Fernández, P.C.; Braccini, C.L.; Dávila, C.; Barrozo, R.B.; Aráoz, M.V.C.; Cerrillo, T.; Gershenzon, J.; Reichelt, M.; Zavala, J.A. "The use of Leaf Surface Contact Cues During Oviposition Explains Field Preferences in the Willow Sawfly Nematus Oligospilus" (2019) Scientific Reports. 9(1)
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After an insect herbivore has reached its host plant, contact cues from the leaf surface often determine host acceptance. We studied contact cues during oviposition behavior of a willow pest, the sawfly Nematus oligospilus (Hymenoptera: Tenthredinidae), a specialist feeder on Salix (Salicaceae) trees, and how it determines oviposition preference in lab and field conditions. We described the sequence of behaviors that lead to egg laying on the most and least preferred willow species. Then we studied the morphology of chemosensory structures present on the female antenna, cerci and ovipositor. Since phenolic glycosides (PGs) are the main secondary metabolites present in Salicaceae species, we investigated their role in host acceptance. We quantified these compounds in different willow species and correlated PG content with oviposition preference under lab and natural field conditions. We demonstrated a major role for contact cues in triggering N. oligospilus egg laying on the leaf surface of preferred willow genotypes. Firstly cues are sensed by antennae, determining to leave or stay on the leaf. After that, sensing is performed by abdominal cerci, which finally triggers egg laying. The lack of PGs in non-preferred species and the significant correlation observed between PGs, natural damage and oviposition preference suggest a role for these compounds in host selection. Our study suggests that in specialist feeders, secondary compounds normally acting as defenses can actually act as a susceptibility factor by triggering specific insect behavior for oviposition. These defensive compounds could be selected against to increase resistance. © 2019, The Author(s).


Documento: Artículo
Título:The use of Leaf Surface Contact Cues During Oviposition Explains Field Preferences in the Willow Sawfly Nematus Oligospilus
Autor:Fernández, P.C.; Braccini, C.L.; Dávila, C.; Barrozo, R.B.; Aráoz, M.V.C.; Cerrillo, T.; Gershenzon, J.; Reichelt, M.; Zavala, J.A.
Filiación:Consejo Nacional de Investigaciones Científicas y Tecnológicas, Buenos Aires, Argentina
INTA, Estación Experimental Agropecuaria Delta del Paraná. Paraná de las Palmas y Cl Comas s/n (2804), Campana, Buenos Aires, Argentina
Universidad de Buenos Aires, Cátedras de Química de Biomoléculas y Bioquímica, Facultad de Agronomía. Av. San Martín 4453, Ciudad Autónoma de Buenos Aires, C1417DSE, Argentina
INTA, Instituto de Recursos Biológicos, Centro de Investigación de Recursos Naturales, De los Reseros y Dr. Nicolás Repetto s/n (1686), Hurlingham, Buenos Aires, Argentina
Universidad de Buenos Aires, Departamento Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Instituto Biodiversidad y Biología Experimental y Aplicada, CONICET - UBA, Ciudad Autónoma de Buenos Aires, Argentina
PROIMI-CONICET Biotecnología, Av. Belgrano y Pje, Caseros (T4001 MBV), Tucumán, Argentina and Facultad de Ciencias Naturales e IML, UNT, Miguel Lillo 205, San Miguel de Tucumán, Argentina
Max Planck Institute for Chemical Ecology, Jena, Germany
Palabras clave:adult; article; case report; clinical article; egg laying; female; field study; genotype; host selection; human; Hymenoptera; leaf surface; morphology; nonhuman; willow
Título revista:Scientific Reports
Título revista abreviado:Sci. Rep.


  • Kanno, H., Harris, M.O., Leaf physical and chemical features influence selection of plant genotypes by Hessian fly (2000) J. Chem. Ecol, 26, pp. 2335-2354. , COI: 1:CAS:528:DC%2BD3cXovV2htr4%3D
  • Müller, C., Hilker, M., Host finding and oviposition behavior in a chrysomelid specialist - The importance of host plant surface waxes (2001) J. Chem. Ecol, 27, pp. 985-994
  • Riederer, M., Müller, C., Biology of the plant cuticle (2006) Annu. Plant Rev, p. 438
  • Udayagiri, S., Mason, C.E., Epicuticular wax chemicals in Zea mays influence oviposition in Ostrinia nubilalis (1997) J. Chem. Ecol., 23, pp. 1675-1687. , COI: 1:CAS:528:DyaK2sXlt1Cgurw%3D
  • Morris, B.D., Foster, S.P., Harris, M.O., Identification of 1-octacosanal and 6-methoxy-2-benzoxazolinone from wheat as ovipositional stimulants for Hessian fly, Mayetiola destructor (2000) J. Chem. Ecol, 26, pp. 859-873. , COI: 1:CAS:528:DC%2BD3cXisl2gsr0%3D
  • Brooks, J.S., Williams, E.H., Feeny, P., Quantification of contact oviposition stimulants for black swallowtail butterfly, Papilio polyxenes, on the leaf surface of wild carrot, Daucus carota (1996) J. Chem. Ecol., 22, pp. 2341-2357. , COI: 1:CAS:528:DyaK2sXktlKnug%3D%3D
  • Derridj, S., Wu, B., Stammitti, L., Garrec, J., Derrien, A., Chemicals on the leaf surface, information about the plant available to insects (1996) Entomol. Exp. Appl, 80, pp. 197-201. , COI: 1:CAS:528:DyaK28Xlslyitbw%3D
  • Lombarkia, N., Derridj, S., Incidence of apple fruit and leaf surface metabolites on Cydia pomonella oviposition (2002) Entomol. Exp. Appl., 104, pp. 79-87. , COI: 1:CAS:528:DC%2BD38XptFeisLw%3D
  • Marazzi, C., Patrian, B., Städler, E., Secondary metabolites of the leaf surface affected by sulphur fertilisation and perceived by diamondback moth (2004) Chemoecology, 14, pp. 87-94. , COI: 1:CAS:528:DC%2BD2cXjslers7s%3D
  • Shroff, R., Quantification of plant surface metabolites by matrix-assisted laser desorption-ionization mass spectrometry imaging: Glucosinolates on Arabidopsis thaliana leaves (2015) Plant J., 81, pp. 961-972. , COI: 1:CAS:528:DC%2BC2MXjvFylsL4%3D
  • Tahvanainen, J., Julkunen-Tiitto, R., Kettunen, J., Phenolic glycosides govern the food selection of willow feeding leaf beetles (1985) Oecologia, 67, pp. 52-56. , COI: 1:STN:280:DC%2BC1cznvVemtg%3D%3D
  • Lindroth, R.L., Peterson, S.S., Effects of plant phenols of performance of southern armyworm larvae (1988) Oecologia, 75, pp. 185-189. , COI: 1:STN:280:DC%2BC1cznvFensw%3D%3D
  • Lindroth, R.L., Scriber, J., Hsia, M., Chemical ecology of the tiger swallowtail: mediation of host use by phenolic glycosides (1988) Ecology, 69, pp. 814-822. , COI: 1:CAS:528:DyaL1cXkvFSjt7c%3D
  • Kolehmainen, J., Roininen, H., Julkunen-Tiitto, R., Tahvanainen, J., Importance of phenolic glucosides in host selection of shoot galling sawfly, Euura amerinae, on Salix pentandra (1994) J. Chem. Ecol., 20, pp. 2455-2466. , COI: 1:CAS:528:DyaK2cXmt1Kqsrc%3D
  • Orians, C.M., Willow hybridization differentially affects preference and performance of herbivorous beetles (1997) Entomol. Exp. Appl., 83, pp. 285-294
  • Roininen, H., Price, P.W., Julkunen-Tiitto, R., Tahvanainen, J., Ikonen, A., Oviposition stimulant for a gall-inducing sawfly, Euura lasiolepis, on willow is a phenolic glucoside (1999) J. Chem. Ecol, 25, pp. 943-953. , COI: 1:CAS:528:DyaK1MXjtVOitbg%3D
  • Braccini, C., Vega, A., Chludil, H., Leicach, S., Fernandez, P., Host selection, oviposition behaviour and leaf traits in a specialist willow sawfly on species of Salix (Salicaceae) (2013) Ecol. Entomol., 38, pp. 617-626
  • Dapoto, G., Giganti, H., Bioecología de Nematus desantisi Smith (Hymenoptera: Tenthredinidae: Nematinae) en las provincias de Río Negro y Neuquén (Argentina) (1994) Bosque, 15, pp. 27-32
  • Urban, A., Eardley, C., A recently introduced sawfly, Nematus oligospilus Förster (Hymenoptera: Tenthredinidae), that defoliates willows in southern Africa (1995) African Entomol, 3, pp. 23-27
  • Charles, J.G., Allan, D.J., Development of the willow sawfly, Nematus oligospilus, at different temperatures, and an estimation of voltinism throughout New Zealand (2000) New Zeal. J. Zool., 27, pp. 197-200
  • Smith, D., A synopsis of the sawflies (Hymenoptera: Symphyta) of America south of the United States: Tenthredinidae (Nematinae, Heterarthrinae, Tenthredininae) (2003) Trans. Am. Entomol. Soc., 129, pp. 1-45
  • Alderete, M., Liljesthrom, G., Fidalgo, P., Bio-ecología y perspectivas para el manejo de la avispa sierra del sauce, Nematus oligospilus. Ser. Técnica Manejo Integr (2010) Plagas For, p. 10
  • Charles, J.G., Allan, D.J., Fung, L., Susceptibility of willows to oviposition by the willow sawfly, Nematus oligospilus (1998) Proc. 51St New Zeal. Plant Prot. Conf, pp. 230-234
  • Braccini, C.L., Both volatiles and cuticular plant compounds determine oviposition of the willow sawfly Nematus oligospilus on leaves of Salix spp. (Salicaceae) (2015) J. Chem. Ecol., 41, pp. 985-996. , COI: 1:CAS:528:DC%2BC2MXhs1ehsrrN
  • Sniezko, R., Koch, J., Breeding trees resistant to insects and diseases: Putting theory into application (2017) Biol. Invasions, pp. 3317-3400
  • Renwick, J., Chew, F.S., Oviposition behavior in Lepidoptera (1994) Annu. Rev. Entomol., 39, pp. 377-400
  • Carr, T.G., Roininen, H., Price, P.W., Oviposition preference and larval performance of Nematus oligospilus (Hymenoptera: Tenthredinidae) in relation to host plant vigor (1998) Environ. Entomol, 27, pp. 615-625
  • Boeckler, G.A., Gershenzon, J., Unsicker, S.B., Phenolic glycosides of the Salicaceae and their role as anti-herbivore defenses (2011) Phytochemistry, 72, pp. 1497-1509. , COI: 1:CAS:528:DC%2BC3MXptlWrs70%3D
  • Blumstein, D., Daniel, J., (2007) Quantifying Behavior the Jwatcher Way, , Sinauer Associates
  • Buteler, M., Weaver, D.K., Peterson, R.K.D., Oviposition behavior of the wheat stem sawfly when encountering plants infested with cryptic conspecifics (2009) Environ. Entomol., 38, pp. 1707-1715
  • Badenes-Pérez, F.R., Reichelt, M., Gershenzon, J., Heckel, D.G., Phylloplane location of glucosinolates in Barbarea spp. (Brassicaceae) and misleading assessment of host suitability by a specialist herbivore (2011) New Phytol, 189, pp. 549-556
  • Jetter, R., Schäffer, S., Chemical composition of the Prunus laurocerasus leaf surface. Dynamic changes of the epicuticular wax film during leaf development (2001) Plant Physiol, 126, pp. 1725-1737. , COI: 1:CAS:528:DC%2BD3MXlvFOis78%3D
  • Abràmoff, M.D., Magalhães, P.J., Ram, S.J., Image Processing with ImageJ (2004) Biophotonics Int, 11, pp. 36-42
  • Gammell, M., Vries, H., Jennings, D., Carlin, C., Hayden, T., David’s score: a more appropriate dominance ranking method than Clutton-Brock et al.’s index (2003) Anim. Behav., 66, pp. 601-605
  • (2012) R: A Language and Environment for Statistical Computing, , R Foundation for Statistical Computing, Vienna, Austria
  • Snyder, D.T., Schilling, M.C., Hochwender, C.G., Kaufman, A.D., Profiling phenolic glycosides in Populus deltoides and Populus grandidentata by leaf spray ionization tandem mass spectrometry (2015) Anal. Methods, 7, pp. 870-876. , COI: 1:CAS:528:DC%2BC2cXitFCru7%2FL
  • Pirk, G., López de Casenave, J., Seed preference of three harvester ants of the genus Pogonomyrmex (Hymenoptera: Formicidae) in the Monte desert: are they reflected in the diet? (2011) Ann. Entomol. Soc. Am., 104, pp. 212-220
  • Hemmi, J.M., Zeil, J., Animals as prey: perceptual limitations and behavioural options (2005) Mar. Ecol. Prog. Ser., 287, pp. 274-278
  • Hemmi, J.M., Pfeil, A., A multi-stage anti-predator response increases information on predation risk (2010) J. Exp. Biol., 213, pp. 1484-1489
  • Gripenberg, S., Mayhew, P.J., Parnell, M., Roslin, T., A meta-analysis of preference-performance relationships in phytophagous insects (2010) Ecol. Lett, 13, pp. 383-393
  • Altesor, P., González, A., Preference–performance in a specialist sawfly on congeneric host plants (2018) Entomol. Exp. Appl, pp. 1-10
  • Price, P.W., (2003) Macroevolutionary Theory on Macroecological Patterns Peter W. Price, , Cambridge University Press
  • Ferrier, S.M., Price, P.W., Oviposition preference and larval performance of a rare bud-galling sawfly (Hymenoptera: Tenthredinidae) on willow in Northern Arizona (2004) Environ. Entomol., 33, pp. 700-708
  • Müller, C., Riederer, M., Plant surface properties in chemical ecology (2005) J. Chem. Ecol., 31, pp. 2621-2651
  • Bargel, H., Barthlott, W., Koch, K., Schreiber, L., Neinhuis, C., (2004) The Evolution of Plant Physiology, , eds Hemsley, A. & Poole, I, Elsevier Academic Press
  • Mercado, M., Coll Araoz, M., Ruiz, A., Grau, A., Ponessa, G., Tricomas glandulares de yacón, Smallanthus sonchifolius (Asteraceae). Desarrollo ontogenético, análisis estructural y ultraestructural (2012) Lilloa, 49, pp. 40-51
  • Roessingh, P., Oviposition and tarsal chemoreceptors of the cabbage root fly are stimulated by glucosinolates and host plant-extracts (1992) Entomolgia Exp. Appl., 65, pp. 267-282. , COI: 1:CAS:528:DyaK3sXitlSls7k%3D
  • Spencer, J.L., Waxes enhance Plutella xylostella oviposition in response to sinigrin and cabbage homogenates (1996) Entomol. Exp. Appl., 81, pp. 165-173
  • Spencer, J.L., Pillai, S., Bernays, E.A., Synergism in the oviposition behavior of Plutella xylostella: sinigrin and wax compounds (1999) J. Insect Behav, 12, pp. 483-500
  • Bernays, E.A., Neural limitations in phytophagous insects: implications for diet breadth and evolution of host affiliation (2001) Annu. Rev. Entomol., 46, pp. 703-727. , COI: 1:CAS:528:DC%2BD3MXitlSmt7c%3D
  • Reifenrath, K., Riederer, M., Müller, C., Leaf surface wax layers of Brassicaceae lack feeding stimulants for Phaedon cochleariae (2005) Entomol. Exp. Appl., 115, pp. 41-50. , COI: 1:CAS:528:DC%2BD2MXkvFOktbY%3D
  • Stenberg, J., Lehrman, A., Björkman, C., Uncoupling direct and indirect plant defences: novel opportunities for improving crop security in willow plantations (2010) Agric. Ecosyst. Environ, 139, pp. 528-533
  • Torp, M., Lehrman, A., Stenberg, J.A., Julkunen-Tiitto, R., Björkman, C., Performance of an herbivorous leaf beetle (Phratora vulgatissima) on Salix F2 hybrids: the importance of phenolics (2013) J. Chem. Ecol., 39, pp. 516-524. , COI: 1:CAS:528:DC%2BC3sXlsVGrsr0%3D


---------- APA ----------
Fernández, P.C., Braccini, C.L., Dávila, C., Barrozo, R.B., Aráoz, M.V.C., Cerrillo, T., Gershenzon, J.,..., Zavala, J.A. (2019) . The use of Leaf Surface Contact Cues During Oviposition Explains Field Preferences in the Willow Sawfly Nematus Oligospilus. Scientific Reports, 9(1).
---------- CHICAGO ----------
Fernández, P.C., Braccini, C.L., Dávila, C., Barrozo, R.B., Aráoz, M.V.C., Cerrillo, T., et al. "The use of Leaf Surface Contact Cues During Oviposition Explains Field Preferences in the Willow Sawfly Nematus Oligospilus" . Scientific Reports 9, no. 1 (2019).
---------- MLA ----------
Fernández, P.C., Braccini, C.L., Dávila, C., Barrozo, R.B., Aráoz, M.V.C., Cerrillo, T., et al. "The use of Leaf Surface Contact Cues During Oviposition Explains Field Preferences in the Willow Sawfly Nematus Oligospilus" . Scientific Reports, vol. 9, no. 1, 2019.
---------- VANCOUVER ----------
Fernández, P.C., Braccini, C.L., Dávila, C., Barrozo, R.B., Aráoz, M.V.C., Cerrillo, T., et al. The use of Leaf Surface Contact Cues During Oviposition Explains Field Preferences in the Willow Sawfly Nematus Oligospilus. Sci. Rep. 2019;9(1).