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Investigating preference-performance relationships in aboveground-belowground life cycles: a laboratory and field study with the vine weevil (Otiorhynchus sulcatus)

Published online by Cambridge University Press:  26 August 2011

K.E. Clark ,
S.E. Hartley ,
R.M. Brennan ,
K. MacKenzie  and
S.N. Johnson
K.E. Clark
Affiliation:
The James Hutton Institute (Dundee site), Invergowrie, Dundee, DD2 5DA, UK Department of Biology and Environmental Science, School of Life Sciences, University of Sussex, Falmer, Brighton, BN1 9QG, UK
S.E. Hartley
Affiliation:
Department of Biology and Environmental Science, School of Life Sciences, University of Sussex, Falmer, Brighton, BN1 9QG, UK
R.M. Brennan
Affiliation:
The James Hutton Institute (Dundee site), Invergowrie, Dundee, DD2 5DA, UK
K. MacKenzie
Affiliation:
Biomathematics and Statistics Scotland, Invergowrie, Dundee, DD2 5DA, UK
S.N. Johnson*
Affiliation:
The James Hutton Institute (Dundee site), Invergowrie, Dundee, DD2 5DA, UK Hawkesbury Institute for the Environment, University of Western Sydney, Locked Bag 1797, Penrith South, NSW 2751, Australia
*
*Author for correspondence Fax: +61 (0)2 4570 1103 E-mail: [email protected]
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Abstract

The preference-performance hypothesis has principally considered insect herbivores with aboveground lifecycles, although the hypothesis could be equally relevant to insects with life stages occurring both aboveground and belowground. Moreover, most studies have focussed on either laboratory or field experiments, with little attempt to relate the two. In this study, the preference-performance hypothesis was examined in an aboveground-belowground context in the laboratory using the vine weevil (Otiorhynchus sulcatus (F.)) (Coleoptera: Curculionidae) and two cultivars of red raspberry (Rubus idaeus), Glen Rosa and Glen Ample. A two-year field study (2008–2009) was also undertaken to characterise the population dynamics of adult weevils on the two raspberry cultivars. Larval performance (abundance and mass) differed significantly between Glen Rosa and Glen Ample, with Glen Rosa resulting in 26% larger but 56% fewer larvae compared to Glen Ample. Larval abundances were significantly and positively correlated with root nitrogen and magnesium concentrations, but negatively correlated with root iron. However, concentrations of these minerals were not significantly different in the two cultivars. Adult weevils did not preferentially select either of the two cultivars for egg laying (laying 3.08 and 2.80 eggs per day on Glen Ample and Glen Rosa, respectively), suggesting that there was no strong preference-performance relationship between adult vine weevils and their belowground offspring. Field populations of adult vine weevils were significantly higher on Glen Ample than Glen Rosa, which may reflect the higher larval survival on Glen Ample observed in laboratory experiments.

Keywords

host plant preferencesinsect performanceinsect–plant interactionsovipositionred raspberryRubus idaeus
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 102 , Issue 1 , February 2012 , pp. 63 - 70
Copyright
Copyright © Cambridge University Press 2011

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References

Alyokhin, A., Porter, G., Groden, E. & Drummond, F. (2005) Colorado potato beetle response to soil amendments: A case in support of the mineral balance hypothesis? Agriculture, Ecosystems & Environment 109, 234–244.CrossRefGoogle Scholar
Awmack, C.S. & Leather, S.R. (2002) Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology 47, 817–844.CrossRefGoogle ScholarPubMed
Baur, R., Koštál, V., Patrian, B. & Städler, E. (1996a) Preference for plants damaged by conspecific larvae in ovipositing cabbage root flies: influence of stimuli from leaf surface and roots. Entomologia Experimentalis et Applicata 81, 353–364.CrossRefGoogle Scholar
Baur, R., Koštál, V. & Städler, E. (1996b) Root damage by conspecific larvae induces preference for oviposition in cabbage root flies. Entomologia Experimentalis et Applicata 80, 224–227.CrossRefGoogle Scholar
Bernays, E.A. (2001) Neural limitations in phytophagous insects: Implications for diet breadth and evolution of host affiliation. Annual Review of Entomology 46, 703–727.CrossRefGoogle ScholarPubMed
Bernays, E.A. & Chapman, R.F. (1994) Host-Plant Selection by Phytophagous Insects. London, UK, Chapman & Hall.CrossRefGoogle Scholar
Clancy, K.M. & King, R.M. (1993) Defining the western spruce budworm's nutritional niche with response-surface methodology. Ecology 74, 442–454.CrossRefGoogle Scholar
Cowles, R.S. (2004) Susceptibility of strawberry cultivars to the vine weevil Otiorhynchus sulcatus (Coleoptera: Curculionidae). Agricultural and Forest Entomology 6, 279–284.CrossRefGoogle Scholar
Coyle, D.R., Clark, K.E., Raffa, K.F. & Johnson, S.N. (2011) Prior host feeding experience influences ovipositional but not feeding preference in a polyphagous insect herbivore. Entomologia Experimentalis et Applicata 138, 137–145.CrossRefGoogle Scholar
Craig, T.P., Itami, J.K. & Price, P.W. (1989) A strong relationship between oviposition preference and larval performance in a shoot-galling sawfly. Ecology 70, 1691–1699.CrossRefGoogle Scholar
Cram, W.T. & Daubeny, H.A. (1982) Responses of black vine weevil adults fed foliage from genotypes of strawberry, red raspberry, and red raspberry-blackberry hybrids. Hortscience 17, 771–773.CrossRefGoogle Scholar
Denno, R.F., Larsson, S. & Olmstead, K.L. (1990) Role of enemy-free space and plant quality in host-plant selection by willow beetles. Ecology 71, 124–137.CrossRefGoogle Scholar
Digweed, S.C. (2006) Oviposition preference and larval performance in the exotic birch-leafmining sawfly Profenusa thomsoni. Entomologia Experimentalis et Applicata 120, 41–49.CrossRefGoogle Scholar
Elser, J.J., Fagan, W.F., Denno, R.F., Dobberfuhl, D.R., Folarin, A., Huberty, A., Interlandi, S., Kilham, S.S., McCauley, E., Schulz, K.L., Siemann, E.H. & Sterner, R.W. (2000) Nutritional constraints in terrestrial and freshwater food webs. Nature 408, 578–580.CrossRefGoogle ScholarPubMed
Fisher, J.R. (2006) Fecundity, longevity and establishment of Otiorhynchus sulcatus (Fabricius) and Otiorhynchus ovatus (Linnaeus) (Coleoptera: Curculionidae) from the Pacific North-west of the United States of America on selected host plants. Agricultural and Forest Entomology 8, 281–287.CrossRefGoogle Scholar
Gripenberg, S., Morrien, E., Cudmore, A., Salminen, J.P. & Roslin, T. (2007) Resource selection by female moths in a heterogeneous environment: what is a poor girl to do? Journal of Animal Ecology 76, 854–865.CrossRefGoogle Scholar
Gripenberg, S., Mayhew, P.J., Parnell, M. & Roslin, T. (2010) A meta-analysis of preference-performance relationships in phytophagous insects. Ecology Letters 13, 383–393.CrossRefGoogle ScholarPubMed
Hanula, J.L. (1988) Oviposition preference and host recognition by the black vine weevil, Otiorhynchus sulcatus (Coleoptera, Curculionidae). Environmental Entomology 17, 694–698.CrossRefGoogle Scholar
HDC (Horticultural Development Council) (2003) Vine Weevil Control in Soft Fruit Crops. Kent, UK, Horticultural Development Council.Google Scholar
Heisswolf, A., Obermaier, E. & Poethke, H.J. (2005) Selection of large host plants for oviposition by a monophagous leaf beetle: nutritional quality or enemy-free space? Ecological Entomology 30, 299–306.CrossRefGoogle Scholar
Huberty, A.F. & Denno, R.F. (2006) Consequences of nitrogen and phosphorus limitation for the performance of two planthoppers with divergent life-history strategies. Oecologia 149, 444–455.CrossRefGoogle ScholarPubMed
Jaenike, J. (1978) On optimal oviposition behaviour in phytophagous insects. Theories in Population Biology 14, 350–356.CrossRefGoogle ScholarPubMed
Johnson, S.N. & Gregory, P.J. (2006) Chemically-mediated host-plant location and selection by root-feeding insects. Physiological Entomology 31, 1–13.CrossRefGoogle Scholar
Johnson, S.N., Birch, A.N.E., Gregory, P.J. & Murray, P.J. (2006) The ‘mother knows best’ principle: should soil insects be included in the preference-performance debate? Ecological Entomology 31, 395–401.CrossRefGoogle Scholar
Johnson, S.N., Hawes, C. & Karley, A.J. (2009) Reappraising the role of plant nutrients as mediators of interactions between root- and foliar-feeding insects. Functional Ecology 23, 699–706.CrossRefGoogle Scholar
Johnson, S.N., Hallett, P.D., Gillespie, T.L. & Halpin, C. (2010a) Belowground herbivory and root toughness: a potential model system using lignin-modified tobacco. Physiological Entomology 35, 186–191.CrossRefGoogle Scholar
Johnson, S.N., Petitjean, S., Clark, K.E. & Mitchell, C. (2010b) Protected raspberry production accelerates onset of oviposition by vine weevils (Otiorhynchus sulcatus). Agricultural and Forest Entomology 12, 277–283.CrossRefGoogle Scholar
Johnson, S.N., Barton, A.T., Clark, K.E., Gregory, P.J., McMenemy, L.S. & Hancock, R.D. (2011) Elevated atmospheric carbon dioxide impairs the performance of root-feeding vine weevils by modifying root growth and secondary metabolites. Global Change Biology 17, 688–695.CrossRefGoogle Scholar
Jones, T.H. & Finch, S. (1987) The effect of a chemical deterrent, released from the frass of caterpillars of the garden pebble moth, on cabbage root fly oviposition. Entomologia Experimentalis et Applicata 45, 283–288.CrossRefGoogle Scholar
La Lone, R.S. & Clarke, R.G. (1981) Larval development of Otiorhynchus sulcatus (Coleoptera, Curculionidae) and effects of larval density on larval mortality and injury to Rhododendron. Environmental Entomology 10, 190–191.CrossRefGoogle Scholar
Levins, R. & Macarthur, R. (1969) An hypothesis to explain the incidence of monophagy. Ecology 50, 910–911.CrossRefGoogle Scholar
Maier, C.T. (1981) Reproductive success of the black vine weevil, Otiorhynchus sulcatus (F.), (Coleoptera, Curculionidae) fed different foliar diets and evaluation of techniques for predicting fecundity. Environmental Entomology 10, 928–932.CrossRefGoogle Scholar
Mattson, W.J. (1980) Herbivory in relation to plant nitrogen content. Annual Review of Ecology and Systematics 11, 119–161.CrossRefGoogle Scholar
Mayhew, P.J. (2001) Herbivore host choice and optimal bad motherhood. Trends in Ecology and Evolution 16, 165–167.CrossRefGoogle ScholarPubMed
McKinnon, M.L., Quiring, D.T. & Bauce, E. (1999) Influence of tree growth rate, shoot size and foliar chemistry on the abundance and performance of a galling adelgid. Functional Ecology 13, 859–867.CrossRefGoogle Scholar
McMenemy, L.S., Mitchell, C. & Johnson, S.N. (2009) Biology of the European large raspberry aphid (Amphorophora idaei): its role in virus transmission and resistance breakdown in red raspberry. Agricultural and Forest Entomology 11, 61–71.CrossRefGoogle Scholar
Moorhouse, E.R., Charnley, A.K. & Gillespie, A.T. (1992) A review of the biology and control of the vine weevil, Otiorhynchus sulcatus (Coleoptera, Curculionidae). Annals of Applied Biology 121, 431–454.CrossRefGoogle Scholar
Nielsen, D.G. & Dunlap, M.J. (1981) Black vine weevil (Coleoptera, Curculionidae) – reproductive potential on selected plants. Annals of the Entomological Society of America 74, 60–65.CrossRefGoogle Scholar
Payne, R.W., Murray, D.A., Harding, S.A., Baird, D.B. & Soutar, D.M. (2007) Genstat for Windows (11th edn) introduction. Hemel Hempstead, UK, VSN International.Google Scholar
Penman, D.R. & Scott, R.R. (1976) Impact of black vine weevil, Otiorhynchus sulcatus (F.), on blackcurrants and strawberries in Canterbury. New Zealand Journal of Experimental Agriculture 4, 381–384.CrossRefGoogle Scholar
Price, P.W. (1991) The plant vigor hypothesis and herbivore attack. Oikos 62, 244–251.CrossRefGoogle Scholar
Rath, L.K. (2004) Influence of certain micronutrients on the growth and development of white backed planthopper, Sogatella furcifera (Horváth) infesting rice. Journal of Plant Protection and Environment 1, 19–23.Google Scholar
Rausher, M.D. (1979) Larval habitat suitability and oviposition preference in three related butterflies. Ecology 60, 503–511.CrossRefGoogle Scholar
Scheirs, J. & De Bruyn, L. (2002) Integrating optimal foraging and optimal oviposition theory in plant-insect research. Oikos 96, 187–191.CrossRefGoogle Scholar
Scheirs, J., De Bruyn, L. & Verhagen, R. (2000) Optimization of adult performance determines host choice in a grass miner. Proceedings of the Royal Society of London, Series B: Biological Sciences 267, 2065–2069.CrossRefGoogle Scholar
Scheirs, J., Zoebisch, T.G., Schuster, D.J. & De Bruyn, L. (2004) Optimal foraging shapes host preference of a polyphagous leafminer. Ecological Entomology 29, 375–379.CrossRefGoogle Scholar
Schread, J.C. (1972) The Black Vine Weevil. Connecticut Agricultural Experiment Station Circular 211, State of Connecticut, USA.Google Scholar
Scutareanu, P. & Loxdale, H.D. (2006) Ratio of nutrient and minerals to defensive compounds indicative of plant quality and tolerance to herbivory in pear trees. Journal of Plant Nutrition 29, 629–642.CrossRefGoogle Scholar
Shanks, C.H. (1980) Strawberry and yew as hosts of adult black vine weevil (Coleoptera, Curculionidae) and effects on oviposition and development of progeny. Environmental Entomology 9, 530–532.CrossRefGoogle Scholar
Smith, F.F. (1932) Biology and Control of the Black Vine Weevil. Washington, DC, USA, United States Department of Agriculture.Google Scholar
Staley, J.T., Stewart-Jones, A., Poppy, G.M., Leather, S.R. & Wright, D.J. (2009) Fertilizer affects the behaviour and performance of Plutella xylostella on brassicas. Agricultural and Forest Entomology 11, 275–282.CrossRefGoogle Scholar
Stamp, N.E. (1994) Interactive effects of rutin and constant versus alternating temperatures on performance of Manduca sexta caterpillars. Entomologia Experimentalis et Applicata 72, 125–133.CrossRefGoogle Scholar
Stearns, S.C. (1992) The Evolution of Life Histories. Oxford, UK, Oxford University Press.Google Scholar
Thangavelu, K. & Bania, H.R. (1990) Preliminary investigation on the effects of minerals in the rain water on the growth and reproduction of silkworm Bombyx mori L. Indian Journal of Sericulture 29, 37–43.Google Scholar
Thompson, J.N. (1988a) Co-evolution and alternative hypotheses in insect-plant interactions. Ecology 69, 893–895.CrossRefGoogle Scholar
Thompson, J.N. (1988b) Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomologia Experimentalis et Applicata 47, 3–14.CrossRefGoogle Scholar
Van Tol, R.W.H.M., Van Dijk, N. & Sabelis, M.W. (2004) Host plant preference and performance of the vine weevil Otiorhynchus sulcatus. Agricultural and Forest Entomology 6, 267–278.CrossRefGoogle Scholar
Warner, R.E. & Negley, F.B. (1976) Genus Otiorhynchus in America North of Mexico (Coleoptera, Curculionidae). Proceedings of the Entomological Society of Washington 78, 240–262.Google Scholar
White, T.C.R. (1993) The Inadequate Environment: Nitrogen and the Abundance of Animals. Heidelburg, Germany, Springer-Verlag.CrossRefGoogle Scholar