The giant willow aphid [Tuberolachnus salignus (Gmelin)] has recently become noteworthy as a potential pest species due to the increased uptake of willow, its host-plant, for use in growing biomass for energy production. In this paper we describe host selection studies of T. salignus on short rotation coppice (SRC) willow varieties in laboratory bioassays and field experiments. In laboratory olfactometry tests, T. salignus was significantly attracted to certain SRC willow varieties, but not to others. Field trials during 2007 and 2008 showed that T. salignus infestation levels varied significantly on different SRC willow varieties and that levels are highest on the varieties to which they are most strongly attracted in the laboratory bioassays

Aradottir, G

Collins, CM

Dewhirst, S

Hanley, SJ

Harrington, R

Karp, A

Leather, SR

Woodcock, C

Redia

English

Spiral - Imperial College Digital Repository

REDIA, XCII, 2009: 223-225(*) Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, UK; richard.harrington@bbsrc.ac.uk(**) Imperial College London, Silwood Park Campus, Ascot, Berkshire, SL5 7PY, UK.Aradottir G., Karp A., Hanley S., Shield I., Woodcock C., Dewhirst S., Collins C., Leather S., Harrington R. – Host selec-tion of the giant willow aphid (Tuberolachnus salignus).The giant willow aphid [Tuberolachnus salignus (Gmelin)] has recently become noteworthy as a potential pestspecies due to the increased uptake of willow, its host-plant, for use in growing biomass for energy production. In thispaper we describe host selection studies of T. salignus on short rotation coppice (SRC) willow varieties in laboratorybioassays and field experiments. In laboratory olfactometry tests, T. salignus was significantly attracted to certain SRCwillow varieties, but not to others. Field trials during 2007 and 2008 showed that T. salignus infestation levels variedsignificantly on different SRC willow varieties and that levels are highest on the varieties to which they are most stronglyattracted in the laboratory bioassays.KEY WORDS: Willow, aphid, Tuberolachnus salignus, chemical ecology, host selection.GUDBJORG ARADOTTIR (*) (**) - ANGELA KARP (*) - STEVE HANLEY (*) - IAN SHIELD (*)CHRISTINE WOODCOCK (*) - SARAH DEWHIRST (*) - MATILDA COLLINS (**)SIMON LEATHER (**) - RICHARD HARRINGTON (*)HOST SELECTION OF THE GIANT WILLOW APHID(TUBEROLACHNUS SALIGNUS)INTRODUCTIONWillow (Salix spp) grown as short rotation coppice(SRC) is one of the main biomass crops in the UK and hasbeen identified as appropriate for the production ofbiomass energy in the Palearctic and North America dueto its potential for rapid growth in temperate climates(KARP and SHIELD 2008). Previous work has shown that willow plantings arebeneficial to biodiversity. Bird diversity is high, generallyexceeding that of agricultural land (VOLK et al., 2006) andinvertebrate surveys have also shown that butterflyabundance is higher in the margins of willow fields thanaround arable crops (HAUGHTON et al., 2009).There are a number of insect pests associated withwillow trees. Among these is the giant willow aphid[Tuberolachnus salignus (Gmelin)], which has becomemore noticeable in willow plantings in recent years.Tuberolachnus salignus is a large aphid species, measuringup to 5,8 mm in length. It lives on stems and branches ofvarious willow species, where it builds up large coloniesand attracts insects, such as wasps, that feed onhoneydew. Tuberolachnus salignus is found almost every -where willows are planted, except for Australasia(BLACKMAN and EASTOP, 1994). Many aspects of theecology of this aphid species and its interactions with hostplants are poorly understood. The species is known to beanholocyclic, but where and how it overwinters is notknown. Studies by COLLINS et al. (2001a, 2001b) showedthat, in laboratory conditions, infestation by T. salignuscould reduce above- and below-ground growth and themass of existing wood tissue of willow. The presence of T.salignus on willow trees also increases photosynthetic rate,water use and nitrogen content in leaves (COLLINS, 2001;COLLINS et al., 2001b).The predicted expansion of land under SRC willow, aswell as the possibility of springs and summers in the UKbecoming warmer, has raised concerns that this aphid maybecome a serious pest on willow crops. There is thereforea need to understand the threat of this potential pestspecies by studying its biology and host selectionbehaviour, to inform the development of effectivemanagement strategies.In this research, host selection studies of T. salignus onSRC willow varieties were undertaken to investigate thehypotheses that a) aphid behaviour is affected by chemicalcues from the host and b) differences in host–aphidinteractions have a basis in the genetics of the host. Toaddress these hypotheses, laboratory bioassays and fieldexperiments were carried out on the infestation pattern ofT. salignus on different willow varieties. METHODSBIOASSAYSCultures of the giant willow aphid (T. salignus) wereestablished in an insectary in October 2006. The aphidswere collected from trees in the National Willow Col -lection at Rothamsted Research, Harpenden, UK, andreared on the willow variety ‘Resolution’ [(Salix viminalisL. x viminalis ‘Jorrun’) x (S. viminalis x S. schwerinii Wolf‘Bjorn’)]. Aphids were kept at 18°C with a regime of 16hours of light per 24 hours. Alate T. salignus which hadbeen starved overnight were used for the bioassays.Plant material was obtained from the National WillowCollection at Rothamsted Research. The list of accessionsused in testing is shown in Table 1. The non-host speciespoplar, variety ‘Unal’, was also included as a control.Olfactometer tests were performed in the laboratoryusing a Linear Track Olfactometer (LTO) modified fromthe original design (SAKUMA and FUKAMI, 1985), and sixwillow genotypes were initially chosen for use in thebioassays. The treatments were placed in glass jars out ofsight of the olfactometer. Using airflow of 3 l/min and aplant mass of 30±2 g (stem and leaf), aphids were– Received 30 July 2009     Accepted 2 September 2009     Published 1 December 2009observed for ten minutes climbing up a vertical wire to aT-junction with a horizontal wire, leading to a choice oftwo directions. Only responding aphids were counted andthe decision at the T-junction was recorded. To avoid bias,the direction from which the odour was presented wasalternated.Each of the different plants was tested against a controlof a Whatman filter paper moistened with distilled water.To test T. salignus attraction to conspecifics, ten apteraewere tested against the same control. The data wereanalysed using a one-tailed chi-square probability test fordistribution. FIELD TRIALThe field trial comprised six SRC willow varieties(Table 2), replicated six times in plots of 40 plants(10x4), using a 6x6 Latin square design, and a plot sizeof 4.5x4.8 m.The willow material was obtained from the NationalWillow Collection at Rothamsted Research. Cuttings forthe trial were taken on 19th and 30th January 2007 andstored in a cold room at -4°C. Before planting, the cuttingswere soaked in water for 24 hours at room temperature.The field trial was planted on 2nd April 2007, in HighfieldIV at Rothamsted Research, and cut back in March 2008after the first year of growth, in accordance with standardmanagement methods for SRC willows.Measurements of aphid infestation were recorded usingseven size classes (Table 3). Two trees from each plot wereassessed.The infestation level data were analysed using Anova,testing for differences in aphid infestation level betweenvarieties, and for each date separately, in Genstat 10(PAYNE et al., 2007).RESULTSOut of the alatae placed in the holding pot of the LTO,61.7% (n=474) responded. Tuberolachnus salignus224 G. ARADOTTIR ET AL. REDIA, Vol. XCII, 2009Table 1 – Willow varieties used for bioassays and their parentage.Variety name ParentageBowles Hybrid S. viminalis L.Discovery S. schwerinii Wolf ‘K3 Hilliers’ x(S. viminalis L. x S. schwerinii Wolf ‘Bjorn’)Tordis S. viminalis L. x S. schwerinii WolfStott 10 S. burjatica Nasarov x S. viminalis L.Baldwin S. triandra L.S. gilgiana S. gilgiana SeemenUnal (poplar) Populus trichocarpa L. x P. deltoides Bartr.Ex Marsh.Table 2 – Willow varieties planted in field trial and their parentage.Variety name ParentageBowles Hybrid S. viminalis L.Resolution (S. viminalis L. x S. viminalis L. ‘Jorrun’) x(S. viminalis L. x S. schwerinii Wolf ‘Bjorn’)Tora S. viminalis L. x S. schwerinii WolfTordis S. viminalis L. x S. schwerinii WolfQ83 S. triandra L. x S. viminalis L.Baldwin S. triandra L.Table 3 –  Size classes used to measure area of aphid colonies onwillow trees in the field. Area Area mid-pointno infestation 0≤ 1 cm2 0.5> 1 cm2, ≤ 8 cm2 4.5> 8 cm2, ≤ 27 cm2 17.5> 27 cm2, ≤ 64 cm2 45.5> 64 cm2, ≤ 125 cm2 94.5> 125 cm2, ≤ 216cm2 170.5Table 4 – Results from Linear Track Olfactometer bioassays testing different willows against the control. Number of starved alatae choos-ing willow or control: n, total number tested; pobs, proportion observed going towards the willow odour; chi square; df, degrees of free-dom and P-value.Varietyname Willow Control n pobs χ2 d.f. PDiscovery 43 18 61 0.70 5.12 1 0.02Bowles Hybrid 28 10 38 0.74 4.26 1 0.04Tordis 24 18 42 0.57 0.43 1 0.51Stott 10 18 23 41 0.44 0.30 1 0.58Baldwin 20 27 47 0.43 0.52 1 0.47Salix gilgiana 28 41 69 0.41 1.22 1 0.27Poplar 14 14 28 0.50 0.00 1 1.0010 aphids 30 48 78 0.38 2.08 1 0.15Table 5 – Results from Linear Track Olfactometer bioassaytesting ‘Bowles Hybrid’ against ‘Baldwin’. Number of starvedalatae choosing willow or control: n, total number tested; pobs,proportion observed going towards the willow odour; chi square;d.f., degrees of freedom and P-value.Bowles Baldwin n pobs χ2 d.f. PHybrid42 28 70 0.60 1.40 1 0.24showed a significant positive response to ‘Bowles Hy -brid’ and ‘Discovery’, but no willow variety elicited anegative response from the aphids (Table 4). Whentesting for responses to poplar, a non-host plant, theresults were not significant, with half going towards theplant odour and half going to the control. The alatae didnot show an attraction to the apterous aphids. In contrast to results found when ‘Bowles Hybrid’ wastested against the control, when the aphids were giventhe choice between ‘Bowles Hybrid’ and ‘Baldwin’ in theLTO (Table 5), they did not show a significant responseto ‘Bowles Hybrid’.Preliminary analysis on results from field trials during2007 and 2008 have shown that T. salignus infestationlevels vary significantly on different SRC willow varietieswhen infestation is at its peak density (18 September 07,P=0.005; 28 October 08 P=0.007) and that levels werehighest on the varieties which give the highest positiveresponse in the laboratory bioassays. This work needsfurther substantiation. The infestation peaked just over amonth earlier in 2007 than in 2008.DISCUSSIONThe results confirm the hypothesis that T. salignus isaffected by the chemical cues from their host plant, as theyrespond differently to the odour of different willowvarieties in the olfactometer. Salix viminalis ‘BowlesHybrid’, which has been shown to be susceptible to T.salignus infestation (COLLINS, 2001), had a significantpositive response from the aphids in the olfactometer.COLLINS (2001) tested the variety Q83, a S. triandra L. x S.viminalis hybrid, and found it to be a poor quality foodplant for T. salignus, in an experiment comparing six willowvarieties. Here, a pure S. triandra variety (‘Baldwin’) wastested, but the aphids were not significantly repelled by thisspecies in the olfactometer. The four most attractive willowvarieties to T. salignus all have S. viminalis in theirparentage. The most attractive were the pure S. viminalis‘Bowles Hybrid’ and ‘Discovery’. The least attractivevarieties were ‘Baldwin’, a pure S. triandra, and S. gilgianaSeemen, but there was no significant difference betweenaphids going to the control over the odour of these threewillows. Salix triandra has recently been shown to begenetically distant from other species of the subgenus Salix(TRYBUSH et al., 2008). This is an interesting finding asS. triandra seems to have a low number of associated pests(COLLINS et al., 2001a; TOPP et al., 2002; HJALTEN et al.,2007). The unattractiveness of this species has beenattributed to its secondary compound composition, as itcontains phenolic glucosides which can be detrimental toherbivores (LINDROTH, 1988; KOLEHMAINEN et al., 1995).Based on the genetic diversity studies of willows, S. gilgianais closely related to S. purpurea L. (TRYBUSH et al., 2008),which has been shown to be resistant to several insects inAmerica (NORDMAN et al., 2005).Tuberolachnus salignus did not show a significantattraction to ‘Bowles Hybrid’ when tested against ‘Bal -dwin’, a less attractive willow variety. The fact that ‘Bal -dwin’ was not significantly repellent to the aphids whentested on its own may explain the lack of a clear differencein responses to these two varieties when tested together.When T. salignus was presented with a choice between acontrol and 10 conspecific apterae, no significantpreference was detected. This is surprising given that thespecies is entirely parthenogenetic, with no requirement tofind a mate. Also, landing on a plant with a pre-existingcolony could mean competition for resources.There was a significant difference in infestation densitieson the six willow varieties in the field trial for both fieldseasons 2007 and 2008. COLLINS (2001) showed that T.salignus has different reproductive output on differentwillow hosts. This raises the question whether theobserved differences in infestation densities on differentwillow varieties are due to pre- or post-alighting behaviourby the aphids, or to a combination of both. ACKNOWLEDGEMENTSThis work was funded by the Biotechnology andBiological Sciences Research Council.REFERENCESBLACKMAN R.L., EASTOP V.F., 1994 – Aphids on the World’sTrees, an Identification and Information Guide, 1st edn.CABI, Wallingford, 921 pp.COLLINS C.M., 2001 – Aspects of the Ecology of Two Stem-feeding Willow Aphid Species. - PhD Thesis, ImperialCollege, London.COLLINS C.M., FELLOWES M.D.E., SAGE R.B., LEATHERS.R., 2001a – Host selection and performance of the giantwillow aphid, Tuberolachnus salignus Gmelin -implications for pest management. - Agric. ForestEntomol., 17: 183-189.COLLINS C.M., ROSADO R.G., LEATHER S.R., 2001b – Theimpact of the aphids Tuberolachnus salignus andPterocomma salicis on willow trees. - Ann. Appl. Biol.,138: 133-140.HAUGHTON A.J., BOND A.J., LOVETT A.A., DOCKERTY T.,SUNNENBERG G., CLARK S.J., BOHAN D.A., SAGE R.B.,MALLOTT M.D., MALLOTT V.E., CUNNINGHAM M.D.,RICHE A.B., SHIELD I.F., FINCH J.W., TURNER M.M.,KARP A., 2009 – A novel, integrated approach to assessingsocial, economic and environmental implications ofchanging rural land-use: a case study of perennial biomasscrops. - J. Appl. Ecol., 46: 315-322.HJALTEN J., NIEMI L., WENNSTROM A., ERICSON L.,ROININEN H., JULKUNEN-TIITTO R., 2007 – Variableresponses of natural enemies to Salix triandra phenotypeswith different secondary chemistry. - Oikos, 116: 751-758.KARP A., SHIELD I., 2008 – Bioenergy from plants and thesustainable yield challenge. - New Phytol., 179: 15-32.KOLEHMAINEN J., JULKUNEN-TIITTO R., ROININEN H.,TAHVANAINEN J., 1995 – Phenolic glucosides as feedingcues for willow-feeding leaf beetles. - Entomol. Exp.Appl., 74: 235-243.LINDROTH R.L., 1988 – Hydrolysis of phenolic glycosides bymidgut beta-glucosidases in Papilio glaucus subspecies. -Insect Biochem., 18: 789-792.NORDMAN E.E., ROBISON D.J., ABRAHAMSON L.P., VOLKT.A., 2005 – Relative resistance of willow and poplarbiomass production clones across a continuum ofherbivorous insect specialization: Univariate andmultivariate approaches. - Forest Ecol. Manage., 217:307-318.PAYNE R.W., MURRAY D.A., HARDING S.A., BAIRD D.B.,SOUTAR D.M., 2007 – Genstat for Windows -Introduction, 10th edn. VSN International, HemelHempstead.SAKUMA M., FUKAMI H., 1985 – The linear trackolfactometer - an assay device for taxes of the German-cockroach, Blatella germanica (Dictyoptera, Blatellidae)toward their aggregation pheromone. - Appl. Entomol.Zool., 20: 387-402.TOPP W., KULFAN J., ZACH P., NICOLINI F., 2002 – Beetleassemblages on willow trees: do phenolic glycosidesmatter? - Diversity Distrib., 8: 85-106.TRYBUSH S., JAHODOVA S., MACALPINE W., KARP A., 2008 –Salix for Bioenergy: Genetic studies of germplasm resourcereveal new insights into relationships among subgenera,sections and species. - BioEnergy Res., 1: 67-79.VOLK T.A., ABRAHAMSON L.P., NOWAK C.A., SMART L.B.,THARAKAN P.J., WHITE E.H., 2006 – The development ofshort-rotation willow in the northeastern United States forbioenergy and bioproducts, agroforestry andphytoremediation. - Biomass Bioenergy, 30: 715-727.HOST SELECTION OF THE GIANT WILLOW APHID (TUBEROLACHNUS SALIGNUS) 225226 Bianca

Host Selection of the giant willow aphid (Tuberolachnus salignus)

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Host Selection of the giant willow aphid (Tuberolachnus salignus)

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