Zabaras D Wyllie G Spooner-Hart R N Tronson D Semiochemicals of Rose Aphid, Black Citrus Aphip (Hemiptera Aphididae) and Greenhouse Thrips (Thysanoptera Thripidae)

8/9/2019 Zabaras D Wyllie G Spooner-Hart R N Tronson D Semiochemicals of Rose Aphid, Black Citrus Aphip (Hemiptera Aphi

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Semiochemicals of rose aphid, black citrus aphidHemiptera: Aphididae) and greenhouse thrips

Thysanoptera: Thripidae)

D. Zabaras,'.' S G Wyllie,' R N Spooner-Hart: and D Tronson ''Centre for Biostructural and Biomolecular Research, U.W.S. Hawkesbury, Richmond,

New South Wales, Australia 753

Centre for Horticulture and Plant Sciences, U.W.S. Hawkesbury, Richmond,New South Wales, Australia 753

BSTR CT

Macrosiphum rosae L or rose aphid. Toxoptera citricida Kirkaldy or black citrus aphid(Hemiptera: Aphididae) and Heliothrips haemorrhoidaiis Bouch6 or greenhouse thrips(Thysanoptera: Thripidae) are serious cosmopolitan phytophagous pests that can cause severedamage to many cultivated crops.

The aim of this study was to investigate the chemical signals utilized by these pests inorder to carry out their everyday functions. This was achieved by determining the nature of

volatile compounds in the secretions of the rose aphid, the black citrus aphid and thegreenhouse thrips.

The results obtained showed similarities not only between the two aphid species but alsobetween aphids and thrips with acids and their methyl esters, aldehydes and alkanes beingcommon components of the secretions.

E-B-farnesene, a known alarm substance in many aphid species, was confirmed to be aconstituent of the secretions of the rose aphid and was isolated for the first time from theblack citrus aphid. Results indicated that the sesquiterpene is metabolically produced by theinsects and used when required.

Key words: Rose aphid, Bla citrus aphid. Greenhor~se hrips. Aphididae, Thripidae. Volatiies,E-8-farnesene, Secretions. Semiochemicals.

INTRODUCTION

Rose and black citrus aphids

Aphids are considered serious agriculturaland horticultural pests (Hill 1997). They causemajor damage to crops by their feeding, and,more importantly, by transmitting variousplant viruses that are pathogenic to their hosts(Schepers 1987). In addition , honeydewexcreted by the aphids attracts saprophyticfungi which cover the leaves leading toreduction of photosynthetic capacity of thehost plant (Schepers 1987).

Toxoptera citricida Kirkaldy or black citrusaphid (Hemiptera: Aphididae), is oriental inorigin and is widespread world-wide (Carver1978). 1: citricidus exhibits a distinct preferencefor citrus and a few other members of theRutaceae (Carver 1978). In Australia T citricidahas been reported to restrict growth of itshosts and affect fruit setting (Hely 1968) dueto its feeding.

Macrosiphum rosae L . or rose aphid(Hemiptera: Aphididae), is also a cosmopolitanpest that can cause severe damage to variousmembers of the Rosaceae (Hill 1997). This

pest may have various hosts during the year,however, it is most commonly found feedingon roses (Mound and Teulon 1995).

All aph ids a r e characterized by twospecialized, tube-like structures which protrudefrom the dorso-lateral surface of the posteriorpart of the abdomen called siphunculi orcornicles (Dixon a nd Stewart 1975). Manyaphid species escape from their predators byproduci ng an oily liquid from theirsiphunculi which they smear on the

mouthparts of the attacking predator (Biisgen1891). Escape i s facilitated by the rapidsolidification of the cornicle droplet and theresulting immobilization of the attackingpredator or parasitoid (Miyazaki 1987).Furthermore, it wa s reported that green peachaphids Myxus pe~ sica eSulzer) are repelled bythe odour of droplet s released from thecornicles of crushed aphids of the same species(Kislow and Edwards 1972). Subsequently itwas found that the sesquiterpene hydrocarbonE-b-farnesene is utilized as an alarmpheromone in several economically importantaphids including M . rosae L (Bowers et al1972; Edwards et al 1973).

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Greenhouse thrips MATERIAIS AND METHODS

Heliothrips haemorrhoidalis Bouche orgreenhouse thrips' (Thysanoptera: Thripidae),is a minute, slender-bodied insect (1-2 mm inlength) that occurs outdoors in warmerclimates and in greenhouses in the colder

regions of the globe (Borror et al. 1992). It isa cosmopolitan, polyphagous pest and cancause severe damage to both agricultural andgreenhouse crops (Beattie and Jiang 1990;Hill 1997; Lewis 1973) feeding on young andmature leaves and fruits (Mound and Teulon1995). Greenhouse thrips cause damage totheir host not only by feeding, but also bydepositing anal excrement on the surface ofthe leaves or fruits . Although the flesh is notdamaged, the grade of the fruit is reduced(Beattie and Jiang 1990).

The number of biological observations

dealing with thrips secretions is limitedperhaps due to the small size of these insects.Nevertheless, adults of many thrips speciesare known to raise and lower their abdomenswhen disturbed whilst some thrips adults andlarvae produce a drop of anal exudate inorder to deter predators (Froggatt 1906; Buffa1911; Lewis 1973; Suzuki et al. 1990).

Secretions emitted by many species withinthe sub-order Tubulifera have been the subjectof chemical investigations. Compoundsidentified so far include: y-decalactone(Howard el al. 1983), perillene (Suzuki et al.

1986), cetyl and myristyl acetates (Suzukiet al. 1988), 3- and 5-dodecenoic acids (Hagaet al. 1989), b-acaridial (Suzuki et aE. 1989).b-myrcene (Haga et al. 1990), mellein (Blumet al. 1992) and plumbagin (Suzuki et al. 1995).

Secretions from species within the sub-orderTerebrentia have not been investigated to thesame extent as those from tubuliferous species.The western flower thrips, Frankliniellaoccidentalis Pergande was, until this study theonly terebrantious species to have hadits secretion chemically analysed. Decyland dodecyl acetates were reported as

constituents of the anal exudate (Teerlinget al. 1993a), a mixture of which was foundto have pheromonal (Teerling et al. 1993a)and kairomonal properties (Teerlinget al. 1993b).

The objectives of this study were todetermine the nature of volatile organicchemicals in the secretions of : ccilricidus andH haemorrhoidalis and to expand on the earlierchemical analysis of the secretions of M rosae.The possible biological function of thecompounds identified is discussed.

Insects

The aphids used in this study were collecteddaily during winter from host plants locatedin Richmond (New South Wales, Australia). 7:citricida was collected from a round kumquatFortunella japonica tree, whilst M. rosae wascollected from hybrid tea roses Rosa hybridu

Greenhouse thrips from a four year oldlaboratory cul ture were used. T he culture wasestablished from field collected specimens(Richmond, New South Wales, Australia). Thethrips were reared on lime fruits Citrus auranti-

folia at 28C with a photoperiod of 16 hours.

: citricida and H. haemorrhoidalis specimenswere ident ified by Assoc. Prof. G A. C Beattie(Former Senior Research Scientist, New SouthWales Department of Agriculture). M. rosae

specimens were identified by Assoc. Prof.R. N. Spooner-Hart (Horticulture Precinct,University of Western Sydney, Hawkesbury).

Collection of insect uolatile secretions

i) Solvent extraction Fifty mixed adultsand nymphs of each insect species (onlyadults for the thrips) were crushed inliquid nitrogen to a fine powder, whichwas the n extracted with hexane (3 mL).The extract was then concentrated to100 kL

ii) Headspace above crushed insects Onehundred mixed adults and nymphs ofeach insect species (only adults for thethrips) were placed in a 2 mL vial andwere crushed with a metallic pin throughthe cap. Th e headspace above the crushedinsects was sampled (at room temperature)for 1 hour using polar and non-polarsolid phase micro-extraction (SPME).

iii) Direct collection of th cornicle/anol ex @To collect aphid secretions, aphids of allstages were placed under a stereo micro-scope and were prodded gently on their

head and thorax with a metallic pin. Thecornicle exudate released by the aphids wascollected o n polar an d non-polar SPMEfibres (Sigma-Aldrich Pty. Ltd., New SouthWales, Aust ralia) by touching 10 cornicledroplets with the end of the fibres.

Anal exudate from greenhouse thripsnymphs was collected in a similar way to thatdescribed above. However, in this case thenymphs were not prodded. The anal exudateis carried by the nymphs on the tip of theirabdom en as they walk around .

mripsll bc use For both singular

and plum1 t o m

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Analysis of the inseet aolatile secretions

The volatiles obtained from above wereanalysed by gas chromatography (GC) and gaschromatogra phy coupled mass spectrometry(GC-MS).

GC analysis was performed using a HP 6890gas chromatograph equipped with a flameionization detector and a HP 7673 GC/SFEauto-injector. The column used was 50QC2lBPX-5 (SGE Scientific, Melbourne, Australia).

GC-MS analysis was carried out on aHPs890 Series II gas chromatographconnected to a HP 59714 mass selectivedetector. The column used was BP-l (SGEScientific, Melbourne, Australia).

Compounds were identifred based on massspectral evidence and by comparison of theirretention time to those of authentic samoles.

RESULTS

Rose and blach citrus aphids

Qualitatively the results obtained from theblack citrus and the rose aphids were almostidentical (Fig. 1). E-p-farnesene was present nsolvent and headspace extracts of whole

crushed individuals- rom both species; hesame compound was also found to be acomponent of the cornicle droplets producedby aphids when attacked. Long chain alkanes,acids and their methyl esters, and aldehydeswere also solated rom both aphid species. Anunknown sesquiterpene which is believed tobe an c-farnesene isomer based on massspectral evidence) was present n the secretionsof the rose aphid but was not detected inthose from the black citrus aphid. A completelist of the compounds identified and theirsource s given in Thble 1.

frgurc 1. Gas chromatograms of whole crushed body extracts from aphids. The identity of peaks

is given in Thble l. (a)-Rose phids and (b) black citrus aphids.

I

It

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Thble L Volatile components in the secretions of the rose and black citrus aphids and theirsource. Bold numbers in brackets efer to Figure l.

Source Rose aphid volatiles Black citrus aphid volatiles

Whole crushedbody solventextraction

alkanes (C'n-Crr) (7), decanal (4),E-p-farnesene (5), hexanoic acid (l),methyl hexanoate (2), nonanal (3),ct-farnesene isomer (6)

alkanes Ctn-Crr)decanal, E-P-farnesene,hexanoic acid, nonanal

Headspaceabove crushedaphids

c,-farnesene isomer,decanal, E- -farnesene, nonanaly-terpinene,

decanal,E-p-farnesene, imonene,nonanal

Cornicle droplet alkanes (C,n-Ctr), d-farnesene isomer,decanal, E-p-farnesene, nonanal

alkanes (Crn-Ctr ), decanal,E-p-farnesene, nonanal

None of the volatiles present in secretionsfrom black citrus and rose aphids (Thble 1)were found in extracts from the aphids' hosts.As expected the volatile profiles of the twohosts, round-kumquat tree and hybrid tearoses, were totally different (Fig. 2) .

Greenhouse hripsLong chain alkanes, acids (and their methyl

esters) and aldehydes were isolated fromthe solvent extracts of whole crushed adultgreenhouse thrips. Previously reported(Njoroge et al. 1996) citrus volatiles such as

Figure 2. Gas chromatograms rom the extracts of the aphids' hosts. a) Hybrid tea-roses and

b) round-cumquat tree.

&unance50@00

45m00

40@00

35@00

300000

2500o0

20m00

15@00

10m00

50m0

'nre> o

45mm

40@00

35m00

300m

25m0

2mm

15m00

10m00

50m0

- nil|r> -

406 Australian Zoologist 31(2) December 999


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monoterpenes and sesquiterpenes wereidentified as constituents of the headspaceabove crushed adult greenhouse thrips. Thesaturation of the insects' body with limevolatiles during rearing is the most probablecause of the above result. Long chainalkanes, coumaran (Fig. 3a) and 3-methoxy-acetophenone (Fig. 3b) were identified asconstituents of the anal fluid produced bygreenhouse thrips' nymphs. A complete list ofthe compounds isolated from the thrips'secretions and their source is given in Table 2.

Figure 3 Structures of some compounds found insecretions of greenhouse thrips: a Coumaran andb) 3-methoxyacetophenone.

Table 2. Volatile components in the secretions of thegreenhouse thrips and their source.

Source Green hous e thrips volatiles

Whale crushed alkanes C 2 , C,,-C,,), decanal,body solvent hexan oic acid,extraction methyl tetrade canoa te,

methyl hexadecanoate nonanal

Headspace above 0-bisabalene, y-terpinene.crushed aphids E-ocim ene, geranyl acetate,limonene, neryl acetate

Cornicle droplet alkanes C,,-C ,,), coumaran,3-methoxyacetophenane

DISCUSSION

Rose and black citrus aphids

E-P-farnesene has been identified as analarm substance in several economicallyimportant aphids, including the rose aphid(Bowers et a l 1972). This study confirmed thepresence of E-P-farnesene in the secretions ofthe rose aphid and in addition showed thatthis sesquiterpene is also a component of thesecretions of the black citrus aphid.

The minor qualitative differences observedbetween the secretions from the two aphidspecies may be very important biologically.Synergistic effects to the activity ofE-b-farnesene have been so far attributed toa-pinene (vetch aphid) and a mixture of(E,E)-a- an d (Z,E)-a-farnesene (gr een peachaphid) (Pickett and Griffiths 1980). There fore

it is possible that compounds such aslimonene, E-ocimene and y-terpinene for theblack citrus aphid and the a-farnesene isomer

for the rose aphid, may be important inproducing the alarm response synergisticallywith E-P-farnesene in the present aphid species.

Two aldehydes, non ana l (C,) an d decanal(C,,), were identified in secretions from bothaphid species. Aldehydes are odorous and

irritant in nature and many are known tobe employed as constituents of the defensivesecretions of many other hemipteran species,especially pentatomid bugs (Waterhouse et a l1961; Aldrich 1988 ). Th ei r presence in t hecornicle droplet of both rose and black citrusaphids suggests that they are utilized asdefensive allomones against aphid predators.

The other identified components of thesecretions (carboxylic acids and their methylesters, long alkanes) are known to be associatedwith all insects' exoskeleton and cuticle (Borroret a l 1976) and it is unlikely they are involvedin insect chemical communication.

reenhouse thrips

A mixture of decyl- and dodecyl- acetateswas found to be utilized as an alarmphero mone by th e western flower thrips(Teerling et a l 1993a). T h e headspace abovecrushed adult greenhouse thrips (Table 2)contained the stereoisomers neryl- andgeranyl-acetate; it is possible that a mixture ofthe two may elicit alarm response in thegreenhouse thrips. However, the two isomers

were found to be constituents (in smallamounts) of the oil obtained from limes(Njoroge e l a l 1996 ) and therefore it ispossible the two acetates were found in theheadspace extracts due to the saturation ofthe greenhouse thrips' body during rearing.There is no evidence to support or refutepossible biological activity.

The two aldehydes (nonanal and decanal)found in aphid secretions were alsoencountered in secretions of greenhousethrips. However, it appears that these are notthe only defensive allomones employed by

greenhouse thri ps. T he function of coumaran2,3-dihydro-benzofuran) and 3-methoxy-

acetophenone (Fig. 3), determined to hecomponents of the anal fluid produced bygreenhouse thrips' nymphs, is believed tobe similar to that of the two aldehydes.Acetophenone-based products are knowninsect repel lents an d are widely employedfor that pur pos e du rin g field studies (Torret a l 1996). 3-Methoxyacetophenone is alsoknown for its bird-repellent properties (Clarket a l 1991). Benzofuran-based productsappear to be toxic to several insect species

an d recently, tw naturally occuring hydroxy-benzofuran derivatives were found to be toxicagainst spruce budworms (Findlay el a l 1997).

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It appears that thips nymphs employ a greatervariety of natural products for their protectionthan the adults. This may be related to thefact that the adults posses other means toavoid predation such as flying, while thenymphs do not have this option (Lewis 1973).

Comparison between aphids a nd thripsThe results obtained from the chemical

analysis of secretions from aphids (Order:Hemiptera) and thrips (Order: Thysanoptera)support the phylogenetic theory proposed byKristensen (1991) according to which, the twoinsect orders have evolved from a commonancestor (Sub-division: Paraneoptera). Thequalitative analysis of the secretions emittedby aphids and thrips showed that there aremany compounds or groups of compoundscommon to the two orders and, this suggestsa relationship between the Hemiptera andthe Thysanoptera. Aphids and thrips exhibita similar secreting behaviour and the commoncomponents of their secretions may beassociated with that behaviour.

Effect of diet on insect seeretwnsMost compounds identified in aphid secretions

were absent from extracts of the aphid hosts.This suggests that E-p-farnesene and mostof the other components of the secretions aremetabolically synthesized by the rose andblack citrus aphids. Similarly, it is likely thatthe volatile components identified withinthe anal fluid produced by g reenhouse

thrips nymphs are metabolically produced.The volatile constituents of lime oil have beenreported to be monoterpenes, sequiterpenesand hydrocarbons; components identified withinthe anal fluid were not found as constituentsof the lime oil (Njoroge et al 1996).

Some compounds, such as E-p-farnesene andaldehydes, were found to be components ofthe aphid cornicle fluid and, were also presentin the solvent extracts derived from crushedaphids. The presence of these compounds inthe solvent extracts indicates that they werefound within the aphids' body at the time ofsampling. This suggests that the abovevolatiles are produced and subsequently storedwithin the aphids' body until required.

An oppor tunist ic observation was madeduring this project: the removal of rose aphidsfrom their host for a period of 12 hours wasfound to decrease their ability to producecornicle fluid. Therefore, it is likely thatnutrients derived from the host are utilizedas precursors for the metabolic production ofthe natural products contained within thecornicle fluid.

There are many differences between the

chromatograms obtained from the two aphid

hosts (Fig. 2 . However, the chromatogramsproduced from the whole, crushed bodyextracts of the two different aphid species arealmost identical (Fig. 1). Thi s suggests thatvarious metabolites are utilized as precursorsby dierent metabolic pathways for the pmd-uction of the chemicals emitted by the aphids.

E-p-farnesene is known to be secreted byseveral economically important aphid speciesthat feed on di ie re nt hosts (Bowers et al 1972;Edwards et a l 1973). It is likely that differentmetabolites are found in different host plants.Therefore, the metabolic pathways utilized byeach aphid species are possibly modifiedaccording to their diet in order to synthesizecommon semiochemicals such as E-j3-farnesene.

Future work

If behavioural studies were to be carried outto determine the activity (if any) and the

biological function of the compoundsidentified during this study, the activechemicals could then be incorporated intomodern IPM strategies for pest control.Examples of other insect-derived naturalproducts already used in IPM strategies forpest control include the alarm substances citraland isopiperitenone which are used tosynergize the effects of acaricides against mites(Kuwahara t a l 1987; Howse et al 1998).

Secretions from the insect species in thisstudy could he analysed for the presence ofnon-volatile semiochemicals possibly by high

performance liquid chromatography (HPLC).Aphid and thrip parasitoids are known tolocate their host using contact pheromones(non-volatile compounds) (Budenberg 1990)therefore, future investigations in this areacould be rewarding.

ON LUSION

Many volatile organic compounds wereidentified as constituents of the secretionsemitted by t he rose aph ids , the black citrusaphids and t he greenhouse thrips. The inter-specific aphid al arm pheromone E-B-farnesenewas identified in secretions from the blackcitrus aphid f o r th e first time. Many of theidentified components appear to be utilizedfor defensive purpose s by the above pestsand results obtained indicated that theyare metabolically produced and stored untilrequired. However, the qualitative compositionof the secretions emitted by the above pestsdoes not depend to a great extent on theirdiet. Behavioural studies are required todetermine which of the compounds identifiedfrom the secretions could be incorporated inmodern IPM strategies for improved controlof the above pests.

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ACKNOWLEDGEMENTS

We would like to thank the Royal ZoologicalSociety of New South Wales the Ethel MaryReid Grants Committee and the University ofWestern Sydney Hawkesbury for their financialsupport during this study.

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