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180 Zargaran et al. – Powdery Mildew Reduced Diversity of Cynipid Gall Wasps Rabat. Mirabad had the lowest Shannon’s indices. An increase in either the Gini-Simpson index or Shannon’s H index reduced the evenness of gall wasps (Table 4). The highest and lowest species evenness values were found at Mirabad and Ghabre-hossein, respectively. Cluster analysis dendrogram are shown in figures 1 and 2. Dendrograms cluster sites according to how strongly correlated the sites are, and if sites are highly correlated, they will have a correlation value of 1 or close to 1. In the current study, the highest value of the Sorensen similarity between Dare-ghabr and Ghabre-hossein was 0.72 for uninfected trees in 2009, while the similarity between these 2 sites measured from infected trees was 0.41. The lowest index of similarity was recorded between Rabat and Dare-ghabr on infected trees in 2009. In 2010, Sorensen similarity indices of infected and uninfected trees at Ghabre-hossein and Rabat were 0.27 and 0.40 respectively. The mean number of oak galls was generally higher on uninfected trees than infected trees at all sites in 2 the consecutive years (Table 5). Trees infected with powdery mildews showed the lowest mean number of cynipid galls. Among uninfected trees, the mean number of galls on uninfected trees ranged from14.8 at Rabat in 2010 to 61.2 at Ghabre-hossein in 2009, while the same means for infected trees ranged from 6.2 at Rabat to 25.4 at Ghabre-hossein in 2009. The maximum and minimum uninfected: infected ratios were 2.8 and 2.1 in Dare-ghabr in 2009 and 2010, respectively. Pearson’s correlation coefficients between the number of galls and percent infection showed significant negative correlations in 2009 (r = -0.714, n = 20, p < 0.01) and 2010 (r = -0.581, n = 20, p < 0.01) (Fig. 3). On infected oak trees, leaf gall abundances declined with increasing levels of powdery mildew. Table 4. Species diversity indices and the true diversity of oak gall wasps in 2009 and 2010 Diversity indices Sites Simpson D Species richness Gini-Simpson True diversity Shannon’s H’ True diversity Evenness Infected oak trees (2009) Ghabre-hossein 0.9012 11.95 2.48 13.21 0.91 14 0.08 Dare-ghabr 0.9104 7.38 1.99 9.95 0.89 11 0.10 Rabat 0.9188 3.91 1.36 5.33 0.81 6 0.19 Mirabad 0.9342 3.21 1.16 3.49 0.71 4 0.29 All sites pooled 6.61 1.75 8.00 0.84 8.7 0.16 Uninfected oak trees (2009) Ghabre-hossein 0.8958 18.36 2.91 19.65 0.95 21 0.05 Dare-ghabr 0.9197 16.96 2.83 17.21 0.94 18 0.06 Rabat 0.9176 7.32 1.99 7.79 0.87 9 0.13 Mirabad 0.9419 4.86 1.58 5.27 0.81 6 0.19 All sites pooled 11.875 2.33 12.48 0.89 13.5 0.11 Infected oak trees (2010) Ghabre-hossein 0.8311 8.86 2.18 8.12 0.89 10 0.11 Dare-ghabr 0.8422 8.29 2.12 8.42 0.88 9 0.12 Rabat 0.9140 3.98 1.38 4.39 0.77 5 0.23 Mirabad 0.9205 3.25 1.18 3.29 0.69 4 0.30 All sites pooled 6.095 1.71 6.06 0.81 7 0.19 Uninfected oak trees (2010) Ghabre-hossein 0.8957 12.72 2.54 16.27 0.94 17 0.06 Dare-ghabr 0.9114 11.46 2.44 15.48 0.94 16 0.06 Rabat 0.9272 8.79 2.17 7.04 0.85 8 0.14 Mirabad 0.9380 3.86 1.35 4.31 0.77 5 0.24 All sites pooled 9.21 2.13 10.78 0.87 11.5 0.13
<strong>Zoological</strong> <strong>Studies</strong> 51(2): 175-184 (2012) 181 100 Rescaled Distance Chister Combine (A) 80 60 40 20 0 DISCUSSION Mirabad & Rabat Ghabre-hossein & Dare-ghabr Rabat & Dare-ghabr Mirabad & Dare-ghabr Ghabre-hossein & Mirabad Ghabre-hossein & Rabat Ghabre-hossein & Mirabad Rabat & Dare-ghabr Mirabad & Dare-ghabr Ghabre-hossein & Rabat Mirabad & Rabat Ghabre-hossein & Dare-ghabr 100 Rescaled Distance Chister Combine (B) 80 60 40 20 Fig. 1. Sorensen cluster analysis dendrogram of similarity coefficients for oak gall wasps occurring on infected (A, above) and uninfected (B, below) trees in 2009. Ghabre-hossein & Dare-ghabr Mirabad & Rabat Ghabre-hossein & Rabat Ghabre-hossein & Mirabad Mirabad & Dare-ghabr Rabat & Dare-ghabr Mirabad & Dare-ghabr Rabat & Dare-ghabr Ghabre-hossein & Mirabad Ghabre-hossein & Rabat Mirabad & Rabat Ghabre-hossein & Dare-ghabr 100 100 Rescaled Distance Chister Combine (A) 80 60 40 20 Rescaled Distance Chister Combine (B) 80 60 40 20 Fig. 2. Sorensen cluster analysis dendrogram of similarity coefficients for oak gall wasps occurring on infected (A, above) and uninfected (B, below) trees in 2010. 0 0 0 Our results clearly demonstrated an indirect plant-mediated interaction between Erysiphe alphitoides and a community of cynipid oak gallforming wasps, and we found that pathogen infection significantly reduced the abundance and species richness of the native oak gall wasps. Although there were differences among sites, the highest and lowest abundance and richness values were always respectively associated with healthy and diseased oak trees, at any given site. This is the 1st study to demonstrate plantmediated interactions between a leaf pathogen and a community of gall-forming wasps. It was commonly reported that pathogen or insect attacks can affect the composition of insect and pathogen communities associated with plants and mediate the incidences and abundances of subsequent attackers (Stout et al. 2006, Eyles et al. 2010). In the current study, the mechanism of the plantmediated interaction between E. alphitoides and gall-forming wasps is not known although, based on earlier publications on cynipid gall wasps, we Table 5. t-test comparison of the mean number (± S.E.) of oak galls per trees between infected and uninfected oak trees in 2009 and 2010. A significant difference was accepted at < 0.05 20.00 year 2009 2010 Site Year Mean number (± S.E.) of oak galls per tree Uninfected Infected Number of leaf gall wasps 15.00 10.00 5.00 Ghabre-hossein 2009 61.2 (±5.3) 25.4 (±6.1) 2010 32.4 (±7.1) 17.3 (±3.2) Dare-ghabr 2009 54.2 (±8.2) 19.4 (±11.1) 2010 38.4 (±1.8) 18.3 (±4.3) Mirabad 2009 22.5 (±9.4) 10.4 (±5.8) 2010 16.9 (±2.7) 7.1 (±4.6) Rabat 2009 20.3 (±1.4) 8.7 (±3.3) 2010 14.8 (±6.3) 6.2 (±2.4) Site Year Statistics t-value p-value 0.00 0.00 10.00 20.00 30.00 40.00 50.00 60.00 70.00 Percent of leaf infection Fig. 3. Correlation between the number of leaf gall wasps and percent of leaf infection by oak powdery mildew on oaks in 2009 and 2010. An increased percent of disease infection led to a decrease in leaf oak gall wasp numbers. Ghabre-hossein 2009 20.16 0.002 2010 12.23 0.036 Dare-ghabr 2009 19.05 0.001 2010 15.64 0.026 Mirabad 2009 14.52 0.031 2010 9.37 0.048 Rabat 2009 7.78 0.043 2010 8.44 0.029
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