Hostname: page-component-7479d7b7d-qs9v7 Total loading time: 0 Render date: 2024-07-13T09:58:55.425Z Has data issue: false hasContentIssue false

Previous herbivory alerts conspecific gravid sawflies to avoid unsuitable host plants

Published online by Cambridge University Press:  09 December 2019

G. A. Valladares
Affiliation:
Facultad de Agronomía y Zootecnia, Universidad Nacional de Tucumán, Florentino Ameghino S/N. B° Mercantil (4105), El Manantial, Tucumán, Argentina Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), CABA, Argentina
M. V. Coll-Aráoz
Affiliation:
PROIMI-CONICET, Av. Manuel Belgrano 2960 (T4001MVB), S. M. de Tucumán, Tucumán, Argentina
M. Alderete
Affiliation:
Facultad de Ciencias Naturales e Instituto Miguel Lillo, Universidad Nacional de Tucumán, M. Lillo 205 (4000), S. M. de Tucumán, Tucumán, Argentina
M. T. Vera
Affiliation:
Facultad de Agronomía y Zootecnia, Universidad Nacional de Tucumán, Florentino Ameghino S/N. B° Mercantil (4105), El Manantial, Tucumán, Argentina Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), CABA, Argentina
P. C. Fernández*
Affiliation:
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), CABA, Argentina INTA EEA Delta del Paraná, Paraná de las Palmas y Cl Comas S/N (2804), Campana, Buenos Aires, Argentina Cátedra de Química de Biomoléculas, Departamento de Química Aplicada y Alimentos, Facultad de Agronomía, Universidad de Buenos Aires. Av. San Martín 4453 (C1417DSE), Ciudad Autónoma de Buenos Aires, Argentina
*
Author for correspondence: P. C. Fernández, E-mail: pcfernan@agro.uba.ar

Abstract

The willow sawfly, Nematus oligospilus (Förster), is a pest in Salix commercial forests and has been reported worldwide. Female adults must recognize a suitable host plant to oviposit, since her offspring lack the ability to move to another host. We evaluated the effect of conspecific herbivory on the oviposition choices of N. oligospilus females by providing damaged (DP) and undamaged (UP) plants of Salix humboldtiana, a native willow from South America, as oviposition substrates. Local and systemic effects were studied. For the local treatment, a twig from the DP with damaged leaves was contrasted to a twig from a UP in dual choice experiments. For systemic treatment, a twig from the DP with intact leaves was contrasted to a twig from a UP. We estimated the use of olfactory and contact cues by comparing volatile emission of DP and UP, and by analysing the behaviour of the females during host recognition after landing on the leaf surface. In the context of the preference–performance hypothesis (PPH), we also tested if oviposition site selection maximizes offspring fitness by evaluating neonate hatching, larval performance and survival of larvae that were born and bred on either DP or UP. Our results demonstrate that previous conspecific herbivory on S. humboldtiana has a dramatic impact on female oviposition choices and offspring performance of the sawfly N. oligospilus. Females showed a marked preference for laying eggs on UP of S. humboldtiana. This preference was found for both local and systemic treatments. Volatile emission was quantitatively changed after conspecific damage suggesting that it could be related to N. oligospilus avoidance. In the dual choice preference experiments, the analysis of the behaviour of the females once landing on the leaf surface suggested the use of contact cues triggering egg laying on leaves from UP and avoidance of leaves from DP. Furthermore, 48 h of previous conspecific feeding was sufficient to dramatically impair neonate hatching, as well as larval development and survival, suggesting a rapid and effective reaction of the induced resistance mechanisms of the tree. In agreement with the PPH, these results support the idea that decisions made by colonizing females may result in optimal outcomes for their offspring in a barely studied insect model, and also opens the opportunity for studying tree-induced defences in the unexplored South American willow S. humboldtiana.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adams, RP (2007) Identification of Essential Oil Components By Gas Chromatography/Mass Spectrometry Allured Publishing Corporation, Carol Stream, Illinois, USA, p. 840.Google Scholar
Agrawal, AA and Fishbein, M (2006) Plant defense syndromes. Ecology 87, 132149.CrossRefGoogle ScholarPubMed
Alderete, M (2005) Estudios poblacionales de Nematus oligospilus Föerster (Hymenoptera: Tenthredinidae), en Tucumán, plaga de sauces (Salicáceas) en Argentina (PhD's Thesis). Facultad de Ciencias Naturales, Universidad Nacional de Tucumán, Argentina. 276 pp.Google Scholar
Alderete, M, Liljesthrom, G and Fidalgo, P (2010) Bio-ecología y perspectivas en el manejo de la avispa sierra del sauce, Nematus oligospilus (Hymenoptera; Tenthredinidae). In Villacide, JM and Corley, JC (eds), Series Técnicas: Manejo integrado de plagas forestales. Argentina, Cambio Rural – Laboratorio de Ecología de Insectos INTA Bariloche ISSN 1851-4103. pp. 112.Google Scholar
Allman, S, Späthe, A, Bisch-Knaden, S, Kallenbach, M, Reinecke, A, Sachse, S, Baldwin, I and Hansson, BS (2013) Feeding-induced rearrangement of green leaf volatiles reduces moth oviposition. eLife 2, e00421.CrossRefGoogle Scholar
Altesor, P and González, A (2018) Preference–performance in a specialist sawfly on congeneric host plants. Entomologia Experimentalis et Applicata. Special Issue: Multilevel Feeding Ecology, 166, 442451.CrossRefGoogle Scholar
Amo, L, Jansen, JJ, van Dam, NM, Dicke, M and Visser, ME (2013) Birds exploit herbivore-induced plant volatiles to locate herbivorous prey. Ecology Letters 16, 13481355.CrossRefGoogle ScholarPubMed
Arimura, G, Huber, BPW and Bohlmann, J (2004) Forest tent caterpillars (Malacosoma disstria) induce local and systemic diurnal emissions of terpenoid volatiles in hybrid poplar (Populus trichocarpa x deltoides): cDNA cloning, functional characterization and patterns of gene expression of germacrene-D synthase, PtdTPS1. Plant Journal 37, 603616.CrossRefGoogle ScholarPubMed
Arimura, G, Matsui, K and Takabayashi, J (2009) Chemical and molecular ecology of herbivore-induced plant volatiles: proximate factors and their ultimate functions. Plant Cell Physiology 50, 911923.CrossRefGoogle ScholarPubMed
Awmack, CS and Leather, CR (2002) Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology 47, 817844.CrossRefGoogle ScholarPubMed
Banchio, E, Valladares, G, Zygadlo, J, Bogino, PC, Rinaudi, LV and Giordano, W (2007) Changes in composition of essential oils and volatile emissions of Minthostachys mollis, induced by leaf punctures of Liriomyza huidobrensis. Biochemical Systematics and Ecology 35, 6874.CrossRefGoogle Scholar
Bennett, RN and Wallsgrove, RM (1994) Secondary metabolites in plant defence mechanisms. New Phytologist 127, 617633.CrossRefGoogle Scholar
Bergelson, J, Fowler, S and Hartley, S (1986) The effects of foliage damage on casebearing moth larvae, Coleophora serratella, feeding on birch. Ecological Entomology 11, 241250.CrossRefGoogle Scholar
Berry, JA (1997) Nematus oligospilus (Hymenoptera: Tenthredinidae), a recently introduced sawfly defoliating willows in New Zealand. New Zealand Entomologist 20, 5154.CrossRefGoogle Scholar
Beyaert, I, Köpke, D, Stiller, J, Hammerbacher, A, Yoneya, K, Schmidt, A, Gershenzon, A and Hilker, M (2011) Can insect egg deposition ‘warn’ a plant of future feeding damage by herbivorous larvae? Proceedings of the Royal Society of London B 279, 101108.Google ScholarPubMed
Blenn, B, Bandoly, M, Küffner, A, Otte, T, Geiselhardt, S, Fatouros, NE and Hilker, M (2012) Insect egg deposition induces indirect defense and epicuticular wax changes in Arabidopsis thaliana. Journal of Chemical Ecology 38, 882892.CrossRefGoogle ScholarPubMed
Braccini, CL, Vega, AS, Chludil, HD, Leicach, SR and Fernández, PC (2013) Host selection, oviposition behaviour and leaf traits in a specialist willow sawfly on species of Salix (salicaceae). Ecological Entomology 38, 617626.CrossRefGoogle Scholar
Braccini, CL, Vega, AS, Coll-Aráoz, MV, Teal, PE, Cerrillo, T, Zavala, JA and Fernández, PC (2015) Both volatiles and cuticular plant compounds determine oviposition of the willow sawfly Nematus oligospilus on leaves of Salix spp. (Salicaceae). Journal of Chemical Ecology 41, 985996.CrossRefGoogle Scholar
Bruzzese, E and McFadyen, R (2006) Arrival of leaf-feeding willow sawfly Nematus oligospilus Förster in Australia-pest or beneficial? Plant Protection Quarterly 21, 4344.Google Scholar
Caesar, AJ (2003) Synergistic interaction of soilborne plant pathogens and root-attacking insects in classical biological control of an exotic rangeland weed. Biological Control 28, 144153.CrossRefGoogle Scholar
Cerrillo, T (2009) Panorama de los sauces en Argentina: avances en el mejoramiento genético y en la identificación. Proceeding of the 3rd International Congress of the Salicaceae, Neuquén, Argentina.Google Scholar
Chaudhary, B (2013) Plant domestication and resistance to herbivory. International Journal of Plant Genomics, 572784, 114.CrossRefGoogle Scholar
Chen, YH, Gols, R and Benrey, B (2015) Crop domestication and its impact on naturally selected trophic interactions. Annual Review of Entomology 60, 3558.CrossRefGoogle ScholarPubMed
Clavijo, MA, Irmisch, S, Reinecke, A, Boeckler, GA, Veit, D, Reichelt, M, Hansson, BS, Gershenzon, J, Köllner, TG and Unsicker, SB (2014) A herbivore-induced volatile emission in black poplar: regulation and role in attracting herbivore enemies. Plan Cell & Environment 37, 19091923.CrossRefGoogle Scholar
Cook, JL, Houseweart, MW, Kulman, HM and Thompson, LC (1978) Foliar mineral difference related to sawfly defoliation of white spruce. Environmental Entomology 7, 780781.CrossRefGoogle Scholar
Di Rienzo, JA, Casanoves, F, Balzarini, MG, Gonzalez, L, Tablada, M and Robledo, CW InfoStat versión 2018 Grupo InfoStat, FCA. Argentina, Universidad Nacional de Córdoba. http://www.infostat.com.ar.Google Scholar
Dicke, M and van Loon, JJA (2000) Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context. Entomologia Experimentalis et Applicata 97, 237249.CrossRefGoogle Scholar
Dicke, M and Baldwin, IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends in Plant Science 15, 167175.CrossRefGoogle ScholarPubMed
Dickmann, D and Kuzovkina, YA (2014) Poplars and willows in the world. In Poplars and Willows: Trees for Society and the Environment. Isebrands JG and Richardson J (eds). Rome: FAO UN and CABI, pp. 891.CrossRefGoogle Scholar
Ede, FJ (2009) Can international experience help us to predict the potential impacts of willow sawfly (Nematus oligospilus Förster) on willow populations in Australia? Plant Protection Quarterly 24, 6266.Google Scholar
Fabisch, T, Gershenzon, J and Unsicker, SB (2019) Specificity of herbivore defense responses in a woody plant, Black Poplar (Populus nigra). Journal of Chemical Ecology 45, 162177.CrossRefGoogle Scholar
Fernández, PC, Braccini, CL, Dávila, C, Barrozo, RB, Coll-Araoz, MV, Cerrillo, T, Gershenzon, J, Reichelt, M and Zavala, JA (2019) The use of leaf surface contact cues during oviposition explains field preferences in the willow sawfly Nematus Oligospilus. Scientific Reports 9, 4946.CrossRefGoogle ScholarPubMed
Fordyce, JA (2006) Between-clutch interactions affect a benefit of group feeding for pipevine swallowtail larvae. Ecological Entomology 31, 7583.CrossRefGoogle Scholar
Forister, ML, Nice, CC, Fordyce, ML and Gompert, Z (2009) Host range evolution is not driven by the optimization of larval performance: the case of Lycaeides melissa (Lepidoptera: Lycaenidae) and the colonization of alfalfa. Oecologia 160, 551561.CrossRefGoogle Scholar
Frost, CJ, Appel, HM, Carlson, JE, De Moraes, CM, Mescher, MC and Schultz, JC (2007) Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecology Letters 10, 490498.CrossRefGoogle ScholarPubMed
Frost, CJ, Mescher, MC, Carlson, JE and De Moraes, CM (2008 a) Plant defense priming in plant-herbivore interactions: getting ready for a different battle. Plant Physiology 146, 818824.CrossRefGoogle Scholar
Frost, CJ, Mescher, MC, Dervinis, C, Davis, JM, Carlson, JE and De Moraes, CM (2008 b) Priming defense genes and metabolites in hybrid poplar by the green leaf volatile cis-3-hexenyl acetate. New Phytologist 180, 722734.CrossRefGoogle ScholarPubMed
Füssel, U, Dötterl, A, Jürgens, A and Aas, G (2007) Inter and intraspecific variation in floral scent in the genus Salix and its implication for pollination. Journal of Chemical Ecology 33, 749765.CrossRefGoogle ScholarPubMed
Gómez Jiménez, MI, Sarmiento, CE, Díaz, MF, Chautá, A, Peraza, A, Ramírez, A and Poveda, K (2014) Oviposition, larval preference, and larval performance in two polyphagous species: does the larva know best? Entomologia Experimentalis et Applicata 153, 2433.CrossRefGoogle Scholar
Gonzalez, RH, Barria, G and Guerrero, A (1986) Nematus desantisi Smith, a new species of forest importance in Chile (Hymenoptera: Tenthredinidae). Revista Chilena de Entomología 14, 1315.Google Scholar
Gripenberg, S, Mayhew, PJ, Parnel, LM and Roslin, T (2010) A meta-analysis of preference–performance relationships in phytophagous insects. Ecology Letters 13, 383393.CrossRefGoogle ScholarPubMed
Harris, MO, Sandanayake, M and Foster, SP (1999) Chemical stimuli from apple influence the behavior of neonate caterpillars of the generalist herbivore, Epiphyas postvittana (Lepidoptera: Tortricidae). Journal of Chemical Ecology 25, 17171738.CrossRefGoogle Scholar
Hatano, E, Ahmed, M, Saveer, AM, Borrero-Echeverry, F, Strauch, M, Ali Zakir, A, Bengtsson, M, Ignell, R, Anderson, P, Becher, PG, Witzgall, P and Dekker, T (2015) A herbivore-induced plant volatile interferes with host plant and mate location in moths through suppression of olfactory signalling pathways. BMC Biology 13, 75.CrossRefGoogle ScholarPubMed
Hauenstein, E, Pena-Cortes, F, Gonzalez, M and Schlatter, R (2005) New distribution range limits of Salix humboldtiana willd., Salicaceae, in Chile. Gayana Botanica 62, 4446.CrossRefGoogle Scholar
Heil, M and Karban, R (2010) Explaining evolution of plant communication by airborne signals. Trends in Ecology & Evolution 25, 137144.CrossRefGoogle ScholarPubMed
Herms, DA and Matton, WJ (1992) The dilemma of plants: to grow or defend. Quarterly Review of Biology 67, 283335.CrossRefGoogle Scholar
Hilker, M and Meiners, T (2006) Early herbivore alert: insect eggs induce plant defense. Journal of Chemical Ecology 32, 13791397.CrossRefGoogle ScholarPubMed
Hilker, M and Fatouros, NE (2015) Plant responses to insect egg deposition. Annual Review of Entomology 60, 493515.CrossRefGoogle ScholarPubMed
Holopainen, JK, Himanen, S and Poppy, GM (2013) Climate changes and their effects in the chemical ecology of insect parasitoids. In Wajnberg, E and Colazza, S (eds), Chemical Ecology of Insect Parasitoids. New Jersey, USA: Wiley-Blackwell, pp. 168190.CrossRefGoogle Scholar
Hopkins, RJ, van Dam, NM and van Loon, JJA (2009) Role of Glucosinolates in insect-plant relationships and multitrophic interactions. Annual Review of Entomology 54, 5783.CrossRefGoogle ScholarPubMed
Jaenike, J (1990) Host specialization in phytophagous insects. Annual Review of Ecology, Evolution and Systematics 21, 243273.CrossRefGoogle Scholar
Kessler, A and Baldwin, IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291, 21412144.CrossRefGoogle ScholarPubMed
Kessler, A and Baldwin, IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annual Review of Plant Biology 53, 299328.CrossRefGoogle ScholarPubMed
Kim, J, Tooker, JF, Luthe, DS, De Moraes, CM and Felton, GW (2012) Insect eggs can enhance wound response in plants: a study system of tomato Solanum lycopersicum L. and Helicoverpa zea Boddie. PLoS ONE 7, e37420.CrossRefGoogle ScholarPubMed
Koch, F and Smith, DR (2000) Nematus oligospilus Förster (Hymenoptera: Tenthredinidae), an introduced willow sawfly in the Southern Hemisphere. Proceedings of the Entomological Society of Washington 102, 292300.Google Scholar
Lehrman, A, Boddum, T, Stenberg, JA, Orians, CM and Bjorkman, C (2013) Constitutive and herbivore-induced systemic volatiles differentially attract an omnivorous biocontrol agent to contrasting Salix clones. AoB Plants 5, 8.CrossRefGoogle ScholarPubMed
Levins, R and MacArthur, RH (1969) An hypothesis to explain the incidence of monophagy. Ecology 50, 910911.CrossRefGoogle Scholar
McCormick, AC, Reinecke, A, Gershenzon, J and Unsicker, SB (2016) Feeding experience affects the behavioral response of polyphagous gypsy moth caterpillars to herbivore-induced poplar volatiles. Journal of Chemical Ecology 42, 382393.CrossRefGoogle ScholarPubMed
Niemela, P, Tuomi, J, Manila, R and Ojala, P (1984) The effect of previous damage on the quality of Scots pine foliage as food for diprionid sawflies. Journal of Applied Entomology 98, 3343.Google Scholar
Reich, PB, Walters, MB, Krause, SC, Van der Wal, D and Raffa, KF (1990) Effects of defoliation on growth carbon allocation, leaf chemistry and gas exchange rates of red pine. Bulletin of the Ecological Society of America 71, 297.Google Scholar
Rosenthal, JP and Dirzo, R (1997) Effects of life history, domestication and agronomic selection on plant defence against insects: evidence from maizes and wild relatives. Evolutionary Ecology 11, 337355.CrossRefGoogle Scholar
Saad, KA, Roff, MNM, Hallett, RH and Idris, AB (2015) Aphid-induced defences in chilli affect preferences of the whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae). Scientific Reports 5, 13697.CrossRefGoogle Scholar
Schoonhoven, LM, van Loon, JAA and Dicke, M (2005) Insect-Plant Biology, 2nd Edn. Oxford and New York: Oxford University Press.Google Scholar
Steppuhn, A and Baldwin, IT (2008) Induced defenses and the cost − benefit paradigm. In Schaller, A (ed.), Induced Plant Resistance to Herbivory. Berlin: Springer, pp. 6183.CrossRefGoogle Scholar
Thompson, JN (1988) Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomologia Experimentalis et Applicata 47, 314.CrossRefGoogle Scholar
Tortorelli, LA (2009) Tomo I: Maderas y Bosques Argentinos, Segunda Edición. Orientación gráfica Editora SRL, Argentina. pp. 1515.Google Scholar
Urban, AJ and Earldley, CD (1995) A recently introduced sawfly Nematus oligospilus Förster (Hymenoptera: Tenthredinidae), that defoliates willows in Southern Africa. African Entomology 3, 2327.Google Scholar
Valladares, G and Lawton, JH (1991) Host-plant selection in the holly leaf-miner: does mother know best? Journal of Animal Ecology 60, 227240.CrossRefGoogle Scholar
Wagner, M and Raffa, K (1993) Sawfly Life History Adaptations to Woody Plants. Massachusetts, USA: Academic Press Limites.Google Scholar
Wallner, WE (1987) Factors affecting insect population dynamics: difference between outbreak and non-outbreak species. Annual Review of Entomology 32, 317340.CrossRefGoogle Scholar
Walters, DR (2010) Plant Defense. Warding off Attack by Pathogens, Herbivores and Parasitic Plants. New Jersey, USA: Wiley.CrossRefGoogle Scholar
Zalucki, MP, Clarke, AR and Malcolm, SB (2002) Ecology and behavior of first instar larval Lepidoptera. Annual Review of Entomology 47, 361393.CrossRefGoogle ScholarPubMed