A quantitative review of the relationship between insect galls and host plant chemical defence
Journal; Arthropod-Plant Interactions
Casey R. Hall*, Anthony R. Carroll and Roger L. Kitching
*Corresponding author: ; School of Biological Sciences, University of Adelaide
Online Resource 1: Transformations used to calculate effect sizes for different statistics provided in the sampled studies:
Group means to Cohen’s d:
where X1 and X2= group means
andSDwithin= the estimated common standard deviation of the two groups:
where n1 and n2= the sample sizes for groups X1 and X2 respectively and
SD1 and SD2= standard deviations for groups X1 and X2 respectively.
Student’s t and Fisher’s F to Cohen’s d:
r to Cohen’s d:
The variance of d (converted from r) is:
Cohen’s d to Hedge’s g:
Hedge’s g to Hedge’s d:
Online Resource 2: List of literature selected to include in the meta-analysis:
Abrahamson WG, McCrea KD, Whitwell AJ, Vernieri LA (1991) The role of phenolics in goldenrod ball gall resistance and formation. Biochem Syst Ecol19:615–622
Allison SD, Schultz JC (2005) Biochemical responses of chestnut oak to a galling cynipid. J Chem Ecol31:151–166
Bailey JK, Wooley SC, Lindroth RL, Whitham TG (2006) Importance of species interactions to community heritability: a genetic basis to trophic-level interactions. Ecol Lett9:78–85
Cornelissen T, Fernandes GW, Coelho MS (2011) Induced responses in the neotropical shrub Bauhinia brevipes Vogel: does early season herbivory function as cue to plant resistance? Arthropod Plant Interact5:245–253
Cornelissen TG, Fernandes GW (2001) Defence, growth and nutrient allocation in the tropical shrub Bauhinia brevipes (Leguminosae). Austral Ecol26:246–253
Coruh S, Ercisli S (2010) Interactions between galling insects and plant total phenolic contents in Rosa canina L . genotypes. Sci Res Essays5:1935–1937
Damasceno FC, Nicolli KP, Caramão EB, Soares GL, Zini CA (2010) Changes in the volatile organic profile of Schinus polygamus (Anacardiaceae) and Baccharis spicata (Asteraceae) induced by galling psyllids. J Brazillian Chem Soc21:556–563
Detoni ML, Vasconcelos EG, Rust NM, IsaiasRS, Soares GG (2011) Seasonal variation of phenolic content in galled and non-galled tissues of Calliandra brevipes Benth (Fabaceae: Mimosoidae). Acta Bot Brasilica25:601–604
Formiga AT, Gonçalves SJ de MR, Soares GG, Isaias RS (2009) Relações entre o teor de fenóis totais e o ciclo das galhas de Cecidomyiidae em Aspidosperma spruceanum Müll. Arg. (Apocynaceae). Acta Bot Brasilica23:93–99
Foss LK, Rieske LK (2004) Stem galls affect oak foliage with potential consequences for herbivory. Ecol Entomol29:273–280
Frost CJ, Dean JM, Smyers EC, Mescher MC, Carlson JE, De Moraes CM, Tooker JF (2012) A petiole-galling insect herbivore decelerates leaf lamina litter decomposition rates. Funct Ecol26:628–636
Furlan CM, Salatino A, Domingos M (2004) Influence of air pollution on leaf chemistry, herbivore feeding and gall frequency on Tibouchinapulchra leaves in Cubatao (Brazil). BiochemSystEcol 32:253–263.
Gonçalves-Alvim SJ, Collevatti RG, Fernandes GW (2004) Effects of genetic variability and habitat of Qualea parviflora (Vochysiaceae) on herbivory by free-feeding and gall-forming insects. Ann Bot94:259–68
Gopichandran R, Peter AJ, Subramaniam VR (1992) Age-correlated biochemical profiles of thrips galls in relation to population density of thrips. J Nat Hist 26:609–619
Guimarães AA, Bizarri CB, Barbosa LS, Nakamura MJ, Ramos MS, Vieira AM (2013) Characterization of the effects of leaf galls ofClusiamyianitida(Cecidomyiidae) onClusialanceolataCambess. (Clusiaceae): anatomical aspects and chemical analysis of essential oil. Flora 208:165–173
Hjältén J, Niemi L, Wennström A, Ericson L, Roininen H, Julkunen-Tiitto R. (2007) Variable responses of natural enemies to Salix triandra phenotypes with different secondary chemistry. Oikos116:751–758
Kolehmainen J, Roininen H, Julkunen-Tiitto R, Tahvanainen J (1994) Importance of phenolic glucosides in host selection of shoot galling sawfly, Euura amerinae, on Salix pentandra. J Chem Ecol20:2455–2466
McKinnon ML, Quiring DT, Bauce E (1999) Influence of tree growth rate, shoot size and foliar chemistry on the abundance and performance of a galling adelgid. Funct Ecol13:859–867
Motta LB, Kraus JE, Salatino A, Salatino MF (2005) Distribution of metabolites in galled and non-galled foliar tissues of Tibouchina pulchra. Biochem Syst Ecol33:971–981
Nyman T, Julkunen-Tiitto R (2000) Manipulation of the phenolic chemistry of willows by gall-inducing sawflies. Proc Natl Acad Sci USA97:13184–13187
Pascual-Alvarado E, Cuevas-Reyes P, Quesada M, Oyama K (2008) Interactions between galling insects and leaf-feeding insects: the role of plant phenolic compounds and their possible interference with herbivores. J Trop Ecol24:329–336
Rehill BJ, Schultz JC (2012) Hormaphis hamamelidis fundatrices benefit by manipulating phenolic metabolism of their host. J Chem Ecol38:496–498
Rostás M, Maag D, Ikegami M, Inbar M. (2013) Gall volatiles defend aphids against a browsing mammal. BMC Evol Biol13:193
Soetens P, Rowell-Rahier M, Pasteels J (1991) Influence of phenolglucosides and trichome density on the distribution of insect herbivores on willows. Entomol Exp Appl59:175–187
Sugiura S, Yamazaki K, Osono T (2006) Consequences of gall tissues as a food resource for a tortricid moth attacking cecidomyiid galls. Can Entomol138:390–398
Taper M, Case T (1987) Interactions between oak tannins and parasite community structure: unexpected benefits of tannins to cynipid gall-wasps. Oecologia71:254–261
Tooker JF, DeMoraes CM (2007) Feeding by Hessian fly [Mayetiola destructor (Say)] larvae does not induce plant indirect defences. Ecol Entomol 32:153-161
Tooker JF, Rohr JR, Abrahamson WG, De Moraes CM (2008) Gall insects can avoid and alter indirect plant defences. New Phytol 178:657–671
Torres-Gurrola G, Delgado-Lamas G, Espinosa-Garcia F (2011) The foliar chemical profile of criollo avocado, Perseaamericanavar. drymifolia(Lauraceae), and its relationship with the incidence of a gall-forming insect, Trioza anceps (Triozidae). Biochem System Ecol 39:102–111
Valladares GR, Zapata A, Zygaldo J, Banchio E (2002) Phytochemical induction by herbivores could affect quality of essential oils from aromatic plants. J Agric Food Chem50:4059–4061
Zucker WV (1982) How aphids choose leaves: the roles of phenolics in host selection by a galling aphid. Ecology63:972–981
Online Resource 3: Raw data extracted for each data point and results from the meta-analysis.
Table S3 References, categories and effect sizes extracted from articles analysing effects of insect galling on host plant defence chemistry. d is the effect size (adjusted) and SV is sample variance calculated from the meta-analysis.
Study / Chemical class / N / d / SV / Gall species / Host plant species / Main chemical constituents / Habitat / Data sourceAbrahamson et al. 1991 / Phenolics / 20 / 1.8 / 0.3 / Eurostasolidaginis / Solidago altissima / terpenes and flavonoids / Temperate forest / from fig 5, clone B
Allison & Schultz 2005 / Phenolics / 28 / 0.8 / 0.2 / Andricuspetiolicolus / Quercusprinus / flavonoids and tannins / Temperate forest / from fig 3
Allison & Schultz 2005 / Tannins / 28 / 1.7 / 0.2 / Andricuspetiolicolus / Quercusprinus / flavonoids and tannins / Temperate forest / from fig 3
Bailey et al. 2006 / Phenolics / 11 / -0.2 / 0.4 / Pemphigus betae / Populusangustifolia / flavonoids / Temperate forest / table 1
Bailey et al. 2006 / Tannins / 11 / 0.8 / 0.4 / Pemphigus betae / Populusangustifolia / flavonoids / Temperate forest / table 1
Cornelissen & Fernandes 2001 / Tannins / 170 / 0.2 / 0.0 / Contarinia sp. / Bauhinia brevipes / flavonoids and isoflavonoids / Mediterranean and savanna / in text
Cornelissen et al. 2011 / Tannins / 50 / 0.2 / 0.1 / Contarinia sp. / Bauhinia brevipes / flavonoids and isoflavonoids / Mediterranean and savanna / in text
CoruhErcisli 2010 / Phenolics / 20 / -0.6 / 0.2 / Diplolepis sp. / Rosa canina / flavonoids and tannins / Mediterranean and savanna / Average from table 1
Damascenoet al. 2010 / Volatiles / 10 / 1.8 / 0.6 / Psyllidae sp. / Baccharisspicata / terpenes and flavonoids / Mediterranean and savanna / text and fig 5
Damascenoet al. 2010 / Volatiles / 10 / -2.5 / 0.7 / Psyllidae sp. / Baccharisspicata / terpenes and flavonoids / Mediterranean and savanna / text and fig 6
Damascenoet al. 2010 / Volatiles / 10 / 4.0 / 1.2 / Psyllidae sp. / Schinuspolygamus / alkyl resorcinols / Mediterranean and savanna / text and fig 5
Damascenoet al. 2010 / Volatiles / 10 / -0.6 / 0.4 / Psyllidae sp. / Schinuspolygamus / alkyl resorcinols / Mediterranean and savanna / text and fig 4
Detoniet al. 2011 / Phenolics / 60 / 7.6 / 0.5 / Tanaostigmodes sp. / Calliandrabrevipes / flavonoids and isoflavonoids / Mediterranean and savanna / fig 1, Aug 03
Formigaet al. 2009 / Phenolics / 60 / 3.2 / 0.2 / Cecidomyiidae sp. / Aspidospermaspruceanum / alkaloids, terpenes / Tropical forest / table 2, first entry
Foss & Rieske 2004 / Tannins / 60 / -0.2 / 0.1 / Callirhytiscornigera / Quercuspalustris / flavonoids and isoflavonoids / Temperate forest / table 3, 6 may, gg and u/g
Frost et al. 2012 / Tannins / 30 / -1.4 / 0.2 / Ectoedemiapopulella / Populustremuloides / flavonoids / Temperate forest / fig 2a, P. tremuloides
Frost et al. 2012 / Tannins / 30 / -0.4 / 0.1 / Ectoedemiapopulella / Populusgranidentata / flavonoids / Temperate forest / P. grandidentata
Furlanet al. 2004 / Phenolics / 6 / 0.8 / 0.7 / Lepidoptera / Tibouchinapulchra / tannins / Tropical forest / correlation from table 2
Furlanet al. 2004 / Tannins / 6 / 0.4 / 0.7 / Lepidoptera / Tibouchinapulchra / tannins / Tropical forest / correlation from table 3
Goncalves-Alvimet al. 2004 / Phenolics / 30 / 0.2 / 0.1 / Unknown / Qualeaparviflora / triterpenes, simple phenols / Mediterranean and savanna / tables 3 and 5
Goncalves-Alvimet al. 2004 / Tannins / 30 / 0.7 / 0.1 / Unknown / Qualeaparviflora / triterpenes, simple phenols / Mediterranean and savanna / tables 3 and 6
Gopichandranet al. 1992 / Phenolics / 50 / 1.5 / 0.1 / Austrothripscochinchinensis / Calycopterisfloribundus / tannins / Tropical forest / fig 4M, C. floribundus
Gopichandranet al. 1992 / Phenolics / 50 / 0.9 / 0.1 / Liothripsviticola / Vitislanceolaria / flavonoids and tannins / Tropical forest / fig 4 V. lanceolaria
Gopichandran et al. 1992 / Phenolics / 50 / 1.3 / 0.1 / Phorainothripsloranthi / Loranthuselasticus / terpenes, xanthones / Tropical forest / fig. 4 L. elasticus
Guimaraeset al. 2013 / Volatiles / 70 / 0.0 / 0.1 / Clusiamyianitida / Clusialanceolata / beta triketones and xanthones / Tropical forest / table 4
Hjälténet al. 2007 / Phenolics / 36 / 1.4 / 0.1 / Pontaniatriandrae / Salix triandra / flavonoids / Boreal forest / in text, MANOVA
Hjältén et al. 2007 / Tannins / 36 / 1.4 / 0.1 / Pontaniatriandrae / Salix triandra / flavonoids / Boreal forest / in text, MANOVA
Kolehmainen 1994 / Phenolics / 21 / 3.0 / 0.4 / Euuraamerinae / Salix pentandra / flavonoids / Boreal forest / table 1
McKinnon et al. 1999 / Phenolics / 30 / 1.0 / 0.1 / Adelgesabietis / Piceaglauca / terpenes / Boreal forest / in text
McKinnon et al. 1999 / Tannins / 30 / 1.4 / 0.2 / Adelgesabietis / Piceaglauca / terpenes / Boreal forest / in text
McKinnon et al. 1999 / Volatiles / 30 / -0.9 / 0.1 / Adelgesabietis / Piceaglauca / terpenes / Boreal forest / in text
Motta et al. 2005 / Tannins / 20 / 0.8 / 0.2 / Lepidoptera / Tibouchinapulchra / tannins / Tropical forest / table 1, G and OL
Nyman & Julkunen-Tiitto 2000 / Phenolics / 20 / -1.6 / 0.3 / Pontaniaarcticornis / Salix phylicifolia / flavonoids / Boreal forest / fig 1, S. phylicifolia
Nyman & Julkunen-Tiitto 2000 / Phenolics / 20 / 0.1 / 0.2 / Pontaniamyrsiniticola / Salix myrsinities / flavonoids / Boreal forest / S. myrsinities
Nyman & Julkunen-Tiitto 2000 / Phenolics / 20 / -1.7 / 0.3 / Pontanianivalis / Salix glauca / flavonoids / Boreal forest / S. glauca
Nyman & Julkunen-Tiitto 2000 / Phenolics / 20 / -1.2 / 0.2 / Pontaniasamolad / Salix lapponum / flavonoids / Boreal forest / S. lapponum
Nyman & Julkunen-Tiitto 2000 / Phenolics / 20 / -0.1 / 0.2 / Pontaniaaestiva / Salix borealis / flavonoids / Boreal forest / S. borealis
Nyman & Julkunen-Tiitto 2000 / Phenolics / 20 / 2.2 / 0.3 / Pontaniareticulatae / Salix reticulata / flavonoids / Boreal forest / S. reticulata
Nyman & Julkunen-Tiitto 2000 / Tannins / 20 / 6.6 / 1.3 / Pontaniaarcticornis / Salix phylicifolia / flavonoids / Boreal forest / fig 1, S. phylicifolia
Nyman & Julkunen-Tiitto 2000 / Tannins / 20 / 3.4 / 0.5 / Pontaniamyrsiniticola / Salix myrsinities / flavonoids / Boreal forest / S. myrsinities
Nyman & Julkunen-Tiitto 2000 / Tannins / 20 / 3.3 / 0.5 / Pontanianivalis / Salix glauca / flavonoids / Boreal forest / S. glauca
Nyman & Julkunen-Tiitto 2000 / Tannins / 20 / 1.7 / 0.3 / Pontaniasamolad / Salix lapponum / flavonoids / Boreal forest / S. lapponum
Nyman & Julkunen-Tiitto 2000 / Tannins / 20 / 5.4 / 0.9 / Pontaniaaestiva / Salix borealis / flavonoids / Boreal forest / S. borealis
Nyman & Julkunen-Tiitto 2000 / Tannins / 20 / 3.6 / 0.5 / Pontaniareticulatae / Salix reticulata / flavonoids / Boreal forest / S. reticulata
PascualAlvaradoet al. 2008 / Phenolics / 50 / 0.9 / 0.1 / Cecidomyiidae sp. / Achatocarpusgracilis / unknown / Tropical forest / table 2, A. gracilis
PascualAlvaradoet al. 2008 / Phenolics / 50 / 0.0 / 0.1 / Cecidomyiidae sp. / Guapira macrocarpa / flavonoids / Tropical forest / G. macrocarpa
PascualAlvaradoet al. 2008 / Phenolics / 50 / 0.9 / 0.1 / Cecidomyiidae sp. / Ruprechtiafusca / flavonoids / Tropical forest / R. fusca
PascualAlvaradoet al. 2008 / Phenolics / 50 / 1.3 / 0.1 / Cecidomyiidae sp. / Guettardaelliptica / tannins and alkaloids / Tropical forest / G. elliptica
PascualAlvaradoet al. 2008 / Phenolics / 50 / 0.9 / 0.1 / Cecidomyiidae sp. / Cordia alliodora / terpenes and naphthoquinones / Tropical forest / C. alliodora
Rehill & Schultz 2012 / Phenolics / 6 / 0.5 / 0.7 / Hormaphishamamelidis / Hamamelisvirginiana / flavonoids and tannins / Tropical forest / fig 1, June 6
Rehill & Schultz 2012 / Tannins / 6 / 1.1 / 0.8 / Hormaphishamamelidis / Hamamelisvirginiana / flavonoids and tannins / Tropical forest / Fig 1, June 6
Rostaset al. 2013 / Tannins / 12 / 4.4 / 1.1 / Slavumwertheimae / Pistaciaatlantica / alkyl resorcinols / Mediterranean and savanna / fig 2a
Soetenset al. 1991 / Phenolics / 76 / 1.3 / 0.1 / Pontaniaproxima / Salix alba x fragilis / flavonoids / Temperate forest / table 1, PP - Sc
Sugiuraet al. 2006 / Phenolics / 12 / -1.1 / 0.4 / Asteralobiasoyogo / Ilex pedunculosa / unknown / Temperate forest / fig 3d (1)
Taper and Case 1987 / Tannins / 11 / 2.4 / 0.6 / Cynipidae sp. / Quercus sp. / flavonoids and tannins / Temperate forest / in text
Tookeret al. 2008 / Volatiles / 40 / 0.2 / 0.1 / Eurostasolidaginis / Solidago altissima / terpenes and flavonoids / Temperate forest / text, field based volatile collections
Tookeret al. 2008 / Volatiles / 40 / 0.2 / 0.1 / Gnorimoschemagallaesolidaginis / Solidago altissima / terpenes and flavonoids / Temperate forest / text, field based volatile collections
Tooker and DeMoraes 2007 / Volatiles / 18 / 0.6 / 0.2 / Mayetiola destructor / Triticumaestivum / flavonoids and tannins / Mediterranean and savanna / Figure 1
Torres-Gurrolaet al. 2011 / Volatiles / 291 / 0.4 / 0.0 / Trioza anceps / Perseaamericana / alkaloids / Tropical forest / table 2, beta for total mixture
Valladareset al. 2002 / Volatiles / 28 / -1.0 / 0.2 / Cecydomyiidae sp. / Mintosthachysmollis / terpenes / Mediterranean and savanna / figure 1 (add both volatiles)
Zucker 1982 / Phenolics / 4 / -2.7 / 1.9 / Pemphigus betae / Populusangustifolia / flavonoids / Temperate forest / table 2
Online Resource 4: The variation in effect size of the data used in the meta-analyses.
Reference Effect size [95% CI]
Fig. S4 Forest plot depicting the variation in effect sizes for each of the 60 data points (unique gall-host plant interactions for each chemical type) extracted from the studies included in the meta-analysis of the effect of insect galls on host plant defence chemistry.