Effect of Cardinal Directions on Gall Morphology and Parasitization of the , quercusfolii Author(s): Mohammed Reza Zargaran, Mohammed Hassan Safaralizadeh, Ali Asghar Pourmirza and Orouj Valizadegan Source: Journal of Science, 11(169):1-10. 2011. Published By: Entomological Society of America DOI: http://dx.doi.org/10.1673/031.011.16901 URL: http://www.bioone.org/doi/full/10.1673/031.011.16901

BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.

BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Journal of Insect Science: Vol. 11 | Article 169 Zargaran et al.

Effect of cardinal directions on gall morphology and parasitization of the gall wasp, Cynips quercusfolii Mohammed Reza Zargarana*, Mohammed Hassan Safaralizadehb, Ali Asghar Pourmirzac, and Orouj Valizadegan

Urmia University, Faculty of Agriculture, Department of Entomology, Uremia University, West Azerbaijan, Iran Abstract This survey investigated the relationship between gall morphology and some fitness components in the asexual generation of Cynips quercusfolii L. (: Cynipidae). Results showed that larger C. quercusfolii galls were formed on the south side of oak trees Quercus infectoria Olivier (Fagales: Fagaceae). Larval chamber diameter in the gall was similar, but gall diameter and gall wall thickness varied with the location of the gall on the tree. Cynips quercusfolii was attacked by parasitoids, and the south-facing galls suffered significantly lower parasitoid attacks. Thickness of gall walls and parasitism rate were negatively correlated. Mean gall diameter and gall wall thickness were significantly larger in south-facing galls than other directions, but the difference in the mean larval chamber diameter was not significant. These results suggest that the position of galls on the tree affected gall wall thickness, and this plays an important role in parasitoid attacks. These results suggest that C. quercusfolii prefer to attack the south side of oak trees, and selection of this side by wasps led to formation of larger galls with thick walls that decreased parasite attack, which will affect growth and survival of wasp larvae.

Keywords: oak, parasitoids Correspondence: a [email protected], b [email protected], c [email protected], [email protected], * Corresponding author Editor: Nadir Erbilgin was Editor of this paper. Received: 25 December 2010, Accepted: 25 April 2011 Copyright : This is an open access paper. We use the Creative Commons Attribution 3.0 license that permits unrestricted use, provided that the paper is properly attributed. ISSN: 1536-2442 | Vol. 11, Number 169 Cite this paper as: Zargaran MR, Safaralizadeh MH, Pourmirza AA, Valizadegan O. 2011. Effect of cardinal directions on gall morphology and parasitization of the gall wasp, Cynips quercusfolii. Journal of Insect Science 11:169 available online: insectscience.org/11.169 Journal of Insect Science | www.insectscience.org 1 Journal of Insect Science: Vol. 11 | Article 169 Zargaran et al.

Introduction 1998). Normally, nutritive cells provide the food required for gall wasp larva. However, Iran lies at the eastern limit of the Western parenchyma cells of the gall may be converted Palaearctic ecoregion, and recent surveys to nutritive cells when needed, compensating confirm that this country has a rich Cynipid food supply shortages (Stone et al. 2002). The fauna (Azizkhani 2006; Sadeghi et al. 2010) outer part of a gall is comprised of the central and includes many of the widespread Western part of the gall to the sclerenchyma layer and Palaearctic species, including Cynips beyond it. The outer parts of galls are used as quercusfolii L. (Hymenoptera: Cynipidae) characters to specify various gall wasps (Melika et al. 2004). (Schonrogge et al. 2000). The outer structures of the galls include layers of woody or spongy The asexual generation of the cynipid wasp (sometimes with hollow spaces) tissue, Cynips quercusfolii causes hemispherical leaf superficially covered with thick layers of vein galls on oak trees, Quercus infectoria resins or hairs, lint, or spines (Price et al. Olivier (Fagales: Fagaceae). Galls of C. 1987; Stone and Cook 1998). The size of a quercusfolii are distributed in oak forests of gall is most likely directly related to many West Azerbaijan in Iran. The asexual factors such as wasp potential fecundity, generation of C. quercusfolii forms galls on which is positively correlated with gall size oak with a hemispherical single larval (Kato and Hijii 1993; Gilbert et al. 1994). chamber on the upper leaf surface. The C. quercusfolii oak gall has a single chamber and Parasitoids and probably inquiline attacks are a single attacking parasitoid. In Sardasht, the principal factors in the mortality of the galls appear successively from mid–August to cynipids (Washburn and Cornell 1981). Gall September, and each gall matures within one size, size of larval chamber, and wall month. Larvae grow rapidly in late September thickness affect the ability of parasitoids to to early October, pupate in late September to successfully attack the cynipids (Washburn mid–October, and adults emerge from the and Cornell 1981; Schonrogge et al. 1996). galls in late October. Some mature galls fall These factors affect parasitoid attack on from the leaves, while many immature galls galling , and are related to the that are attacked by parasitoids remain on the morphological traits of the gall. leaves (Zargaran et al. 2008). Evaluation of the relationship between gall Typically the sexual generation occurs in the morphology in different geographical spring and the asexual female generation is in directions and climate, such as avoidance of the fall. Structurally, galls induced by sexual parasitoid attack, will provide a better or asexual generation of gall wasps are understanding of the population dynamics of divided into two larval chambers surrounded C. quercusfolii galls and probably for other by an outer layer. Larval chambers are alike in cynipids. The objective of this study was to most galls. Surrounding each larval chamber evaluate the relationships between climate and is a mass of nutritive cells surrounded with a C. quercusfolii gall placement within Q. single layer of parenchyma cells. In most infectoria canopies in relation to gall galls, these two layers are covered with a third morphology and parasitoid activity. layer of sclerenchyma cells (Stone and Cook

Journal of Insect Science | www.insectscience.org 2 Journal of Insect Science: Vol. 11 | Article 169 Zargaran et al. Materials and Methods quercusfolii oak galls of (100 galls in each direction) were surveyed from 20 Q. Sampling was carried out in the oak forest of infectoria trees (trees with 3 m in height and West Azerbaijan province in the Sardasht and open canopy) in each location on 20 October Piranshahr City in two locations (with similar 2010 by pruning branches with galls within plant covering): Ghabre-hosein (36° 28 N, 4m of ground level, for a total of 800 galls in 45° 18 W) with a humid–cold climate, and the two locations. The galls were placed in Rabat (36° 14 N, 45° 33 W) with a nylon bags along with the branches pruned Mediterranean–humid climate, based on from each direction, and were kept under Dumarten's climate classification method. outdoor conditions. Adult cynipids and Table 1 shows the environmental conditions parasitoids emerging from the galls were of these two locations from July to December collected every day for 10 days and were 2010. The oak forest of West Azerbaijan is stored in 75% ethyl alcohol. Only parasitoids composed mainly of Q. infectoria (comprising that reached the adult stage were surveyed and 90% of plant cover); this species is identified to the species level. predominant. Ten days later, the morphological traits of The optimal number of samples was these collected galls were studied. All galls determined according to the formula of formed on a leaf located in a middle position Southwood and Henderson (2000): on each shoot were sampled, because gall morphologies might be affected by variation N = ((t  s) / (d  m))2 in leaf quality.

where t is student’s t–test using standard The galls were then dissected, and the statistical tables, d is the predetermined percentage of galls parasitized was calculated confidence limit for the estimation of the based on this formula: [number of extracted mean express as a decimal, m is sampling parasitoids in each side/(100 – the empty mean, and s is the standard deviation. galls)]*100.

The best number of samples was determined Mortality of C. quercusfolii in this study was to be 20 trees. On each tree, as a unit of only caused by parasitoids. After calculating sampling, galls were collected on one branch the rate of parasitism, the gall size, gall wall (branch length was 90 cm) in each cardinal thickness, and larval chamber diameter were direction (north, south, east, west)—totaling measured as follows: galls were cut open four branches in one tree—on 20 October longitudinally and examined under a 2010. The effect of cardinal directions on C. dissecting microscope, the largest and quercusfolii gall abundance was analyzed with smallest diameters of each gall were measured these data. Additionally, a total of 400 C. with digital calipers to the nearest 0.02 mm, Table 1. Descriptions of collecting sites in west Azerbaijan, 2010.

Journal of Insect Science | www.insectscience.org 3 Journal of Insect Science: Vol. 11 | Article 169 Zargaran et al. Table 2. Contents of galls and the percent parasitized Cynips quercusfolii galls in two locations, 2010.

Table 3. Relationships of gall diameter vs. gall wall thickness and percentage parasitism.

ns = Not significant; *p < 0.05. and the diameter of the larval chamber was value was less than  = 0.05 then the data measured with an ocular micrometer to the were considered not normal. Thus, data were nearest 0.08 mm. Then, gall wall thickness transformed by (x + 0.5). was defined as such: gall wall thickness = (gall diameter  larval chamber diameter)/2. Student's t–test was used between gall Empty galls and galls with a hole at the time diameter vs. gall wall thickness vs. larval– of dissection were also recorded. chamber diameter and percentage parasitized in the locations. When necessary, Tukey's Data analyses Honestly Significant Difference test was used The galls with living inhabitants were used for for multiple comparisons of mean values. If the analysis of gall morphology. Pearson's homogeneity of variances between groups was correlation coefficient was used to test the not certain, the Kruskal-Wallis test was used. relationship between paired trait variables in The emerging rate of C. quercusfolii from the four cardinal directions: gall diameter vs. each direction was calculated for the gall wall thickness, gall diameter vs. larval determination the stability in each direction. chamber diameter, and gall wall thickness vs. parasitism. To examine the changes in gall Results morphology, the mean values for gall diameter, gall wall thickness, larval chamber There was a significant difference in the mean diameter, percent of parasitism, and number of collected galls from all directions geographical direction of gall occurrence were in both humid–cold (df = 3; p < 0.05) and tested among sampling places using a one– Mediterranean–humid climate (df = 3;p < way ANOVA. 0.05). The mean number of galls was higher in the southern direction (in humid–cold: The data were tested for normality by mean ± SD; 4.85 ± 0.72, and in Shapiro-Wilk (data less than 50); if significant Mediterranean–humid: mean ± SD; 4.12 ±

Journal of Insect Science | www.insectscience.org 4 Journal of Insect Science: Vol. 11 | Article 169 Zargaran et al. 0.34) than the other directions in each two stations; the northern (in humid–cold: mean ± SD; 3.16 ± 0.72, and in Mediterranean– humid: mean ± SD; 3.09 ± 0.51), eastern (in humid–cold: mean ± SD; 3.27 ± 0.89, and in Mediterranean–humid: mean ± SD; 3.18 ± 0.57), and western (in humid–cold: mean ± SD; 3.11 ± 0.41, and in Mediterranean– humid: mean ± SD; 3.19 ± 0.61) directions were in the same statistical group (Tukey's test;p < 0.05 in each two stations). In general it seems that oak gall wasp females prefer to Figure 1. Percent of empty galls at different directions in Rabat and lay eggs on the southern side where exposure Ghabre-hosein station. High quality figures are available online. to the sun is most intense. The lowest number of empty galls (Figure 1) and also the highest of gall–maker emergence holes (Table 2) were recorded in south direction in Mediterranean– humid and humid–cold climate, and was significantly different from the other directions.

Mean gall diameter and also gall wall thickness among different cardinal directions differed from each other and were significantly different (df = 3;p < 0.05) in each two stations. The highest mean values of Figure 2. Mean gall diameter of galls at different directions in Rabat the gall diameter were recorded in the south and Ghabre-hosein station. High quality figures are available online. direction both in humid–cold and Mediterranean–humid climates (Figure 2). morphological traits gall diameter and gall Also, the highest mean values of gall wall wall thickness, but does not affect larval– thickness were seen in humid–cold and chamber diameter. Mediterranean–humid climate in the galls occurring in the south direction, and the least In this survey, three solitary parasitoid species of above listed morphological traits was seen were recorded from asexual galls of C. in other directions. North, west, and east quercusfolii: Sycophila biguttata Swederus directions were placed in one statistical group (Hymenoptera: Eurytomidae) from humid– (Tukey's test;p < 0.05 in each two stations) cold and Mediterranean–humid climate, that were similar in gall diameter and gall wall Eurytoma brunniventris Ratzeburg thickness value. But the larval–chamber (Eurytomidae) from humid–cold climate, and diameter of the collected galls in all directions Megastigmus dorsalis Fabricius (Torymidae) was not significant among them in the two from humid–cold and Mediterranean–humid stations (df = 3;p > 0.05). These results climate. The parasitoid species E. suggest that selection of the cardinal brunniventris was not seen at Mediterranean– directions by C. quercusfolii affect the humid climate.

Journal of Insect Science | www.insectscience.org 5 Journal of Insect Science: Vol. 11 | Article 169 Zargaran et al. between directions. Gall wall thickness Of these three parasitoids E. brunniventris between the galls on the south side of trees in was the most abundant. The mean percentage two humid–cold and Mediterranean–humid of parasitism was significantly lower (df = 3, climates was significant (Student’s t–test; t = p < 0.05) (Table 2) on south-facing galls than 0.59, p < 0.05), but this morphological trait in other directions, but showed no significant did not differ in other directions. Also, the difference among the east, west, and north percentage of parasitism in the south direction direction (placed in one statistical group). The in humid–cold and Mediterranean–humid value of Pearson's correlation coefficient climate was significant (Student’s t–test; t = between gall diameter and gall wall thickness 3.56,p < 0.05) and this was higher in showed a significant positive correlation (p < Mediterranean–humid, while the number of 0.05) for all galls in the two stations. Also, species of parasitoids was greater in humid– gall diameter and larval chamber diameter cold. The structure of the galls is an important were not significantly correlated (p > 0.05). factor affecting parasitism. Also, the larger The mean percentage of parasitism with gall galls that were formed in humid–cold climate diameter and also with gall wall thickness have thicker walls, which may be one of the showed significant negative correlation (p < reasons for the lower the percentage of 0.05) only for the galls on the south side of the parasitism. trees in humid–cold and Mediterranean– humid climate (Table 3) and was not Discussion significant between other directions (p > 0.05). These results suggest that C. These results show that larger galls with quercusfolii prefer to select the south side of thicker walls were formed on the south side of trees for gall forming, because galls in this the oak trees in humid–cold climate. In direction are large in comparison with other addition to genetic factors, other factors such galls and presence of a thick gall wall as location of gall formation and climate can decreases the parasitism rate. Thus, it might affect gall size. It is likely that larger galls can increase the survival of the cynipid wasps, be effective in survival of the cynipid wasp especially the larvae. larvae in at least three ways: (1) greater food availability, (2) maintenance of favorable Effects of differences in climate on gall environmental conditions within the gall, and morphology and parasitism were examined in (3) increased protection against natural the two humid–cold and Mediterranean– enemies including parasitoids. Gall size humid climates. Mean gall diameter was affects the morphological traits of some larger in the galls that were formed on south galling insects (Weis and Abrahamson 1985; side of trees in humid–cold than those in Kato and Hijii 1993; Gilbert et al. 1994), and Mediterranean–humid climate (Student’s t– larger gall size may directly affect the test; t =2.58,p < 0.05), but comparison percentage of parasitism. between the other directions (north, east, and west) using Student’s t–test were not The higher numbers of holes in the galls on significant (p > 0.05). The larger galls provide the south side of the oak trees show that these more food and protection for the parasitoid gall wasps successfully exited and wasp larvae. However, mean larval chamber development was completed. The percentage diameter was not significantly different of parasitoid attacks was lower for the galls

Journal of Insect Science | www.insectscience.org 6 Journal of Insect Science: Vol. 11 | Article 169 Zargaran et al. established on the south side of the trees than others, which suggests that the preference of on three other directions; gall wall thickness is wasps for warmer places for oviposition has a the main reason for this result. selective advantage because development of a gall is more likely to occur. One of the rare parasitoids that attacks smaller host larvae, Eurytoma brunniventris, was not Parasitoids depend on a series of adaptations found in Mediterranean–humid climate. Many to the ecology and physiology of their hosts factors other than the presence of a host limit and host plants for survival, and are thus the distribution of parasitoids and herbivores, likely to be highly susceptible to changes in but the most obvious one is climate (Barratt environmental conditions (Hance et al. 2007). 2004). Weis et al. (1985) reported that E. In many cases, the galls have been found to gigantea spends a great amount of time contain higher concentrations of defense probing galls too big to penetrate, which in chemicals than normal plant tissues. Some of turn leads to a decrease in foraging efficiency them are phenolics that have a defensive role, when many large galls are present. Moreover, while others are tannins that have been shown the chance of successfully penetrating into a to act as feeding deterrents, growth inhibitors, gall is affected by the thickness of the gall and toxins against insect herbivores (Nyman wall and the length of the parasitoid's and Julkunen-Tiitto 2000). It is possible that ovipositor. However, larger galls represent a secondary plant compounds accumulate in the more profitable resource for those natural south side of trees. enemies that can gain access to them (Williams and Cronin 2004). Large galls also have characteristics that deter parasitoid attacks (Weis and Abrahamson Cynipid wasps have been shown to control the 1985; Price and Clancy 1986). If small C. physiology of gall tissues (Abe 1997; quercusfolii individuals are large enough for Schonrogge et al. 2000; Ronquist and parasitoids, the higher rate of parasitoid attack Liljeblad 2001). Clearly, a food supply of high on smaller galls in three directions (east, west, nutritional quality is required for the growth and north) suggests that parasitoids can and development of the wasp larvae; oviposit more easily on the host in smaller therefore, gall formation on the south side of galls. Gall size was correlated both with gall trees will enhance survival of the larvae. In wall thickness and parasitism rates. A thick our results, the lower number of oak galls on gall wall can protect the wasp larvae against east, north, and west sides of trees may be due parasitoid attack, as the ovipositor cannot to the reduced oviposition of oak gall wasps penetrate the galls. or inappropriate conditions for continued larval growth. Although the egg is often Life–history traits affected by cold exposure positioned on the plant surface with only the and extreme temperatures can reduce tip inserted into the epidermis, sometimes the endosymbiont populations inside parasitoids, whole egg is embedded in plant tissue. The and eventually eliminate populations of attacked plant tissue eventually produces a endosymbionts that are susceptible to high gall, inside of which the wasp larva feeds on a temperatures (Hance et al. 2007). One good specially developed tissue (Vardal et al. measure of gall fitness is the probability that a 2003). This may be because of warmer larva will survive. In some cases this is greatly conditions of the southern side compared with influenced by the size of the gall that gall

Journal of Insect Science | www.insectscience.org 7 Journal of Insect Science: Vol. 11 | Article 169 Zargaran et al. wasps induce in the plant, which depends on mukaigawae (Hymenoptera: Cynipidae) several different factors. In places where the against the gall–inhibiting moth, parasitoids are abundant there is strong Oedematopoda sp. Applied Entomology and selection for large galls; larvae are protected Zoology 32: 135-141. because large galls have walls that are too thick for wasp ovipositors to penetrate. Azizkhani E. 2006. Parasitoid fauna of oak Indirect effects of climate conditions affect gall wasps in Lorestan province. Ph.D. gall size and increase the ability of the gall Thesis, Tehran University, Tehran, Iran. wasps to produce large galls. Although gall wasps do have some genetically–determined Barratt BIP. 2004. Microctonus parasitoids influence over gall size, the plant itself plays a and New Zealand weevils: comparing greater role in determining gall size (Weis and laboratory estimates of host ranges to realized Abrahamson 1998). host ranges. In: Van Driesche RG, Reardon R, Editors. Assessing host ranges for parasitoids Climate change can influence plant and predators used for biological control: A productivity both directly and indirectly. guide to best practice. pp. 103-120. USDA Indirectly, climate change can affect the Forest Service. phenology of the relationship between climatic settings and periodic biological Gilbert F, Astbury C, Bedingfield J, Ennis B, events of certain regions (Thomson et al. Lawson S, Sitch T. 1994. The ecology of the 2009). Romeis et al. (2005) reported that pea galls of Cynips divisa. In: William MAJ, parasitism levels by Trichogramma varied Editor. Plant galls. pp 331-349. Oxford greatly among different habitats, plants, or University Press. plant structures. Considering the low parasitism rate in humid–cold climate, we Hance T, Baaren J, Vernon P, Boivin G. 2007. hypothesize that a habitat’s annual climate Impact of Extreme Temperatures on patterns might determine oviposition rates, Parasitoids in Climate Change Perspective. lifetime fecundity, and the number of Annual Review of Entomology 52: 107-126. generations in a year. Abiotic factors such as soil quality, weather, humidity, and others Kato K, Hijii N. 1993. Optimal clutch size of affect the structure the galls (Price 2005), and the chestnut gall–wasps Dryocusmus their direct or indirect effects must not be kuriphilus Yasumatsu (Hymenoptera: ignored. Cynipidae). Population Ecology 35: 1-14.

Acknowledgements Melika G, Stone GN, Sadeghi SE, Pujad- Villar J. 2004. New species of cynipid gall Our cordial thanks to the head of the Plant wasps from Iran and Turkey (Hymenoptera: Protection Group, Agricultural Faculty, Urmia Cynipidae: Cynipini). Acta Zoological University for scientific and financial support. Academia Scienta Hungarica 50: 139-151.

References Nyman T, Julkunen-Tiitto R. 2000. Manipulation of the phenolic chemistry of Abe Y. 1997. Well–developed gall tissues Willows by gall–inducing sawflies. protecting the gall wasps Andricus

Journal of Insect Science | www.insectscience.org 8 Journal of Insect Science: Vol. 11 | Article 169 Zargaran et al. Proceedings of the National Academy of Southwood TR, Henderson PA. 2000. Sciences USA 97: 13184-13187. Ecological methods. Blackwell Science Ltd. Stone GN, Cook JM. 1998. The structure of Price PW, Clancy KM. 1986. Interaction Cynipid oak galls: patterns in the evolution among three trophic levels: gall size and phenotype. Proceedings of the Royal Society parasitoid attack. Ecology 67: 1593-1600. of London, Series B 265: 979-988.

Price PW, Fernandes GW, Waring GL. 1987. Stone GN, Schonrogge K, Atkinson RJ, Adaptive nature of insect galls. Environmental Bellido D, Pujade-Villar J. 2002. The Entomology 16: 15-24. population biology oak gall wasps. Annual Review of Entomology 47: 633-668. Price PW. 2005. Adaptive radiation of gall– inducing insects. Applied Ecology 6: 413-421. Thomson L, Macfadyn S, Hoffmann, A. 2009. Predicting the effects of climate change on Romeis J, Babendreier D, Wackers FL, natural enemies of agricultural pests. Shanower TG. 2005. Habitat and plant Biological Control 10: 1016-1018. specificity of Trichogramma egg parasitoids– underlying mechanisms and implications. Vardal H, Sahlen G, Ronquist F. 2003. Basic and Applied Ecology 6: 215-236. Morphology and evolution of the Cynipoid egg. Zoological Journal of Linnean Society Ronquist F, Liljebld J. 2001. Evolution of the 139: 247-260. gall wasp–host plant association. Evolution 55(12): 2503-2522. Washburn JO, Cornell HV. 1981. Parasitoids, patches and phenology: their possible role in Sadeghi SE, Melika G, Stone GN, Assareh the local extinction of a cynipid gall wasp MA, Askary H, Tavakoli M, Yarmand H, population. Ecology 62: 1597-1607. Azizkhani E, Zargaran MR, Barimani H, Dordaii AA, Aligholizadeh D, Salehi M, Williams M, Cronin J. 2004. Response of a Mozafari M, Zeinali S, Mehrabi A. 2010. Oak gall–forming guild (Hymenoptera: Cynipidae) gall wasps fauna of Iran (Hymenoptera: to stressed and vigorous prairie Roses. Cynipidae: Cynipini). 7th International Environmental Entomology 33: 1052-1061. Congress of Hymenoptroists: 112. Weis AE, Abrahamson W. 1985. Potential Schonrogge K, Stone GN, Crawley MJ. 1996. selective pressure by parasitoids on a plant– Abundance patterns and species richness of herbivore interaction. Ecology 66: 1261-1269. the alien gall–former Andricus quercuscalicis (Hymenoptera: Cynipidae). Oikos 77: 507- Weis AE, Abrahamson W, McCrea KD. 1985. 518. Host gall size and oviposition success by the parasitoid Eurytoma gigantea. Ecological Schonrogge K, Walker P, Crawley MJ. 2000. Entomology 10: 341-348. Parasitoid and inquiline attack in the gall of four alien, Cynipid gall wasp. Ecological Weis AE, Abrahamson W. 1998. Ecology and Entomology 25: 208-219. evolution. Natural History 2: 60-63.

Journal of Insect Science | www.insectscience.org 9 Journal of Insect Science: Vol. 11 | Article 169 Zargaran et al. Zargaran MR, Sadeghi SE, Hanifeh S. 2008. Identification of oak gall wasps and their parasitoids in west Azerbaijan province of Iran. Institute of Forests and Rangelands.

Journal of Insect Science | www.insectscience.org 10