Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Oviposition of a leaf-miner on Erythroxylum tortuosum (Erythroxylaceae) leaves: hierarchical variation of physical leaf traits

P. R. De Sibio A and M. N. Rossi B C
+ Author Affiliations
- Author Affiliations

A Department of Botany, IB, São Paulo State University (Unesp), Botucatu, São Paulo, Brazil.

B Department of Biological Sciences, Federal University of São Paulo (Unifesp), Diadema, São Paulo, Brazil.

C Corresponding author. Email: rossi.unifesp@gmail.com

Australian Journal of Botany 60(2) 136-142 https://doi.org/10.1071/BT11268
Submitted: 23 October 2011  Accepted: 2 February 2012   Published: 16 March 2012

Abstract

Plants do not offer homogeneous supplies of the resources required by herbivorous insects as many resource traits show considerable variation both within and between plants. The distribution of variation among host-plant attributes determines the optimal spatial resolution level for insect females to select the best resource patches for oviposition. In this study, we examine whether variation in fluctuating asymmetry and size of Erythroxylum tortuosum Mart. (Erythroxylaceae) leaves influence oviposition of the specialist leaf-miner Agnippe Chambers (Lepidoptera: Gelechiidae). By partitioning the variance across five hierarchical levels, the oviposition pattern was investigated at the spatial resolution level where these leaf traits varied the most. We confirm that the largest variation in both these leaf attributes occurs at the leaf level. We hypothesise that leaf-miner females will respond to this variation by selecting the best leaves (resources) on which to lay their eggs. We find that the probability of oviposition is not significantly related to fluctuating asymmetry or to leaf size (oviposition preference test), suggesting that these two physical traits are not relevant to leaf-miners as indicators of resource patch quality. Therefore, although we show that females laid significantly more eggs on larger leaves, this behaviour appears not to be a result of active selection of leaves. Our results suggest that Agnippe females probably adjust their oviposition proportionally to leaf area because the relationship between egg density and leaf area was not statistically significant.

Additional keywords: Agnippe, Cerrado, fluctuating asymmetry, insect–plant interaction, leaf size.


References

Amaral A, Jr (1973) O gênero Erythroxylum no município de Botucatu, São Paulo. Doctorate Thesis, School of Medical and Biological Science of Botucatu, São Paulo, Brazil.

Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology 47, 817–844.
Host plant quality and fecundity in herbivorous insects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvVWlug%3D%3D&md5=9657e0edfb62e2781b3beae5d73395e4CAS |

Ayres M, Ayres M, Jr, Ayres DL, Dos Santos AS (2007) ‘BioStat: aplicações estatísticas nas áreas das ciências biológicas e médicas.’ (Instituto de Desenvolvimento Sustentável Mamirauá, IDSM/MCT/CNPq: Belém, PA)

Briese DT (1996) Oviposition choice by the Onopordum capitulum weevil Larinus latus (Coleoptera: Curculionidae) and its effect on the survival of immature stages. Oecologia 105, 464–474.
Oviposition choice by the Onopordum capitulum weevil Larinus latus (Coleoptera: Curculionidae) and its effect on the survival of immature stages.Crossref | GoogleScholarGoogle Scholar |

Cornelissen T, Stiling P (2005) Perfect is best: low leaf fluctuating asymmetry reduces herbivory by leaf miners. Oecologia 142, 46–56.
Perfect is best: low leaf fluctuating asymmetry reduces herbivory by leaf miners.Crossref | GoogleScholarGoogle Scholar |

Cornelissen T, Stiling P, Drake B (2004) Elevated CO2 decreases leaf fluctuating asymmetry and herbivory by leaf miners on two oak species. Global Change Biology 10, 27–36.
Elevated CO2 decreases leaf fluctuating asymmetry and herbivory by leaf miners on two oak species.Crossref | GoogleScholarGoogle Scholar |

Cornelissen T, Fernandes GW, Vasconcellos-Neto J (2008) Size does matter: variations in herbivory between and within plants and the plant vigor hypothesis. Oikos 117, 1121–1130.
Size does matter: variations in herbivory between and within plants and the plant vigor hypothesis.Crossref | GoogleScholarGoogle Scholar |

Craig TP, Ohgushi T (2002) Preference and performance are correlated in the spittlebug Aphrophora pectoralis on four species of willow. Ecological Entomology 27, 529–540.
Preference and performance are correlated in the spittlebug Aphrophora pectoralis on four species of willow.Crossref | GoogleScholarGoogle Scholar |

Crawley MJ (2007) ‘The R book.’ (John Wiley & Sons: Chichester, UK)

De Sibio PR (2008) Aspectos ecológicos de um minador foliar em Erythroxylum tortuosum Mart. (Erythroxylaceae): qualidade da planta, anatomia das minas e variação hierárquica de traços vegetais. MSc Thesis, Bioscience Institute, Department of Botany, Botucatu, São Paulo, Brazil.

Faeth SH (1991) Effect of oak leaf size on abundance, dispersion, and survival of the leafminer Cameraria sp. (Lepidoptera, Gracillariidae). Environmental Entomology 20, 196–204.

Felfili JM, Silva-Júnior MC (2001) ‘Biogeografia do bioma Cerrado: estudo fitofisionômico da Chapada do Espigão Mestre do São Francisco.’ (Department of Forest Engineering, School of Technology, University of Brasília: Brazil)

Fortin M, Mauffette Y (2002) The suitability of leaves from different canopy layers for a generalist herbivore (Lepidoptera: Lasiocampidae) foraging on sugar maple. Canadian Journal of Forest Research 32, 379–389.
The suitability of leaves from different canopy layers for a generalist herbivore (Lepidoptera: Lasiocampidae) foraging on sugar maple.Crossref | GoogleScholarGoogle Scholar |

Freeman DC, Brown ML, Duda J, Graham JH, Emlen JM, Krzysik AJ, Balbach H, Kovacic DA, Zak JC (2004) Developmental instability in Rhus Copallinum L.: multiple stressors, years, and responses. International Journal of Plant Sciences 165, 53–63.
Developmental instability in Rhus Copallinum L.: multiple stressors, years, and responses.Crossref | GoogleScholarGoogle Scholar |

Fritz RS, Nobel J (1989) Plant resistance, plant traits, and host plant choice of the leaf-folding sawfly on the arroyo willow. Ecological Entomology 14, 393–401.
Plant resistance, plant traits, and host plant choice of the leaf-folding sawfly on the arroyo willow.Crossref | GoogleScholarGoogle Scholar |

Gotelli NJ, Ellison AM (2004) ‘A primer of ecological statistics.’ (Sinauer Associates: Sunderland, MA)

Graham JH, Emlen JM, Freeman DC, Leamy LJ, Kieser JA (1998) Directional asymmetry and the measurement of developmental instability. Biological Journal of the Linnean Society. Linnean Society of London 64, 1–16.
Directional asymmetry and the measurement of developmental instability.Crossref | GoogleScholarGoogle Scholar |

Graham MH (2003) Confronting multicollinearity in ecological multiple regression. Ecology 84, 2809–2815.
Confronting multicollinearity in ecological multiple regression.Crossref | GoogleScholarGoogle Scholar |

Gratton C, Welter SC (1998) Oviposition preference and larval performance of Liriomyza helianthi (Diptera: Agromyzidae) on normal and novel host plants. Environmental Entomology 27, 926–935.

Gripenberg S, Roslin T (2007) Up or down in space? Uniting the bottom-up versus top-down paradigm and spatial ecology. Oikos 116, 181–188.
Up or down in space? Uniting the bottom-up versus top-down paradigm and spatial ecology.Crossref | GoogleScholarGoogle Scholar |

Gripenberg S, Salminen JP, Roslin T (2007a) A tree in the eyes of a moth – temporal variation in oak leaf quality and leaf-miner performance. Oikos 116, 592–600.

Gripenberg S, Morriën E, Cudmore A, Salminen JP, Roslin T (2007b) Resource selection by female moths in a heterogeneous environment: what is a poor girl to do? Journal of Animal Ecology 76, 854–865.
Resource selection by female moths in a heterogeneous environment: what is a poor girl to do?Crossref | GoogleScholarGoogle Scholar |

Hódar JA (2002) Leaf fluctuating asymmetry of Holm oak in response to drought under contrasting climatic conditions. Journal of Arid Environments 52, 233–243.
Leaf fluctuating asymmetry of Holm oak in response to drought under contrasting climatic conditions.Crossref | GoogleScholarGoogle Scholar |

Ishino MN (2007) Efeito da assimetria flutuante nos padrões de herbivoria de um minador foliar em Erythroxylum tortuosum Mart. (Erythroxylaceae). MSc Thesis, Bioscience Institute, Department of Botany, Botucatu, São Paulo, Brazil.

Ishino MN, De Sibio PR, Rossi MN (2011) Leaf trait variation on Erythroxylum tortuosum (Erythroxylaceae) and its relationship with oviposition preference and stress by a host-specific leaf-miner. Austral Ecology 36, 203–211.
Leaf trait variation on Erythroxylum tortuosum (Erythroxylaceae) and its relationship with oviposition preference and stress by a host-specific leaf-miner.Crossref | GoogleScholarGoogle Scholar |

Leather SR (1994) Life history traits of insect herbivores in relation to host quality. In ‘Insect plant interactions’. (Ed. EA Bernays) pp. 175–207. (CRC Press: Boca Raton)

Leather SR, Awmack CS (2002) Does variation in offspring size reflect strength of preference performance index in herbivorous insects? Oikos 96, 192–195.
Does variation in offspring size reflect strength of preference performance index in herbivorous insects?Crossref | GoogleScholarGoogle Scholar |

Lempa K, Martel J, Koricheva J, Haukioja E, Ossipov V, Ossipova S, Pihlaja K (2000) Covariation of fluctuating asymmetry, herbivory and chemistry during birch leaf expansion. Oecologia 122, 354–360.
Covariation of fluctuating asymmetry, herbivory and chemistry during birch leaf expansion.Crossref | GoogleScholarGoogle Scholar |

Mayhew PJ (1997) Adaptive patterns of host-plant selection by phytophagous insects. Oikos 79, 417–428.
Adaptive patterns of host-plant selection by phytophagous insects.Crossref | GoogleScholarGoogle Scholar |

Møller AP (1995) Leaf-mining insects and fluctuating asymmetry in Ulmus glabra leaves. Journal of Animal Ecology 64, 697–707.
Leaf-mining insects and fluctuating asymmetry in Ulmus glabra leaves.Crossref | GoogleScholarGoogle Scholar |

Mopper S (1996) Adaptive genetic structure in phytophagous insect populations. Trends in Ecology & Evolution 11, 235–238.
Adaptive genetic structure in phytophagous insect populations.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFCnug%3D%3D&md5=a16bd310e3f5c7889025a587ae3ceedbCAS |

Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403, 853–858.
Biodiversity hotspots for conservation priorities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhs1Olsr4%3D&md5=840bd8071649149017b866db1ca1ddb1CAS |

Orians CM, Jones CG (2001) Plants as resource mosaics: a functional model for predicting patterns of within-plant resource heterogeneity to consumers based on vascular architecture and local environmental variability. Oikos 94, 493–504.
Plants as resource mosaics: a functional model for predicting patterns of within-plant resource heterogeneity to consumers based on vascular architecture and local environmental variability.Crossref | GoogleScholarGoogle Scholar |

Palmer AR, Strobeck C (1986) Fluctuating asymmetry: measurement, analysis, patterns. Annual Review of Ecology and Systematics 17, 391–421.
Fluctuating asymmetry: measurement, analysis, patterns.Crossref | GoogleScholarGoogle Scholar |

Palmer AR, Strobeck C (2003) Fluctuating asymmetry analysis revisited. In ‘Developmental instability: causes and consequences’. (Ed. M Polak) pp. 279–319. (Oxford University Press: New York)

Pérez-Contreras T, Soler JJ, Soler M (2008) Needle asymmetry, pine vigour and pine selection by the processionary moth Thaumetopoea pityocampa. Acta Oecologica 33, 213–221.
Needle asymmetry, pine vigour and pine selection by the processionary moth Thaumetopoea pityocampa.Crossref | GoogleScholarGoogle Scholar |

Price PW (1991) The plant vigor hypothesis and herbivore attack. Oikos 62, 244–251.
The plant vigor hypothesis and herbivore attack.Crossref | GoogleScholarGoogle Scholar |

Puerta-Piñero C, Gómez JM, Hódar JA (2008) Shade and herbivory induce fluctuating asymmetry in a Mediterranean oak. International Journal of Plant Sciences 169, 631–635.
Shade and herbivory induce fluctuating asymmetry in a Mediterranean oak.Crossref | GoogleScholarGoogle Scholar |

R Development Core Team (2009) ‘R: a language and environment for statistical computing. Version 2.10.1.’ (R Foundation for Statistical Computing: Vienna)

Renwick JAA, Chew FS (1994) Oviposition behavior in Lepidoptera. Annual Review of Entomology 39, 377–400.
Oviposition behavior in Lepidoptera.Crossref | GoogleScholarGoogle Scholar |

Ribeiro JELS, Hopkins MJG, Vicentini A, Sothers CA, Costa MAS, Brito JM, Souza MAD, Martins LHP, Lohmann LG, Assunção PACL, Pereira EC, Silva CF, Mesquita MR, Procópio LC (1999) ‘Flora da Reserva Ducke: guia de identificação das plantas vasculares de uma floresta de terra-firme na Amazônia Central.’ (INPA: Manaus)

Riipi M, Haukioja E, Lempa K, Ossipov V, Ossipova S, Pihlaja K (2004) Ranking of individual mountain birch trees in terms of leaf chemistry: seasonal and annual variation. Chemoecology 14, 31–43.
Ranking of individual mountain birch trees in terms of leaf chemistry: seasonal and annual variation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhvFajt7g%3D&md5=6b6344fb614c4ec1bf9bc557b563255aCAS |

Roslin T, Gripenberg S, Salminen JP, Karonen M, O’hara RB, Pihlaja K, Pulkkinen P (2006) Seeing the trees for the leaves – oaks as mosaics for a host-specific moth. Oikos 113, 106–120.
Seeing the trees for the leaves – oaks as mosaics for a host-specific moth.Crossref | GoogleScholarGoogle Scholar |

Ruusila V, Morin JP, van Ooik T, Saloniemi I, Ossipov V, Haukioja E (2005) A short-lived herbivore on a long-lived host: tree resistance to herbivory depends on leaf age. Oikos 108, 99–104.
A short-lived herbivore on a long-lived host: tree resistance to herbivory depends on leaf age.Crossref | GoogleScholarGoogle Scholar |

Schoonhoven LM, Van Loon JJA, Dicke M (2005) ‘Insect-plant biology.’ (Oxford University Press: New York)

Seligmann P, Mittermeier RA, Da Fonseca GAB, Gascon C, Crone N, Da Silva JMC, Famolare L, Bensted-Smith R, Rajaobelina L, Beehler B (2007) ‘Centers for biodiversity conservation: bringing together science, partnerships, and human well-being to scale up conservation outcomes.’ (Conservation International: Arlington, VA)

Singer MC, Wee B (2005) Spatial pattern in checkerspot butterfly-host plant association at local, metapopulation and regional scales. Annales Zoologici Fennici 42, 347–361.

Stiling P, Rossi AM (1997) Experimental manipulations of top-down and bottom-up factors in a tri-trophic system. Ecology 78, 1602–1606.
Experimental manipulations of top-down and bottom-up factors in a tri-trophic system.Crossref | GoogleScholarGoogle Scholar |

Suomela J, Nilson A (1994) Within-tree and among tree variation in growth of Epirrita autumnata on mountain birch leaves. Ecological Entomology 19, 45–56.
Within-tree and among tree variation in growth of Epirrita autumnata on mountain birch leaves.Crossref | GoogleScholarGoogle Scholar |

Suomela J, Kaitaniemi P, Nilson A (1995) Systematic within-tree variation in mountain birch leaf quality for a geometrid, Epirrita autumnata. Ecological Entomology 20, 283–292.
Systematic within-tree variation in mountain birch leaf quality for a geometrid, Epirrita autumnata.Crossref | GoogleScholarGoogle Scholar |

Teder T, Tammaru T (2002) Cascading effects of variation in plant vigour on the relative performance of insect herbivores and their parasitoids. Ecological Entomology 27, 94–104.
Cascading effects of variation in plant vigour on the relative performance of insect herbivores and their parasitoids.Crossref | GoogleScholarGoogle Scholar |

Thompson JN, Pellmyr O (1991) Evolution of oviposition behavior and host preference in Lepidoptera. Annual Review of Entomology 36, 65–89.
Evolution of oviposition behavior and host preference in Lepidoptera.Crossref | GoogleScholarGoogle Scholar |

Walker M, Hartley SE, Jones H (2008) The relative importance of resources and natural enemies in determining herbivore abundance: thistles, tephritids and parasitoids. Journal of Animal Ecology 77, 1063–1071.
The relative importance of resources and natural enemies in determining herbivore abundance: thistles, tephritids and parasitoids.Crossref | GoogleScholarGoogle Scholar |

Wanderley MGL, Shepherd GJ, Giulietti AM (2002) ‘Flora fanerogâmica do Estado de São Paulo. Vol. 2.’ (Hucitec/Fapesp: São Paulo)

Waring CL, Cobb NS (1992) The impact of plant stress on herbivore population dynamics. In ‘Insect-plant interactions’. (Ed. EA Bernays) pp. 168–215. (CRC Press: Boca Raton)

Whitham TG (1978) Habitat selection by Pemphigus aphids in response to resource limitation and competition. Ecology 59, 1164–1176.
Habitat selection by Pemphigus aphids in response to resource limitation and competition.Crossref | GoogleScholarGoogle Scholar |

Wiggins DA (1997) Fluctuating asymmetry in Colophospermum mopane leaves and oviposition preference in an African silk moth Imbrasia belina. Oikos 79, 484–488.
Fluctuating asymmetry in Colophospermum mopane leaves and oviposition preference in an African silk moth Imbrasia belina.Crossref | GoogleScholarGoogle Scholar |

Zar JH (1999) ‘Biostatistical analysis.’ (Prentice Hall: New Jersey)

Zvereva E, Kozlov M, Haukioja E (1997) Stress responses of Salix borealis to pollution and defoliation. Journal of Applied Ecology 34, 1387–1396.
Stress responses of Salix borealis to pollution and defoliation.Crossref | GoogleScholarGoogle Scholar |