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Annals of Applied Biology ISSN 0003-4746

R E S E A R C H A RT I C L E

Plant-derived compounds and extracts with potential


as aphid repellents
S.E. Halbert1,2, D. Corsini1, M. Wiebe1 & S.F. Vaughn1,3
1 Department of Plant, Soil, & Agricultural Sciences, Aberdeen Research and Extension Center, University of Idaho, Aberdeen, ID, USA
2 Present address: Florida State Collection of Arthropods, Florida Department of Agriculture and Consumer Services, Division of Plant Industry,
PO Box 147100, Gainesville, FL 32614-1285, USA
3 New Crops Processing and Technology Research Unit, USDA-ARS, National Center for Agricultural Utilization Research, Peoria, IL, USA

Keywords Abstract
Aphididae; Homoptera; plant volatiles;
repellent. We devised a method for screening various substances for possible aphid repel-
lency. Corn leaf aphids (Rhopalosiphum maidis) were released in an arena and
Correspondence allowed to select paired green tiles coated with petroleum jelly alone or petro-
S.E. Halbert, FDACS/Division of Plant leum jelly containing 1% of the substance being tested. Aphids adhering to
Industry, PO Box 147100, Gainesville,
tiles were counted 24 h later. If significantly fewer aphids landed on treated
FL 32614-7200, USA.
Email: halbers@doacs.state.fl.us
tiles, the substance was considered to have potential for repelling aphids.
Fifty-five substances were tested. Most showed no activity, but several includ-
Received: 15 June 2008; revised version ing b-citronellol, farnesol, geraniol, linalool, oils distilled from several species
accepted: 15 October 2008. of Artemisia and Achillea millefolia (yarrow) oil showed some promise.

doi:10.1111/j.1744-7348.2008.00300.x

(Sulzer) as their experimental aphid. Gutiérrez et al.


Introduction
(1997) tested bisabolene, farnesol and geraniol in assays
Viruses transmitted non-persistently by aphids cause using apterous aphids and leaf discs embedded in agar.
major problems for many cultivated plants, particularly All three compounds showed activity, but only bisabo-
crops that rely on vegetative propagation. These viruses lene was tested further because the others proved phyto-
often are transmitted by aphid vectors that do not colonise toxic to Capsicum annuum leaves. Farnesol apparently
the affected crops (Halbert et al., 1981; Ryden et al., also may have been toxic to the aphids. The leaf-disc
1983), so insecticide treatment is ineffective for control- method allowed testing of the compounds in a tiny
ling virus spread. Various types of visual repellents such space, but only walking behaviour could be tested.
as reflective mulch (George & Kring, 1971) and white- Bruce et al. (2005) tested the aphid alarm pheromone,
wash paint (Marco, 1993) have been used to suppress (E)-b-farnesene, and related compounds, including the
virus incidence through reduced transmission; however, oil of an African plant, Hemizygia petiolata Ashby, which
plants tend to overgrow the mulches and paints can cut has a high natural concentration of (E)-b-farnesene,
down on photosynthesis. If chemical repellents could be against M. persicae, Acyrthosiphon pisum (Harris) and
found, they could be added to an oil spray to further Sitobion avenae (Fabricius). Most of the experiments were
reduce virus spread. For example, potato virus Y (PVY) is performed in an olfactometer, although one experiment
a major problem in potato seed production. If early gen- was performed in the field using sachets of H. petiolata
eration seed potato plants could be protected with re- oil in treated plots. There were differences among species
pellents and oil during the major aphid flight periods, in olfactometer tests. The sachets of H. petiolata oil
virus incidence and subsequent virus increase in the showed activity as repellents against A. pisum in the
seed supply could be reduced. field. Hori (1998, 1999) tested the effects of rosemary
Several authors have tested some plant-derived com- and ginger oils and several other plant compounds on
pounds as aphid repellents. Most used Myzus persicae M. persicae and some other species known to be vectors

Ann Appl Biol 154 (2009) 303–307 ª 2008 The Authors 303
Journal compilation ª 2008 Association of Applied Biologists
Potential aphid repellents S.E. Halbert et al.

of PVY. Hori (1999) showed that rosemary (probably The aphids were collected just prior to use. They were
Rosmarinus officinalis L., but not specified) and ginger raised in a large (approximately 1.5  1  1 m) cage con-
(probably Zingiber officinale Roscoe, but not specified) oils taining a robust colony of R. maidis. Healthy spring barley
could decrease the incidence of yellow spotted streak plants of at least 6 weeks old were used to rear the
virus and PVY in field plots. Perforated bottles were used aphids. Only healthy active winged aphids were selected
to release the volatiles from tested compounds. from the plants or the cage walls and top for use in the
The purpose of our research was to assess a variety of experiments.
potential repellents for efficacy against alate aphids. We In preliminary experiments, we tried using several
have devised a convenient method of screening a large aphid species, including Rhopalosiphum padi (L.),
number of substances for potential aphid repellency. We S. avenae, Metopolophium dirhodum (Walker) and R. maidis.
present the results below. Although all the species were easy to raise and produced
sufficient alate under our laboratory conditions, percent
recovery on (untreated) tiles was highest for R. maidis.
Materials and methods
We averaged 3.34 aphids per tile recovered after 24 h, or
Various natural and commercial substances were screened about 80% of the aphids we released, for R. maidis. Only
to determine whether they repel alate aphids. We released about half that many were recovered using the other
approximately 50 winged Rhopalosiphum maidis (Fitch) species. We also tested several sticky substances, includ-
into an arena containing paired treated and untreated ing corn syrup, STP oil (STP Products, St Joseph, MO,
green tiles (Irwin, 1980), each 5  5 cm (Fig. 1). Each USA), Tanglefoot (Tanglefoot Company, Grand Rapids,
tile was coated with 1 ml petroleum jelly to trap landing MI, USA) and petroleum jelly. Petroleum jelly had the
aphids. Treated tiles were coated with petroleum jelly highest percent recovery of released aphids (nearly five
containing 1% of the substance being tested, while times the number recovered with the other sticky sub-
untreated tiles were coated with petroleum jelly alone. stances), was miscible with the substances we proposed
Mixing and application were carried out just prior to to test and was relatively easy to clean up. Thus, the
testing. The arenas were 60  60  60 cm. They had combination of R. maidis and petroleum jelly was found
glass tops, glossy white walls and matte brown floors and to work best under our laboratory conditions.
windows on all four sides covered with aphid-proof The substances we tested came from a variety of sources.
mesh for ventilation to prevent the air from becoming Dr Vaughn synthesised some substances (Spencer, 1994;
saturated with the substances being tested. In the centre Vaughn & Spencer, 1996). Others came from commercial
of the floor, we mounted a vertical dowel 40 cm high sources. Commercial substances were chosen because of
with a release platform on the top. The tiles were ar- known repellency towards other insects [e.g. N,N-diethyl-
ranged in randomised pairs on the floor (six pairs per m-methylbenzamide (DEET)] or because of advertised
arena). The arenas were arranged in a large growth efficacy. Others were steam distilled from plants grown at
chamber with overhead fluorescent lighting. the Aberdeen R&E Center, Aberdeen, ID, USA, or har-
vested from local wild sources. The amount of oil ob-
tained from a given amount of plant material was
variable, but only the pure oil was used. Garlic oil and
cashew oil were ether extracted from bulbs and nuts pur-
chased at the local grocery store. After ether extractions,
the ether was evaporated away to leave only the oil.
For our own distillations, we chose plants that had
highly specific aphid faunas rather than generalist feeders.
Artemisia species are a case in point. Although the peren-
nial Artemisia spp. in Idaho, for example, have a very
rich aphid fauna (Halbert et al., 1995), all the species are
specific to Artemisia. Thus, we reasoned that plant vola-
tiles from Artemisia spp. might prove repellent to the
generalist species and agricultural pests that most often
are virus vectors in crops.
Aphids were released from a small plastic Petri dish
Figure 1 Arena used for repellent experiments. Approximately 50 alate
Rhopalosiphum maidis were released from a dish on the top of the placed on the platform. Twenty-four hours later, the num-
release platform in the centre. Each arena had six randomised pairs of bers on the tiles were counted and recorded. Although we
treated and untreated 5 cm2 tiles placed on the floor of the arena. did observe aphids stuck to the edges of the tiles, it was not

304 Ann Appl Biol 154 (2009) 303–307 ª 2008 The Authors
Journal compilation ª 2008 Association of Applied Biologists
S.E. Halbert et al. Potential aphid repellents

Table 1 Mean number of Rhopalosiphum maidis (Fitch) per tile on treated and untreated tiles and probability values for substances tested for aphid
repellency
Mean Number: Mean Number: Number of
Substance Tested Source Treated Tiles Untreated Tiles P Significance Pairs Tested
Achillea millefolia L. Distilled (E. Eldridge) 1.72 3.94 0.0041 ** 18
Aloe vera (L.) Burm. f. Forever Living Products 4.11 3.50 0.3726 NS 18
International, Inc.,
Scottsdale, AZ, USA
Artemisia absinthium L. Distilled 2.56 5.11 0.0022 ** 18
Artemisia dracunculus L. Distilled 2.81 4.72 0.0070 ** 36
Artemisia tridentata Nutt.1 Distilled 2.50 4.21 0.0261 * 24
A. tridentata Nutt.2 Distilled 2.61 4.56 0.0039 ** 18
Bay oil IN Botanical Gardens, Inc., 2.83 3.67 0.3335 NS 18
Hammond, IN, USA
Benzyl carvyl ether Synthesised 2.44 4.50 0.0624 NS 18
Benzyl citronellyl ether Synthesised 3.72 3.89 0.8218 NS 18
Benzyl fenchyl ether Synthesised 2.50 4.17 0.1775 NS 12
Benzyl geranyl ether Synthesised 3.33 5.08 0.2157 NS 18
Benzyl pulegyl ether Synthesised 2.67 3.17 0.3655 NS 18
(+)-Borneol Aldrich Chemical, Inc., 4.39 4.00 0.6514 NS 18
Milwaukee, WI, USA
Camphor Aldrich Chemical 4.44 3.55 0.5020 NS 18
Capsaicin KALSEC, Denver City, TX, USA 2.44 4.50 0.1123 NS 18
Capsaicin (98%) Sigma Chemical, St Louis, 4.39 5.61 0.2287 NS 18
MO, USA
(+)-Carvone Aldrich Chemical 3.61 3.72 0.9264 NS 18
(2)-Carvone Aldrich Chemical 2.63 2.54 0.8905 NS 24
Cashew oil Ether extraction from nuts 2.56 2.89 0.6101 NS 18
Cedarwood oil IN Botanical Gardens 3.44 3.89 0.5346 NS 18
Cineole Aldrich Chemical 3.17 2.78 0.7475 NS 18
Citronella IN Botanical Gardens 2.94 3.33 0.5812 NS 36
b-Citronellol Aldrich Chemical 2.06 4.78 0.0013 ** 18
Cyanoethyl pulegyl ether Synthesised 3.33 3.83 0.5721 NS 18
N,N-diethyl-m-methylbenzamide Purchased locally 2.42 3.42 0.2927 NS 24
(100%)
Ethyl pulegyl ether Synthesised 3.33 3.89 0.5550 NS 18
Ethylene glycol pulegyl ether Synthesised 1.83 3.00 0.1100 NS 18
Eucalyptus extract IN Botanical Gardens 2.67 2.83 0.7492 NS 18
(E)-b-farnesene Aldrich Chemical 2.83 3.55 0.2716 NS 18
Farnesol Aldrich Chemical 1.78 4.00 0.0337 * 18
Fenchone Aldrich Chemical 3.00 2.72 0.6881 NS 18
Garlic barrier Garlic Research Labs Inc., 3.22 2.89 0.7810 NS 18
Glendale, CA, USA
Garlic oil Ether extraction from bulbs 2.50 4.00 0.2371 NS 18
Geraniol Aldrich Chemical 2.61 4.56 0.0210 * 18
Juniper tar cade IN Botanical Gardens 2.50 3.89 0.1137 NS 18
Lavandula angustifolia Miller Distilled 2.94 3.50 0.4886 NS 18
D-Linalool Aldrich Chemical 2.28 4.83 0.0396 * 18
Melaleuca alternifolia Tri-K Industries, Northvale, 2.58 4.38 0.0343 * 24
(Maiden and Betche) Cheel NJ, USA
Mentha spicata L. Distilled (E. Eldridge) 3.06 2.67 0.4930 NS 18
Methyl pulegyl ether Synthesised 4.05 3.56 0.3523 NS 18
Menthol Aldrich Chemical 3.33 3.44 0.8685 NS 18
L-Menthone Aldrich Chemical 4.05 2.72 0.2431 NS 18
2-Nitropropyl pulegyl ether Synthesised 3.56 3.83 0.6392 NS 18
Pennyroyal IN Botanical Gardens 3.44 3.55 0.8303 NS 18
Pennyroyal Distilled 2.72 4.11 0.1897 NS 18
(+)-Pulegone Aldrich Chemical 3.39 3.67 0.8325 NS 18
Pulegyl citronellyl ether Synthesised 3.63 4.00 0.5675 NS 18
Pulegyl alcohol Synthesised 2.08 4.58 0.0341 * 12
Salicylaldehyde Aldrich Chemical 3.44 3.00 0.6268 NS 18
Tagetes sp. 1 Distilled 3.33 3.56 0.6823 NS 18

Ann Appl Biol 154 (2009) 303–307 ª 2008 The Authors 305
Journal compilation ª 2008 Association of Applied Biologists
Potential aphid repellents S.E. Halbert et al.

Table 1 Continued

Mean Number: Mean Number: Number of


Substance Tested Source Treated Tiles Untreated Tiles P Significance Pairs Tested
Tagetes sp. 2 Distilled 2.94 3.33 0.6525 NS 18
Tanacetum vulgare L. 1 Distilled 4.67 4.00 0.5007 NS 6
T. vulgare L. 2 Distilled 3.17 3.67 0.6376 NS 18
Tridecanone Aldrich Chemical 2.89 2.78 0.7873 NS 18
NS, not significant.
*P < 0.05.
**P < 0.01.

possible to determine if they walked or flew to their death the non-oxygenated monoterpene a-terpinene being more
on the tiles. The behaviour of R. maidis is such that they repellent than the commercial repellent DEET. The oxy-
all flew to escape the Petri dish from which they were genated monoterpene verbenone strongly suppressed
released. They crawled to the rim of the dish and began feeding by the pine weevil, Hylobius abietis L. (Lindgren
to fly. The few that could not fly out of the dish were et al., 1996). Ricci et al. (2006) found that lemongrass [Cym-
observed in the dish (usually dead) when we did the bopogon citratus (D. C. ex Nees) Stapf.] oil, which consists
counts. The data were analysed using a paired t-test primarily of the monoterpenes citral, geraniol and myr-
(SAS). If significantly fewer aphids landed on treated cene, effectively repelled the Russian wheat aphid, Diur-
tiles, the substance was deemed to have potential effi- aphis noxia (Mordvilko). Geraniol also showed some
cacy as an aphid repellent. efficacy in our experiments. Myrcene and citral were not
tested in this study.
Hori (1998), Gabrys et al. (2005) and Bruce et al.
Results and discussion
(2005) found efficacy with linalool, but the response may
Most of the substances tested showed no efficacy as re- vary with species. All the three studies found that linal-
pellents, but several including b-citronellol, oils from seve- ool repelled M. persicae, but it had no efficacy on S. avenae
ral species of Artemisia, farnesol, geraniol, linalool, and (Bruce et al. (2005) or Neotoxoptera formosana (Takahashi)
Achillea millefolia (yarrow) oil showed some promise (Hori, 1998). In our experiments, (E)-b-farnesene, the
(Table 1). Most of the substances were colourless, so the aphid alarm pheromone, had no effect, but farnesol had
repellency was likely because of the volatiles; however, statistically significant efficacy. Farnesol also was very
Artemisia absinthium oil is blood red and A. millefolia oil is effective in experiments by Gutiérrez et al. (1997).
blue, so repellency may have had a visual component in Gabrys et al. (2005) found differences between isomers
those two cases. of some compounds, including pulegone, which we also
Many terpenoids have been shown to act as insect feed- tested. We found no activity but did not test R and S iso-
ing/oviposition deterrents and often are toxic at higher lev- mers separately.
els. Raffa et al. (1985) demonstrated that monoterpenes Our method makes it relatively easy to screen a large
present in Grand fir [Abies grandis (Douglas) Lindl.] were number of substances for potential repellency for alate
toxic as volatiles to the fir engraver beetle (Scotylus ven- aphids; however, further testing is needed to determine
tralis LeConte), with limonene being the most inhibitory. whether the putative aphid repellents have any effect in
Hwang et al. (1985) found that the mugwort (Artemisia protecting plants from potyviruses. Similarly, repellents
vulgaris L.) contains volatile insect repellents against the would have to be tested for longevity under field conditions.
yellow fever mosquito [Aedes aegypti (L.)]. The most active It is intriguing that Melaleuca alternifolia (Maiden and Bet-
compounds were ()-linalool, ()-camphor, (+)-camphor, che) Cheel showed some efficacy. Unfortunately, we were
(2)-camphor, isoborneol, (2)-borneol, terpinen-4-ol and unable to test Melaleuca quinquenervia (Cav.) S. T. Blake,
isobornyl acetate, all of which are oxygenated mono- a noxious weed that causes major problems in the Florida
terpenes. The non-oxygenated compounds b-pinene, myr- Everglades. If steam distilled leaves of M. quinquenervia
cene, a-terpinene, (+)-limonene were considerably less showed similar efficacy, leaves could be harvested easily
repellent to the mosquitoes. Interestingly, all the mono- and distilled for an almost unlimited supply of oil.
terpenes that were active in our studies were oxygenated
monoterpenes, although other researchers have found
Acknowledgements
that non-oxygenated monoterpenes also were inhibitory.
Park et al. (2005) demonstrated that several monoterpenes We thank Irene Shackelford and Amy Miles for technical
repelled the mosquito Culex pipiens pallens Coquillett, with assistance and Dr Eric Eldridge for use of the mint still at

306 Ann Appl Biol 154 (2009) 303–307 ª 2008 The Authors
Journal compilation ª 2008 Association of Applied Biologists
S.E. Halbert et al. Potential aphid repellents

Caldwell, ID, USA. Forever Living Products International, Hori M. (1998) Repellency of rosemary oil against Myzus
Growth Products and Services and Tri-K Industries pro- persicae in a laboratory and in a screenhouse. Journal of
vided free products for testing. The research was supported Chemical Ecology, 24, 1425–1432.
by the Idaho Potato Commission and the National Potato Hori M. (1999) The effects of rosemary and ginger oils on
Council. This is Entomology Contribution No. 1084, Flor- the alighting behavior of Myzus persicae (Sulzer) (Homo-
ida Department of Agriculture and Consumer Services ptera: Aphididae) and on the incidence of yellow spotted
(FDACS), Division of Plant Industry (DPI), Bureau of streak. Applied Entomology and Zoology, 34, 351–358.
Entomology, Nematology and Plant Pathology. We thank Hwang Y.-S., Wu K.-H., Kumamoto J., Axelrod H., Mulla
M.S. (1985) Isolation and identification of mosquito
Bruce Sutton, Greg Hodges and Wayne Dixon (FDACS/
repellents in Artemisia vulgaris. Journal of Chemical
DPI) and two anonymous reviewers for excellent advice
Ecology, 11, 1297–1306.
to improve this manuscript. We thank Richard Weaver
Irwin M.E. (1980) Sampling in soybean fields. In Sampling
and Patti Anderson, FDACS/DPI botanists, for help with
Methods in Soybean Entomology, pp. 239–259. Eds M. Kogan
the plant names. We thank Dr Michael C. Thomas (DPI)
and D.C. Herzog. New York, NY: Springer-Verlag.
for help with formatting our photo. Lindgren B.S., Norlander G., Birgersson G. (1996) Feeding
deterrence of verbenone to the pine weevil, Hylobius abietis
L. Journal of Applied Entomology, 120, 397–403.
Marco S. (1993) Incidence of nonpersistently transmitted
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