Biologia 68/5: 966—973, 2013 Section Zoology DOI: 10.2478/s11756-013-0234-y

Aphid (: : ) in cultivated and non-cultivated areas of Markazi Province, Iran

Mahmoud Alikhani1,AliRezwani2,PetrStarý3, Nickolas G. Kavallieratos 4 &EhsanRakhshani5*

1Department of Entomology, Faculty of Agriculture, Islamic Azad University, Arak Branch, Mail box: 38135-567,I.R.Iran; e-mail: [email protected] 2Department of Agricultural Entomology, Iranian Research Institute of Plant Protection, Tehran 1454-19395 Iran, e-mail: [email protected] 3Institute of Entomology, Academy of Sciences of the Czech Republic, Branišovská 31, 37005 České Budějovice, Czech Republic; e-mail: [email protected] 4Laboratory of Agricultural Entomology, Department of Entomology and Agricultural Zoology, Benaki Phytopathological Institute, 8 Stefanou Delta str., 14561, Kifissia, Attica, Greece; e-mail: nick [email protected] 5Department of Plant Protection, College of Agriculture, University of Zabol, 98615–538,I.R.Iran; e-mail: [email protected]

Abstract: The fauna of parasitoids (Hymenoptera: Braconidae: Aphidiinae), as well as their diversity and tritrophic (-host aphid-host plant) associations in cultivated and non-cultivated areas of Markazi province, was studied during 2004–2009. Thirty species of Aphidiinae belonging to 9 genera were identified. There are presented, in total, 73 associations with 32 host occurring on 42 host plants. Five parasitoid-aphid associations are newly recorded from Iran. cardui (Marshall) is newly recorded for the fauna of Iran. Lysiphlebus fabarum (Marshall) and (M’Intosh) were the most abundant species in non-cultivated (72.96%) and cultivated (41.17%) areas, respectively. In the non-cultivated areas, L. fabarum was found on eight aphid species, while in cultivated areas it was only found on Aphis craccivora Koch. In cultivated areas, Sitobion avenae (F.) has the greatest diversity of parasitoids (Shanon-Weiner H = 0.875) whereas in non-cultivated areas the greatest diversity of parasitoids was recorded upon Acyrthosiphon pisum (Harris) (Shanon-Weiner H = 1.149). Significant differences were found between diversity of two ecosystems based on the overall diversity indices. Both species diversity and evenness were greater in cultivated ecosystems. The results are discussed in relation to the over-all parasitoid-aphid-plant associations in the area. Key words: Aphidiinae; diversity; tritrophic associations; cultivated areas; non-cultivated areas; Iran; Lysiphlebus cardui

Introduction 1991). The subfamily Aphidiinae includes about 60 gen- era and subgenera and over than 400 species worldwide Aphids are categorized as serious pests causing dam- (Starý 1988). All of them are exclusively solitary en- ages in different crops, both directly and indirectly, doparasitoids of aphids (Starý 1970). i.e., stunting, leaf curling, yellowing premature death Iran has been classified as a cross-road of flora of leaves, twisting of growing shoots, injecting toxic and fauna, including aphids (Starý et al. 2000). The salivary secretions during feeding, secreting honeydew, geographic position and landscape of Iran yields a which cause the growth of sooty molds on the leaf sur- high species biodiversity which can be manifested in face (Blackman & Eastop 2006; Jouraeva et al. 2006; the composition of the fauna both in the natural van Emden & Harrington 2007). and cultivated ecosystems as well as in their interac- However, aphids have a great number of various tions. Research not only at the faunal level, but also natural enemies known over the world. Among in- at the trophic levels is required on the background sect parasitoids, all species in the subfamily Aphidi- of broader ecological studies at least at the ecosys- inae (Hym.: Braconidae) and some genera in the family tem levels (Tomanovi´c et al. 2009). Aphids and as- Aphelinidae (Hym.: Chalcidoidea) develop as endopara- sociated food webs represent one of the related top- sitoids of aphids (van Emden & Harrington 2007). They ics contributing to such approaches. The knowledge have an important role in control of aphid population on about local fauna of the aphid parasitoids and their different crop plants (Hughes 1989; Hagvar & Hofsvang trophic associations has also significant ecological in-

* Corresponding author

c 2013 Institute of Zoology, Slovak Academy of Sciences Aphid parasitoids of Markazi province 967

Fig. 1. Map of the sampling localities at Markazi province. The numbers on the map are listed to the right of the figure along with the coordinated (DM) and altitudes in meters (m) above mean sea level (AMSL). formation about potential biocontrol agents (Starý information about host range pattern and distribution 2006). of those aphidiines occurring in a wide range of habitats Starý et al. (2000) reviewed the Aphidiinae species in the Markazi province of Iran. and their host association in Iran and listed 49 species. Since then, further investigations have been performed Material and methods on the taxonomy and faunal diversity of Aphidiinae in Iran (Starý et al. 2005; Rakhshani et al. 2005a, Samples of cultivated and non-cultivated plants bearing b, c, 2006, 2007a, b, 2008a, b; Tomanovi´cetal. aphid colonies, were collected from 21 locations in Markazi 2007; Kazemzadeh et al. 2009; Barahoei et al. 2010; province (Fig. 1), over 2004–2009. Samplings were per- formed in discrete but in a non-selective pattern. The col- Mossadegh et al. 2011). lected samples were directly placed within transparent plas- Markazi province is located at eastern junction tic boxes and covered with mesh for ventilation. At the lab- point of Alborz and Zagros Mountains with altitudi- oratory, samples were subdivided, with part used to obtain nal range of 1000–2500 m a.s.l. Various field crops voucher aphids for identification and part held for rearing of and fruit orchards, as well as large scale nurseries of parasitoids. Voucher aphids were preserved in a solution of 90% ethanol and 75% lactic acid at a ratio of 2:1 (Eastop & ornamental plants are located at this area, neighbor- ◦ ing with the plains and high mountains covered with van Emden 1972). The boxes were held at 22.5 Cuntilpar- natural vegetation. Given that the available informa- asitoid emergence. The rearing boxes were checked daily for emergence of adult parasitoids and the emerged were tion about Aphidiinae of the above province is limited collected using an aspirator and directly dropped into the and only sporadically can be found in previous studies 75% ethanol for preservation. Parasitoid adults were point- (Rakhshani et al. 2005b, 2007a, 2008a). and usually slide-mounted for detailed examination. Spec- The determination of the tritrophic associations imens for slides were washed in distilled water, boiled in for each parasitoid species brings the information to 10% KOH for about two minutes, re-washed, then placed in a higher taxonomical ecological level. The knowledge of a drop of Faure-Berlese medium (Krantz 1978) for dissection the host aphid species is often rather useful in the de- or whole mounting. The external morphology of parasitoid termination of the parasitoid species identity and even- was studied using a NIKON SMZ645 stereomicroscope and tual detection of the biotypes. Also, information on a NIKON Eclipse E200 microscope. Aphid nomenclature follows Remaudiére & Remaudiére (1997). The Aphidiinae tritrophic associations is a key background in the de- specimens are deposited in the collection of Depart- tection of the trophic interactions in the communities ment of Entomology, Islamic Azad University, Arak branch. and in biodiversity studies. The aim of the present con- New records of parasitoid species and parasitoid-host aphid tribution is to identify the aphidiines attacking aphids associations are indicated with an asterisk (*) and a dagger feeding on crop or non-crop plants as well as to provide (†), respectively. 968 M. Alikhani et al.

To compare the diversity of aphid parasitoids in two rhopalosiphi De Stefani-Perez, 1902 cultivated and non-cultivated ecosystems, the parasitoid Metopolophium dirhodum on Triticum aestivum, Deli-

specimens, that emerged from each aphid species were

 ¾  jan, 25.IV.2006, (8¾,5 ); Saveh, 15.V.2005, (5 ,6 ); counted and sorted based on the species. The regional di- Schizaphis graminum (Rondani, 1852) on Triticum aes-

versity of the parasitoid species and diversity of the para-  tivum, Saveh, 14.V.2005, (2 ¾,2 ); Sitobion avenae on

sitoid complex of each aphid species at the two ecosystems  Triticum aestivum, Saveh, 15.V.2005, (8¾,5 ). were analyzed based on Simpson D and Shanon-Weiner H indices separately (Magurran, 2004), using SDR version 4.0 (Seaby & Henderson 2006). Additionally, the species even- Aphidius rosae Haliday, 1834

ness was also assessed, considering the number of individuals Macrosiphum rosae (L., 1758) on Rosa damascena,Ma-  per species. The Simpson E and Pielou J indices were used hallat, 20.IV.2007, (6¾,2 ). for analyzing the species evenness. Randomization test was based on Solow (1993) with 10000 replications to assess the Aphidius salicis Haliday, 1834

Delta values for each diversity index. Cavariella aegopodii (Scopoli, 1763) on Apiaceae host  plant, Shanaq, 05.VI.2009, (20¾,6 ) Results Aphidius smithi Sharma and Subba Rao, 1959

Thirty species of aphidiinae belong to nine genera were Acyrthosiphon pisum on Vicia villosa, Saveh, 14.V.  found. In total, 73 associations with 32 host aphids oc- 2005, (7¾,11 ). curring on 42 host plants are presented. Lysiphlebus cardui (Marshall, 1896) is newly recorded for the fauna Aphidius transcaspicus Telenga, 1958

of Iran. Hyalopterus pruni (Geoffroy, 1762) on Prunus armeni-  aca, Tafresh, 10.V.2007, (19¾,14 ). Parasitoid-aphid-plant associations Aphidius uzbekistanicus Luzhetzki, 1960

Adialytus salicaphis (Fitch, 1855) Schizaphis graminum on Avena fatua, Gavar, 11.V. 

Chaitophorus pakistanicus Hille Ris Lambers, 1966 on 2005, (14¾,16); Sitobion avenae on Triticum aes-

 ¾  Salix alba, Bazeneh, 18.VI.2009, (26 ¾,3 ); Chaitopho- tivum, Saveh, 15.V.2005, (12 ,5 ).

rus vitellinae (Schrank, 1801) on Salix alba, Mahallat,  22.IV.2005, (5¾,4 ). acalephae (Marshall, 1896)

Aphis craccivora Koch, 1854 on Robinia pseudacacia,  Aphidius colemani Viereck, 1912 Arak, 01.VII.2009, 12.V.2009, (7¾,4 ); on Medicago †

Metopolophium dirhodum (Walker, 1849) on Triticum sativa, Mohajeran, 28.V.2009, (2¾).  aestivum, Delijan, 25.IV.2006, (3¾,1 ). Binodoxys angelicae (Haliday, 1833)

Aphidius eadyi Starý, Gonzalez and Hall, 1980 Aphis fabae fabae Scopoli, 1763 on Vicia faba, Arak, 

Acyrthosiphon pisum (Harris, 1776) on Vicia villosa, 29.V.2004, (32¾,19 ); Aphis fabae solanella Theobald,

 ¾  Saveh, 14.V.2005, (8¾,9 ). 1914 on Solanum nigrum, Saveh, 12.V.2005, (17 ,13 ).

Aphidius ervi Haliday, 1834 Binodoxys brevicornis (Haliday, 1833)

Acyrthosiphon pisum on Vicia villosa, Saveh, 14.V.2005, Cavariella aegopodii (Scopoli, 1763) on Salix alba,Ma-

 ¾  (4 ¾ 2 ); Sitobion avenae (F., 1775) on Triticum aes- hallat, 22.IV.2005, (2 ,1 ).

tivum, Saveh, 15.V.2005, (2). Diaeretiella rapae (M’Intosh, 1855) Aphidius funebris Mackauer, 1961 Aphis fabae fabae on Capsella bursa-pastoris,Hafteh,

Uroleucon sp. on Centaurea iberica, Mohajeran, 27.V. 07.V.2009, (1¾); Brevicoryne brassicae (L., 1758) on 

2009, (16¾,5 ). Brassica napus var. oleifera, Gavkhaneh, 18.IV.2009,

 ¾ 

(46 ¾,11); Sarsakhtie Paein, 04.VI.2009, (3 ,2);  Aphidius matricariae Haliday, 1834 Shahrjerd, 23.IV.2009, (74¾,13); on Descurainia

Aphis punicae Passerini, 1863 on Punica granatum sophia, Alborz, 27.V.2009, (1¾); on Brassica oleraceae,

¾  var. sativa, Mohajeran, 28.V.2009, (1¾); Brachycaudus Arak, 23.IV.2009, (378 ,92 ); Diuraphis noxia Kurd-

tragopogonis (Kaltenbach, 1843) on Tragopogon grami- jumov, 1913 on Triticum aestivum, Delijan, 25.IV.2006,

 † ¾  ¾  † nifolius, Arak, 16.IV.2009, (6¾,1); Ovatus cratae- (5 ,6); Saveh, 14.V.2005, (14 ,12); Dysaphis

garius (Walker, 1850) on Cydonia oblonga, Mohajeran, devecta (Walker, 1849) on Malus orientalis,Hafteh,

 ¾ 28.V.2009, (10¾,2 ). 07.V.2009, (1 ).

Aphidius persicus Rakhshani and Starý, 2006 Ephedrus niger Gautier, Bonnamour and Gaumont,

Uroleucon chondrillae (Nevsky, 1929) on Chondrilla 1929

 †

juncea, Mahallat, 14.IV.2005, (16¾,9); Uroleucon Macrosiphoniella sanborni (Gillette, 1908) on Chrysan- 

jaceae (L., 1758) on Centaurea virgata ssp. sequarrosa, themum morifolium, Arak, 29.V.2004, (5¾,2 ); Uroleu-  Hafteh, 07.V.2009, (3¾,1 ). con chondrillae on Chondrilla juncea, Mahallat, 14.IV.

Aphid parasitoids of Markazi province 969

 ¾ 2005, (10¾,6 ). craccivora on Cardaria draba, Hafteh, 07.V.2009, (1 ,

2 ); Aphis fabae solanella on Solanum nigrum,Saveh, 

Ephedrus persicae Froggatt, 1904 12.V.2005, (6¾,2 ); Hyalopterus pruni on Prunus ar- 

Brachycaudus amygdalinus (Schouteden, 1905) on Pru- meniaca, Tafresh, 10.V.2007, (4¾,2); Macrosiphum

 ¾ nus amygdalinus, Gavkhaneh, 18.IV.2009, (1¾,6); rosae on Rosa damascena, Mahallat, 20.IV.2007, (3 ,

Brachycaudus helichrysi (Kaltenbach, 1843) on Prunus 1 ); Rhopalosiphum maidis (Fitch, 1856) on Zea mays,

† ¾ 

domestica, Hafteh, 07.V.2009, (2¾); Dysaphis devecta Saveh, 15.V.2005, (13 ,6 ).  on Malus orientalis, Hafteh, 07.V.2009, (17¾,10);

Schizaphis graminum on Triticum aestivum,Saveh, yomenae Takada, 1968 

14.V.2005, (5¾,1 ). Uroleucon chondrillae on Chondrilla juncea, Mahallat,  14.IV.2005, (3¾,2 ); Uroleucon compositae (Theobald,

Lipolexis gracilis (Forster, 1862) 1915) on Carthamus tinctorius, Kazaze Olya, 17.IX.  Aphis salviae Walker, 1852 on Salvia nemorosa, Baze- 2009, (26¾,9 ).

neh, 07.V.2009, (1¾) Trioxys asiaticus Telenga, 1953

*Lysiphlebus cardui (Marshall, 1896) Acyrthosiphon gossypii on Sophora alopecuroides,Ma-  Aphis fabae cirsiiacanthoidis Scopoli, 1763 on Cirsium hallat, 22.IV.2005, (3¾,4 ).

arvense (L.), Mahallat, 14.V.2005, (3¾) Trioxys complanatus Quilis, 1931

Lysiphlebus confusus Tremblay and Eady, 1978 Therioaphis trifolii on Medicago sativa, Saveh, 14.IX.

¾  Aphis fabae fabae on Vicia faba, Arak, 29.V.2004, (19¾, 2004, (31 ,35 ).

8 ). Trioxys pallidus (Haliday, 1834) Lysiphlebus fabarum (Marshall, 1896) Chromaphis juglandicola (Kaltenbach, 1843) on Juglans

Aphis craccivora on Alhagi maurorum, Mahallat, 25.IV. regia, Arak, 18.VI.2009, (9¾); Tinocallis sp. on Ulmus

 ¾ 

2005, (131¾,87 ); on Medicago sativa, Arak, 04.V.2009, sp., Arak, 23.VI.2009, (1 ,1 ).

¾ 

(3 ¾); Mohajeran, 28.V.2009, (59 ,12); on Robinia 

pseudacacia, Arak, 29.V.2004, (27¾,22 ), 12.V.2009, Diversity of aphid parasitoids  (15 ¾,1 ); on Sophora pachycarpa, Mohajeran, 14.V. Frequency and diversity of aphid parasitoids associ-

2009, (1¾); on Onobrychis altissima, Far, 29.V.2009, ated with various host aphid species were accessed 

(5 ¾,6 ); on Astragalus ovinus, Chepeqli, 02.VI.2009, separately within cultivated and non-cultivated areas. 

(49 ¾,19); on Astragalus brevidens, Shanaq, 05.VI. Based on the nature of our discrete sampling methods,

 ¾  2009, (5¾,1 ); on Astragalus podocarpus, (158 42 ), few aphid species were found to share both ecosystems.

Shanaq, 05.VI.2009; on Vicia sativa, Shanaq, 05.VI. This can be directly resulting by the host specificity of 

2009, (363¾,87 ); Aphis fabae cirsiiacanthoidis on Cir- aphids which were in association with their specific host  sium arvense, Mahllat, 14.V.2005, (12¾,16 ); Shanaq, plants in different ecosystems. At the same time, few

05.VI.2009, (16¾); Aphis fabae fabae on Capsella bursa- aphids including A. craccivora, A. fabae fabae, B. bras-

pastoris, Hafteh, 07.V.2009, (1¾); on Torilis lepto- sicae and S. graminum were found in both ecosystems

phylla, Toure, 23.V.2009, (2¾); Aphis fabae solanella on sharing either the same or a different parasitoid com-  Solanum nigrum, Saveh, 12.V.2005, (15 ¾ 11 ); Aphis plex. Among parasitoids, L. fabarum and D. rapae were

umbrella (B¨orner, 1950) on Althaea sp., Mehdiabad, the most abundant species in non-cultivated (72.96%) 

25.VI.2009, (46¾ 10 ); Aphis sp. on Cousinia cylin- and cultivated (41.17%) areas, respectively. In non-  dracea, Shanaq, 05.VI.2009, (18¾,10 ); Brachycaudus cultivated areas, L. fabarum was found on eight aphid

cardui (L., 1758) on Cirsium arvense, Toure, 23.V.2009, species belonging to two genera, Aphis and Brachy- 

(50 ¾,16 ); on Borago officinalis, Mahallat, 22.IV.2005, caudus, while in cultivated areas it was found only on 

(6 ¾,8); Brachycaudus tragopogonis onTragopogon A. craccivora.AlargenumberofD. rapae was found 

graminifolius, Arak, 16.IV.2009, (5¾,2), Sarsakhtie on its two preferred host aphids, D. noxia and B. bras-  Paein, 04.VI.2009, (5¾,2 ). sicae in cultivated areas. Occurrence of this parasitoid in non-cultivated areas was rather limited (Table 2). Praon barbatum Mackauer, 1959 Diversity indices were used both for measuring the Acyrthosiphon pisum on Vicia villosa, Saveh, 14.V. parasitoid complexes of each aphid species (Tables 1

2005, (2¾). and 2) and comparing the cultivated and non-cultivated areas (Table 3). Praon exsoletum (Nees, 1811) In the cultivated areas the greatest diversity of par-

Therioaphis trifolii (Monell, 1882) on Medicago sativa, asitoids were found to be on S. avenae (Shanon-Weiner  14.IX.2004, Saveh, (22¾,14 ). H = 0.875), followed by S. graminum (Shanon-Weiner H = 0.673), while in non-cultivated areas A. pisum pre- Praon volucre (Haliday, 1833) sented the greatest diversity of parasitoids (Shanon-

Acyrthosiphon gossypii Mordvilko, 1914 on Sophora Weiner H = 1.149), followed by A. fabae solanella  alopecuroides, Mahallat, 22.IV.2005, (4¾,3); Aphis (Shanon-Weiner H = 0.981). The Simpson D generally 970 M. Alikhani et al.

Table 1. Occurrence and frequency of the aphid parasitoids on their host aphids in cultivated areas of Markazi province.

Diversity Parasitoids indices Host aphids H D A. colemani A. ervi A. matricariae A. rhopalosiphi A. rosae A. transcaspicus A. uzbekistanicus B. acalephae B. angelicae D. rapae E. niger E. persicus L. confusus L. fabarum P. exsoletum P. volucre P. yomenae T. complanatus T. pallidus Shanon-Weiner Simpson

A. craccivora –––––––2– – –––517–––––0.0251.008 A. fabae fabae ––––––––51– ––27––––––0.6451.847 A. punicae ––1–––––– – ––– – –––––0.0001.000 B. amygdalinus ––––––––– – –7– – –––––0.0001.000 B. helichrysi ––––––––– – –2– – –––––0.0001.000 B. brassicae –––––––––619––– – –––––0.0001.000 C. juglandicola ––––––––– – ––– – ––––90.0001.000 D. noxia –––––––––37––– – –––––0.0001.000 D. devecta ––––––––– 1 –27–– –––––0.1541.077 H. pruni –––––33–––– ––– – –6–––0.4291.365 M. sanborni ––––––––– – 7–– – –––––0.0001.000 M. rosae ––––8–––– – ––– – –4–––0.6361.941 M. dirhodum 4––24–––––– ––– – –––––0.4101.340 O. crataegarius ––12–––––– – ––– – –––––0.0001.000 R. maidis ––––––––– – ––– – –19–––0.0001.000 S. graminum –––4––––– – –6– – –––––0.6732.143 S. avenae –2–13––17––– ––– – –––––0.8752.307 T. trifolii ––––––––– – ––– –36––66–0.6491.865 U. compositae ––––––––– – ––– – ––35––0.0001.000

Relative 0.25 0.12 0.81 2.57 0.50 2.07 1.06 0.13 3.20 41.17 0.44 2.63 1.69 32.39 2.26 1.82 2.19 4.14 0.56 abundance (%)

Total number of parasitoids: 1596 specimens also supported this situation. On the other hand, only a icae, B. brevicornis, E. niger, L. cardui, P. barbatum, single parasitoid species (Shanon-Weiner H =0,D =1) P. exsoletum, P. yomenae, T. asiaticus, T. complana- was found on many aphids in both ecosystems (Tables tus, T. pallidus) and broadly oligophagous species (A. 1 and 2). Significant differences were found between di- colemani, A. ervi, A. matricariae, D. rapae, E. per- versity of two ecosystems based on the overall diversity sicae, L. gracilis, L. confusus, L. fabarum, P. volu- indices (Table 3). Species diversity and evenness were cre) (Kavallieratos et al. 2004; Starý 2006). On the both greater in cultivated ecosystems. other hand, Acyrthosiphon and Urolecuon species were attacked by the specific parasitoid guilds which com- Discussion prise both groups of parasitoids (Rakhshani et al. 2006, 2007b, 2012; González et al. 1978). In addition, the ce- Lysiphlebus cardui is newly detected in Iran in associa- real aphids had a similar model of parasitoid guild, tion with A. fabae cirsiiacanthoidis on C. arvense.Ac- which was at least locally specific, as indicated by cording to Starý (1986a, 1999) L. cardui is a dominant Rakhshani et al. (2008b). parasitoid of this aphid and it often co-exists with L. In many cases, aphids were found to be para- fabarum on same host. Separation of these two closely sitized by a single parasitoid species as instances of related species is based on the setation of the hind legs, a strictly specific association (C. juglandicola/T. pal- but the complicated taxonomy of L. fabarum group lidus, B. brassicae/D. rapae, Chaitophorus spp./A. sal- puts the identity of this species under some doubts icaphis). On the other hand, there were aphids which (Belshaw et al. 1999). On the other hand, L. cardui is expected to have a wider range of parasitoid complex in considered as a European species with no records in cen- their natural habitats, however only a single parasitoid tral Asian area (Starý 1979). L. fabarum is frequently species was collected in the studied areas (A. salviae, found in association with different species of Aphis and A. umbrella, B. cardui parasitized by L. fabarum). Oc- Brachycaudus in the studied area. This species has also currence of such local dominance of a single parasitoid been recorded as the most abundant and dominant par- species can be the result of a short-term sampling, while asitoid of A. craccivora in Iran (Rakhshani et al. 2005a). long term studies can discover the “real” parasitoid The collected aphid parasitoids can be clearly cate- complexes in both ecosystems. gorized as narrowly oligophagous species (A. salicaphis, It has generally been found that more aphids A. eadyi, A. funebris, A. persicus, A. rosae, A. sali- and aphid parasitoids occurred in non-cultivated plants cis, A. smithi, A. transcapicus, B. acalephae, B. angel- than to the cultivated ones. This could be partially Aphid parasitoids of Markazi province 971

Table 2. Occurrence and frequency of aphid parasitoids on their host aphids in non–cultivated areas of Markazi province.

Diversity Parasitoids indices Host aphids H D Ad. salicaphis A. eadyi A. ervi A. funenris A. matricariae A. persicus A. salicis A. smithi A. uzbekistanicus B. acalephae B. angelicae B. brevicornis D. rapae E. niger L. gracilis L. cardui L. fabarum P. barbatum P. volucre P. yomenae T. asiaticus T. pallidus Shanon–Weiner Simpson

A. gossypii –––––––––––––––– – –7–7–0.6932.167 A. pisum –176––––18––––––––– 2––––1.1492.961 A. craccivora –––––––––11––––––553–3–––0.1281.051 A. fabae –––––––––––––––328–––––0.3181.220 cirsiiacanthoidis A. fabae fabae ––––––––––––1––– 3 –––––0.5622.000 A. fabae solanella ––––––––––30–––––26–8–––0.9812.558 A. salviae ––––––––––––––1– – –––––0.0001.000 A. umbrella ––––––––––––––––56–––––0.0001.000 Aphis sp. ––––––––––––––––28–––––0.0001.000 B. cardui ––––––––––––––––80–––––0.0001.000 B. tragopogonis ––––7–––––––––––14–––––0.6361.875 B. brassicae ––––––––––––1––– – –––––0.0001.000 C. aegopodii ––––––26––––3––––– –––––0.3331.238 C. pakistanicus 29–––––––––––––––– –––––0.0001.000 C. vitellinae 9––––––––––––––– – –––––0.0001.000 U. chondrillae –––––25–––––––16––– ––5––0.9392.407 U. jaceae –––––4–––––––––– – –––––0.0001.000 Uroleucon sp.–––21––––––––––––– –––––0.0001.000 S. graminum ––––––––30–––––––– –––––0.0001.000 Tinocallis sp.–––––––––––––––– – ––––20.0001.000

Relative 3.52 1.57 0.55 1.94 0.65 2.68 2.41 1.67 2.78 1.02 2.78 0.28 0.18 1.48 0.09 0.28 72.96 0.19 1.67 0.46 0.65 0.19 abundance (%)

Total number of parasitoids: 1080 specimens.

Table 3. Comparison of the diversity and evenness indices for the aphid parasitoid species within cultivated and non–cultivated areas.

Diversity indices Cultivated areas Non–cultivated areas Delta value

Shanon Weiner H 1.767 1.279 –0.4879* (1.697–1.827)** (1.170–1.370) Simpson D 3.620 1.819 –1.8009* (3.415–3.841) (1.702–1.947) Pielou J 0.515 0.373 0.1421* (0.494–0.531) (0.341—0.399) Simpson E 0.181 0.0866 0.0944* (0.173–0.204) (0.082–0.0980)

Species number 20 21 –

Explanations: * indicating significant difference at 5% level, ** 95% confidence limits. explained by the complex flora of the natural ecosys- hypothesis in the Markazi province. The knowledge on tems in comparison to those in the mono-cultured field pattern of distribution and the identity of the mem- crops and fruit orchards, as well as by absence of the ber of parasitoid guild, as well as the management of chemical pesticides in wild habitats. Similar results be- the non-crop habitats are the critical points in the im- tween crop and non-crop habitats have been reported provement of conservation of biological control (Starý by Tomanovi´c et al. (2009). Aphids occurring on non- 1986a; Kavallieratos et al. 2002; Havelka et al. 2012). cultivated plants have been considered as important Furthermore, the effect of agricultural intensifications reservoirs of common aphid parasitoids (Starý 1970, on the diversity, i.e., species richness and species even- 1986b; Starý & Pike 1998; Kavallieratos et al. 2002; ness should not be ignored (Tscharntke et al. 2005). Havelka et al. 2012). This situation is evident in the Yet, there is a great deal of evidence about how farm- present study in the case of Aphis spp. However, fur- ing practices influence species richness and abundance ther investigation is required in order to support this of taxa (Vickery et al. 2001; Firbank et al. 2003). In 972 M. Alikhani et al. many cases, the positive effects of agricultural (organic) for biological control of Acyrthosiphun pisum (Hom.: Aphidi- farming on diversity have been evidenced (Bengtsson et dae). Entomophaga 23: 239–248. DOI: 10.1007/BF02373098 al. 2005; Hole et al. 2005). Hagvar E.B. & Hofsvang T. 1991. Aphid parasitoids (Hy- menoptera: Aphidiidae): biology, host selection, and use in The higher values of parasitoids diversity origi- biological control. Biocontrol News and Information 12: 13– nated from the higher number of the recorded par- 41. asitoid individuals in cultivated areas than in non- Havelka J., Tomanovi´c Ž., Kavallieratos N.G., Rakhshani E., cultivated areas. Simpson’s E index is greatly affected Pons X., Pike K.S. & Starý P. 2012. Review and key to the world parasitoids (Hymenoptera: Braconidae: Aphidi- by the dominant species and has a low sensitivity to inae) of Aphis ruborum (Hemiptera: Aphididae) and its role the species richness (Magurran, 2004). In this case, as a reservoir. Ann. Entomol. Soc. Am. 105: 386–394. DOI: the great dominance of L. fabarum in non-cultivated http://dx.doi.org/10.1603/AN11108 ecosystems led to a vast reduction of evenness (0.0866) Hole D.G., Perkins A.J., Wilson J.D., Alexander I.H., Grice F. & Evans A.D. 2005. Does organic farming benefit biodiversity? compared to cultivated ecosystems (0.181). Shanon- Biol. Conserv. 122: 113–130. DOI: 10.1016/j.biocon.2004.07. Weiner index and its deviated evenness, Pielou J,are 018 sensitive to occurrence of the rare species (Pielou 1975), Hughes R.D. 1989. Biological control in the open field, pp. 167– resulting to values with smaller differences between two 198. In: Minks A.K. & Harrewijn P. (eds), Aphids, Their Biology, Natural Enemies and Control, Crop Pests, Vol. 2C, ecosystems. The desertic climate of the non-cultivated Elsevier, Amsterdam, 332 pp. ISBN: 0444427996. areas in Markazi province provides unfavorable condi- Jouraeva V.A., Johnson D.L., Hassett J.P., Nowak D.J., Shipu- tions for the development of plants due to lack of water nova N.A. & Barbarossa D. 2006. Role of sooty mold fungi sources. However, the agricultural areas are normally in accumulation of fine-particle-associated PAHs and met- als on deciduous leaves. Environ. Res. 102: 272–282. DOI: irrigated and the produced relative humidity favors the 10.1016/j.envres.2006.06.004 increase of numbers of aphids and consequently their Kavallieratos N.G., Stathas G.J., Athanassiou C.G. & Papadoulis parasitoids’ numbers. Long-term biodiversity studies G.T. 2002. 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Received August 24, 2012 Accepted June 6, 2013