Analele Ştiinţifice ale Universităţii Al.I. Cuza Iaşi, s. Biologie animală, Tom LI, 2005

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1 Analele Ştiinţifice ale Universităţii Al.I. Cuza Iaşi, s. Biologie animală, Tom LI, 2005 THE HYPERPARASITOID COMPLEX WHICH LIMITS THE ACTION OF THE PRIMARY PARASITOIDS OF THE PIERIDAE SPECIES (INSECTA: LEPIDOPTERA), DEFOLIATORS IN CABBAGE CROPS BY GABRIELA PATRICHE (COSTEA) 1, IONEL ANDRIESCU 2, GHEORGHE MUSTAŢĂ 2 Keywords: Pieridae, cabbage crops, hyperparasitoid complex, host parasitoid relationship The paper presents data about the reduction of the efficiency of the primary parasitoids controlling two species of Pieridae (Pieris brassicae L. and P. rapae L.) in the cabbage cultures from the South-Eastern Romania, by several hyperparasitoid species. Comparing the results with those obtained 30 years ago in Moldova province, we found that the intervention of the hyperparasitoid species increased, especially in the case of Pieris rapae. The most efficient hyperparasitoid species in controlling the primary parasitoids was Baryscapus galactopus Ratz. Four host-parasitoid relationships are new to science. Introduction Hyperparasitoids are secondary insect parasitoids that develop at the expense of a primary parasitoid, thereby representing a highly evolved fourth trophic level. Pieris brassicae and Pieris rapae (Pieridae) are some of the most frequent pests of cabbage crops alongside Mamestra brassicae Linné, 1758 (Noctuidae) and Plutella xylostella Linné, 1758 (Plutellidae). The identified hyperparasitoid species, especially for Pieris brassicae, were made for Romania s climate conditions, primarily Moldavia, 30 years ago (Mustaţă, 1973; Andriescu & coll ; Andriescu 1982). This paper presents the hyperparasitoid complex relevant for Pieridae species, pests to cabbage crops in the south- east of Romania in This review evaluates multitrophic relationships and hyperparasitoid ecology. 1 Natural Sciences Complex Museum, Galaţi 2 University Al.I. Cuza of Iasi

2 Gabriela Patriche (Costea) and all. Materials and methods The study regarding the parasitoid complex which limits the population of Lepidoptera species, pests to cabbage crops in the south- east of Romania, was carried out between from 33 collecting sites and 54 collecting dates. Among these, Pieris brassicae has been identified in 16 sites (26 collecting dates) and Pieris rapae has been identified in 24 sites (43 collecting dates). The Pieridae species have been collected as eggs, larvae and pupae but their presence has also been identified based on specific parasitoids found on plants. In laboratory, different species of hyperparasitoids have been obtained from cocoons of primary parasitoid collected or reared from Pieridae larvae. The data we obtained following our collectings from the field show the impact of hyperparasitism on the regulating capacity of parasitoids in biological control. In some cases the low level of biological control by parasitoids has been attributed to the high level of hyperparasitism. The impact of hyperparasitism on biological control is reviewed. Results and Discussions 6 species of Lepidoptera defoliators were identified in the cabbage crops in the south- east of Romania: Pieris brassicae, Pieris rapae (Pieridae), Mamestra brassicae, Autographa gamma Linné, 1758 şi Helicoverpa armigera Hubner, 1808 (Noctuidae), Plutella xylostella (Plutellidae). The Pieridae damage predominated among these 6 species of defoliators Lepidoptera in the cabbage crops for the mentioned period, excepting the year 2000 when Plutella xylostela had a peak of attack. The hyperparasitoid complex of the Pieris brassicae: Only 5 primary parasitoid species were found from Pieris brassicae in : Cotesia glomerata Linné, 1758; Cotesia rubecula Marshall, 1885 (Braconidae); Hyposoter ebeninus Gravenhorst, 1829 (Ichneumonidae); Trichogramma evanescens Westwood,1833 (Trichogrammatidae); Compsilura concinnata Meigen, 1824 (Tachinidae) (Fig. 1) and two hyperparasitoid species as: Baryscapus galactopus Ratzeburg, 1844 (Chalcidoidea) reared from Cotesia glomerata, Cotesia rubecula and Hyposoter ebeninus and the second hyperparasitoid: Trichomalopsis submarginatus Thomson, 1878 (Chalcidoidea) reared from Hyposoter ebeninus (Fig. 1). The gregarious parasitoid, Cotesia glomerata had the main part in limiting the larvae stage of the Pieris brassicae (Fig. 1). It was reared from 355 caterpillars. 7.3% (519) of all individuals of the Cotesia glomerata (7180) were parasitised by Baryscapus galactopus (Fig. 1). These averages of parasitism varied from in 2000 to 20.8% in 1999 (Fig.2). Hyposoter ebeninus played a secondary role in limiting the larvae populations of the defoliators Pieris brassicae (Fig. 1). Baryscapus galactopus and Trichomalopsis submarginatus parasitised of the primary parasitoid, Hyposoter ebeninus (Fig. 1). These hyperparasitoids were reared only in two years: 1998 and 2001 (Fig. 3). 24

3 The hyperparasitoid complex which limits the action of the primari parasitoids ( ) of the Cotesia rubecula, an insingnificant primary parasitoid of the P. brassicae, was parasitised by Baryscapus galactopus, too (Fig. 1). The hyperparasitoid complex of the Pieris rapae: There were eight species of primary parasitoids which have been identified for Pieris rapae: Cotesia rubecula Marshall, 1885 (Braconidae); Hyposoter ebeninus Gravenhorst, 1829 (Ichneumonidae); Brachymeria femorata Panzer, 1801 (Chalcididae); Pteromalus puparum Linné, 1758 (Pteromalidae); Trichogramma evanescens Westwood (Trichogrammatidae); Compsilura concinnata Meigen, 1824; Phryxe vulgaris Fallen, 1810; Exorista larvarum Linné, 1758 (Tachinidae). There were two dominant and characteristic primary parasitoid species for these complex: Cotesia rubecula and Hyposoter ebeninus. Cotesia rubecula was parasitised by five secondary parasitoid species: Pteromalus semotus Walker, 1834; Trichomalopsis sp.a, Trichomalopsis sp.b, Catolaccus ater Ratzeburg, Baryscapus galactopus (Chalcidoidea) and Hyposoter ebeninus was parasitised by two species: Eurytoma infracta Mayr, 1904 (Chalcidoidea) and Baryscapus galactopus (fig. 1). Figure 1 shows the hyperparasitoid interventions for this period. The proportion of parasitised Cotesia rubecula by secondary parasitoid ranged from 16.9% in 2000 up to 45.5% in 1999 (average 34.1%) (Fig. 4). Pteromalus semotus, Trichomalopsis sp.a, Trichomalopsis sp.b. and Catolaccus ater are recorded for the first time as parasitoids on Cotesia rubecula. Baryscapus galactopus - Cotesia rubecula is host-parasitoid relationship new for Romania. The secondary parasitoids belonging to the Hyposoter ebeninus constantly diminished the action of the primary parasitoids, during the four years of study, reaching the highest point in 1998 (68.6%) and the lower point in 2000 (36.4%), with an average of 46.4% (Fig.5, Fig 1). Eurytoma infracta is recorded for the first time as parasitoid on Hyposoter ebeninus. Baryscapus galactopus dominates by limitating the Cotesia rubecula and Hyposoter ebeninus populations and the other hyperparasitoid species having an accidental appearance and insignificant role in the study period. Cotesia rubecula, a characteristic primary parasitoid for Pieris rapae had a grater number of secondary parasitoid (5 species) by comparison with Hyposoter ebeninus which had only two species. 25

4 Gabriela Patriche (Costea) and all. 26

5 The hyperparasitoid complex which limits the action of the primari parasitoids ( ) Figure 2 The mortality of the Cotesia glomerata L. cocoons, reared from Pieris brassicae L., due to secondary parasitoid, Baryscapus galactopus Ratz emerged Cotesia glomerata dead cocoons parasited cocoons Figure 3 The mortality of the Hyposoter ebeninus Grav. cocoons, reared from Pieris brassicae L., due to secondary parasitoids emerged Hyposoter sp. dead cocoons parasited cocoons 27

6 Gabriela Patriche (Costea) and all. 10 Figure 4 The mortality of the Cotesia rubecula Marsh. cocoons, reared from Pieris rapae L., due to secondary parasitoids emerged Cotesia rubecula dead cocoons parasited cocoons Figure 5 The mortality of the Hyposoter ebeninus Grav. cocoons, reared from Pieris rapae L., due to secondary parasitoids emerged Hyposoter sp. dead cocoons parasited cocoons Conclusions Seven hyperparasitoid species diminished the role of the primary parasitoid belonging to the Pieridae dofoliators in the cabbage crops in the south-east of Romania. The efficiency of the primary parasitoid in limiting the Pieris brassicae populations wasn t reduced by the secondary parasitoids, for the period subjected to 28

7 The hyperparasitoid complex which limits the action of the primari parasitoids ( ) study but the reaction of the hyperparasitoid complex belonging to the Pieris rapae, was quite direct proportional with the action of the primary parasitoid species. Baryscapus galactopus was the major hyperparasitoid species by limitating the Cotesia glomerata, Cotesia rubecula and Hyposoter ebeninus populations and the other hyperparasitoid species having an accidental appearance(presence ) and an insignificant role in the study period. These results indicate that the rate of hyperparasitism is much higher, especially for Pieris rapae, in comparison with the research carried out 30 years ago, and, in some cases, it has the potential to alter the primary parasitoid effects. Bibliography 1. Andriescu, I; Sauciniţianu, Veronica; Oancea, Irinel, Trav. St. Stejaru, Ecol. terrestre et Génétique: Andriescu, I., Advances in Parasitic Hymenoptera Research, pp Andriescu, I. D., Contribuţii la studiul Calcididelor (familiile: Chalcididae, Eurytomidae, Pteromalidae, Eulophidae şi Encyrtidae) din R. S. România, din punct de vedere sistematic, biologic, ecologic şi economic. (Chalcidoidea Ashmead 1904, Hym. Insecta), teză de doctorat, Cluj-Napoca. pp Graham, M.W.R. de V., Bull. of the British Museum (Natural History) Entomology, Supplement 16; pp Graham, M.W.R. de V., A reclassification of the european Tetrastichinae (Hymenoptera: Eulophidae): Revision of the remaining genera in Memoirs of the American Entomological Institute, Number 49, pp Mustaţă, Gh., Insecte dăunătoare legumelor din Moldova şi duşmanii lor naturali. PhD Thesis, Al. I. Cuza. University, Iaşi. 7. Mustaţă, Gh. & Andriescu, I., Trav. St. Stejaru, Ecol. terrestre et Génétique: Mustaţă, Gh.; Costea, Gabriela, Mitt. Dtsch. Ges. Allg. Angew. Ent. 12, Mustaţă, Gh.; Mustaţă, Mariana, The role of the parasitoid biocoenoses in keeping the equilibrum of nature. Ed. Univ. Al. I. Cuza Iaşi, pp Triapitzin, V.A.; Kostiukov, V. V., Izd. Nauka, Leningrad, pp Triapitzin, V.A., Leningrad Nauka Leningrad Division. pp Zerova, M. D., Kiev Naukova Dumka, pp