NORTH-WESTERN JOURNAL OF ZOOLOGY 8 (1): 125-131 ©NwjZ, Oradea, Romania, 2012 Article No.: 121107 http://biozoojournals.3x.ro/nwjz/index.html

Parasitoid community of fructuum (Rübsaamen) (Hym.: Cynipidae) in Kerman Province, with checklist of associated fauna in Iran

Hosseinali LOTFALIZADEH1*, Mojtaba RAJABI2 and Seyed Massoud MADJDZADEH2

1. Department of Plant Protection, East-Azarbaijan Research Center for Agriculture & Natural Resources, Tabriz, Iran. 2. Department of Biology, Shahid Bahonar University of Kerman, Kerman, Iran * Corresponding author e-mail: [email protected]

Received: 09. September 2011 / Accepted: 10. January 2012 / Available online: 11. February 2012 / Printed: June 2012

Abstract. Fourteen species of hymenopterous associated with rose wasp Diplolepis fructuum (Rübsaamen) are found in Kerman Province, Southeast Iran. These wasps belong to seven families for which two new distributional records (Eurytoma adleriae Zerova and Eurytoma cynipicola Zerova) are now added to the Iranian fauna. Four new biological associations were found belonging to E. adleriae, E. cynipicola, Hobbya stenonota (Ratzeburg) and Periclistus brandtii (Ratzeburg) that are reported for the first time as trophically associated with D. fructuum in Iran. The studied community is compared with a previously reported community from East-Azarbaijan Province, Northwest Iran. Checklist of the species associated with D. fructuum in Iran is presented, including 24 hymenopterous species.

Key words: Rose , Diplolepis fructuum, biological association, community, new records, Iran.

Introduction namely E. caninae Lotfalizadeh & Delvare, 2007 (Lotfalizadeh et al. 2007). Recently an ichneu- The cynipid gall wasps of the Diplolepis monid wasp, Exeristes roborator (Fabricius, 1793) Geoffroy (Hymenoptera: Cynipidae) are known has been added to this list (Lotfalizadeh et al. pests of Rosa species. A large community of 2009). parasitoids attacks rose gall wasps around the Main aims of the present study were: 1) to world (Askew 1960, Schröder 1967, Nordlander present complementary information on the parasi- 1973, Zerova & Djakontshuk 1976, Nieves-Aldrey toids community of D. fructuum in Iran, 2) to re- 1981, Pujade-Villar 1992, Shorthouse 1993). This port some new information concerning the associ- community was recently studied in Iran (Rakh- ated complex from Kerman Province (Southeast shani et al. 2003, Talebi et al. 2004, Daneshvar et al. Iran), and 3) to present a checklist of D. fructuum's 2009, Askew et al. 2006a, Lotfalizadeh et al. 2006). associated community. Despite these studies, there are many undiscov- ered aspects of this interesting community and re- cent studies lead researchers to describe several Materials and Methods new species (Askew et al. 2006a, Lotfalizadeh et al. During our collection program of chalcidoid wasps 2006). (Hym.: Chalcidoidea) in Kerman Province, Southeast About 45 species of parasitoids belonging to Iran, we bred some hymenopterous parasitoids from rose 18 genera are known to be associated with Diplole- caused by Diplolepis fructuum (Rübsaamen) (Hym.: pis species on Rosa spp. in the Palaearctic region Cynipidae), collected on Rosa beggeriana Schrenk, in April- (Askew 1960, Schröder 1967, Nordlander 1973, Ze- May 2008 and 2010. In this study about 500 galls were col- rova & Djakontshuk 1976, Nieves-Aldrey 1981, lected. The rose galls were collected at three sites in Ker- man Province: Pujade-Villar 1992, Noyes 2010), which were 1- Sar-Cheshmeh Mountains (N 29° 59' 52'' E 55° 51' summarized by Lotfalizadeh et al. (2006). 26'', 2564 m), 17 April 2008 There are limited data on parasitoids of Dip- 2- Kouh-Payeh Mountains (N 30° 31' 55'' E 57° 13' lolepis fructuum Rübsaamen () in the 44'', 2515 m), 2 May 2009 Western Palaearctic. Askew et al. (2006b) listed 3- Sar-Bizhan Mountains (N 29° 08' 09'' E 57° 30' 01'', only one species associated with D. fructuum, 2705 m), 28 April 2010 while Lotfalizadeh et al. (2006) listed 17 species The collected galls were moved to the laboratory and kept at room temperature in mesh covered transparent from the Northwest of Iran. Later, from the same plastic rearing boxes until the emergence of parasitoids. community a new Eurytoma species was described The emerged parasitoid wasps were preserved in 75 % 126 Lotfalizadeh, H. et al. ethanol and then were card-mounted and identified using Different taxa of Hymenoptera species were Lotfalizadeh et al. (2006) and Zerova (1995). The obtained found attacking D. fructuum galls in Kerman Prov- list was compared with that of Lotfalizadeh et al. (2006). ince (see Table 1). In the present study, 14 species Finally a checklist of associated community to rose gall were reared from galls of D. fructuum. These spe- wasp, D. fructuum, was prepared. cies belong to seven families: Cynipidae, Eulophi- dae, Eupelmidae, , , Results and Discussion and , while earlier only five families of chalcid wasps have been reported Diplolepis fructuum was reared for the first time on on D. fructuum (Lotfalizadeh et al. 2006) and four Rosa beggeriana Schrenk, known to be occurring in on D. mayri (Askew et al. 2006a). Iran, Afghanistan, Kazakhstan, China and Mongo- Associated fauna of D. mayri has been re- lia. While the general form of galls (Fig. 1), briefly ported from Iran by Askew et al. (2006a) which discussed by Lotfalizadeh et al (2006), is plurilocu- make gall on fruits as well. Based on the key of lar and not covered by branching hairs, most of Pujade-Villar and Plantard (2001), D. mayri and D. the collected galls have a special form, rare for D. fructuum are closely allied species. Morphological fructuum (Fig. 2). evidences for the separation of these species from Within the reared samples of D. fructuum both the "rosae" species complex have been discussed male and female individuals were found while by Pujade-Villar and Plantard (2001). Fruit galls of Lotfalizadeh et al. (2006) did not report male indi- D. mayri and D. fructuum are externally similar but viduals in their rearing. In the galls collected in galls of the first one do not split the external enve- 2008, 2009 and 2010, the percentage of male indi- lope of the fruit while D. fructuum galls are pro- viduals was 33 %, 20 % and 6 %, respectively. duced by the hypertrophy of seeds and can split

Table 1. Hymenoptera species reared from galls of D. fructuum in Kerman and East-Azarbaijan provinces.

Hymenoptera families and species Kerman Province East-Azarbaijan Province* aurantiacus (Ratzeburg, 1852) – + Aprostocetus eurytomae (Nees, 1834) + + Eupelmidae Eupelmus fulvipes Förster, 1860 – + Eupelmus urozonus Dalman, 1820 + + Eurytomidae Aximopsis collina (Zerova, 1984) + + Eurytoma adleriae Zerova, 1995 + – Eurytoma caninae Lotfalizadeh & Delvare, 2007 + + Eurytoma cynipicola Zerova, 1976 + – Eurytoma rosae Nees, 1834 + + «Eurytoma» sp.1 + + «Eurytoma» sp. 2 – + «Eurytoma» sp. 3 – + Sycophila biguttata (Swederus, 1795) + + Pteromalidae Caenacis inflexa (Ratzeburg, 1848) – + Hobbya stenonota (Ratzeburg, 1848) + – Pteromalus bedeguaris (Thomson, 1878) + + Torymidae Glyphomerus stigma (Fabricius, 1793) – + Torymus auratus (Müller, 1764) – + Torymus bedeguaris (Linnaeus, 1758) + + Ichneumonidae Exeristes roborator (Fabricius, 1793) – + Orthopelma mediator (Thunberg, 1882) + + Cynipidae Periclistus brandtii (Ratzeburg, 1831) + –

* The East-Azarbaijan province data are compiled from Lotfalizadeh et al. (2006) and Lotfalizadeh et al. (2009).

Hymenopterous parasitoids community of Diplolepis fructuum in Iran 127

total of four eulophid species from three genera (Aulogymnus Förster, Aprostocetus Westwood and Baryscapus Förster) have been recorded on Diplole- pis galls according to Askew et al. (2006b) without any report of D. fructuum. Lotfalizadeh et al. (2006) found two species in the Northwest of Iran (see Table 1). Eulophid species in the gall communities of Diplolepis species are represented by 22.9 % (Askew et al. 2006b).

Eupelmidae Figure 1. Usual form of Diplolepis fructuum galls Eupelmus urozonus Dalman, 1820 on Rosa spp.. Materials examined: Kerman, Kouh-Payeh Moun-

tains, N30° 31' 55'' E 57° 13' 44'', 2515 m, 2 May 2009, M. Rajabi, 1♀. Kerman, Sar-Bizhan Moun- tains, N 29° 08' 09'' E 57° 30' 01'', 2705 m, 28 April 2010, M. Rajabi, 3♀♀. Based on Lotfalizadeh et al. (2006) two Euple- mus species have been recorded to be associated with D. fructuum from which, Eupelmus urozonus has been found in the reared material from Ker- man province (see Table 1). However, Moham- madi et al. (2011) added two other Eupelmus spe- cies, E. microzonus Förster, 1860 and E. vesicularis (Retzius, 1783), to this community.

Only four species of eupelmids have been Figure 2. Dissected gall of rare form of D. fructuum. reared from Diplolepis species in the Western Palaearctic region (Askew et al. 2006b). They are the external envelope. represented by 8.6 % in the Diplolepis parasitoid communities. This percent varies in the parasitoid Cynipidae fauna of different cynipid tribes because it is a Periclistus brandtii (Ratzeburg, 1831) very polyphagous family. Materials examined: Kerman, Sar-Bizhan Moun- tains, N 29° 08' 09'' E 57° 30' 01'', 2705 m, 28 April Eurytomidae 2010, M. Rajabi, 1♀. Aximopsis collina (Zerova, 1984) This species belongs to the subfamily Cynipi- Materials examined: Kerman, Sar-Cheshmeh nae and tribe Synergini. This is the first record of Mountains, N 29° 59' 52'' E 55° 51' 26'', 2564 m, 17 this species as an in D. fructuum, earlier it April 2008, M. Rajabi, 1♂. was reported only from Diplolepis mayri and D. Eurytoma adleriae Zerova, 1995 rosae (Pujade-Villar et al. 2003, Askew et al. 2006b). Materials examined: Kerman, Sar-Cheshmeh Only one specimen of P. brandtii was reared as as- Mountains, N 29° 59' 52'' E 55° 51' 26'', 2564 m, 17 sociated species with D. fructuum, while it was not April 2008, M. Rajabi, 10♀♀ & 7♂♂. Kerman, Kouh- reported from materials collected in the North of Payeh Mountains, N 30° 31' 55'' E 57° 13' 44'', 2515 Iran (Lotfalizadeh et al. 2006). m, 2 May 2009, M. Rajabi, 15♀♀ & 24 ♂♂.

Eulophidae Eurytoma caninae Lotfalizadeh & Delvare, 2007 Aprostocetus eurytomae (Nees, 1834) Materials examined: Kerman, Sar-Cheshmeh Materials examined: Kerman, Kouh-Payeh Moun- Mountains, N 29° 59' 52'' E 55° 51' 26'', 2564 m, 17 tains, N30° 31' 55'' E 57° 13' 44'', 2515 m, 2 May April 2008, M. Rajabi, 1♀ & 1♂. Kerman, Sar- 2009, M. Rajabi, 1♀. Kerman, Sar-Bizhan Moun- Bizhan Mountains, N 29° 08' 09'' E 57° 30' 01'', 2705 tains, N 29° 08' 09'' E 57° 30' 01'', 2705 m, 28 April m, 28 April 2010, M. Rajabi, 6♀♀ & 1♂.

2010, M. Rajabi, 10♀♀. Eurytoma cynipicola Zerova, 1976 Only A. eurytomae was found in this study. A Materials examined: Kerman, Sar-Bizhan Moun- 128 Lotfalizadeh, H. et al. tains, N 29° 08' 09'' E 57° 30' 01'', 2705 m, 28 April on oak. It occurs in the Eastern Europe (Bulgaria, 2010, M. Rajabi, 5♀♀ & 3♂♂. Hungary and Ukraine) (Melika et al. 2001, Zerova

Eurytoma rosae Nees, 1834 et al. 2006). Materials examined: Kerman, Sar-Bizhan Moun- The diagnostic characters of E. adleriae and E. tains, N 29° 08' 09'' E 57° 30' 01'', 2705 m, 28 April caninae have been discussed by Lotfalizadeh et al. 2010, M. Rajabi, 5♀♀. (2007). The head of E. adleriae is longer in dorsal view (1.7 times as broad as long) than that of E. Eurytoma sp. (group pistaciae) caninae and its lower face is partly punctured (Fig. Materials examined: Kerman, Sar-Cheshmeh 5). Moreover, in the former species on the gaster, Mountains, N 29° 59' 52'' E 55° 51' 26'', 2564 m, 17 T4 completely covers T5 laterally and is strongly April 2008, M. Rajabi, 3♀♀. emarginated dorsally on its posterior margin. Sycophila biguttata (Swederus, 1795) Four species belonging to two genera (Eury- Materials examined: Kerman, Sar-Cheshmeh toma Illiger and Sycophila Walker) have been re- Mountains, N 29° 59' 52'' E 55° 51' 26'', 2564 m, 17 corded on Diplolepis species in the Western Palae- April 2008, M. Rajabi, 2♂♂. arctic (Askew et al. 2006b). We listed nine eury-

Six species of Eurytomidae were found in this tomid species belonging to three genera (see Table study. Two species, Eurytoma cynipicola Zerova, 2). Askew et al. (2006b) estimated representation 1976 and Eurytoma adleriae Zerova, 1995 which be- percentage of eurytomids on Diplolepidini as 14.3 long to the rosae species group (Lotfalizadeh et al. %. 2007) are reported for the first time for the Iranian Pteromalidae fauna. Pteromalus bedeguaris (Linnaeus, 1758) Eurytoma cynipicola was reported earlier as a Materials examined: Kerman, Kouh-Payeh Moun- parasitoid of Diplolepis galls, while E. adleriae has tains, N30° 31' 55'' E 57° 13' 44'', 2515 m, 2 May been previously known only from oak galls (Ze- 2009, M. Rajabi, 17♀♀ & 20♂♂. rova 1995). Four genera, Aximopsis (one species), Eurytoma Hobbya stenonota (Ratzeburg, 1848) (eight species), Sycophila (two species) and Tenui- Materials examined: Kerman, Kouh-Payeh Moun- petiolus (one species), within Eurytomidae have tains, N30° 31' 55'' E 57° 13' 44'', 2515 m, 2 May been reported as associated with Diplolepis in the 2009, M. Rajabi, 16♀♀. Palaearctic (Noyes 2010, Lotfalizadeh et al. 2006). Two pteromalids, Caenacis inflexa (Ratzeburg, Earlier six eurytomid species associated with rose 1848) and Pteromalus bedeguaris (Linnaeus, 1758), galls have been listed for Iran including a newly have been recorded as associated with D. fructuum described species (Lotfalizadeh et al. 2007, Lotfali- in the Palaearctic region (Lotfalizadeh et al. 2006). zadeh et al. 2006, Rakhshani et al. 2003). Beside We added another pteromalid, Hobbya stenonota them, E. cynipicola Zerova, 1976 (on D. mayri and (Ratzeburg, 1848) that has already been recorded D. magna), E. nikolskayae Zerova, 1989 (on D. mayri) as a rare species on D. mayri (Askew et al. 2006a), and E. parvula Thomson, 1876 (on D. rosae) have nevertheless it is obtained usually from oak galls. been reported from the Palaearctic region (Lotfali- In Kerman Province it was observed as a common zadeh et al. 2006, Zerova & Djakontshuk 1976). species. Association of H. stenonota and D. mayri Eurytoma cynipicola (Fig. 6) is reared for the has been reported only from Iran (Askew et al. first time from D. fructuum galls on Rosa beggeriana 2006a) while the present study shows that beside in the present study and is a new record for the D. mayri, D. fructuum can also serve as a host for Iranian fauna. Within the rosae group of Eurytoma, this species. This species has recently been re- antennal flagellum of E. cynipicola males are com- ported on oak from Iran (Lotfalizadeh & Gharali pletely different, showing very elongate segments 2008). (Fig. 8) (Zerova 1995: Fig. 12 of plate 45, p. 359). Pteromalidae are evenly represented in galls Also its antennal segments are yellowish-brown of all tribes of Cynipidae but seven pteromalids (Figs 8 & 9). have been reared on Diplolepis galls (Askew et al. Eurytoma adleriae Zerova, 1995 (Fig. 3) was also 2006b). reared from D. fructuum galls for the first time. Ze- Torymidae rova (1995) described this species based on mate- Torymus bedeguaris (Linnaeus, 1758) rials collected from Ukraine. This species is associ- Materials examined: Kerman, Sar-Cheshmeh ated with Adleria conglomerata (Hym.: Cynipidae) Mountains, N 29° 59' 52'' E 55° 51' 26'', 2564 m, 17 Hymenopterous parasitoids community of Diplolepis fructuum in Iran 129

Figures 3-5. (3.) Eurytoma adleriae in lateral view, female; (4.) Forewing of E. adleriae; (5.) Head of E. adleriae in frontal view, female.

Figures 6-10. (6.) Eurytoma cynipicola in lateral view, female; (7.) Female antenna of E. cynipicola; (8.) Male antenna of E. cynipicola; (9.) Head of E. cynipicola in lateral view, female; (10.) Head of E. cynipicola in frontal view, female. 130 Lotfalizadeh, H. et al.

Table 2. Associated Hymenopterous community of Diplolepis fructuum in Iran.

Parasitoid Distribution in Iran References Eulophidae Aprostocetus eurytomae (Nees, 1834) East-Azarbaijan, Kerman Lotfalizadeh et al. (2006), This paper Aprostocetus aurantiacus (Ratzeburg, 1852) East-Azarbaijan Lotfalizadeh et al. (2006) Eupelmidae Eupelmus fulvipes Förster, 1860 East-Azarbaijan Lotfalizadeh et al. (2006) Eupelmus impennis (Nikol'skaya, 1952) West-Azarbaijan Mohammadi et al. (2011) Eupelmus urozonus Dalman, 1820 East-Azarbaijan, Kerman Rakhshani et al. (2003), Lotfalizadeh et al. (2006), This paper Eupelmus vesicularis (Retzius, 1783) West-Azarbaijan Mohammadi et al. (2011) Eurytomidae Aximopsis collina (Zerova, 1984) East-Azarbaijan, Kerman Lotfalizadeh et al. (2006), This paper Eurytoma adleriae Zerova, 1995 Kerman This paper Eurytoma caninae Lotfalizadeh & Delvare, 2007 East-Azarbaijan, Kerman Lotfalizadeh et al. (2006), This paper Eurytoma cynipicola Zerova, 1976 Kerman This paper «Eurytoma» sp.1 East-Azarbaijan, Kerman Lotfalizadeh et al. (2006), This paper «Eurytoma» sp. 2 East-Azarbaijan, Lotfalizadeh et al. (2006) «Eurytoma» sp. 3 East-Azarbaijan, Lotfalizadeh et al. (2006), This paper Eurytoma rosae Nees, 1834 East-Azarbaijan, Kerman Rakhshani et al. (2003), Lotfalizadeh et al. (2006), This paper Sycophila biguttata (Swederus, 1795) East-Azarbaijan, Kerman Lotfalizadeh et al. (2006), This paper Pteromlaidae Caenacis inflexa (Ratzeburg, 1848) East-Azarbaijan Lotfalizadeh et al. (2006) Pteromalus bedeguaris (Linnaeus, 1758) East-Azarbaijan, Kerman Rakhshani et al. (2003), Lotfalizadeh et al. (2006), This paper Hobbya stenonota (Ratzeburg, 1848) Kerman This paper Torymidae Glyphomerus stigma (Fabricius, 1793) East-Azarbaijan, Rakhshani et al. (2003), Lotfalizadeh et al. (2006) Torymus auratus (Müller, 1764) East-Azarbaijan, Lotfalizadeh et al. (2006) Torymus bedeguaris (Linnaeus, 1758) East-Azarbaijan, Kerman Rakhshani et al. (2003), Lotfalizadeh et al. (2006), This paper Icheneumonidae Orthopelma mediator (Thunberg, 1882) East-Azarbaijan, Kerman Lotfalizadeh et al. (2006), This paper Exeristes roborator (Fabricius, 1793) East-Azarbaijan Talebi et al. (2004), Lotfalizadeh et al. (2009) Cynipidae Periclistus brandtii (Ratzeburg, 1831) Kerman This paper

April 2008, M. Rajabi, 8♀♀ & 1♂. Kerman, Kouh- m, 2 May 2009, M. Rajabi, 2♀♀. Kerman, Sar- Payeh Mountains, N30° 31' 55'' E 57° 13' 44'', 2515 Bizhan Mountains, N 29° 08' 09'' E 57° 30' 01'', 2705 m, 2 May 2009, M. Rajabi, 50♀♀ & 87♂♂. m, 28 April 2010, M. Rajabi, 7♀♀ & 1♂. Lotfalizadeh et al. (2006) reported three This ichneumonid species is a common species torymid species from two genera on D. fructuum in on different species of Diplolepis and widely dis- the Northwest of Iran. Nine species of Torymidae tributed in the Northwest of Iran (Lotfalizadeh et belonging to two genera (Glyphomerus Förster and al. 2006). Beside this species, Exeristes roborator Torymus Dalman), with 25.7 % representation, are (Fabricius, 1793) has been found in East- the most abundant species in Diplolepidini galls Azarbaijan (Northwest of Iran) (Lotfalizadeh et al. (Askew et al. 2006b). 2009).

Ichneumonidae

Orthopelma mediator (Thunberg, 1882)

Materials examined: Kerman, Sar-Cheshmeh Acknowledgment. We thank Dr. G. Melika (Kőszeg, Mountains, N 29° 59' 52'' E 55° 51' 26'', 2564 m, 17 Hungary) for identification of Diplolepis fructuum. April 2008, M. Rajabi, 2♀♀ & 2♂♂. Kerman, Kouh- Payeh Mountains, N30° 31' 55'' E 57° 13' 44'', 2515 Hymenopterous parasitoids community of Diplolepis fructuum in Iran 131

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