) Merr. & L.M. Perry (syn. Eugenia caryophyllata Thunb.) Cloves EO PDR using nymphal I. ricinus 100 68 ND Carvacrol, thymol, eugenol, cinnamaldehyde Chaieb et al. (2007)b, Thorsell et al. (2006)a Poaceae Cymbopogon nardus (L.) Rendle Citronella grass AP (EtOH) FR using nymphal A. cajennense 0.28 100 0.09 Linalool, citronellal Soares et al. (2010)a, Avoseh et al. (2015)b Cymbopogon nardus (L.) Rendle EO PDR using nymphal I. ricinus 100 89 ND Thorsell et al. (2006)a Rutaceae Ruta graveolens L. Rue AP (EtOH) FR using nymphal A. cajennense – – 4.14 2-undecanone, 2-nonanone, α-limonene, 5, 6-diethenyl-1-methyl-cyclohexane Soares et al. (2010)a, Haddouchi et al. (2013)b Spiranthera odoratissima A. St.- Hil. Manaca L (EtOH) FR using nymphal A. cajennense – – 8.43 Dictamine, γ-fagarine, skimmianine, 1-methyl-2-phenylquinolin-4-one, limonexic acid, limonin Soares et al. (2010)a, Terezan et al. (2010)b Verbenaceae Callicarpa americana L. American beautyberry EO FR using nymphal A. cajennense 1.0 85 0.1 Callicarpenal, intermedeol Soares et al. (2010)a, b Lippia javanica (Burm. f.) Spreng. Lemon bush AP (EO) TCR using adult H. marginatum rupifes 53 69.2 ND Myrcene, 1,8-cineole, dyhrodrotagetone, ipsenone, bicycle(3.1.1)heptanes-2-one, 2-butanone Magano et al. (2011)a, b Plant parts: AP- Aerial parts; L- Leaves; D- Drupes; Fl- Flowers; Fr- Fruit; Re- Resin. Plant peparations: EO- Essential Oil; EtOH- Ethanolic extract; MeOH- Methanolic extract; HX- Hexane extract. Ticks: A - Amblyomma; H.- Hyalomma; I.- Ixodes; R.- Rhipicephalus. Test type: FR- Fingertip Repellency; TCR- Tick Climbing Repellency; PDR- Petri Dish Repellency; FVR- Falcon Vial Repellency; VFP- Vertical Filter Paper Repellency. Others: Syn. - Synonym; ND- Not determined yet; Conc.- Concentration; EC50 - Effective concentration 50. a Reference for repellent activity. b Reference for isolated compounds. 3.2. Plant species with acaricidal and growth inhibitory potential In total, 55 plant species from 22 families had activities that were in line with the criteria we set (Table 4). The families with the highest frequencies were: Lamiaceae (20%), Asteraceae (13%), Rutaceae and Fabaceae (9%) and Solanaceae (7%). The Meliaceae and Poaceae had 6% representation each, Euphorbiaceae and Piperaceae had 4% representation each while the remaining 13 plant families were represented by 1 plant species each (2%) (Table 4). Table 4. Plant species evaluated for their acaricidal and growth inhibitory activities and their possible bioactives. Plant family and species Common name Plant part/Extractant Acaricidal bioassay, tick species and life stage studied Conc.* (mg/ml) Effect (%) IO (%) EHI (%) Some active isolated compounds Mechanism of action References Acanthaceae Andrographis paniculata (Burm.f) Nees King of bitters L (MeOH) APT using field adult Haemaphysalis bispinosa 3(0.33) 100 ND ND Andrographolide, andrograpine, panicoline, paniculide-A, B, C ND Elango and Rahuman (2011)a, Hossain et al. (2014)b Amaryllidaceae Allium sativum L. Garlic C (MeOH) AIT using field EF R. (B.) microplus 100 80 85.8 100 Allicin, alliin ND Hughes and Lawson (1991)b, Shyma et al. (2014)a, C (DCM) CB using lab-reared adult H. marginatum rufipes 240 (59) 100 ND ND ND Nchu et al. (2005)a Annonaceae Annona squamosa L. Sugar apple FP (Aq) AIT using field adult Haemaphysalis bispinosa 2(0.44) 100 ND ND 1H- cycloprop[e]azulen-7-ol decahydro-1,1,7-trimethyl-4-methylene-[1ar-(1aα,4aα, 7β, 7 a, β, 7bα)], retinal 9-cis- 3,17-dioxo-4-androsten-11alpha-yl hydrogen succinate, 1-naphthalenepentanol decahydro-5-(hydroxymethyl)-5,8a-dimethyl-y,2-bis(methylene)-(1α,4aβ,5α,8aα), 1-naphthalenemethanol decahydro −5-(5-hydroxy-3-methyl-3-pentenyl)- 1,4a-di methyl - 6-methylene -(1S-[1α, 4aα, 5α(E), 8aβ], (−)-spathulenol, podocarp-7-en-3-one13β-methyl-13-vinyl, 1-phenanthrene carboxaldehyde 7-ethenyl-1,2,3,4,4a,4,5,6,7,9,10,10a-dodecahydro-1,4a,7-trimethyl-[1R-(1α,4aβ.4bα,7β, 10aα)] ND Madhumitha et al. (2012)a, b Araceae Acorus calamus L. Sweet flag Rh (50%EtOH/DW) AIT using lab-reared EF R. (B.) microplus; in vivo 100 100 100 ND α-asarone, β-asarone ND Ghosh et al. (2011)a, b Apocynaceae Calotropis procera (Aiton) Dryand. Apple of Sodom LX (EtOH) AIT using field EF H. dromedarii (1.1) – ND ND Digitoxin, cardenolide Inhibition of Na+, K+-ATPase of ticks Al‐Rajhy et al. (2003)a, b Asteraceae Artemisia absinthium L. Absinthe wormwood AP (CH) AIT using field EF R. sanguineus 200 (88) 93.3 85.1 100 Artemisinin Reacts with the heme groups of the haemoglobin molecules digested by parasites, altering the cell structure and its functions, thus affecting growth and reproduction Godara et al. (2014)a, b Calea serrata Less. Snake herb AP (HX) AIT using field EF R. (B.) microplus 50 14.6 ND 100 Precocene II Interferes with tick oviposition, development and reproduction Ribeiro et al. (2011)a, b Eupatorium adenophorum Spreng. (syn. Ageratina adenophora) Sticky snakeroot AP (EtOH) AIT using field nymphal Haemaphysalis longicornis 1500 100 ND ND Quercetagetin 7-β-O-glucoside, 6-methoxykaempferol 7-methyl ether 3- β-O-glucoside, quercetagetin 4^-methy lether 7- β-O-glucoside, 6-hydroxykaempferol-7- β-O-glucoside, 6-methoxygenkwanin; umbelliferone; 3-(2^- β-O-pyranoglaucoside)-phenyl-2-trans-trans-propenoic acid, dotriacontanol. ND Li et al. (2008)b, Nong et al. (2013)a Matricaria (Chamomilla) chamomilla L. Chamolile Fl (EtOH) AIT using field EF R. (B.) annulatus 80 26.7 46.7 ND Angelic acid (2-meyhyl-2-butenoic acid), azolen, chamazulene (1,4-dimethyl-7-etazulene), α-bisablol, sineol, maricarin, matricin ND Pirali-Kheirabadi and Razzaghi-Abyaneh, (2007)a, b Tagetes erecta L. Mexican marigold L (AC) APT using field adult Haemaphysalis bispinosa 3 84 ND ND Benzaldehyde, limonene, linalool, myroxide, β-ocimene, phenylacetaldehyde, piperitone ND Elango and Rahuman (2011) Tagetes minuta L. Southern marigold AP (EO) NPT using lab-reared nymphal H. marginatum rufipes 0.10 60 ND ND Cis-ocimene, β-ocimene, 2-butanone, 3-methyl-2-(2-methyl-2-butenyl)-furan, piperitenone ND Nchu et al. (2012)a, b Tagetes patula L. French marigold AP (EtOH) AIT using lab-reared EF R. sanguineus 50 0 21.5 ND 50 - hydroxymethyl-5-(3-butene-1-ynil)-2,20 -bithiophene; methyl-5-[4-(3- methyl-1- oxobutoxy)-1-butynyl]-2,2’ bithiophene; cholesterol; β-sitosterol (24-R-stigmast-5- ene-3β-ol) (4); stigmasterol [24-(S)-stigmast-5,22E-dien- 3β-ol], lupeol, kaempferol, quercetina, patuletin-7-O-glucoside (patulitrin), patuletin, quercetagetin, quercetagetin-7-O-glucoside, luteolin ND Politi et al. (2012)a, b Bromeliaceae Ananas comosus (L.) Merr. Pineapple Sk (Aq) AIT using field EF R. (B.) microplus 500 59.4 39.1 33.3 Bromelain May be attributed to enzyme complex of bromelain which promote digestion of the cuticle and death of the parasite Domingues et al. (2013)a, b Caricaceae Carica papaya L. Pawpaw Sd (MeOH) AIT using field EF R. (B.) microplus 100 93.3 100 100 Papain, chymopapain, peptidase A, peptidase B, lysozyme ND Shyma et al. (2014)a, b Combretaceae Guiera senegalensis J.F.Gmel. Moshi medicine L (EtOH) AIT using field EF. H. anatolicum 150 100FI 100 100 (0.508%) Catechin, myricitrin, rutin, quartterin, 3,4,5-tri-O-galloylquinic acid Antifeedant property Osman et al. (2014)a, b Euphorbiaceae Jatropha curcas L. Barbados nut L (EtOH) AIT using field EF R. (B.) annulatus 100 0 10.1 90 Apigenin 7-O-β-D-neohesperidoside, apigenin 7-O-β-D-galactoside), orientin, vitexin, vicenin II, di-C-β-Dglucopyranoside-methylene-(8, 8’)-biapigenin Could be attributed to apigenin which can cause decrease in the level of active ecdysteroid by inhibiting the P450 enzyme, leading to decreased incorporation of free ecdysteriods into the eggs or interference with the uptake of modified egg yolk protein, itellin into the oocytes both being important for egg maturation and development Juliet et al. (2012)a, b Ricinus communis L. Castorbean L (EtOH) AIT using field EF R. (B.) microplus; in vivo 99 85 39 ND Quercetin, gallic acid, flavone, kaempferol, ricin Inhibition of the development and maturation of oocytes Ghosh et al. (2013)a, b Fabaceae Calpurnia aurea (Ait.) Benth Wild laburnum L (AC/DW) CB using lab-reared adult R. pulchellus 200 100 DA – – Calpurmenin, 13α-(2’-pyrrolecarboxylic acid) ester, virgiline, lupanine ND Zorloni et al. (2010)a, b Leucaena leucocephala (Lam.) de Wit White leadtree L (AC/DW) AIT using field EF R. (B.) microplus 192 0 7.3 29.0 Tannins, quercetin, caffeic acid, scopoletin High levels of tannins present probably responsible for activity Fernández-Salas et al. (2011)a, Von Son-de Fernex et al. (2015)b Lysiloma latisiliquum (L.) Benth. False tamarind L (AC/DW) AIT using field EF R. (B.) microplus 192 0 36.4 69.3 Tannins High levels of tannins present probably responsible for activity Fernández-Salas et al., (2011)a, b Piscidia piscipula (L.) Sarg. (Syn. Piscidia erythrina L.) Fishpoison tree L (AC/DW) AIT using field EF R. (B.) microplus 192 0 15.7 39.2 Tannins, 5,7-dihydroxylated isoflavones, coumaronochromones, 5-deoxyisoflavones High levels of tannins present probably responsible for activity Fernández-Salas et al. (2011)a, Tahara et al. (1993)b Pongamia glabra Vent. (Syn. Miliettia pinnata (L.) Panigrahi Pongam oiltree L (EtOH) AIT using field EF R. (B.) annulatus 100 17 13 50 Karinjin, pongamol, kaempferol, β-sitosterol ND Ravindran et al. (2017)a, b Hypericaceae Hypericum polyanthemum Klotzch ex Reichardt St. John’s wort AP (MeOH) AIT using field EF R. (B.) microplus 25 0 12.8 0 Benzopyrans Disturb the development process and reproduction Ribeiro et al. (2007)a, b Lamiaceae Anisomeles malabarica (L.) R. Br. Ex Sims Malabar catmint L (MeOH) APT using field adult Haemaphysalis bispinosa 3(0.72) 100 ND ND Anisomelic acid, ovatodiolide, pedalitin, acteoside, terniflorin ND Rao et al. (2012)b, Zahir et al. (2010)a Hesperozygis ringens (Benth.) Epling Pulegium L (EO) AIT using field EF R. (B.) microplus 50 ND 76.4 95 Pulegone, limonene, linalool, β-caryophyllene, bicyclogermacrene Due to chemosterilant effect of pulegone Ribeiro et al. (2010)a, b Hyptis verticillata Jacq. John Charles AP (EO) CB using field EF R. (B.) microplus 4 45 87.2 90 Cadina- 410(15)-dien-3-one (1), aromadendr-1(10)- en-9-one (squamulosone), viridiflorol, hexadecyl acetate ND Facey et al. (2005)a, Picking et al. (2013)b Leucas aspera (Willd.) Link Thumbai AP (EtOH) AIT using field EF R. (B.) annulatus 100 54.2 69.4 100 Nicotine, acacetin, apigenin Inhibit the action of prostaglandins Ravindran et al. (2011)a, b Leucas indica (L.) Sm – L (EtOH) AIT using field EF R. (B.) annulatus 500 66.7 55.2 0 Leucolactone, sitosterol, campesterol, stigmasterol, nicotine ND Divya et al. (2014)a, b Ocimum basilicum L. Great basil L (CH) AIT using field adult R. (B.) microplus 100 (55) 100 ND ND Linalool, (Z)-cinnamic acid methyl ester, cyclohexene, α- cadinol, 2,4-diisopropenyl-1-methyl-1-vinylcyclohexane, 3,5-pyridine-dicarboxylic acid, 2,6-dimethyl-diethyl ester, β-cubebene, guaia-1(10),11-diene, cadinene, (E)-cinnamic acid methyl ester, β-guaiene ND Zhang et al. (2009)b, Veeramani et al. (2014)a Origanum minutiflorum O. Schwarz & P.H. Davis Wild origanum AP (EO) VP using field adult R. turanicus 10 100 ND ND Carvacrol, p-cymene, borneol, γ-terpinene, myrcene, camphene, α-pinene, thymol ND Cetin et al. (2009a)a, b Origanum onites L. Turkish oregano L (EO) APT using field adult R.turanicus 250 (23) 100 ND ND Carvacrol, p-cymene, linalool, γ-terpinene, myrcene, camphene, α-pinene, thymol ND Coskun et al. (2008)a, b Satureja thymbra L. Savory AP (EO) VP using field adult H. marginatum rufipes 5 100 ND ND Carvacrol, γ-terpinene ND Cetin et al. (2009b)a, b Tetradenia riparia (Hochst.) Codd Ginger bush L (EO) AIT using field EF R. (B.) microplus 18 100 100 100 14-hydroxy-9-epi-cariophyllene, cismuurolol-5-en-4-a-ol, ledol, a-cadinol, limonene, fenchone ND Gazim et al. (2011)a, b Vitex negundo L. Five-leaved chaste tree L (EtOH) AIT using field EF R. (B.) microplus 50 (7.02) 53.9 100 Terpenoids, irridoids, steroids, phenolic compounds, lignane derivatives, amino acids, fatty acids, aliphatic alcohol ND Singh et al. (2014)a, b Meliaceae Azadirachta indica AJuss. Neem L (MeOH) AIT using field EF R. (B.) microplus 100 33.3 20.7 20 Azadirachtin, meliacarpin Anti-feedant effect and causes delay in the production of ecdysone Akhtar et al. (2008)b Shyma et al. (2014)a S, L, B (EtOH) AIT using lab-reared EF R. (B.) microplus; in vivo 80 (51) 80 ND ND Srivastava et al. (2008)a Carapa guianensis Aubl. Andiroba S (E)O) AIT using field EF R. (B.) microplus 6 ND ND 93.3 Palmtic acid, oleic acid, stearic acid, α-copaene ND de Souza Chagas et al. (2012)a, b Melia azedarach L. Chinaberry Fr (HX) AIT using field EF R. (B.) microplus 2 0 100 100 Azadirachtin, meliacarpin Due to alterations on the neuroendocrine system of the tick. Borges et al. (2003)a, Akhtar et al. (2008)b Myrtaceae Melaleuca alternifolia (Maiden & Betche) Cheel Narrow-leaved paperback L (EO) AIT using field EF R. (B.) microplus 50 ND 100 100 1, 8-cineole, terpinen-4-ol. ND Pazinato et al. (2014)a, b Syzygium aromaticum (L.) Merr & L.M. Perry Clove L (EO) AIT using field EF R. (B.) microplus 10 100 90.3 ND Eugenol, trans-β-caryophyllene ND Yessinou et al. (2016)a, b Papaveraceae Argemone mexicana L. Mexican poppy WP (EtOH) AIT using lab-reared EF R. (B.) microplus 100 90 65.5 ND Alkaloids, terpenoids, flavonoids, phenolics ND Ghosh et al. (2015)a, b Phytolaccaceae Petiveria alliacea L. Guinea henweed S (MeOH) AIT using field EF R. (B.) microplus 200 86.6 91 17 Benzyltrisulfide, benzyldisulfide ND Rosado-Aguilar et al. (2010)a, b Piperaceae Piper aduncum L. Spiked pepper L (EA) AIT using field EF R. (B.) microplus 100 22 46.78 ND Dillapiole, neorodiol, globulol, spathulenol, croweacin, apiole Alter development and metabolism producing physiological disturbances that may lead to inhibition of reproduction or death due to interference with feeding and growth Silva et al. (2009)a, b Piper tuberculatum Jacq. Painful pepper Fr (HX) AIT using field EF R. (B.) microplus 75 (18.4) 100 100 100 Piperine, piplartine ND da Silva Lima et al. (2014)a, b L (EA) AIT using field EF R. (B.) microplus (38) ND ND 81.7 ND de Souza Chagas et al. (2012)a, b Poaceae Cymbopogon citratus (DC.) Stapf Lemon grass L (EO) AIT using field EF R. (B.) microplus, in vivo 125 92 ND ND Citral ND Chungsamarnyart and Jiwajinda (1992)a, b Cymbopogon martini (Roxb.) W. Watson Ginger grass L (E)O) AIT using field EF R. (B.) microplus (29) ND ND 86.7 Geraniol, geranyl acetate, linalool, trans-ocimene, myrcene, β-caryophyllene ND de Souza Chagas et al. (2012)a, b Cymbopogon nardus (L.) Rendle Citronella grass L (EO) AIT using field EF R. (B.) microplus, in vivo 125 100 ND ND Citronellal, d-limonene ND Chungsamarnyart and Jiwajinda (1992)a, b Rutaceae Aegle marmelos (L.) Correa Golden apple L APT using field adult Haemaphysalis bispinosa 3(0.36) 100 ND ND Skimmiarepins A, Skimmiarepins C ND Elango and Rahuman, (2011)a, b Citrus hystrix DC. Kaffir lime FP (E)O) AIT using lab-reared EF R. (B.) microplus 200 80 ND ND Citronellal, β-pinene, sabinene ND Chungsamarnyart and Jansawan (1996)a, Sato et al. (1990)b Citrus maxima (Burm.) Merr. Pomelo FP (E)O) AIT using lab-reared EF R. (B.) microplus 200 100 ND ND d-limonene ND Chungsamarnyart and Jansawan (1996)a, b Citrus reticulata Blanco Tangerin FP (E)O) AIT using lab-reared EF R. (B.) microplus 100 100 ND ND d-limonene, geranial, neral, geranyl acetate, geraniol ND Chungsamarnyart and Jansawan (1996)a, Chutia et al. (2009)b Citrus sinensis (L.) Osbeck Sweet orange FP (E)O) AIT using lab-reared EF R. (B.) microplus 100 98.59 ND ND d-limonene, terpineol, 1,8-cineole, sinsetin ND Chungsamarnyart and Jansawan (1996)a, Favela-Hernández et al. (2016)b Solanaceae Capsicum frutescens L. Malagueta pepper Fr (EtOH) AIT using field EF R. (B.) microplus 50 10 25.3 84.6 Capsaicin, dihydrocapsaicin, pentadecanoic acid, hexadecanoic acid, octadecanoic acid Interference with the conversion of blood ingested by ticks in eggs Vasconcelos et al. (2014)a, b Datura stramonium L. Devil’s snare L (MeOH) AIT using field EF R. (B.) microplus 100 73.33 77.17 70 Scopolamine, hyoscyamine, meteloidine, atropine Similar to organophosphates Shyma et al. (2014)a, b Datura metel L. Devil’s trumpet Fr (EtOH) AIT using lab-reared EF R. (B.) microplus 90 100 100 ND Yangjinhualine A, megastigmane sesquiterpenes, alkaloids, glycosides ND Ghosh et al. (2015)a, b Kuang et al. (2008)b Withania somnifera (L.) Dunal Indian ginseng L (EtOH) AIT using field EF R. (B.) microplus 61 20 21.36 100 Isopelletierine, anaferine, withanolides, withaferins, sitoindoside VII, VIII, IX, X Due to the decreased levels of ecdysteroids leading to decreased incorporation of free ecdysteroids into the eggs necessary for oocyte maturation Singh et al. (2014)a, b Stemonaceae Stemona collinsae Craib. – R (MeOH) AIT using field engorged adult R. (B.) microplus, in vivo 250 100 ND ND Stemofoline, didehydrostemofoline, stemofurans A-K, dihydrostilbene Reduces tick attachment Pacher et al. (2002)b, Kongkiatpaiboon et al. (2014)a, b Verbernaceae Lippia sidoides Cham. Pepper-rosmarin L (EO) NPT using lab-reared nymphal R. sanguineus 19 96.1 ND ND Thymol, o-cymene, E-caryophyllene, myrcene Blocks the GABA receptors, impairing the flow of Cl- ions, leading to alterations on nerve impulses and death Gomes et al. (2014)a, b Plant parts: L- Leaves; S- Stem; B- Bark; R- Root; AP- Aerial parts; WP- Whole plant; Sd- Seed, Fl- Flowers; F- Fruit; FP- Fruit peel; Sk- Skin; C- Cloves; Rh- Rhizome. Extractant: EO- Essential Oil; EtOH- Ethanol; MeOH-Methanol; HX- Hexane; AC- Acetone; DW- Distilled Water; CH- Chloroform; Aq- Aqueous; DCM- Dichloromethane; EA- Ethyl acetate. Ticks: H.- Hyalomma; R.- Rhipicephalus. Test: IO- Inhibition of oviposition; EHI- Egg hatching inhibition; AIT- Adult Immersion Test; APT- Adult Packet Test; NPT- Nymphal Packet Test; CB- Contact Bioassay; VPB- Vapour Phase Bioassay. Others: EF- Engorged adult female; ND- Not determined yet; Conc. – Concentration. a Reference for acaricidal activity. b Reference for isolated compounds. * LC50 – Lethal concentration 50 in bracket; DA- decidedly affected (dead plus very weak). Rhipicephalus (Boophilus) microplus was the most studied tick and the adult immersion test was the most commonly employed method. Most of the studies used essential oils followed by ethanol extracts of the plants, as well as methanol, acetone, hexane, chloroform, water, dichloromethane and ethyl acetate extracts. Engorged female ticks obtained from the field were mostly used and 30% of the studies checked for growth inhibition. The bioactive compounds in the plants were evaluated in 93% of the studies while only 17% attempted to determine the mechanism of action of the plant extract or isolated compound. Active phytochemicals include geraniol, eugenol, β-caryophyllene, carvacrol, linalool, 1, 8-cineole, azadirachtin, thymol, nicotine and scopolamine (Table 4, Table 6). Only 5 of the studies progressed to in vivo experiments. 3.3. Plant species with larvicidal potential In total, 40 plant species from 19 families with larvicidal activity were found (Table 5). The family with the highest frequency was Lamiaceae (25%). This was followed by Asteraceae and Poaceae (10% each), Piperaceae (7.5%), Verbenaceae, Solanaceae, Amaryllidaceae (5% each). The other 12 plant families were represented by 1 plant species each (2.5%) (Table 5). Rhipicephalus (Boophilus) microplus larvae were also mostly studied and the average age was 14 days old. Most of the studies also used essential oils more than organic extracts. Active phytochemicals include geraniol, eugenol, β-caryophyllene, limonene, borneol, artemisinin and 1, 8-cineole (Table 5, Table 6). Table 5. Plant species evaluated for larvicidal activity using the Larval Packet or Larval Immersion Tests and their possible bioactives. Plant family and species Common name Plant part/Extractant Tick species and age of larvae Conc. (mg/ml) Effect (%) LC50 (mg/ml) Some active isolated compounds Mechanism of action References Acanthaceae Andrographis paniculata (Burm.f) Nees King of bitters L (MeOH) 7–14 days old LV R. (B.) microplus – – 0.2 Andrographolide, andrograpine, panicoline, paniculide-A, B, C ND Elango and Rahuman (2011)a, Hossain et al. (2014)b Amaryllidaceae Allium sativum L. Garlic C (MeOH) 12 days old LV R. (B.) microplus 100 69 ND Allicin, alliin ND Shyma et al. (2014)a EO 10 days old LV R. (B.) microplus 50 100 ND Allicin, diallyl trisulfide, diallyl disulphide, ajoene ND Martinez-Velazquez et al. (2011)a, Mikaili et al. (2013)b Bl (EO) 15 days old LV R. (B.) annulatus 50 100 ND Allicin, allin, dially disulfide, methyl alkyl disulphide, diallyl trisulfide Interaction with several glycosylated receptor proteins in the mid gut of the parasite leading to inhibition of nutrient absorption and death. Also gets accumulated into the haemolymph and ovarioles thereby interfering with development and reproduction Aboelhadid et al. (2013)a, b Allium cepa L. Onion Bl (EO) 15 days old LV R. (B.) annulatus 50 100 ND Dipropyl disulphide, methyl propyl disulphide, methyl propyl trisulphide Chemical reaction with thiol groups of various enzymes which affects the essential metabolism of cysteine proteinase activity involved in virulence of the parasite Aboelhadid et al., 2013a, b Annonaceae Annona squamosa L. Sugar apple FP (Aq) 14–21 days old LV R. (B.) microplus 2 100 0.5 1H- cycloprop[e]azulen-7-ol decahydro-1,1,7-trimethyl-4-methylene-[1ar-(1aα,4aα, 7β, 7 a, β, 7bα)], retinal 9-cis- 3,17-dioxo-4-androsten-11alpha-yl hydrogen succinate, 1-naphthalenepentanol decahydro-5-(hydroxymethyl)-5,8a-dimethyl-y,2-bis(methylene)-(1α,4aβ,5α,8aα), 1-naphthalenemethanol decahydro −5-(5-hydroxy-3-methyl-3-pentenyl)- 1,4a-di methyl - 6-methylene -(1S-[1α, 4aα, 5α(E), 8aβ], (−)-spathulenol, podocarp-7-en-3-one13β-methyl-13-vinyl, 1-phenanthrene carboxaldehyde 7-ethenyl-1,2,3,4,4a,4,5,6,7,9,10,10a-dodecahydro-1,4a,7-trimethyl-[1R-(1α,4aβ.4bα,7β, 10aα)] ND Madhumitha et al. (2012)a, b Apocynaceae Calotropis procera (Aiton) Dryand. Apple of Sodom AP 14 days old LV H. dromedarii – – 0.58 Digitoxin, cardenolide Inhibition of Na+, K+-ATPase of ticks Al‐Rajhy et al. (2003)a, b L (MeOH) 12 days old LV R. (B.) microplus 100 63.2 ND Shyma et al. (2014) Asteraceae Artemisia absinthium L. Absinthe wormwood AP (CH) 14 days old LV R. sanguineus – – 11 Artemisinin Reacts with the heme groups of the haemoglobin molecules digested by parasites, altering the cell structure and thus affect the growth and reproduction Godara et al. (2014)a, b Calea serrata Less Snakeherb AP 14 days old LV R. (B.) microplus 6.25 100 ND Precocene II, eupatoriochromene Interfere with tick oviposition, development and reproduction Ribeiro et al. (2011)a, b Eupatorium adenophorum Spreng. Sticky snake root AP (EtOH) 7–14 days old LV Haemaphysalis longicornis 1500 100 ND Cadinene sesquiterpenes ND Nong et al. (2013)a, b Tagetes patula L. French marigold AP (EtOH) LV R. sanguineus – – 7.43 50 - hydroxymethyl-5-(3-butene-1-ynil)-2,20 -bithiophene; methyl-5-[4-(3- methyl-1- oxobutoxy)-1-butynyl]-2,2’ bithiophene; cholesterol; β-sitosterol, stigmasterol, lupeol, kaempferol, quercetina, patuletin-7-O-glucoside (patulitrin), patuletin, quercetagetin, quercetagetin-7-O-glucoside, luteolin ND Politi et al. (2012)a, b Caricaceae Carica papaya L. Pawpaw Sd (MeOH) 12 days old LV R. (B.) microplus 100 82.2 ND Papain, chymopapain, peptidase A. peptidase B, lysozyme ND Shyma et al. (2014)a, b Combretaceae Guiera senegalensis J.F. Gmel Moshi medicine L (EtOH) 10-14 days old LV H. anatolicum 150 100 8 Catechin, myricitrin, rutin, quartterin ND Osman et al. (2014)a, b Euphorbiaceae Croton sphaerogynus Baill Croton L (DCM) 14-21 days old LV R. (B.) microplus 200 100 67 Abieta-8,11-diene-3-one, abieta-8,11,13-trien-12-ol, podocarp-7-ene,13-methyl-13-vinyl-3-one ND Righi et al. (2013)a, b Fabaceae Leucaena leucocephala (Lam.) de Wit White leadtree L (AC/DW) LV R. (B.) microplus 4.8 66.8 ND Tannins, quercetin, caffeic acid, scopoletin Tannins responsible confirmed by using a specific blocker, polyethylene glycol Fernández-Salas et al. (2011)a, b Hypericaceae Hypericum polyanthemum Klotzch ex Reichardt St. John’s wort AP (HX) 14 days old LV R. (B.) microplus 6.25 100 ND 6-isobutyryl-5,7-dimethoxy-2,2-dimethylbenzopyran, 7-hydroxy-6-isobutyryl-5-methoxy-2,2-dimethylbenzopyran and 5- hydroxy-6-isobutyryl-7-methoxy-2,2-dimethylbenzopyran Affect development and reproduction of the tick Ribeiro et al. (2007)a, b Lamiaceae Cunila angustifolia Benth. – AP (EO) 14 days old LV R. (B.) microplus 2.5 100 ND Sabinene, γ-terpinene, limonene ND Apel et al. (2009)a, b Cunila incana Benth. – AP (EO) 14 days old LV R. (B.) microplus 2.5 100 ND α-pinene, β-pinene, β-caryophyllene ND Apel et al. (2009)a, b, Agostini et al. (2010)b, Cunila spicata Benth. – AP (EO) 14 days old LV R. (B.) microplus 5 100 ND Menthofurane, borneol ND Apel et al. (2009)a, b Hesperozygis ringens (Benth.) Epling Pulegium L (EO) 14 days old LV R. (B.) microplus 0.62 100 0.26 Pulegone, limonene, linalool, β-caryophyllene, bicyclogermacrene Due to chemosterilant effect of pulegone Ribeiro et al. (2010)a, b Ocimum canum L. Camphor basil L (aq) LV H. a. anatolicum 0.03 96 0.02 α-thujene, myrcene, α-pinene, sabinene, α-phellandrene, α-terpinene, limonene, γ-terpinene, terpinolene, β-caryophyllene, trans-α-bergarmotene, α-caryophyllene, germacrene D,β-seliene, biocyclogermacrene, estragole, thymol, carvacrol ND Jayaseelan and Rahuman (2012)a, b Ocimum suave Willd (syn. Ocimum gratissimum, L.) Clove basil L (EO) LV R. appendiculatus; in vivo 2 100 0.2 Germacrene-D, β-caryophyllene, β-eudesmol, α-humulene ND Mwangi et al. (1995)a, Runyoro et al. (2010)b, Ocimum urticaefolium Roth – L (EO) 14–21 days old LV R. (B.) microplus 50 100 9 Eugenol, elemicin, β-bisabolene ND Hüe et al. (2015)a, b Rosmarinus officinalis L. Rosemary L 10 days old LV R. (B.) microplus 100 89 ND α-pinene, verbenone,1,8-cineole Martinez-Velazquez et al. (2011), Tetradenia riparia (Hochst.) Codd Ginger bush L (EO) 14–21 days old LV R. (B.) microplus 250 100 122 14-hydroxy-9-epi-cariophyllene, cismuurolol-5-en-4-a-ol, ledol, limonene, fenchone ND Gazim et al. (2011)a, b Copaifera reticulata Ducke Copaiba L (DMSO/DW) 14-21 days old LV R. (B.) microplus – – 1.6 Oleoresin ND de Freitas Fernandes and de Paula Souza (2007)a, b Meliaceae Melia azedarach L. Chinaberry Fr (HX) 7–21 days old LV R. (B.) microplus 2.5 98 ND Azadirachtin Due to alterations on the neuroendocrine system of the tick Borges et al., (2003)a, b Myrtaceae Corymbia citriodora (syn. Eucalyptus citriodora) (Hook.) K.D. Hill & L.A.S. Johnson Lemon-scented gum L (EO) LV Anocentor nitens 500 100 ND Citronellal ND Clemente et al. (2010)a, b Phytolaccaceae Petiveria alliacea L. Guinea henweed S (HX) 7-14 days old LV R. (B.) microplus 200 100 38.8 Benzyltrisulfide, benzyldisulfide ND Rosado-Aguilar et al. (2010)a, b Piperaceae Piper aduncum L. Spiked pepper L (HX) 14-21 days old LV R. (B.) microplus 20 70.4 9.3 Dillapiole, neorodiol, globulol, spathulenol, croweacin, apiole, β-ocimene ND Silva et al. (2009)a, b, Bernuci et al. (2016)b Piper mikanianum (Kunth) Steud. Betel leaf AP (EO) 14 days old LV R. (B.) microplus – – 2.33 Apiol, dillapiol, myristicin, limonene, bicyclogermacrene, β-caryophyllene, safrole, β-vetivone, (Z)-isoelemicin, (E)-asarone ND de BF Ferraz et al. (2010)a, b, Bernuci et al. (2016)b Piper tuberculatum Jacq. Painful pepper Fr (HX) LV R. (B.) microplus 0.12 100 0.04 Piplartine, piperine ND da Silva Lima et al. (2014)a, b, L (EO) 14-21 days old LV R. (B.) microplus – – 4.1 ND de Souza Chagas et al. (2012)a, b Poaceae Cymbopogon citratus (DC.) Stapf Lemon grass L (EO) LV R. (B.) microplus; in vivo 1:8 99 ND Citral ND Chungsamarnyart and Jiwajinda (1992)a, b, Cymbopogon martini (Roxb.) Wats. Ginger grass L (EO) 14-21 days old LV R. (B.) microplus – – 4.7 Geraniol, geranyl acetate, linalool, trans-ocimene, myrcene, β-caryophyllene ND de Souza Chagas et al. (2012)a, b Cymbopogon nardus (L.) Rendle Citronella grass L (EO) LV R. (B.) microplus; in vivo 1:8 94 ND Citronellal, d-limonene ND Chungsamarnyart and Jiwajinda (1992)a, b Melinis minutiflora P.Beauv Molasses grass L (EO) LV R. (B.) microplus 0.01% 100 ND Propionic acid, 1,8-cineole, butyric acid, phenylethyl alcohol, hexanal, 9-E-eicosene ND Prates et al., (1998)a, b Rutaceae Aegle marmelos (L.) Correa Golden apple L (MeOH) 7-14 days old LV R. (B.) microplus 2 100 0.13 Skimmiarepin A, skimmiarepin C ND Elango and Rahuman (2011)a, b Solanaceae Datura stramonium L. Devil’s snare L (MeOH) 12 days old LV R. (B.) microplus 100 71.8 ND Scopolamine, hyoscyamine, meteloidine, atropine, terpenoids, flavonoids May be similar to organophosphates Shyma et al. (2014)a, b Solanum trilobatum L. Purple fruited pea eggplant L (Aq) LV H. a. anatolicum 0.05 55 0.05 Solamarine, solaine, solasodine, glycoalkaloid, diosogenin, tomatidine ND Shahjahan et al. (2004)b, Rajakumar et al. (2014)a Verbenaceae Lippia graveolens Kunth Mexican oregano L 10 days old LV R. (B.) microplus 25 100 ND Thymol, carvacrol, p-cymene, γ-terpinene ND Martinez-Velazquez et al. (2011), Lippia sidoides Cham. Pepper-rosmarin L (EO) 15-21 days old LV A. cajennense 18.8 100 ND Thymol, o-cymene, myrcene, E-carophyllene ND Gomes et al. (2014)a, b Plant parts: L- Leaves; S- Stem; B- Bark; R- Root; Bl – bulb; AP- Aerial parts; Sd- Seed, Fl- Flowers; F- Fruit; FP- Fruit peel; Sk- Skin; C- Cloves. Extractant: EO- Essential Oil; EtOH- Ethanol; MeOH- Methanol; HX- Hexane; AC- Acetone; DW- Distilled Water; DMSO-Dimethyl sulphoxide; DCM- Dichloromethane. Ticks: A.- Amblyomma; H.- Hyalomma; R.- Rhipicephalus. Others: LV- Larvae; ND- Not determined; Conc.- Concentration; LC50 – Lethal concentration 50. a Reference for larvicidal activity. b Reference for isolated compounds. Table 6. The lethal concentration (LC50) of some known tick repellent and acaricidal compounds isolated from plants. Class of compound Compound Plant species LC 50 mg/ml (molar)a Chemical Structure and Formula Reference Monoterpene α-pinene (insecticidal, acaricidal) Plectranthus barbatus Andrews Rosmarinus officinalis L. Satureja myrtifolia (Boiss & Hohen.) Greuter & Burdet 0.032 (0.0002) C10H16 Govindarajan et al. (2016) β-pinene (repellent) Lindera melissifolia (Walt.) Blume Stylosanthes humilis Kunth Cleome monophyla L. Clausena anisata (Hook.f) ex. Benth Cannabis sativa L. 6.5 (0.047) C10H16 Ogendo et al. (2011) β-citronellol (acaricidal, repellent) Pelargonium graveolens L.Her. Dianthus caryophyllus L. 789 (4.73) C10H20O Pohlit et al. (2011) Borneol (insecticidal) Lavandula angustifolia Mill. Artemisia abrotanum L. Cunila spinate Benth. Origanum minutiflorum O. Schwarz & P.H. Davis 0.5 (0.0032) C10H18O Pohlit et al. (2011) Carvacrol (acaricidal) Chamaecyparis nootkatensis (D. Don) Spach Gynandropsis gynandra (L.) Briq. Origanum minutiflorum O. Schwarz & P.H. Davis Satureja thymbra L. Lippia gracilis Schauer 4.46 (0.029) C10H14O de Oliveira Cruz et al. (2013) Citronellal (acaricidal) Cymbopogon nardus (L.) Rendle Corymbia citriodora (Hook.) K.D. Hill & L.A.S. Johnson Citrus hystrix DC. 210 (1.36) C10H18O Pohlit et al. (2011) Elemol (repellent) Maclura pomifera (Raf.) C.K. Schneid. 0.005 C15H26O Pohlit et al. (2011) Eucalyptol (1,8-cineole) (acaricidal) Eupatorium adenophorum Spreng. Lippia javanica (Burm.f) Spreng. Ocimum species 0.51 (0.003) C10H18O Badawy et al. (2010) Geraniol (acaricidal, repellent) Pelargonium species Cymbopogon species Dianthus caryophyllus L. 178 (1.15) C10H18O Pohlit et al. (2011) Limonene (acaricidal) Citrus species Copaifera reticulata Ducke Hesperozygis ringens (Benth.) Epling Tetradenia riparia (Hochst.) Codd 0.26 (0.001) C10H16 Badawy et al. (2010) Linalool (acaricidal) Tagetes erecta L. Hesperozygis ringens (Benth.) Epling Ocimum basilicum L. Origanum onites L. Cymbopogon martini (Roxb.) W.Watson 0.50 (0.003) C10H18O Badawy et al. (2010) Myrcene (acaricidal) Origanum minutiflorum O. Schwarz & P.H. Davis Lippia javanica (Burm.f) Spreng. Salvia nilotica Juss. ex. Jacq. 0.55 (0.004) C10H16 Badawy et al. (2010) Pulegone (acaricidal) Mentha suaveolens Ehrh. 0.32 (0.002) C10H16O Pohlit et al. (2011) Tagetone (insecticidal) Tagetes species 0.001 C10H16O Gakuubi et al. (2016) Thymol (acaricidal) Thymus vulgaris L. Lippia sidoides Cham. Lippia gracilis Schauer Origanum. Minutiflorum O. Schwarz & P.H. Davis 5.50 (0.036) C10H140 de Oliveira Cruz et al. (2013) Diterpene Callicarpenal (repellent, acaricidal) Callicarpa americana L. 0.08 (0.0003) C16H26O Carroll et al. (2007) Sesquiterpene α-humulene (repellent) Lindera melissifolia (Walt.) Blume Stylosanthes humilis Kunth Cleome monophyla L. 4.82 (0.023) C15H24 Ogendo et al. (2011) β- caryophyllene Syzygium aromaticum (L.) Merr. & L.M. Perry Canabis sativum L. 0.04 (0.0001) C15H24 Govindarajan et al. (2016) Nootkatone (acaricidal) Chamaecyparis nootkatensis(D. Don) Spach Chrysopogon zizanioides (L.) Roberty Citrus grandis (L.) Osbeck 0.02 C15H22O Panella et al. (2005) Tetranotriterpenoid Azadirachtin (acaricidal) Azadirachta indica A.Juss Melia azedarach L. 5 (0.006) C35H14016 Giglioti et al. (2011) Naphthoquinone Plumbagin (acaricidal) Plumbago zeylanica L. 1.37 (0.007) C11H8O3 Annan et al. (2009) Organosulfur Allicin (insecticidal) Allium sativum L. 0.0002 C6H10OS2 Block (2004) Phenylpropanoid Eugenol (insecticidal, acaricidal) Ocimum species Artemisia species Plectranthus barbatus Andrews 0.025 (0.0001) C10H12O2 Govindarajan et al. (2016) Pyrethrin Pyrethrin I (acaricidal, insecticidal) Chrysanthemum species 0.0004 C21H28O3 Akhtar et al. (2008) Resin Oleoresin (acaricidal) Copaifera reticulata Ducke 1.57 (0.002) C18H27NO3 de Freitas Fernandes and de Paula Souza (2007) Steroidal glycoside Digitoxin (acaricidal) Calotropis procera (Aiton) Dyrand Digitalis purpurea L. 0.40 (0.0005) C41H64O13 Al‐Rajhy et al. (2003) a Molar concentration in brackets. 3.4. Meta-analyses of plant extracts with tick repellent and/or acaricidal properties Based on the meta-analyses, a total of 32, 33, 20, 24, 9, 9 and 4 plant species were evaluated separately for acaricidal, larvicidal, egg hatching inhibition, inhibition of oviposition and repellency of various plant extracts, including also the specific acaricidal effects of two selected plant families (Fig. 1, Fig. 2, Fig. 3, Fig. 4, Fig. 5, Fig. 6, Fig. 7). A total of 1 428 events were considered for acaricidal activities with a median efficiency value (MEV) of 80.12% (CI95%: 79.20–81.04; Fig. 1); while 1 924 events were considered for the larvicidal assays with a MEV of 86.05% (CI95%: 85.13–86.97; Fig. 2). For the egg hatching inhibition assays, a total of 574 events with a MEV of 83.39% (CI95%: 82.47–84.31; Fig. 3) while the inhibition of oviposition had the following values: MEV 53.01% (CI95%: 52.08–53.93) (Fig. 4). The repellency assays had MEV of 92.00% (CI95%: 91.08–92.93; Fig. 5) while the specific acaricidal effects of the two selected plant families (Lamiaceae and Asteraceae) with 281 and 68 events respectively was MEV of 80.79% (CI95%: 79.87–81.71; Fig. 6) and 48.34% (CI95%: 47.42–49.26; Fig. 7) respectively. Fig. 1 Download high-res image (396KB)Download full-size image Fig. 1. Meta-analyses of acaricidal effects of extracts of some plant species. 2-Acorus calamus (Sweet flag); 3-Anisomeles malabarica (Malabar catmint); 4-Allium sativum (Garlic); 5-Andrographis paniculata (King of bitters); 6-Artemisia absinthium (Absinthe wormwood); 7-Azadirachta indica (Neem); 8-Calotropis procera (Apple of Sodom); 9-Calpurnia aurea (Wild laburnum); 10-Capsicum frutescens (Malagueta pepper); 11-Carica papaya (Pawpaw); 12-Citrus maxima (Pomelo); 13-Citrus reticulata (Tangerin); 14-Citrus sinensis (Sweet orange); 15-Citrus hystrix (Kaffir lime); 16-Cymbopogon citratus (Lemon grass); 17-Cympobogon nardus (Citronella grass); 18-Datura stramonium (Devil’s snare); 19-Leucas aspera (Thumbai); 20-Leucas indica; 21-Matricaria chamomilla (Chamolile); 22-Melaleuca alternifolia (Narrow-leaved paperback); 23-Ocimum basilicum (Great basil); 24-Origanum onites (Turkish oregano); 26-Petiveria alliaceae (Guinea henweed); 27-Ricinus communis (Castor bean); 28-Satureja thymbra (Savory); 29-Tagetes erecta (Mexican marigold); 30-Tagetes patula (French marigold); 31-Tetradenia riparia (Ginger bush); 32-Piper aduncum (Spiked pepper); 33-Stemona collinsae; Red box on the x axis - Median efficiency value (MEV); Lines running perpendicular to the x-axis - Efficiency values of the various plant extracts; Error bars - 95% confidence interval. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article). Fig. 2 Download high-res image (253KB)Download full-size image Fig. 2. Meta-analyses of larvicidal effects of extracts of some plant species. 0-Allium sativum (Garlic); 1-Andrographis paniculata (King of bitters); 2-Artemisia absinthium (Absinthe wormwood); 3-Calea serrata (Snake herb); 4-Carica papaya (Pawpaw); 5-Citrus maxima (Pomelo); 6-Citrus reticulata (Tangerin); 7-Citrus sinensis (Sweet orange); 8-Citrus hystrix (Kaffir lime); 9-Croton sphaerogyrus (Croton); 10-Copaifera reticulata (Copiaba); 11-Cymbopogon citratus (Lemon grass); 12-Cympobogon nardus (Citronella grass); 13-Datura stramonium (Devil’s snare); 14-Eucalyptus citriodora (Lemon-scented gum); 15-Eupatorium adenophorum (Sticky snakeroot); 16-Guiera senegalensis (Moshi medicine); 17-Hypericum polyanthemum (St. John’s wort); 18- Leucanea leucocephala (White leadtree); 19-Licania tomentosa; 20-Lippia sidoides (Pepper-rosmarin); 21-Lysiloma latisiliquum (False tamarind); 22-Ocimum urticaefolium (Basil); 23-Petiveria alliaceae (Guinea henweed); 24-Piper tuberculatum (Painful pepper); 25-Piscidia piscipula (Fishpoison tree); 26-Simarouba versicolor (Bitter wood); 27- Solanum trilobatum (Nightshade); 28-Tagetes erecta (Mexican marigold); 29-Tagetes patula (French marigold); 30-Tetradenia riparia (Ginger bush); 31-Thymus vulgaris (Thyme); 32-Ocimum canum (Camphor basil); Red box on the x axis - Median efficiency value (MEV); Lines running perpendicular to the x-axis - Efficiency values of the various plant extracts; Error bars - 95% confidence interval. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article). Fig. 3 Download high-res image (307KB)Download full-size image Fig. 3. Meta-analyses of egg hatching inhibition effects of extracts of some plant species. 2-Anisomeles malabarica (Malabar catmint); 3-Allium sativum (Garlic); 4-Ananas comosus (Pineapple); 5-Artemisia absinthium (Absinthe wormwood); 6-Baccharis trimera; 7-Calea serrata (Snake herb); 8-Capsicum frutescens (Malagueta pepper); 9-Guiera senegalensis (Moshi medicine); 10-Jatropha curcas (Psychic nut); 11- Leucanea leucocephala (White leadtree); 12-Leucas aspera (Thumbai); 13-Leucas indica; 14-Lysiloma latisiliquum (False tamarind);15-Melaleuca alternifolia (Narrow-leaved paperback); 16-Petiveria alliaceae (Guinea henweed); 17-Piper tuberculatum (Painful pepper); 18-Piscidia piscipula (Fishpoison tree); 19-Tetradenia riparia (Ginger bush); 20-Vitex negundo (Five-leaved chaste tree); 21-Withania somnifera (Poison gooseberry); Red box on the x axis - Median efficiency value (MEV); Lines running perpendicular to the x-axis - Efficiency values of the various plant extracts; Error bars - 95% confidence interval. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article). Fig. 4 Download high-res image (535KB)Download full-size image Fig. 4. Meta-analyses of inhibition of oviposition effects of extracts of some plant species. 2-Acorus calamus (Sweet flag); 3-Allium sativum (Garlic); 4-Ananas comosus (Pineapple); 5-Artemisia absinthium (Absinthe wormwood); 6-Calea serrata (Snake herb); 7-Capsicum frutescens (Malagueta pepper); 8-Carica papaya (Pawpaw); 9-Datura stramonium (Devil’s snare); 10-Hypericum polyanthemumh (St John’s wort); 11-Jatropha curcas (Psychic nut); 12- Leucanea leucocephala (White leadtree); 13-Leucas indica; 14-Lysiloma latisiliquum (False tamarind);15-Matricaria chamomilla (Chamolile); 16-Melaleuca alternifolia (Narrow-leaved paperback); 17-Petiveria alliaceae (Guinea henweed); 18-Piper tuberculatum (Painful pepper); 19-Piscidia piscipula (Fishpoison tree); 20-Ricinus communis (Castor bean); 21-Tagetes patula (French marigold); 22-Tetradenia riparia (Ginger bush); 23-Vitex negundo (Five-leaved chaste tree); 24-Withania somnifera (Poison gooseberry); Red box on the x axis - Median efficiency value (MEV); Lines running perpendicular to the x-axis - Efficiency values of the various plant extracts; Error bars - 95% confidence interval. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article). Fig. 5 Download high-res image (243KB)Download full-size image Fig. 5. Meta-analyses of repellency effects of extracts of some plant species. 2-Cassia didymobotrya (African senna); 3-Gynandropsis gynandra (Cat’s whiskers); 4-Lavandula angustifolia (English lavender); 5-Lindera melissifolia (Pondberry); 6-Lippia javanica (Lemon bush); 7-Pelargonium graveolens (Rose geranium); 8-Ptaeroxylon obliquum (Sneezewood tree); 9-Tagetes minuta (Southern marigold); 10-Cleome monophylla (Single-leaved cleome); Red box on the x axis - Median efficiency value (MEV); Lines running perpendicular to the x-axis - Efficiency values of the various plant extracts; Error bars - 95% confidence interval. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article). Fig. 6 Download high-res image (254KB)Download full-size image Fig. 6. Meta-analyses of acaricidal effects of extracts of some plant species in the Lamiaceae family. 2-Anisomeles malabarica (Malabar catmint); 3-Leucas aspera (Thumbai); 4-Leucas indica; 5-Ocimum basilicum (Great basil); 6-Origanum minutiflorum (Wild origanum); 7-Origanum onites (Turkish oregano); 8-Satureja thymbra (Savory); 9-Tetradenia riparia (Ginger bush); 10-Vitex negundo (Five-leaved chaste tree); Red box on the x axis - Median efficiency value (MEV); Lines running perpendicular to the x-axis - Efficiency values of the various plant extracts; Error bars - 95% confidence interval. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article). Fig. 7 Download high-res image (141KB)Download full-size image Fig. 7. Meta-analyses of acaricidal effects of extracts of some plant species in the Asteraceae family. 2-Artemisia absinthium (Absinthe wormwood); 3-Matricaria chamomilla (Chamolile); 4-Tagetes erecta (Mexican marigold); 5-Tagetes patula (French marigold); Red box on the x axis - Median efficiency value (MEV); Lines running perpendicular to the x-axis - Efficiency values of the various plant extracts; Error bars - 95% confidence interval. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article). 4. Discussion The use of botanicals for the control of ticks has a long history as an important component of traditional medicine in Africa and Asia, where most resource-poor farmers use plant materials to treat endo- and ectoparasites of livestock (Mondal et al., 2013). Traditional knowledge about the use of these plants is transferred through successive generations, especially in rural communities. Knowledge about the use of individual plant species, however, varies between localities in Africa and scientific validation of their uses may increase the range of plant species available for tick control and reduce the burden substantially on those that are at risk of extinction (Nchu et al., 2012). Pesticidal plant research in veterinary parasitology is a recent area of research globally when compared with screening of plant extracts for the treatment of bacterial diseases. Plant extracts contain mixtures of substances that can act synergistically, in different ways, which makes the development of parasite resistance more difficult than normally occurs with single compound acaricides (Varma and Dubey, 1999). According to Katoch et al. (2007), the efficacy of a single plant can be enhanced by a judicious combination with another plant or active ingredient that has adjuvant properties. This combination of phytochemicals with different mechanisms of action usually lowers the LD50 of the product and hampers the development of resistance by the ticks. 4.1. Tick species studied Rhipicephalus (Boophilus) microplus (Canestrini 1887) (Acari, Ixodidae), a one-host tick, was the most commonly studied tick. This is linked to its wide distribution and importance as a cattle parasite. It portends a major threat to the cattle industry in tropical and subtropical areas with huge economic implications (Domínguez-García et al., 2010). Rhipicephalus (B.) microplus is responsible for severe losses caused by tick worry, blood loss, damage to hides, injection of toxins and is a vector for many tick-borne diseases. In Australia, the overall losses caused by this tick were estimated to be more than 100 million AUD (75 million USD) per annum and in South Africa, losses were projected at between 70–200 million ZAR (5.6–16 million USD) per annum (Peter et al., 2005). It is unclear whether the outcome of these experiments on a one-host tick can be applied to other species of ticks that infest animals and humans. 4.2. Repellency activity From our review also, 27 plant species from 18 families have been shown to have tick repellent activity but relatively little research has been conducted to determine how ticks detect repellents. Carroll et al. (2005) noted that most repellency assays for ticks do not discriminate between repellency via tactile chemoreception or sensory chemoreception. Olfactory sensilla can detect vaporized molecules and evidence suggests that olfaction is involved at least, in part in repellency (Bissinger and Roe, 2013). Nonetheless, very little is known about chemoreception in ticks at the molecular level. Chemoreception in both mammals and insects relies on several families of transmembrane receptors that detect volatile and non-volatile compounds. There are differences in the structures and functioning of the signalling mechanisms of these receptors (Silbering and Benton, 2010). The duration of protection of tick repellent compounds may vary depending on the mode of testing, the formulation of the product, the concentration of the active ingredient, the tick species tested, the developmental stage of the tick species, the fitness of the developmental stage and the absence of adaptation or resistance. Different concentrations of a substance can change the direction of the behavioural response. Unfortunately, in many of the papers reviewed, the concentrations of substances tested are not clearly stated. Another important consideration is that host-seeking ticks respond to host odours and other host cues. Most plant volatiles are generally emitted from the plants and not from tick hosts and as such, may mask the host odours thereby disrupting the host-seeking behaviour or disorientating the host-seeking ticks rather than acting as true repellents. For a repellent to be ideal, it should provide protection against many blood-feeding arthropods for at least eight hours, be non-toxic, non-irritating, odourless and non-greasy (Bissinger and Roe, 2010). Such a repellent is yet to be developed. 4.3. Acaricidal and growth inhibition activities In total, 55 plant species from 22 families had substantial acaricidal and growth inhibition properties. The families with the highest frequencies were: Lamiaceae (20%), Asteraceae (13%), Rutaceae and Fabaceae (9%) and Solanaceae (7%). Most of the studies used essential oils followed by ethanol, methanol, acetone, hexane, chloroform, water, dichloromethane and ethyl acetate extracts of the plants. The number of extracts does not neccesarily indicate which extracts had the highest activity, but rather which extracts were mainly used. The penetration of a parasiticide varies according to the thickness of the layer of lipids on the cuticle and the solubilizing ability of the active compound. This can vary according to the species and developmental phase of the parasite. Therefore, the susceptibility differences between the stages found in many of the studies can be related to the composition and/or thickness of the tick cuticle. The waxy layer only occurs after nymph ecdysis and is most pronounced in adult ticks. Therefore, toxic chemicals may be sequestered within the wax, hampering their efficacy (Sonenshine, 1993). A toxic physical effect through cuticle solubilization by the essential oils in plants cannot be excluded, although terpenes and phenylpropanoids are known to act on the octopaminergic receptor which acts as neurotransmitter, neurohormone and neuromodulator in invertebrates (Regnault-Roger, 2013). Another approach that could be relevant in the sustainable management of ticks is through the disruption of their life cycle by targeting immature stages. This may result in the reduction of tick infestations to low and controllable levels, hence reducing the tick population during favourable climatic conditions. Though some plant species such as Melaleuca alternifolia, Piper tubeculatum, Carica papaya, Guiera seneganlensis, Melia azedarach and Tetradenia riparia did not show high acaricidal mortality, they however caused 100% inhibition of oviposition and hatchability, thereby disrupting life stages of the ticks. The bioactive compound azadirachtin present in Azadirahta indica and Melia azedarach fruit extracts affects tick embryo development and moulting stages. Sheep which consumed feed containing Azadirachta indica fruit and kernel extracts had no noticeable signs of toxicity (Pohlit et al., 2011). This diet, however, negatively affected the ability of the American dog tick Dermacentor variabilis to feed on sheep blood with 4.35–4.81 μg/ml plasma levels of azadirachtin over 14 days. This implies that Azadirachta indica extracts as food additives may have applications in tick control for use in public health and veterinary applications. 4.4. Isolated compounds Plant essential oils are complex mixtures of natural, volatile organic compounds predominantly composed of terpenic hydrocarbons (myrcene, pinene, terpinene, limonene, p-cymene, α- and β-phellandrene), acyclic monoterpene alcohols (geraniol, linalool), monocyclic alcohols (menthol, 4-carvomenthol, terpineol, carveol, borneol), aliphatic aldehydes (citral, citronellal, perillaldehyde), aromatic phenols (carvacrol, thymol, safrol, eugenol) (Tabara et al., 2017), bicyclic alcohol (verbenol), monocyclic ketones (menthone, pulegone, carvone), bicyclic monoterpenic ketones (thujone, verbenone, fenchone), acids (citronellic acid, cinnamic acid) and esters (linalyl acetate) (Nerio et al., 2010). Different arthropod species respond quite differently to specific plant volatiles. Benzaldehyde and benzyl alcohol are toxic to the storage mite Tyrophagus putrescentiae Schranck but are, at lower concentrations, attractants to Amblyomma ticks (Yoder et al., 1998). Eucalyptol (1, 8-cineole), which is a characteristic leaf compound of the genus Eucalyptus, is repellent and toxic to most insects, but exhibits attractant activity for some insects belonging to different orders such as Coleoptera and Lepidoptera (Parra et al., 2009). Linalool, which is ubiquitously present in flowers and induced in wounded plant leaves, is repellent to blood-seeking Culex pipiens female mosquitoes (Choi et al., 2002), but is an attractant to the honey bee, Apis mellifera L. (Henning et al., 1992). Methyl salicylate, a volatile emitted from flowers and stressed plants, is also a component of the aggregation-attachment pheromone of Amblyomma ticks and Sarcoptes scabiei mites but is highly toxic to house dust mites, Dermatophagoides and Tyrophagus (Jaenson et al., 2005). Myrcene is repellent to R. appendiculatus and the maize weevil Sitophilus zeamais but highly toxic to many insects, including house flies, cockroaches and Culex mosquito larvae (Koul et al., 2008). In this review, approximately 26 isolated active compounds have been identified from plant essential oils with tick repellent and/or acaricidal properties. Compounds such as geraniol, 2-undecanone, limonene and azadirachtin already have important commercial applications in a variety of commercial products which are useful for tick control (Benelli et al., 2016a). Geraniol, a monoterpene alcohol found in many plants, is an active ingredient in many commercially available insect repellents and has repellent activity against ticks (Chen and Viljoen, 2010). Geraniol appears on the United States Environmental Protection Agency’s list of compounds that are exempt from federal regulation because they are considered demonstrably safe. Some other compounds such as plumbagin, nootkatone and eugenol, might be interesting as lead molecules for the development of effective repellents. 4.5. Meta-analyses From the meta-analyses results, the efficiency values of various plant extracts showed minimal to wide disparities compared to the MEV for each category. Approximately 63% and 69% of all the plant species evaluated for acaricidal and larvicidal assays respectively surpassed the MEV respectively. This means that there is huge potential for plant-based tick repellents, acaricides and larvicides among the evaluated plant species. 4.6. In vitro tick repellent and acaricidal bioassays One major shortfall in research for new plant-based tick repellents and acaricides is the lack of a standardized testing method (Adenubi et al., 2018). For the papers reviewed, a wide range of methods were employed for testing for tick repellency and acaricidal effects. Tick climbing repellency, Petri dish, larval packet, immersion tests amongst others were used. Studies differed in the time frame in which repellence or toxicity was evaluated, the species and life stages of ticks used, the concentration of active ingredients from crude plant extracts, fractions or essential oils, use of different solvents (extractants) and the use of animal host cues or not. These variations identified made comparing results from different authors difficult. This difficulty has been earlier reported by Bissinger and Roe (2010) and Benelli et al. (2017a,b). Very recently, major challenges for future research have been outlined by Benelli and Pavela (2018) and Adenubi et al. (2018). It becomes expedient to develop a standardized laboratory test as a means of obtaining easily comparable data. 4.7. In vivo tick repellent and acaricidal bioassays Difficulty in transposing the efficacy obtained from the laboratory to the field is one of the main obstacles of phytotherapy research in animal health (Borges et al., 2011). Moreover, toxicity studies to identify risks to animal and human health cannot be neglected. Only about 17% of the studies attempted to determine the mechanism of action of the plant extract or isolated compound tested, while only 5 of the studies progressed to in vivo experiments. Methods used to test for bioactivity in vitro should conform to minimum standards and where possible, should be confirmed with in vivo tests. This recommendation for in vivo use of the plant extracts depends on careful toxicological studies and pharmacokinetic investigations to ensure that standardized extracts are used (Cañigueral et al., 2008). Achieving significant efficacy and adequate residual periods in field conditions are the new challenges of this research area, since the acaricidal activity of various plant species has been well documented in vitro (de Souza Chagas et al., 2012). Very recently Nyahangare et al. (2018) found that a water-detergent oil root extract of Maerua edulis had higher activity in protecting cattle against ticks than Amitraz the commercially used acaricide. Alternatively, if facilities for in vivo studies are not available, a battery of in vitro bioassays designed to investigate potential mechanisms of action will also provide useful information. 4.8. Future potential With the identification of plant species having such great potential use in veterinary parasitology, further studies are necessary to isolate more active compounds, elucidate their mechanisms of action, side effects and formulation development to improve their efficacy and stability (Maia and Moore, 2011). Factors such as seasonality, circadian rhythm, plant age and development stage, temperature, water availability, ultraviolet radiation and soil nutrients, can affect the concentration of secondary metabolites especially volatile compounds in plants (Gobbo-Neto and Lopes, 2007). Formulations to protect the active compounds from environmental degradation (to maintain stability) and enable fast penetration into ticks are needed. Formulation plays a crucial role in extending the duration of efficacy of a repellent. For example, a polymer formulation of DEET and cream formulations of Picaridin and SS220 provided almost complete repellency to nymphal Amblyomma americanum for 12 h (Carroll et al., 2008). The plant-derived repellent, 2-undecanone provided 74% repellency against Dermacentor variabilis 2 h after application when unformulated compared to 98% repellency from 3 to 3.5 h after application when formulated in the product BioUD (Bissinger et al., 2011; Kimps et al., 2011). These studies should be conducted with experts in chemistry, pharmacology, pharmacy formulation, entomology and veterinary drug companies. This is necessary to determine the most appropriate adjuvant and develop formulation models that can be adapted based to the nature of the plant extract or bioactive compound isolated. Simple formulations based on plant extracts or essential oils, tend to have a short residual activity due to instability or volatility of the bioactive compounds. This may possibly be circumvented by a study of the main chemical constituents in each new harvest. Subsequently, dose adjustments could be recommended to farmers in accordance with this variation. Commercial formulations composed of one natural bioactive compound allow greater control of the efficacy and quality of raw materials. Also, in vivo efficacy studies (field trials) using formulated products are clearly essential and the economic feasibility of the products must be demonstrated. The standardization of components, extraction techniques, experimental design, mammalian toxicology profiling and excipient development, as well as further investigation into the residual activities and length of shelf-life of these plant species are required before their potential can be fully explored (Ellse and Wall, 2014). 4.9. Future research The focus of this publication was to do a meta-analysis of which plant extracts had high activities in different assays. Several questions and theories posed by us in this review may have been addressed/resolved in other manuscripts that we missed by the key words we used. For future purposes, some areas of research can be considered: 1) The probable differences in enantiomeric purity of essential oil components which are purchased and used in bioassays to confirm the active tick repellent and acaricidal activities in many of the references cited. 2) Deciphering the synergistic, suppressive and other interactions of the components of plant extracts and essential oils. In many of the papers reviewed herein, the active compounds isolated have lesser efficacies than the plant extracts and essential oils from which they were isolated. It remains unclear whether the compound in itself is more active or whether synergism (a cocktail of components) is responsible for the effects of the plant species. 3) Determining the mechanisms of action of the bioactives. 5. Conclusion The use of plant species in the control of veterinary ectoparasites is an exciting area which holds much potential for the future. The potential use of this knowledge by pastoral farmers using low level technology also requires serious attention, especially in developing countries. The overview presented in this work could be useful to scientists who are new in the field and should attract necessary funding for future research to present viable alternatives in overcoming the problem of acaricidal drug resistance. Conflict of interest The authors declare no conflict of interest. Acknowledgements The Phytomedicine Programme at University of Pretoria, the Schlumberger Faculty for the Future Foundation and the National Research Foundation of South AfricaIPPR95991 to JNE) provided funding. References Aboelhadid et al., 2013 S. Aboelhadid, A. Kamel, W. Arafa, K. Shokier Effect of Allium sativum and Allium cepa oils on different stages of Boophilus annulatus Parasitol. Res., 112 (2013), pp. 1883-1890 CrossRefView Record in Scopus Adenubi et al., 2016 O. Adenubi, F. Fasina, L. McGaw, J. Eloff, V. 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