Exp Appl Acarol (2009) 48:31–41 DOI 10.1007/s10493-009-9254-2 In vitro efficacies of oils, silicas and plant preparations against the poultry red mite Dermanyssus gallinae Veronika Maurer Æ Erika Perler Æ Felix Heckendorn Received: 15 December 2008 / Accepted: 6 February 2009 / Published online: 20 February 2009 Ó Springer Science+Business Media B.V. 2009 Abstract The aim of this study was to test the effectiveness of physically acting substances (oils and silicas) and plant preparations for the control of the poultry red mite Dermanyssus gallinae (De Geer 1778). Reproduction and survival of fed D. gallinae females were evaluated in vitro for a total of 168 h using the ‘‘area under the survival curve’’ (AUC) to compare survival of the mites between treatments. Four oils (two plant oils, one petroleum spray oil and diesel), one soap, three silicas (one synthetic amorphous silica, one diatomaceous earth (DE) and one DE with 2% pyrethrum extract) and seven plant preparations (derived from Chrysanthemum cineariaefolium, Allium sativum, Tanacetum vulgare, Yucca schidigera, Quillaja saponaria, Dryopteris filix-mas, and Thuja occidentalis) were tested at various concentrations. All the oils, diesel and soap significantly reduced D. gallinae survival. All silicas tested inhibited reproduction. DE significantly reduced mite survival, but amorphous silica was less effective in vitro. Except for pure A. sativum juice and the highest concentration of C. cineariaefolium extract, the plant preparations tested resulted in statistically insignificant control of D. gallinae. Keywords Dermanyssus gallinae
Ectoparasite
Control
Silicas
Oils
Plant extracts Introduction The poultry red mite Dermanyssus gallinae (De Geer 1778) is regarded as the most important ectoparasite of laying hens in organic as well as conventional egg production in Europe (Maurer et al. 1993; Höglund et al. 1995; Fiddes et al. 2005). The haematophagous mite is a nocturnal feeder and spends the daylight hours in refugia in the vicinity of the hens. At high population densities D. gallinae can cause severe anaemia and associated V. Maurer (&)
E. Perler
F. Heckendorn Research Institute of Organic Agriculture (FiBL), Ackerstrasse, 5070 Frick, Switzerland e-mail: veronika.maurer@fibl.org 123 32 Exp Appl Acarol (2009) 48:31–41 mortality (Kirkwood 1967). Even low mite populations can irritate hens to the extent that they refuse to use the henhouse or rest on the perches (Maurer et al. 1995; Kilpinen et al. 2005). Production can also be affected by reductions in egg production and egg quality, where mites may cause staining of the egg shell surface (Cencek 2003). Since D. gallinae may also act as a vector for numerous pathogens of medical and veterinary importance, spread of disease is another problem associated with this mite in poultry systems (Chirico et al. 2003). D. gallinae causes nuisance and dermatitis in people working in heavily infested poultry houses (Rosen et al. 2002). Dermanyssus gallinae are typically controlled by treating the poultry house installations rather than the hens themselves (Hoop 2008). Several synthetic acaricide classes are widely used for mite control (organophosphates, pyrethroids, carbamates), but D. gallinae has developed resistance against some of these compounds (Zeman and Zelezny 1985; Beugnet et al. 1997; Nordenfors et al. 2001). In addition, some compounds are unsuitable for food safety and environmental reasons (Chauve 1998). On organic farms, synthetic acaricides may be used as a last resort, but D. gallinae control should primarily be achieved by preventive measures and acaricides of natural origin according to national and international regulations (e.g. the Council Regulation (EC) No 834/2007; EC 2007). A three-stage control system is widely applied on Swiss organic farms. The concept includes management practices as a first stage (such as cleaning and disinfection of the empty house after each cycle). As a second stage, physically acting substances (such as oil and desiccant dusts) are used during flocks. As a third and final stage, acaricides of natural origin are selectively applied to highly infested sites in the house. Physically acting substances such as oils and dusts offer an attractive alternative to synthetic acaricides because resistance is less likely to occur. Acaricides of natural origin have been researched for several areas of pest management with encouraging results (Isman 2006). Varroa destructor and the tracheal mite Acarapis woodi are examples for parasitic mite species which can successfully be controlled with acaricides of natural origin (Rice et al. 2002). Some work has already been conducted with natural plant preparations for their effect on D. gallinae where recent studies have focused on in vitro effects of oriental medicinal plant extracts (Kim et al. 2007) and plant essential oils (Kim et al. 2004; George et al. 2008a, b). With both natural plant preparations and physically acting substances showing promise for D. gallinae management, it is important that comparisons are made between these methods to maximize the effectiveness of existing or potential non-synthetic D. gallinae control strategies. This paper deals with the in vitro effectiveness of oils, silicas, and selected plant preparations for the control of D. gallinae with the aim of comparing the efficacy of these different non-synthetic control options. Materials and methods Dermanyssus gallinae Fed D. gallinae females were obtained from a naturally infested poultry house at the Research Institute of Organic Agriculture, Ackerstrasse, Switzerland. The mites were collected in traps consisting of a u-shaped aluminium-profile containing a strip of fabric in a zigzag fold fixed under the perches during one night (Maurer et al. 1993). All mites were used for the tests within 1 day of collection. 123 Exp Appl Acarol (2009) 48:31–41 33 Test substances Table 1 gives an overview of the test substances, their origin, and concentration tested. A total of four oils (two plant oils, one petroleum spray oil and diesel), one soap, three silicas (one synthetic amorphous silica, one diatomaceous earth (DE) and one DE with 2% pyrethrum extract) and plant preparations based on Chrysanthemum cineariaefolium, Allium sativum, Tanacetum vulgare, Yucca schidigera, Quillaja saponaria, Dryopteris filix-mas, and Thuja occidentalis were tested. Six of these test substances were tested at various concentrations and/or mixtures. In vitro assay Oils and plant preparations Five fed adult female mites were transferred into plastic vials (ø 33 9 16 mm) with a tightly closing lid containing a filter paper disk (ø 27 mm) saturated with the test substance. The following controls were used: untreated (water) for water extracts and alcohol (EtOH 10%) for EtOH extracts. Silicas (powders and liquid formulation) Five fed adult female mites were transferred into the same type of plastic vials containing 0.05 or 0.005 g of the powders (9 or 0.9 mg/cm2) or a filter disk treated with the amount of liquid test product containing 0.05 g of dry matter and air dried before the test. Untreated vials served as controls. Numbers of replicates used per concentration are indicated in Table 1. Vials were placed together to assure a similar macro-environment. Treatments were randomly assigned to the vials. The mites were kept at 27°C in dark during the experiments. Surviving mites were counted after 4, 24, and 168 h under a binocular microscope. Mites showing no symptoms as well as stricken mites (movements, but no locomotion) were classified as ‘‘alive’’. Mites were considered ‘‘dead’’ if no movement was visible even after a gentle touch with a paint brush. The presence of offspring (eggs, larvae and/or unfed protonymphs) was qualitatively recorded at each observation interval. Data analysis For statistical comparison of D. gallinae survival, the integral of the survival curves was estimated for each vial (trapezoidal integration). The calculated ‘‘area under the curve’’ (AUC) has units of ‘‘percent-hours’’ (Campbell and Madden 1990). For each vial, AUCs were calculated for the periods from 0 to 4 h and from 0 to 168 h after treatment, respectively (herein after referred to as AUC4 and AUC168). The non parametric Kruskal–Wallis test was used to provide estimates of the global difference between groups separately for: oils (nine treatment groups including the control), silicas (five treatment groups), water-based plant preparations (13 treatment groups) and ethanol-based plant preparations (three treatment groups). In case of a significant result of the global test, pair-wise comparisons were made between the treatment groups using the Mann–Whitney rank sum test. P-values of the pairwise comparisons where adjusted for multiple comparisons according to the formula: p - value ¼ a  2=kðk  1Þ 123 34 123 Table 1 Test substances used in in vitro assay with Dermanyssus gallinae: origins, concentrations and numbers of replicates Scientific name Supplier Concentrations Specification/brand Active ingredient tested (g/l) name of commercial in commercial product (g/l or g/kg) product 1,000 10 Rapeseed oil Local shop Food-grade 1,000 1,000 10 Orange oil Wigger, Althäusern (CH) ParasitexÒ 50 50, 5, 2.5 10, 15, 10 Diesel (fuel) Local shop Fuel 1,000 1,000 15 Common name Plant part/extraction method Replicates (number of vials) Oils/soap H2 O Water, control Petroleum spray oil Omya, Oftringen (CH) Mineral Oil OmyaÒ 990 990 10 Soap Biocontrol, Grossdietwil (CH) NaturalÒ 1,000 1,000, 100, 10 10 0 20 Synthetic amorphous silica Evonik Degussa, Frankfurt (DE) Indispron D110Ò 1,000 0.005a 10 Diatomaceous earth Biovet, Grossdietwil (CH) Gallo-SecÒ 1,000 0.005, 0.0005a 10 Diatomaceous earth & pyrethrum extract Agro-Hygiene AG, Wald (CH) FLY-END Acaricide powderÒ 9,980 & 20 0.0005a 10 1,000 50 Pyri-FlyÒ 20 2, 0.2, 0.02 10 1,000, 100, 10 10, 5, 5 1,000 10 Silicas Empty vial, control Commercial product, water extracts and mechanically pressed juices H2 O Water, control Chrysanthemum Pyrethrum cinerariaefolium Biovet, Grossdietwil (CH) Allium sativum Garlic Bulb/mechanically Local shop pressed fresh juice Tanacetum vulgare Tansy Superficial parts; start In house production of full bloom/water extract Organic production Exp Appl Acarol (2009) 48:31–41 Plant preparations Concentrations Specification/brand Active ingredient tested (g/l) name of commercial in commercial product (g/l or g/kg) product Replicates (number of vials) Scientific name Common name Plant part/extraction method Supplier Yucca schidigera Mohave yucca Leaves/mechanically pressed, thermally condensed Desert King International, San Diego (USA) 1,000, 100 10, 10 Quillaja saponaria Soapbark tree Bark/water extract Desert King International, San Diego (USA) 1,000, 100 20, 10 Yucca:Quillaja 1:1 See above See above Desert King International, San Diego (USA) 500 : 500 10 Exp Appl Acarol (2009) 48:31–41 Table 1 continued Ethanol extracts a EtOH Ethanol, control 100 10 Dryopteris filix-mas Male-fern Leaves/ethanol extract In house production 960 100 10 Thuja occidentalis Arborvitae Leaves/ethanol extract In house production 100 10 g/vial 35 123 36 Exp Appl Acarol (2009) 48:31–41 (Bonferroni Correction; Lu and Fang 2003), where k = number of comparisons and a = agreed chance of falsely positive result (here 0.05). Reproduction data was analysed separately for oils, silicas and water-based plant preparations using logistic regression models. All data was analysed using STATAÒ 9.0 (StataCorp LP, 4905 Lakeway Drive, TX 77845, USA) software. Results Table 2 presents the proportion of vials with reproduction and the AUC of the oil, silica, and plant preparation treatments. In all control vials reproduction occurred during the experiment and AUCs were close to or at the maximum possible values. Oils Plant (rapeseed and orange) as well as petroleum spray oil and diesel reduced D. gallinae reproduction and the AUCs, including AUC4, which indicates a rapid effect of those products. Treatments with the petroleum spray oil and diesel significantly reduced the AUC168 values by 95% and more. Orange oil was significantly effective at concentrations of 5% only. Mites treated with 100% soap did not reproduce, but the effect on survival was significant only after 1 week (AUC168). Silicas Female mites did not produce eggs in any of the silica treatments. DE with or without additional pyrethrum increased mortality of the mites later than 4 h after treatment, reflected by high AUC4 and low AUC168. Synthetic amorphous silica was not effective. Plant preparations Egg production was observed in all treatments except for the highest dose of pyrethrum and the higher doses of garlic juice. Pure garlic juice was the only plant preparation which quickly killed D. gallinae, as reflected by a significantly reduced AUC4 by 50%. Of the several preparations tested, only pyrethrum 0.2 and 0.02% and garlic juice 10 and 100% significantly reduced AUC168 by more than 50%. A dose-response of the pyrethrum treatment was seen in the % vials with reproduction as well as in the AUC168 values. Discussion Untreated mites reproduced and their survival was close to the maximum possible value. This indicates that the experimental conditions used were favourable for survival and reproduction of the fed D. gallinae females. George et al. (2008b) suggest that D. gallinae are more susceptible to the effects of plant essential oils after starving for 3 weeks than recently fed mites. Our experimental conditions using fed females therefore represent a 123 Name (brand name or specification) Concentration (g/l) Reproduction Proportion of replicates with juveniles AUC4 AUC168 Difference Mean (percent- Difference to control (%) hoursb) to control (%) Mean (percenthoursb) Difference to control (%) Oils/soap Control – 1 Rapeseed oil 1,000 0.4 -60* 284 400 -29.0* 16,470 2,632 -84.1* Orange oil 50 0 -100** 256 -36.0* 2,012 -87.8* -51.4 Orange oil 5 0.66 -34 336 -16.0 8,021 Orange oil 2.5 1 0 392 -2.0 13,976 Diesel 1,000 0 -100** 205 -48.7* 232 Exp Appl Acarol (2009) 48:31–41 Table 2 Area under the curve (AUC) of Dermanyssus gallinae 4 h (AUC4) and 7 days (AUC168) after treatment with potential acaricides -15.4 -98.6* Petroleum spray oil 990 0 -100** 304 -24.0 824 -95.0* Soap 1,000 0 -100** 324 -19.0 3,568 -78.4* Soap 100 0.7 -30 344 -14.0 7,880 -52.3 Control (empty vial) – 1 Synthetic amorphous silica 0.005a 0 -100** 400 0.0 7,796 -51.7 Diatomaceous earth 0.005a 0 -100** 352 -12.0 1,112 -93.1* Diatomaceous earth 0.0005a 0 -100** 352 -12.0* 1,194 -92.6* Diatomaceous earth & Pyrethrum 0.0005a extract 0 -100** 400 1,892 -88.3* Silicas 400 16,152 0.0 Plant preparations commercial product, water extracts and mechanically pressed juices Control (water) 1 0 -100** 400 0.0 1,400 -91.5* Chrysanthemum cinerariaefolium 0.2 0.33 -67* 346 -13.5 5,581 -66.1* 0.0 1,450 Chrysanthemum cinerariaefolium 0.02 Allium sativum 1,000 400 1 0 400 0 -100** 200 16,470 -50.0* 200 -11.7 -98.8* 37 123 – Chrysanthemum cinerariaefolium 2 38 123 Table 2 continued Name (brand name or specification) Concentration (g/l) Reproduction AUC4 AUC168 Proportion of replicates with juveniles Difference Mean (percent- Difference to control (%) hoursb) to control (%) Mean (percenthoursb) Difference to control (%) Allium sativum 100 0 -100** 400 0.0 5,008 -69.6* Allium sativum 10 1 0 400 0.0 15,936 -3.2 Tanacetum vulgare 1,000 1 0 400 0.0 15,504 -5.9 Yucca schidigera 1,000 1 0 400 0.0 11,432 -30.6* -12.9 Yucca schidigera 100 1 0 400 0.0 14,352 Quillaja saponaria 1,000 1 0 392 -1.2 1,244 -24.4* Quillaja saponaria 100 1 0 400 0.0 13,056 -20.7 Yucca:Quillaja 1:1 1,000 1 0 400 0.0 10,320 -37.3* Control (EtOH 10%) 100 1 0 400 Dryopteris filix-mas 100 1 0 400 0.0 14,456 -12.5 Thuja occidentalis 100 1 0 400 0.0 16,665 ?0.9 Ethanol extracts a g/vial b Campbell and Madden (1990) Exp Appl Acarol (2009) 48:31–41 * P \ 0.05; ** P \ 0.01 16,512 Exp Appl Acarol (2009) 48:31–41 39 more severe test of product efficacy than tests with starved mites as proposed e.g. by Thind and Ford (2006). The effects of oils on plant pest insects and mites have been investigated in some detail (e.g. Agnello et al. 2003; Fernandez et al. 2005). Mineral oil was more toxic to adult phytoseiid mites than plant oil (Momen et al. 2006). A study on the effects of oils on D. gallinae showed that a mineral oil developed for agricultural use (OPPA) caused 100% mite mortality after 2 h of exposure when sprayed directly on the mites (Guimaraes and Tucci 1992). None of the oils tested in the current study acted as quickly and completely, probably because the contact of the mites with the test substances in the experimental setup was reduced as compared to that in the aforementioned study, where mites where completely covered by means of spraying. Diesel reduced the AUC4 by 50% in the current study, and the AUC168 by almost 100%. However, odour and associated risk of egg contamination are a serious drawback of diesel, which is not recommended for use in poultry houses on this basis (Hoop 2008). Slightly higher AUC168s were attained by the odourless and relatively cheap petroleum spray oil and rapeseed oil, making these interesting alternatives to diesel. The effects of the undiluted product containing 5% orange oil were similar to those of diesel and petroleum spray oil. The disadvantage of this treatment is the high cost of the effective concentration. Inert dusts based on silica are commonly used as desiccating agents against storedproduct pests (Collins 2006; Palyvos et al. 2006). Silicas act physically and their activity is not dependent on metabolic pathways. In our experiment, neither the treatment dose (mg/ vial) nor the addition of Pyrethrum extract improved upon the already favourable efficiency of DE. Mortality from DE exposure is mainly a result of desiccation (Saez and Fuentes Mora 2007), and arthropods are therefore not expected to develop genetic resistance. However, insects have been shown to develop behavioural responses to avoid contact with such products (Ebeling 1971), and this may also be the case for mites. Drawbacks of DE are the formation of dust during treatment and the decrease of efficacy due to high humidity. Therefore, substantial efforts have been put into the development of liquid formulations (Lamina and Kruner 1966) such as the synthetic amorphous silica used in the present study. In the in vitro setup used in the current work, the liquid formulation completely suppressed reproduction of D. gallinae females, but AUC168 was not significantly different from the control. This result suggests insufficient efficiency of the amorphous silica compared to DE. However, field experiments performed by Maurer and Perler (2006) in heavily infested layer houses revealed a longer residual effect of the liquid amorphous silica compared to DE. Garlic is often used in folk medicine, but scientific studies on the effects of A. sativum on mites are scarce. A study by Birrenkott et al. (2000) showed that repeated topical applications of garlic juice (10%) on hens heavily infested with the Northern fowl mite Ornithonyssus sylviarum significantly reduced the level of infestation. The authors suggest that this was mainly due to a repellent effect preventing re-infestation and not to direct acaricidal effects. In our in vitro test, direct effects on oviposition and on survival of the closely related species D. gallinae have been demonstrated. This indicates that fresh garlic juice can have both, direct and indirect effects on gamasid mites. From the literature, it remains unclear whether garlic oil has the same insecticidal properties as fresh juice. A study of Amonkar and Reeves (1970) demonstrated that partly purified garlic oil had a higher toxic effect on mosquito larvae than the crude extract. In contrast, a 10% concentrate made from commercial chopped garlic provided control of whiteflies, but commercial garlic oil gave little or no control in an experiment by Flint et al. (1995). 123 40 Exp Appl Acarol (2009) 48:31–41 Before garlic can be considered as a valuable component of a strategy against D. gallinae, the question of conservation and standardisation of the crude extract has to be solved. Except for pure garlic juice and the highest concentration of pyrethrum extract, the plant preparations tested in our study resulted in\70% or no significant reduction of D. gallinae. Therefore, and also supported by observations of others (George et al. 2008b), it may be more suitable to use plant preparations as a treatment for starved mites in the poultry houses between layer flocks, rather than to apply them during flocks when mites have the opportunity to recently feed. In contrast, our experiment showed that physically acting products such as rapeseed oil, petroleum spray oil, soap or DE were effective on fed mites. These products therefore seem better suited for application in cases of severe D. gallinae infestations during flocks. Acknowledgments The authors gratefully acknowledge funding from the European Community financial participation under the Sixth Framework Programme for Research, Technological Development and Demonstration Activities, for the Integrated Project QUALITYLOWINPUTFOOD, FP6-FOOD-CT-2003506358. The views expressed in this publication are the sole responsibility of the author(s) and do not necessarily reflect the views of the European Commission. Neither the European Commission nor any person acting on behalf of the Commission is responsible for the use which might be made of the information contained herein. Mention of a proprietary chemical or a trade name does not constitute a recommendation or endorsement. 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